Journal of Threatened Taxa | www.threatenedtaxa.org | 26 June 2016 | 8(6): 8860–8876
A.J. Solomon Raju 1 & Rajendra Kumar 2
1Department of Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India
2Ministry of Environment, Forest and Climate Change, Indira Paryavaran Bhavan, Jorbagh Road, New Delhi 110003, India
email@example.com (corresponding author) firstname.lastname@example.org
doi: 8860-8876Editor: Cleofas Cervancia, University of Philippines Los Baños College Laguna, Philippines. Date of publication: 26 June 2016 (online & print)
Manuscript details: Ms # 2275 | Received 05 September 2015 | Final received 30 April 2016 | Finally accepted 19 May 2016
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.
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 necessary facilities to carry out this research work.
Abstract: Floral biology, sexual system, breeding system, pollinators, fruiting and seed dispersal aspects of three Suaeda species, S. maritima, S. monoica and S. nudiflora (Chenopodiaceae) were studied. The flowers of all the three species are hermaphroditic, dichogamous, strongly protogynous with a pistillage phase during the mature bud stage and staminate phase following anthesis, self-compatible exhibiting mixed breeding systems with special adaptation for cross-pollination; but both self- and cross-pollination are vector-dependent. In all, the flowers display a mix of anemophilous and entomophilous traits. Anemophily is effective in high salt marshes while water currents bring about pollination in low salt marshes; insects pollinate the flowers while collecting the forage from pistillate and staminate phase flowers. In these species, the whole plant breaks off and rolls on the floor while shedding its diaspores. Fruits with seeds intact and/or seeds shed from fruits float on water due to their ability for buoyancy. The fruits and seeds thus disperse, settle in the entire extent of salt marshes or coastal areas and germinate in mid-summer season when salinity is very high in high and low salt marshes.
Keywords: Anemophily, entomophily, hydrophily, seed dispersal, Suaeda.
The genus Suaeda consists of 110 species all over the coastal tropics and sub-tropics of the world (Gelin et al. 2003). It consists mostly of halophytic leaf-succulents that grow in saline and alkaline wetlands and deserts. A number of species are valuable as feed for livestock in arid areas while other species are useful to desalinize irrigated farmlands. This genus has both C3 and C4 photosynthetic pathways. It uses the C4 photosynthetic pathway when exposed to a stressful environment and hence is an adaptive mechanism (Fisher et al. 1997). In central Asia, C4 species of Suaeda are mostly annuals (Glagoleva et al. 1990). Both the C3 and C4 species of Suaeda commonly grow side by side; C4 species grow abundantly in drier and more saline sites. They are enabled by their succulence to persist throughout the dry season. Wetson et al. (2012) stated that S. maritima is a widely occurring halophyte of salt marshes. These authors noted that high marsh and low marsh plants develop different morphologies as a result of different stressful soil conditions - small and less branched mature plants in low marshes and long and much-branched mature plants in high marshes. S. maritima is an annual obligate succulent halophytic annual mangrove herb and thrives in both coastal and inland salt marshes (Flowers et al. 1977). Two varieties, S. maritima ssp. richii and S. maritima ssp. maritima have been reported in Newfoundland and Nova Scotia in northern America; these varieties were classified based on growth habit and seed size. The former is small, procumbent and mat-forming with seeds 1–1.5 mm in diameter while the latter variety is prostrate to ascending with seeds 1.5–2 mm in diameter (Ferren & Schenk 2003). Three principal varieties were described in this species by Chapman (1947). They are var. vulgaris, macrocarpa and flexilis. var. vulgaris is a large plant with spreading branches suffused with red, and with leaves tapering slightly towards each end. The flowering occurs six months after seed germination; it occurs from August to October, the fruit is small, not exceeding 1.5mm diameter. var. macrocarpa is a decumbent or prostrate plant with divaricate branches and short leaves, occupies a higher zone. The flowering occurs 5 months after seed germination; it occurs from mid-July to September, and produces 2mm diameter fruits. var. flexilis is an erect short-stemmed plant with branches from the mid-part of the stem, occupies muddy soils. The flowering occurs 6 months after seed germination; it occurs in August–October and produces 1.1–1.4 mm diameter fruits. In all the three varieties, seed germination occurs from March onwards and fruits disperse from October onwards. Fruit dispersal occurs by tides and they can float for 3 days and then settle in the soil. Of these, var. vulgaris and var. flexilis have been reported to be widespread. var. vulgaris is recorded from Asia, France, Macronesia, the Mediterranean and Russia, the Caucasus; var. macrocarpa from Belgium, France, Spain and Russia; and var. flexilis from Sweden, Germany, Belgium, France, Spain and southern Europe. S. maritima is successful as a colonist of secondary bare areas and salt plans of higher marshes in both Europe and America. Chapman (1947) mentioned that S. maritima flowers are homogamous or feebly protandrous; autonomous autogamy is easily possible. The flowers are nectar-less and hence there were no insect visitors. The insects such as Coleophora suaedivora (Coleophoridae) and Phthozimaea suaedella (Gelechidae) feed on leaves and seeds. Bassett & Crompton (2011) recorded that S. maritima flowers during July–September and is wind-pollinated. Naskar & Mandal (1999) reported that S. maritima is pollinated by wind, water currents and flies. S. monoica is a salt marsh mangrove succulent annual herb similar to S. maritima (Ravikumar et al. 2011). It is a C4 species and grows in hyper saline soils; the plants possessing the C4 photosynthetic pathway grow abundantly in hot, dry, high-light environments (Shomer-Ilan et al. 1975; Ehleringer & Monson 1993). S. nudiflora is a salt mangrove succulent herb that grows well in the highly saline, dry and extreme high tidal belt. It has small, linear and succulent leaves and this succulence is a morphological adaptation. It is a C4 plant (Singh et al. 2004; Patel & Pandey 2009). Dem’yanova (1977) worked on the flowering and pollination ecology of S. microphylla, S. physophora, S. acuminata and S. linifolia in the desert of the Ili valley in USSR. This author reported that these species are predominantly anemophilous and entomophilous but the latter has no significant importance. The flowers receive visits of Halictus bees during staminate phase by which time the stigma begins to wither and does not accept pollen. Keighery (1979) reported that honey bees and syrphid flies collect pollen from the flowers of Suaeda australis; but this author did not mention whether they are pollinators.
