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Pollination and breeding systems of woody plant species in tropical dry evergreen forests, southern India
Flora 205 (2010) 745–753
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Pollination and breeding systems of woody plant species in tropical dry evergreen forests, southern India K. Geetha Nayak ∗ , Priya Davidar Department of Ecology and Environmental Sciences, School of Life Sciences, Pondicherry University, Kalapet, Pondicherry 605014, India
a r t i c l e
i n f o
Article history: Received 12 May 2009 Accepted 18 December 2009 Keywords: Breeding system Dry forest Habitat fragments Pollination mode Sexual system Reproductive phenology
a b s t r a c t Tropical dry evergreen forests (TDEF) are a unique forest type found along the east coast of India. They mostly occur as small, isolated fragments of varying sizes (0.5 to ≈10 ha) and are considered as endangered forests types in peninsular India. Although plant diversity is well documented in these forests, there is a paucity of ecological studies vital for conservation and for planning restoration activities. We studied reproductive biology of 13 woody species: four trees, six shrubs, and three lianas in fragments of TDEF in southern India. The phenology of reproduction, floral biology, anthesis and sexual system of each species were recorded. The pollination mode was assessed through observations of the visitation frequency of pollinators and from the floral characters. The breeding system was determined by handaugmented self- and cross-pollination experiments. The plants flowered during the dry season from January to July. Plants of nine species had both flowers and fruits at the same time. Twelve species were hermaphrodites and one was polygamo-dioecious. Flowers of 11 species opened at dawn and two at dusk. Four species were self-incompatible and six were self-compatible. Natural fruit set ranged from 10% to 56%, self-incompatible species having low fruit set. Cross-pollen augmentation increased fruit set, suggesting presence of outcrossing in all species. The majority of plants species (85%) had a generalized pollination system, receiving visits from diverse insects, such as social bees, solitary bees, wasps, moths and flies. However, only few of them were functionally important for the species. Two species namely: Capparis brevispina and C. zeylanica had butterflies and birds, respectively, as their main pollinators. Our data reveal that there is a predominance of outcrossing in plant species and a generalized pollination system in these forests. We suggest that restoration of TDEFs is crucial as habitats, not only for wild plants but also for pollinating insects. © 2010 Elsevier GmbH. All rights reserved.
Introduction Community wide studies on the reproductive biology of plants can provide information that is vital for the management of biodiversity (Bawa, 1990; Kearns and Inouye, 1997). Animals, primarily insects, are known to pollinate over 90% of plants in tropical forests, and a high proportion of plant species are obligate outcrossers (Bawa, 1990; Bawa et al., 1985). This high degree of dependence on animals for reproduction brings many tropical plants at risk from anthropogenic disturbance such as loss of habitats and changes in land-use patterns (Kearns et al., 1998). Pollination ecology of plant communities can provide information on whether some plants/pollinators are ‘keystone’ species, providing disproportionately important ecosystem services (Bond, 1993; Machado and Sazima, 2008).