The work done so far on Suaeda species as stated above suggests that this genus as a mangrove associate has not been studied at all with reference to their reproductive ecology from the perspective of their importance in the mangrove ecosystem. It is in this context, Suaeda maritima (L.) Dum., S. monoica Forsk. Ex. J.F. Gmel. and S. nudiflora (Willd.) Moq. (Chenopodiaceae) occurring in the Godavari-Coringa mangrove forest in the State of Andhra Pradesh, India, have been thoroughly studied for their floral biology, sexual system, breeding system, floral rewards, pollinators and their foraging behaviour. Further, fruit and seed dispersal aspects have also been studied to the extent possible. The outcome of the work is considered to be immensely valuable for understanding the reproductive ecology of the studied Suaeda species and their potential use for the clean-up of salts from saline soils.
MATERIALS AND METHODS
The Godavari mangrove wetland lies between 16030’–17000’N & 82010’–80023’E in Andhra Pradesh State, India. In this wetland, three Suaeda species, S. maritima, S. monoica and S. nudiflora (Chenopodiaceae) occur with different population densities depending on soil conditions. All the three Suaeda species form thick mats in upper and low salt marshes in the estuarine area and towards land as well. S. maritima and S. monoica grow together successfully while S. nudiflora mostly in areas which are not occupied by the other Suaeda species. The locals use Suaeda species for treating certain skin diseases by external application. All the three Suaeda species were studied in detail for their reproductive ecology. Field studies and lab-work were undertaken from February 2011 to June 2014.
Flowering and floral biology
Flowering seasons were defined based on regular field trips made for three years. Observations regarding the organization of inflorescences, the spatial positioning of flowers, and their position (terminal, axillary, etc.) on the plants were made since these features are regarded as important for foraging and effecting pollination by flower-visitors. The flower life was recorded by marking 50 just anthesed flowers and following them until fall off. Anthesis was initially recorded by observing 50 marked mature buds in the field. Later, the observations were repeated 3 to 4 times on different days in order to provide accurate anthesis schedule for each species. Similarly, the mature buds were followed for recording the time of anther dehiscence. The presentation pattern of pollen was also investigated by recording how anthers dehisced and confirmed by observing the anthers under a 10x hand lens. The details of flower morphology such as flower sex, shape, size, colour, odour, tepals, stamens and ovary were described based on 25 flowers randomly collected from a population of plants for each species. The order of wilting or dropping off of floral parts was recorded. Observations regarding the position and spatial relationships of stamens and stigma in mature bud, at anthesis and after during the flower-life with reference to self and/or cross-pollination were made very carefully.
Determination of pollen output
Twenty-five mature but undehisced anthers from five different plants were collected and placed in a petri dish. Later, a single anther was taken out and placed on a clean microscope slide (75x25 mm) and dabbed with a needle in a drop of lactophenol-aniline-blue. The anther tissue was then observed under the microscope for pollen, if any, and if pollen grains were not there, the tissue was removed from the slide. The pollen mass was drawn into a band, and the total number of pollen grains was counted under a compound microscope (40x objective, 10x eye piece). This procedure was followed for counting the number of pollen grains in each anther collected. Based on these counts, the mean number of pollen produced per anther was determined. The mean pollen output per anther was multiplied by the number of anthers in the flower for obtaining the mean number of pollen grains per flower. The characteristics of pollen grains were also recorded.
Determination of pollen-ovule ratio
The pollen-ovule ratio was determined by dividing the average number of pollen grains per flower by the number of ovules per flower. The value thus obtained was taken as pollen-ovule ratio (Cruden 1977).
Examination of nectar characters
The presence of nectar was determined by observing the mature buds and open flowers. The flowers used for this purpose were bagged at the mature bud stage, opened after anthesis and squeezed nectar into a calibrated micropipette for measuring the volume of nectar. Then, the average volume of nectar per flower was determined and expressed in µl.
Determination of stigma receptivity
The stigma receptivity was observed visually and by H2O2 test. In the visual method, the stigma physical state (wet or dry) and the unfolding of its lobes were considered to record the commencement of receptivity; withering of the lobes was taken as loss of receptivity. H2O2 test as given in Dafni et al. (2005) was followed for noting stigma receptivity period. This test is widely followed although it does not indicate the exact location of the receptive area. In the present study, the period of slow release of bubbles from the surface of stigma following the application of hydrogen peroxide was taken as stigma receptivity.
Determination of natural fruit set
One hundred inflorescences were tagged on different plants prior to anthesis and followed for fruit and seed set rate in open-pollinations. Fruit maturation period, fruit dehiscence and seed dispersal aspects were observed in detail.
Observations of flower-visitors
The foraging activity of insects was observed from 06:00h to 18:00h. After making preliminary observations on the categories of flower visitors, a thorough knowledge of the local insect species was obtained by observing the representative species of insects available with the Pollination Ecology Laboratory in the Department of Environmental Sciences, Andhra University, Visakhapatnam. Some insect species were identified to genus level only and a few insect species could not be identified at all even by the Insect Taxonomic Group with the Division of Entomology, Indian Agricultural Research Institute, New Delhi. With the knowledge of local insect species, attempts were made to observe flower visitors on each plant species chosen for the study. The insect species were observed visually and by using binoculars; the insect species that could not be identified on the spot were captured and later identified with the help of the identified specimens available in the Department. The hourly foraging visits of each insect species on each plant species was recorded on 3 or 4 occasions depending on the possibility and the data was tabulated to use the same for further analysis. For each species, 15–20 inflorescences were selected to record the foraging visits of insects. The data obtained was used to calculate the percentage of foraging visits made by each insect species per day and also to calculate the percentage of foraging visits of each category of insects per day in order to understand the relative importance of each insect species or category of insects.
Determination of pollen carryover efficiency of insects
The flower visitors were captured during 10:00–12:00 h on each plant species and brought to the laboratory. For each insect species, 10 specimens were captured and each specimen was washed first in ethyl alcohol and the contents stained with aniline-blue on a glass slide and observed under the microscope to count the number of pollen grains present. In case of pollen collecting insects, pollen loads on their corbiculae were separated prior to washing them. From this, the average number of pollen grains carried by each insect species was calculated to know the pollen carryover efficiency of different insect species.
Determination of foraging behaviour of insects
The foraging activity of insect species was confined to the daytime only. The insects were observed on a number of occasions on each plant species for their foraging behaviour such as mode of approach, landing, probing behaviour, the type of forage they collect, contact with essential organs to result in pollination, inter-plant foraging activity in terms of cross-pollination, etc. Observations were also made on the bud, flower and fruit feeding activity by insects.
Study area, habitat, plant, flower and fruit details together with insect foraging activity on the flowers were photographed with a Nikon D40X Digital SLR (10.1 pixel), a TZ240 Stereo Zoom Microscope and with an SP-350 Olympus Digital Camera (8.1 pixel). Olympus Binoculars (PX35 DPSR Model) were also used to make field observations. A Magnus Compound Microscope - 5x, 10x, 40x and 100x magnification was used for studying pollen characteristics.
Suaeda maritima, S. monoica and S. nudiflora are halophytic succulent mangrove associates; the first two are erect glabrous annual herbs growing to a height of up to 0.3m while the last one is a perennial prostrate herb growing to a height of up to 1.5m tall. All the three species grow in high and low salt marshes and along tidal banks (Images 1, 7a). These three species invariably show different growth responses depending on the locality, high or low salt marshes. The growth forms could be distinguished, the one which grows in low marsh locality is smaller and less branched than the other one which grows in high marsh locality. In case of S. maritima, the plants that grow at high tide marsh without other species grow taller with many lateral branches. S. maritima and S. monoica usually form dense communities and are usually shiny light green in color, and turn reddish as they age. S. nudiflora grows in more widely spaced communities in relatively semi-dry areas, it tends to be grey in color, and turns blackish as it ages. The leaves are long and sickle-shaped when young, base truncate and apex acute in S. maritima; alternately crowded, linear-oblong, spathulate, flat, rounded at tip and narrowed at base in S. monoica; and linear, ovate, fleshy, terete base acute, apex sub-acute in S. nudiflora. Seeds germinate in April and new plants mature to reproductive phase in three months and flower during July–October in S. maritima and S. monoica (Image 2a,b). In S. nudiflora, the flowering occurs throughout the year with concentrated flowering from July-September (Image 11a–c). Inflorescences are axillary in position and the flowers are clustered in cymes; the number of flowers at each leaf axil is 9–18 in S. maritima (Image 2c–e), 5–8 in S. monoica (Image 7b,c) and 2–4 in S. nudiflora (Image 11d).
The flowers are green and erect in S. maritima and S. monoica while they are greenish-yellow and semi-erect in S. nudiflora. The flowers are bisexual in all the three species; they are 3mm long, 4mm wide in S. maritima, 2–3 mm long and 3mm wide in S. monoica, and 1–2 mm long and 2 mm wide in S. nudiflora. The flowers in all the three species have rosaceous perianth represented by five free equal succulent, glabrous and keeled lobes or tepals. The tepals are abaxially rounded and distally hooded at maturity. The stamens are 5, free, basifixed, the anthers globose-ellipsoid, exserted, introrse, dithecal and tetra-sporangiate in all the species (Image 3b). The staminal filaments are white and ban-shaped in S. maritima and S. monoica while they are light yellow and cylindrical in S. nudiflora; in all the three species, the filaments are soft and glabrous, and inserted near the tepal bases. In all the three species, ovary is pear-shaped, uni-locular with solitary ovule on basal placentation, 1mm long and 1mm wide, whitish green, succulent and glabrous (Images 3g, 8h,i, 12g,h). Stigmas are sessile, filiform, hairy-papillate, and arise from a pit at the top of the ovary; they are 3 in S. maritima (Image 3f) and S. monoica (Image 8f,g) and 2 in S. nudiflora (Image 12g).