∗ Corresponding author. E-mail addresses: [email protected] (K.G. Nayak), [email protected] (P. Davidar). 0367-2530/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2009.12.041
Community-level pollination and breeding system studies in tropical forests were first reported from Neotropics (Bawa et al., 1985; Kress and Beach, 1994), followed by Asia (Appanah, 1993; Devy and Davidar, 2003, 2006; Momose et al., 1998). Studies in India have focused on the pollination mode of species in the wet evergreen forests of the Western Ghats (Devy and Davidar, 2003, 2006), the dry forests of the Eastern Ghats (Aluri, 1990) and of particular taxa such as the Loranthaceae (Davidar, 1985). Here, we assessed the reproductive biology of 13 species of woody plants in small fragments of the tropical dry evergreen forest (TDEF), an endangered forest type in peninsular India that occurs along the coastal regions of south eastern India (Meher-Homiji, 1974). Of 75 TDEF patches surveyed, 149 woody plant species representing 102 trees and 47 lianas along with three native herbaceous species were recorded, with each patch having 25–40 species (Parthasarathy et al., 2008). Population sizes of over 50% of the adult plants in two patches were <10 individuals (Davidar et al., 2007). Based on floral characters, Selwyn and Parthasarathy (2006) predicted that bees could be the principal pollinators of many plant species in TDEF. However, quantitative field assessment of pollina-
Diverse insects Dawn Protandrous Nectar, pollen White Open-Cup/A 60 3 7 SI H Tree Meliaceae Walsura trifolia
dorsata)
Social bees (Apis Dusk Protandrous Shrub Rubiaceae Tarenna asiatica
H
SC
14.7
1
20
Short tubular/A
Pink, purple White Open-cup/A 40 2 8.6 SC Tree Melastomataceae Memecylon umbellatum
H
Cream White Cream Open-Cup/A Closed-Tubular/A Open-Cup/Z 25–40 15 33 1 1 2 9 21 6.9 SC SI SI Shrub Shrub Tree Rutaceae Rubiaceae Sapindaceae Glycosmis pentaphylla Ixora pavetta Lepisanthes tetraphylla
H H H&D
Pollen
Social Bees, wasps Dawn Protandrous
Diverse insects Moths, bees Social bees Dawn Dusk Dawn Protandrous Protandrous Protogynous
Social bees Bees Bees Dawn Dawn Dawn Protandrous – – Cream Yellow Cream Open-extrose/A Open-cup/A Open-cup/A 8–15 36 40 1 1 1 14 5.4 7.3 SC – – Shrub Shrub Tree Myrtaceae Flacourtiaceae Clusiaceae Eugenia bracteata Flacourtia ramontchi Garcinia spicata
H H H
Papilionaceous/A ∼10
Liana Fabaceae
H
SC
18
1
Open-Cup/A Open-extrose/A Open-extrose/A H H H
– SC SI
6.2 71 67
1 3 2
∼28 ∼45 ∼50
White
Nectar, Pollen Pollen Pollen Nectar, pollen Pollen Pollen Nectar, pollen Pollen
Protandrous
Dawn
Butterflies, bees Sunbirds, Flowerpeckers, Social bees, wasps
Dawn Dawn Dawn – Homogamous Homogamous Nectar Nectar
Anther/stigma maturation Reward Flower color Flower shape Fruit set to ripening (days) Flower longevity (days) Mean flower size (mm) Breeding system
Derris ovalifolia
Floral characteristics such as shape: actinomorphic/zygomorphic, size: measured using digital vernier calipers (150 mm with minimum of 0.05 mm), color, anthesis: dawn/dusk, and rewards: pollen, nectar or both, sexuality:
Shrub Liana Liana
Floral biology
Rubiaceae Capparaceae Capparaceae
About 195 individuals were studied in the five study sites. The number of individuals observed per species ranged from 2 to 10, some tree species were very few in certain sites (e.g., there were four trees of Walsura trifolia in Puthupet in 2003, subsequently reduced to three in 2005, and only two plants of Lepisanthes tetraphylla in Pitchandikulam). Weekly observations on flowering and fruiting were recorded for each of these species. Number of days taken for fruit maturation was also noted from tagged flowers.
Canthium coromandelicum Capparis brevispina Capparis zeylanica
Reproductive phenology
Sexual system
Thirteen common species belonging to 10 families were selected. They include three liana species: Capparis brevispina DC., Capparis zeylanica L., Derris ovalifolia Benth., six shrub species: Canthium coromandelicum (Burm.f.) Alston, Eugenia bracteata Roxb., Flacourtia ramontchi L’Hér., Glycosmis pentaphylla (Retz.) DC., Ixora pavetta Andr., Tarenna asiatica (L.)., Kuntze ex K.Schum. four tree species: Garcinia spicata Kurz ex Talbot, Lepisanthes tetraphylla Radlk., Memecylon umbellatum Burm. f., Walsura trifolia (A. Juss.) Harms. A detailed study on their sexual system, breeding system and pollination ecology was conducted from 2003 to 2006 over three flowering seasons (Fig. 1 and Table 1).
Life form
Plant species
Family
Methods
Table 1 Details on life form, floral biology, plant sexual and breeding system (H, hermaphrodites; H&D, Polygamo dioecious; A, actinomorphic; Z, zygomorphic).