The flowers are open from 0800–1100 h in all the three species (Images 3a, 7d, 8a-d, 12a-d). In all, the papillate stigma lobes protrude out of the maturing (bulging) bud and are receptive a day before anthesis (Image 3e). The lobes gradually wither and become unreceptive by the time the anthers protrude due to the unfolding of the hooded perianth lobes during anthesis. The protruded stamens extend beyond the height of withered stigma lobes (Image 12e) and dehisce by longitudinal slits exposing the bright yellow colored and powdery pollen grains. In all the three species, the pollen grains are spheroidal, pantoporate, multiporate and vary in size; it is 25.5 ± 0.86 µm in S. maritima (Image 3c,d), 20.37 ± 1.22 µm in S. monoica (Image 8e) and 18.21 ± 0.29 µm in S. nudiflora (Image 12f). The pollen output per anther is 3,818 ± 28.34 in S. maritima, 3,253 ± 17.34 in S. monoica and 2,035 ± 21.23 in S. nudiflora. The pollen output per flower is 19,090 in S. maritima, 16,265 in S. monoica and 10,175 in S. nudiflora. The pollen-ovule ratio is equal to the pollen output per anther due to 1-ovuled flowers in all the three species. The flowers in all the species produce 1.2 ± 0.21 µl of nectar; it is available only during the staminate phase. In these species, the perianth lobes close back and cover the ovary but not the anthers by the evening of the 2nd day. The stamens fall off subsequently on the 3rd or 4th day. The flower life is 3–4 days. The perianth lobes gradually bulge along with the growing seed, and hence the perianth acts as seed cover.
In all the three species, the flowers are strikingly protogynous, the mature bud stage is pistillate due to the protrusion and receptivity of stigmatic lobes while the post-anthesis stage is staminate due to cessation of stigma receptivity by the time of anthesis and dehiscence of anthers after anthesis. The pistillate and staminate phases are therefore temporally separated and this situation is a type of temporal dioecy. This sexual system completely prevents autogamy but facilitates both geitonogamy and xenogamy. Geitonogamy occurs due to pollen transfer from the pollen of staminate phase flowers to the stigmatic lobes of pistillate phase mature buds within the plant; if pollen transfer occurs between flowers of different plants within or across populations, it results in xenogamy. The hairy-papillate stigmatic lobes in all the three species standing out distinctly from the mature buds were found to capture pollen driven by the wind. The powdery and multi-porate nature of pollen grains enable them to fly and disperse easily by wind and their dispersal is further propelled by vast uniform mats of populations of Suaeda species. The wind-driven pollen deposition on the stigmatic lobes and leaves can be seen with the naked eye and hence anemophily was considered to be effective. Anemophily was very effective in high salt marshes devoid of water-logged conditions. In the low salt marshes where water-logged or water-saturated conditions occur, water currents were found to carry and disperse pollen effectively; here considerable aerial parts of the plants were merged or intermittently exposed and hence pollen was wet, making anemophily mostly ineffective. In all the three species, fruit set in open-pollinations is 93–95 % indicating the success rate of both geitonogamy and xenogamy; this high success rate could be due to the production of a single ovule in the flowers for which the deposition of a few viable pollen grains on the stigmatic lobes is sufficient.
Foraging activity and pollination
In all the three species, the flowers were foraged by bees, wasps and flies during daytime from 08:00–17:00 h with more foraging activity during 09:00–12:00 h and less activity during the afternoon period in high salt marshes and in low salt marshes where soil was not saturated with water (Tables 1, 3, 5; Figs. 1, 2, 4). The foraging activity pattern of all these categories of insects was almost similar and coincided well with the standing crop of floral rewards. S. maritima was foraged by Nomia bees (Image 4a) and one unidentified bee for pollen and nectar; by wasps, Eumenes petiolata (Image 4c), Ropalidia sp. (Image 4d), Rhynchium sp. and three unidentified wasp species (Image 4e–g), and by flies Helophilus sp. and Sarcophaga sp. (Image 4h) for nectar only. Camponotus ants also foraged for nectar (Image 4b), but they were resident foragers and remained on the plants throughout the flowering season. S. monoica was foraged by honey bees, Apis dorsata (Image 9a), A. cerana and A. florea for both pollen and nectar (Image 9b); by wasps, Eumenes petiolata, Rhynchium sp. (Image 9c) and by the fly, Sarcophaga sp for only nectar (Image 9d). S. nudiflora was visited by Nomia bees for both pollen and nectar (Image 13a) while Rhynchium wasps for nectar only (Image 13b). In all the three species, thrips were nectar and pollen feeders (Image 13c); they collected most of the nectar during the mature bud stage and after anthesis, and also pollen during post-anthesis stage as soon as the anthers dehisce. Further, the iridescent green tortoise beetle, Chrysochoris (Scuteleridae) collected S. maritima pollen voraciously (Image 5d) while an unidentified immature stage of an insect was found to feed on the nectar and pollen of S. nudiflora (Image 13d). The percentage of foraging visits made by each category of insects varied with each Suaeda species. In S. maritima, bees made 21%, wasps 62% and flies 17% of the total foraging visits (Fig. 3). In S. monoica, bees made 54%, wasps 35% and flies 11% of the total foraging visits (Fig. 5). In S. nudiflora, Nomia bee made 48% and Rhynchium wasp made 52% of the total foraging visits.
In all the three plant species, the flowers with dehisced anthers representing the staminate phase attracted bees due to the clear-cut display of bright yellow pollen; the bees while collecting pollen and nectar from such flowers invariably also contacted accidentally the flowers in the pistillate phase occurring in the same cluster or nearby clusters on the same flowering branch due to their close proximity to each other and this foraging behavior was considered to be effecting geitonogamy. The production of a few staminate phase flowers each day at the branch or plant level was found to be driving the bees to make frequent inter-plant visits within and between populations in the entire area in order to collect more nectar and pollen. They were effective carriers of pollen and their body washings revealed the presence of 142–156 pollen grains in case of S. maritima (Table 2), 195–219 pollen grains in case of S. monoica (Table 4), and 142 pollen grains in case of S. nudiflora (Table 6). Wasps, flies and ants attempted to collect nectar from pistillate and staminate phase flowers without any discrimination; such a foraging behavior was considered to be facilitating both geitonogamy and xenogamy. The flowers with minute traces of nectar were found to be driving the wasps to make frequent inter-plant visits in order to collect more or optimal levels of nectar due to their high energy requirement. They were found to carry 36–82 pollen grains on their bodies in case of S. maritima (Table 2), 78 pollen grains in case of S. monoica (Table 4), and 61 pollen grains in case of S. nudiflora (Table 6) indicating their pollen carrying capacity. In case of flies, they tended to remain on the same plant for a long time collecting nectar from as many flowers as possible due to their low energy requirement. Their body washings revealed the presence of an average of 41–45 pollen grains in case of S. maritima (Table 2), 46 pollen grains in case of S. monoica (Table 4) and hence they were also pollen carriers to some extent. Ants as resident foragers and with a low energy requirement were considered to be important for geitonogamy if they were confined to the same plant and for xenogamy if they crawled to other nearby plants for nectar collection. They were found to carry an average of 50 pollen grains due to their nectar foraging activity. The nectar and pollen feeding activity of thrips was found to be an important driver, especially for bees and wasps to forage a number of individual flowers within and between populations. Certain of the insects recorded were common to all the three plant species which co-exist in the same area and their alternate foraging visits could lead to the deposition of mixed pollen on each of these plant species. Such mixed pollen deposition could block the receptive area of the stigma lobes and reduce the opportunities for legitimate geitonogamous and xenogamous pollinations in each plant species.
In all the three Suaeda species, the nymphalid butterflies, Danaus genutia (Images 5a, 14a-c), D. chrysippus (Images 5b, 14d), the lycaenid Euchrysops cnejus (Image 14e), and the hesperiid, Borbo cinnara (Image 5c) were found to feed on the sap of leaves prior to flowering and on dry fruited branches. These butterflies mainly concentrated on S. maritima and S. monoica for sap collection. Further, they never visited the flowers for nectar collection and hence were not pollinators.
In all the three species, fruit is an urticle with a 1.5mm wide and 1mm long persistent perianth (Image 3h). Hooded perianth segments cover seeds over the margins. It matures within 3–4 weeks (Image 6, 10a,b, 11e,f). Each fruit invariably produces a single seed. The seeds ripen from August–October. The seeds are brownish-black, smooth, glossy, ovoid, 1.2–1.5 mm diameter, finely punctate near the edges and beaked (Images 3i, 8j,k, 12i). The whole plant breaks off easily and rolls on the floor while shedding its diaspores. Fruits with seeds intact and/or seeds shed from fruits float on water due to their ability for buoyancy. The fruits and seeds thus disperse and settle in the entire extent of salt marshes or coastal areas.
All the three Suaeda species are obligate succulent halophytes and grow well in high and salt marshes in different zonations of mangroves. Their growth within the interiors of mangroves is an excellent indicator of their tolerance level to high salinity. However, their growth rates vary depending on the locality, high or low salt marshes. The plants growing in high marshes are taller and profusely branched than those growing in low marshes. Wetson et al. (2012) reported such plasticity in plant growth pattern in S. maritima growing in the upper and lower salt marshes. Further, these authors also reported that plants growing at the extreme tide mark in the absence of other speciesgrow taller with many lateral branches. Ferren & Schenk (2003) reported two varieties, richii and maritima in S. maritima based on growth habit and seed size. Chapman (1947) also reported three principal varieties, vulgaris, macrocarpa and flexilis based on growth habit and seed size. Redondo-Gomez et al. (2008) reported that several Suaeda species exhibit seed dimorphism and produce both brown and black seeds simultaneously and these varying colorations reflect two different dormancy and germination strategies for survival in saline habitats. Ponnamperuma (1984) explained that occurrence of different growth forms reflect different soil conditions present in high and low salt marshes due to difference in aeration levels. The high salt marshes are well-drained and infrequently inundated by tidal water and hence have stable and good soil aeration due to rapid exchange between air and soil whereas the low salt marshes with water-logged conditions experience reduced availability of oxygen due to very slow diffusion of gases in water than in air. Further, the exchange of gases would fluctuate in both high and low salt marshes at different times due to variation in the frequency of submergence and quantum of tidal water causing inundation. As a result, the plants growing in the high and low salt marshes show different responses due to variation in soil aeration levels. All the three Suaeda species in this study did not show seed dimorphism either in size or in color suggesting that the variations in seed morphological characters could be situational depending on the nutrient and water levels, temperature, and other ecological factors present at the time of production of seeds in both annual and perennial Suaeda species.