Tropical dry evergreen forests are distributed along the east coast of India and sometimes extend inland up to 50 km (Mani and Parthasarathy, 2006). These closed canopy forests have two distinct layers of tree species. The canopy is about 10–12 m in height, dominated by large trees such as Pterospermum canescens and Garcinia spicata, while the sub-canopy is composed of smaller trees such as Memecylon umbellatum and Canthium dicoccum (Champion and Seth, 1968). We selected five study sites in the Pondicherry region in southeastern India, at approximately 12◦ 04 N latitude and 79◦ 53 E longitude. Two of the sites were natural forests: Puthupet, about 8.8 ha in area, located 15 km north of Pondicherry town, and Oorani, about 1.5 ha, surrounded by village and agricultural land. Three of the sites were restored: Pitchandikulam and Shakti about 3–5 ha in area, located in the Auroville green belt, area surrounded by plantations and degraded areas and Lake Estate near Ousteri which is about 3 ha in area. The restored sites were originally dry arid land where almost all the vegetation and soil had been destroyed. Saplings of TDEF species were planted in the 1970s after soil conservation attempts such as contour bund constructions were undertaken. These sites were protected from the collection of minor forest products, livestock grazing and other human impact.
Flower anthesis
Study area
Cream White Red/Pink
Pollination mode
tion modes was lacking and the breeding and sexual system of these species has not yet been assessed. Davidar et al. (2007) found that many species regenerated poorly and there was a potential for the loss of rare tree species from these remnant patches. In this paper we report the sexual and breeding systems of 13 species commonly found in the TDEF.
Trigona sp.
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Fig. 1. Study sites and representation of TDEF species: (a) natural forest; (b) restored forest; (c) fly on Capparis brevispina; (d) Eristalis quinquestriatus on Ixora pavetta; (e) Lycaenidae on Lepisanthes tetraphylla; (f) Memecylon umbellatum.
hermaphroditic/dioecious/monoecious; flower longevity in days was recorded. Flowers were classified as open and closed based on the accessibility of nectar to the insect visitors.
Autogamy (isolated pollination) Flower buds were counted, tagged and covered by a mesh cloth to exclude pollinators and fruit set upon maturity recorded.
Breeding system About 2–8 plants per species were selected for breeding system experiments and assessment of natural fruit set. Inflorescences were selected randomly and the following treatments were assigned to each of the selected plants.
Hand-self-pollination Pollen collected from the anthers and transferred to stigma of the same individual.
Open/natural pollination (control) Hand-cross-pollination In order to monitor natural fruit set, flower buds were counted, tagged and left open for pollinator visits on each plant. The number of fruits upon maturity were noted.
Pollen collected from one to three plants and transferred to the stigma of a different individual.
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Fig. 2. The flowering and fruiting phenology of the study species.
Emasculation The anthers from the flowers were removed and bagged to test if flowers were apomictic. Index of self-incompatibility ISI was calculated to determine the breeding system in hermaphroditic plants. The ISI ratio was calculated between the percentage fruit set resulting from hand-self-pollination over that from hand-cross-pollination. Species with ratios <0.25 are considered self-incompatible and those with ratios >0.25 as selfcompatible (Bawa, 1974). Pollinator observation Pollinator observations were carried out over 125 h, spread across three flowering seasons (December–May) from 2003 to 2006. A branch with 3–5 inflorescences with open flowers was selected and all the insects/birds visiting the flowers were identified and recorded continuously for 5 min, with 2-min intervals between observation periods. Observations were carried out during peak flowering period of plant species in all study sites. Duration of time spent on pollinator observation per plant species is given in Table 4. Unknown pollinator species was collected and identified up to family level. The observations were mostly done during the day when pollinator activity was high. Night observations were made on plant species with white/cream-colored flowers (Ixora pavetta, Glycosmis pentaphylla, Lepisanthes tetraphylla and Walsura trifolia), in the year 2003 and 2006.