Khan & Weber (2003) reported that in annuals there is only one reproductive event in a lifetime, and this necessitates the ability to produce seeds with dormancy characteristics; when the seeds reach maturity, the environmental conditions may not be favorable for seedling growth and so germination is postponed until conditions are again more favourable. On the contrary, perennials reproduce by seed on multiple occasions, which means that producing genetic variations is not so paramount as it is with annuals; they may reproduce clonally, seeking to reproduce only the most successful genotype. However, as a long-term strategy, they may need to introduce new genetic individuals as and when conditions allow. In the present study, S. maritima and S. monoica are annuals and produce seeds once in their life with dormancy characteristics because their seeds germinate with a pause of 5–6 months from seed dispersal to seed germination. In these plants, genetic variation through sexual mode is very essential in order to withstand adverse soil conditions and produce stable populations. S. nudiflora is a perennial and produces seeds more than once in its life time and hence production of genetic variation is not very important for the production of stable populations. However, introduction of new genetic individuals as and when conditions allow is inevitable if this species is to survive and continuously produce stable populations in inhospitable habitats.
Abeywickrama & Arulgnanam (1993) described certain floral sex characters in S. maritima and S. nudiflora. Their descriptions indicate that these two species produce male flowers with a small ovary and female flowers with stamens reduced or absent; the styles vary from 2 to 3. These authors also mentioned that in S. monoica, each flower cluster consists of a large male flower with a rudimentary ovary surrounded by smaller female flowers with or without staminodes. Further, certain individual plants produce only female flowers. The present study contradicts these descriptions because all the three Suaeda species produce only bisexual flowers without styles; S. maritima and S. monoica flowers produce three sessile stigmas while S. nudiflora produces two sessile stigmas. Further, the inflorescences are characteristically axillary in S. maritima and S. monoica while they are borne both in the axils and terminally in S. nudiflora. The clustered cymes produce a varying number of flowers with each Suaeda species; they are 9–18 in S. maritima, 5–8 in S. monoica and 2–4 in S. nudiflora.
Rea (1969) & Kubitzki et al. (1993) reported that polygamy occurs in many species of Chenopodiaceae. Gynomonoecy in combination with protandry or protogyny occurs in some species. Kubitzki et al. (1993) stated that in this family, the presence of inconspicuous, minute, frequently perianth-less and mostly nectar-less flowers have been considered as adaptations for anemophily. These authors also mentioned that typical features of anemophily such as dusting pollen, waving, limp-filaments or simultaneous flower opening are usually required in order to be uniformly anemophilous. Zandonella (1977) noted that a switch-over from entomophily to anemophily or the reverse might have occurred in this family. Dalby (1962) stated that self-pollination also frequently occurs in various genera; one such genus is Salicornia in which the ripe dehiscing anthers stay in contact with the presumably receptive stigmas and in effect, selfing occurs. Kubitzki et al. (1993) felt that probably various degrees of balance between anemophily and self-pollination can be found in the members of this family. Dem’yanova (1977) reported that S. microphylla, S. physophora, S. acuminata and S. linifolia are predominantly anemophilous; entomophily also exists but it has no significant importance. The flowers receive visits of Halictus bees during the staminate phase by which time the stigma begins to wither and does not accept pollen. Keighery (1979) reported that honey bees and syrphid flies collect pollen from the flowers of Suaeda australis but this author did not state whether they are pollinators or not. Chapman (1947) mentioned that S. maritima flowers are homogamous or feebly protandrous; autonomous autogamy is easily possible. The flowers are nectar-less and hence insect activity is absent. Bassett & Crompton (2011) recorded that S. maritima is wind-pollinated. Naskar & Mandal (1999) reported that S. maritima is pollinated by wind, water currents and flies.
In the present study, all the three Suaeda species are nectariferous and offer nectar in minute to trace amounts. The flowers are dichogamous with strong protogyny; they are pistillate during the mature bud stage and staminate after anthesis, the situation of which completely prevents autonomous or facilitated selfing within the flower. This sexual system is almost typical of temporal dioecy. Cruden & Hermann-Parker (1977) coined the term ‘temporal dioecism” to describe the pattern of sexual alternation within the individual plants to facilitate outcrossing through the promotion of xenogamy. The sexual system functional in Suaeda species is a type of temporal dioecy. In these species, the strong dichogamy appears to have evolved to promote outcrossing, however, both pistillate and staminate phase flowers are available at any given point within the individual plants facilitating the occurrence of geitonogamy. Therefore, Suaeda species seem to have evolved temporal dioecy to promote outcrossing through xenogamy while keeping the option open for selfing through geitonogamy. The fruit set recorded in open-pollinations substantiates the functionality of such a sexual system. This sexual system is essential for these species to produce seeds in isolated individuals in news areas in order to build up their populations.
Renner & Feil (1993) stated the plants that possess morphological traits fulfilling the aerodynamic requirements of pollen dispersal and capture favor the evolution of anemophily. Wind pollination might evolve when pollinators are scarce, absent or deliver poor quality pollen when plants colonize areas with low insect abundance (Weller et al. 1998; Gomez & Zamora 1996). Anemophilous plants do not invest in resources that attract pollinators, such as showy flowers, nectar and scent. Instead, they produce a large quantity of light, dry pollen from small, plain flowers that can be carried by wind. Female structures are adapted to capture the passing pollen from the air but the majority of pollen goes waste. Niklas (1985) stated that plants with small, colorless, odorless and nectar-less flowers, reduced or no perianth, projecting exserted stamens away from the boundary layer of main flower to higher wind speeds, production of large quantity of light, dry and dusty pollen, permitting the unobstructed removal of pollen, and well exposed large, hairy and feathery stigma to capture pollen are adapted for anemophily. In all the three Suaeda species, the flowers have a combination of anemophilous and entomophilous traits. The anemophilous traits are odorless, unattractive flowers with inconspicuous perianth, the exserted stamens projected out of the perianth and light, dry and dusty pollen while entomophilous traits are production of nectar, dorsi-fixed stamens, production of a moderate quantity of pollen, and promiscuity of flower for nectar and pollen collection for insects. Field observations indicated that anemophily is effective especially in high salt marshes due to the occurrence of moderate to high wind speeds in the mangrove areas; the pollen deposition by wind on the stigmas can be easily recorded and the leaves also get coated with pollen despite their succulent nature. Insects pollinate the flowers while collecting the forage from pistillate and staminate phase flowers. Bees visit only staminate flowers due to the availability of both nectar and pollen; while approaching these flowers they effect either geitonogamy or xenogamy accidentally because of the clustered form of flowers. Wasps, flies and ants probe pistillate phase mature buds and staminate phase flowers of the concerned plant species indiscriminately, but the pistillate phase flowers are non-rewarding while the staminate phase flowers are rewarding. As a result, these insects effect geitonogamy and xenogamy. Chrysocoris beetle is a voracious pollen feeder and deprives the flowers of pollen in S. maritima; its pollen feeding activity indirectly compels the bees to collect pollen from different plants and such a foraging behavior results in the promotion of xenogamy. Further, thrips in all the three species and one insect in an immature stage in the case of S. nudiflora deplete both nectar and pollen being available considerably and such a state of floral rewards drive all the insect species, except ants to make frequent inter-plant visits within the species and across Suaeda species; this leads to the promotion of outcrossing through xenogamy. The occurrence of these species in the same area and their simultaneous flowering facilitates the insects to deposit mixed pollen consisting of the pollen of all the three species on their stigmas and this pollen discounting diminishes outcross siring success. In this context, it is to be stated that insect activity is not very intense on these plant species, it is prominent on S. maritima and S. monoica while it is not so in S. nudiflora due to the production of very inconspicuous flowers when compared to the other two species. Pollen discounting did not show any affect on seed set rate and it is reflected in the very high fruit set rate in open-pollinations. This could be because of the requirement of a few viable pollen grains for stigmas to produce a single seed per flower. Further, water currents also disperse pollen and pollinate flowers within and between plants of all the three species in inundated or submerged localities. In these localities, anemophily or entomophily is not very effective due to the wet state of pollen or flowers or even plants. Therefore, these three Suaeda species use a combination of pollination by wind, insects and water currents simultaneously. The function of three pollination syndromes in these plant species gives them flexibility to maximize fruit or seed set rate through outcrossing as well as selfing through geitonogamy (Culley et al. 2002).
Ridley (1930) noted that Chenopodiaceous seeds are dispersed by wind, water and animals. Chapman (1947) stated that in S. maritima, seed germination occurs from March onwards and fruits disperse from October onwards. Fruit dispersal occurs by tides and they can float for three days and then settle in the soil. In the present study also, it is found that in all the three Suaeda species, the whole plant breaks off and rolls on the floor while shedding its diaspores. Fruits with seeds intact and/or seeds shed from fruits float on water due to their ability for buoyancy. The fruits and seeds thus disperse, settle in the entire extent of salt marshes or coastal areas and germinate in the mid-summer season when salinity is very high in high and low salt marshes.
Jones & Blum (1983) reported that the pyrrolizidine alkaloids play a key role in host-plant selection and as a sex pheromone in certain danaid butterflies. These butterflies apply from their proboscides a fluid capable of dissolving alkaloids and then re-imbibe it. Both sexes of these butterflies store alkaloids apparently for defense (Edgar et al. 1976; 1979; Rothschild et al. 1979; Conner et al. 1981). Owen (1971) reported that danaine butterflies use withered and damaged plants and floral nectar as sources of alkaloids. D. chrysippus uses the pyrrolizidine alkaloids to protect itself from its predators and synthesizes the courtship pheromone; maternal and parental contributions of alkaloids play an important role to protect the most vulnerable stage, the egg (Meinwald 1990). This butterfly species and also D. plexippus when equipped with these alkaloids have been experimentally proved to be unpalatable to their predators by Edgar et al. (1976). Boppre (1983) reported that Tirumala petiverana collects sap from Heliotropium pectinatum in East Africa. Mathew & Anto (2007) reported that T. limniace uses the pyrrolizidine alkaloids to deter its predators, the garden lizards. In the present study, the nymphalid butterflies, Danaus genutia, D. chrysippus, the lycaenid Euchrysops cnejus, and the hesperiid, Borbo cinnara have been found to collect sap from the leaves before flowering and dry fruiting branches of all the three Suaeda species. The presence of alkaloids, triterpenoids, sterols and various other chemicals have been reported in S. maritima, S. monoica and S. nudiflora (Al-Mohammadi et al. 2005; Suganthy et al. 2009; Gurudeeban et al. 2011; Ravikumar et al. 2011; Satyavani et al. 2012). Therefore, Suaeda species studied now appear to be an important source of alkaloids for all the recorded butterfly species and the latter use them to deter their predators.