and hand-self- and cross-pollination. Data from all 3 years were used to calculate mean fruit set per treatment. Visitation rates from the 5-min observation periods were summarized for each plant species across all sites and years. An interaction matrix for plant species with all the pollinator visitation was generated (irrespective of the time spent on observation) and rarefaction simulation was performed by taking lowest number of visitors recorded for plant species in all years and sites using EcoSim software (Gotelli and Entsminger, 2009). Floral visitors which had highest visitation frequency in the matrix that resulted from rarefaction simulation were identified as the principal pollinators for each plant species. To determine the pool of frequent floral visitors, we used the species which had ≥15 visits after the rarefaction simulations. We performed linear regression to explore the relationship between ISI index and PE. Results Reproductive phenology Walsura trifolia commenced flowering in January followed by other species (Fig. 2). March–April was peak flowering with seven of the 13 species in flower. The time until fruit maturation ranged from eight to 60 days, with Eugenia bracteata and Ixora pavetta having the shortest time of 8 and 15 days, respectively. Capparis brevispina, Capparis zeylanica, Garcinia spicata and Walsura trifolia took about 45–60 days (Table 1). In nine species flowering and fruiting overlapped (Fig. 2). Floral biology and sexual system
Pollinator effectiveness index We calculated “pollinator effectiveness index” (PE) for each species of plants, which is the difference in the proportion of flower to fruit ratio from natural pollination (NP) to isolated pollination (IP). Isolated pollination data was not available for the year 2006. Hence, we used the data from 2004 and 2005 to calculate PE. PE = (NP − IP)
The flowers were mostly small (7 species with flowers <10 mm), white (10 species), open/cup shaped (10 species) with pollen and nectar easily accessible to the visitors, and hermaphroditic (12 species). Flowers of eight species lasted only for 1 day and 10 species opened flowers at dawn, two species Ixora pavetta and Tarenna asiarica at dusk. Seven species had protandrous flowers, and two were homogamous (Table 1). Breeding system
Data analyses Fruit set (percentage flowers that set fruit) was determined for each treatment: Natural pollination (control), isolated (bagged),
Of the ten species studied, six were self-compatible and four were self-incompatible. Hand-pollination experiments were not performed on three species namely Canthium coromandalicum, Fla-
Mean pollinator effectiveness index
– – 0.71 0.54 – – – 0.52 0.95 0.82 0.45 0.48 0.94
Mean ISI ratio
– 0.50 0.05 0.58 0.56 – – 0.56 0.06 0.08 0.59 0.52 0.07
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courtia ramontchii, Garcinia spicata, as the flower size was too small. Natural fruit set did not exceed 56% in all plant species (Table 2). Walsura trifolia and Lepisanthes tetraphylla had the lowest fruit set while Memecylon umbellatum and Tarenna asiatica had higher proportion of fruits (Table 2). Bagged flowers set fruits in all plant species, indicating that they could self-fertilize naturally. The mean fruit set from bagged pollination was lowest in self-incompatible species (Table 2). Emasculated flowers did not set fruit indicating that the flowers were not apomictic.
– 79.3 ± 19.5 70.7 ± 21.9 62.9 ± 17.1 67.8 ± 14 – – 66.3 ± 17 64.9 ± 23.7 67.6 ± 19.7 69.6 ± 21.1 84.8 ± 10.4 51.9 ± 20.9
Mean ± SD Mean ± SD
– 39.2 ± 29.5 4.6 ± 7.7 38.3 ± 17.2 36.3 ± 14.1 – – 37.4 ± 15.8 3.9 ± 4.6 6.2 ± 6.9 43.4 ± 21.8 44.2 ± 13.9 4.1 ± 5 13 46.7 ± 12.8 43.4 ± 16.4 38.8 ± 15.8 47.7 ± 15.4 18 10 ± 4 40.6 ± 14.8 38.1 ± 18.6 31.7 ± 14.5 47.7 ± 14.9 56.4 ± 8.6 13 ± 8.4
Mean ± SD
5.3 19.2 ± 12.1 4±6 23.8 ± 9.9 12.8 ± 10.9 6 1.5 28.7 ± 15.6 3.4 ± 10.2 10.8 ± 6.4 53.4 ± 18.4 32.7 ± 10.3 0.74
Mean ± SD
3 10 15 10 11 2 9 23 32 18 30 6 26 Canthium coromandelicum (Burm.f.) Alston Capparis brevispina DC. Capparis zeylanica L. Derris ovalifolia (Wight & Arn.) Benth. Eugenia bracteata (Willd.) Roxb.ex. DC. Flacourtia ramontchi Garcinia spicata Kurz ex Talbot Glycosmis pentaphylla (Retz.) DC. Ixora pavetta Andr. Lepisanthes tetraphylla (Vahl) Radlk. Memecylon umbellatum Burm. f. Tarenna asiatica (L.) Walsura trifolia (A. Juss.)