The genus Suaeda has both C3 and C4 photosynthetic pathways with both the categories of species commonly growing side by side; C4 species are mostly annuals in central Asia (Glagoleva et al. 1990). C4 pathway is an adaptive mechanism to grow in stressful environments; these species grow abundantly in drier and more saline sites and persist throughout the dry season due to their succulence (Fisher et al. 1997). S. maritima is a C3 species with austrobassioid leaf anatomy and colonizes all areas where perennial species are absent due to sensitivity to competitive interactions (Yeo & Flowers 1980; Andres 1989). S. monoica and S. nudiflora are C4 species and grow abundantly in hot, dry, high-light saline environments (Shomer-Ilan et al. 1975; Ehleringer & Monson 1993; Singh et al. 2004; Patel & Pandey 2009). In the present study, S. maritima and S. monoica are annuals while S. nudiflora is a perennial; all the three grow side by side in both high and low salt marshes. S. nudiflora is dominant particularly in drier, saline areas; its successful growth in such areas could be related to the C4 photosynthetic pathway. Further, S. maritima and S. monoica have been found to grow mostly in areas where S. nudiflora does not grow. Such a growth pattern appears to be related to sensitivity of the first two species to competitive interactions arising from the perennial species, S. nudiflora which is usually available throughout the year and displays extensive mat-forming growth. Nevertheless, C4 species, S. monoica and S. nudiflora can be successfully used for eco-restoration in saline areas where other species do not grow.
Manousaki & Kalogerakis (2011) reported that halophytes are more efficient in withstanding and adapting themselves to several abiotic factors due to their several inherent basic biochemical tolerance mechanisms when compared to glycophytic plants. They are naturally better adapted to cope with environmental stresses including heavy metals compared to salt-sensitive crop plants commonly chosen for phytoremediation purposes for the removal of heavy metals from soils. They are potentially ideal plants for phyto-extraction or phyto-stabilization applications of heavy metal polluted soils and moreover of heavy metal polluted soils affected by salinity. Some salt-excreting halophytes use their excretion mechanism in order to remove the excess of toxic metal ions from their sensitive tissues and hence act as biological pumps for heavy metals. Phyto-desalination has attracted much interest for the desalination of soils with the use of salt-accumulating halophytes which receive and accumulate high concentrations of salt in their aboveground tissues and consequently the saline soils can be improved by harvesting the plants. Cherian & Reddy (2003) stated that salinity is a major problem in irrigated agriculture especially in the arid and semiarid environments. While glycophytes undergo growth inhibition in saline environments either due to a decline in water uptake caused by the increase in external osmotic pressure or due to ionic imbalance in the cytosol, halophytes evolved mechanisms for controlled influx of sodium and chloride ions to be used for their benefit in a saline environment. Reddy et al. (2010) reported that halophytes are widely used due to their high economic values like fodder, oil, fuel and so forth, and also for ecological interests like soil desalination, dune fixation, phyto-remediation, landscaping and ornamental purpose. A further domestication of halophytes as potential crop plants for biomass production is an emerging field towards rehabilitation of salinized lands in semi-arid and arid areas. Soils adjacent to the coastal areas under irrigation or otherwise get enriched with various materials including hazardous elements from the discharges of industrial effluents, which in turn pose a great problem for the reclamation of soils and for their use in cultivation. Manousaki & Kalogerakis (2011) reported that S. maritima accumulates high concentrations of salt in its aboveground tissues, and consequently, saline soils can be upgraded by harvesting the plants on a regular basis. Ravindran et al. (2007) also reported that S. maritima accumulates high concentrations of salts in its tissues and reduces salts in the saline land to a great extent. These authors called it a salt accumulating halophyte and can be used successfully to accumulate salt in highly salinized areas for crop production after a few repeated cultivations and harvests. Reddy et al. (2010) also mentioned that S. nudiflora accumulates and sustains the salinity levels to nearby double that of seawater. It could be cultivated for its economic importance even on highly polluted soils for reclamation. Further, it is also used as a source of biological salt or oil. Singh et al. (2004) reported that the seeds of S. nudiflora contain approximately 30-35% oil and hence has the potential as a future oil seed crop. It is highly suitable for producing high protein biomass in saline soils with its C4 photosynthetic pathway. Therefore, the studied Suaeda species can be used to extract salt, desalinate saline soils and use such soils for normal plantation or cultivation. Salinization is a serious problem confronting sustainable agriculture in irrigated production systems in semi-arid and arid regions where plant growth is directly affected by high levels of sodium chloride and other salts (Marschner 1986). In India, about 30 million ha of coastal land is still barren and uncultivable because of bad soil affected by salinity (Singh & Surendra 1994). In this context, it is quite appropriate to consider the Suaeda species as potential desalinating agents for highly saline soils in order to convert bad soils into fertile soils for crop production. Further, they can also be used for the clean-up of polluted soils through phyto-remediation programs.
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