Natural fruit set (%) Bagged/isolated pollination (%) No. of plants (N) Plant species
Table 2 Results of pollination experiments and breeding systems.
Hand-self-pollination (%)
Hand-cross-pollination (%)
Insect visitors and pollinators We recorded 6070 individuals of 83 floral visitor species during 1494 5-min observations. About 39 floral visitor species from five orders had more than 15 visits during the observation period. Hymenoptera, the social and solitary bees, were the commonest floral visitors, followed by Lepidoptera (butterflies and moths), and Diptera (Table 3). Social bees such as Apis cerana, Apis dorsata, Trigona iridipennis and Braunsapis picitarius visited about eight to ten species of plants studied and had higher proportion of visits. Among the Lepidoptera Euploea core (Indian common crow) were found abundantly in sites and made frequent visits to the plants. A syrphid fly, Eristalis quinquestriatus, had the highest visitation frequency among the Dipterans and visited nine species of plants. Ixora pavetta flowers opened at dusk and were visited by moths such as Syntomis sp., Maraca testularis, and some other species of the family Pyralidae, in addition to Eristalis quinquestriatus and social bees during the day. Capparis zeylanica attracted bird species such as Nectarinia asiatica (Purple sunbird), Nectarinia zeylanica (Purple-rumped sunbird) and Dicaeum erythrorhynchos (Tickell’s flowerpecker) (Table 3). The plants were visited by insects belonging to three orders: Hymenoptera (both bees and wasps), Diptera, Lepidoptera, and only flowers of one species (Capparis zeylanica) were birdpollinated. Five principal pollinators arranged according to descending order of their visitation rates for all plant species are given in Table 4. No species was exclusively visited by only one group of pollinators. However, bees were the dominant pollinators both in visitation frequency and abundance. Flowers with dawn anthesis were mainly visited by social bees, wasps and butterflies (Tables 1 and 3). Most of the diurnal visitations were by Apis cerana, Apis dorsata, Braunsapis picitarius, Trigona sp. (Table 3). Apis cerana visited all the 13 plant species, Trigona iridipennis, a stingless bee, visited eight species. Xylocopa sp. erratically visited many plants. However, their visitation rates to the plants were very low, except for Capparis brevispina where it incessantly hovered on the flowers and had copious pollen on the abdomen after several visits. Even species such as Ixora pavetta that opened at dusk were visited during the day by bees and flies. Species richness of floral visitor for plant species varied, Ixora pavetta, Memecylon umbellatum, Walsura trifolia, had >20 species of insect visitors and similar visitation diversity (Table 4). Relationship between ISI and PE All the plant species studied display some degree of pollinator dependence for the fruit set. However, SC species relied less on the pollinators (Fig. 3). ISI was negatively related to pollination effectiveness index (PE) (y = −1.093x + 1.277, df = 24, R2 = 0.706, p < 0.0001). This indicates that a significant proportion of fruit set in self-incompatible species is achieved by pollinator visitation. Discussion Our study shows that the reproductive activity in the tropical dry evergreen forests is concentrated in the dry season from Jan-
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Table 3 The percentage of visits by frequent visitor species and the number of plant species visited. Order
Species
Birds
Nectarinia asiatica Dicaeum erythrorhynchos Nectarinia zeylanica
0.3 0.4 1.0
2 5 3
Diptera
Bombylidae Platypezidae Unidentified fly Eristalis quinquestriatus
0.3 0.4 1.1 5.3
5 4 8 9
Hymenoptera-bees
Amegilla sp. Megachile hera Coelioxys confusus Megachile disjuncta Ceratina hieroglyphica Megachile sp. Amegilla zonata Nomia sp. Megachile lanata Xylocopa sp. Ceratina (Pithitis) bigahmi Apis florea Apis dorsata Braunsapis picitarius Apis cerana Trigona iridipennis
0.3 0.3 0.6 0.9 0.9 1.1 1.7 1.8 1.9 2.6 3.4 7.2 7.9 12.5 12.8 21.9
3 3 6 6 4 8 7 9 6 8 6 8 8 8 10 8
Hymenoptera-wasp
Scoliidae-3 Vespidae Sphecidae Scoliidae-2 Scoliidae
0.3 0.3 0.5 0.8 2.3
1 5 4 1 7
Lepidoptera
Hesperidae Pyralidae Delias eucharis Acraea violae Neptis hylas Tirumala limniace Jamides celeno Catopsilia pomona Pachliopta hector Lycaenidae Euploea core
0.3 0.3 0.4 0.4 0.4 0.5 0.7 0.8 1.0 1.9 2.5
4 1 6 6 5 7 8 4 7 6 8
uary to May. Flowering progressed sequentially with one species flowering after another, the peak being observed in the dry period (March) (Selwyn and Parthasarathy, 2006). This sequential flowering probably prevents clogging of stigma with heterospecific pollen. Fruiting followed flowering very quickly in many species and fruits and flowers were available on the plant at the same time. Social bees such as Apis cerana and Trigona iridepennis had the highest visitation rates and were found abundantly in all the sites. They were the most common visitors to flowering plants. Selwyn and Parthasarathy (2006) assessed the reproductive traits of 84 species in TDEF based on floral morphology, descriptions in
Fig. 3. Relationship between index of self-incompatibility and pollinator effectiveness index (PE) (y = −1.093x + 1.277, df = 24, R2 = 0.706, p < 0.0001).
% Visits
Number of plants species visited
literature and casual observations, reported four categories of pollination. However they did not note that many of the species were generalists in terms of pollinators. Vertebrate pollination was uncommon compared to other South Indian forests (Nayak and Davidar, 2006), and only Capparis zeylanica was visited by sunbirds and flowerpeckers. Ixora pavetta and Tarenna asiatica displayed a moth-pollinator syndrome, having dusk anthesis but were visited during the day by honeybees and syrphid fly. The diversity of pollination modes was low compared with undisturbed tropical wet forests. Twelve pollination modes were recorded in the lowland rainforests of Malaysia (Momose et al., 1998), 11 in Costa Rica (Kress and Beach, 1994), and 9 in Brazil (Silberbauer-Gottsberger and Gottsberger, 1988). Devy and Davidar (2006) reported seven in wet evergreen forests in India. However, we did not find any species exclusively confined to one group of pollinators (except Capparis brevispina and Capparis zeylanica, butterfly- and bird-pollinated species, respectively). The number of pollination modes present in a forest can vary with degree of disturbance in a habitat (Ramírez, 2004). TDEFs are mostly isolated and have a highly degraded vegetation. Probably there have been losses within the local pollinator pool and many species may receive pollination services from secondary and generalist pollinators such as honey bees. The number of solitary bees was much lower than that of social bees (not quantified but qualitative observations). Honeybees are known to be less efficient pollinators compared to other bee species, as they are more generalist and collect pollen from various floral resources, which may
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Table 4 Visitation diversity and frequency of all insect visitors and principal pollinators in descending order of their visitation rates. Species/site
Capparis brevispina Shannon’s diversty Index (rarefied at 38 individuals) Dominance index Mean visitation per hour (total hours observed – 3.9) Total species Capparis zeylanica Shannon’s diversty index (rarefied at 96) Dominance index Mean visitation per hou r (total hours observed – 5.25) Total species Derris ovalifolia Shannon’s diversity index Dominance index Mean visitation per hour (total hours observed – 7) Total species Eugenia bracteata Shannon’s diversity index (rarefied at 57 individuals) Dominance index Mean visitation per hour (total hours observed – 8) Total species Glycosmis pentaphylla Shannon’s diversity Iindex (rarefied at 110) Dominance index Mean visitation per hour (total hours observed – 18.4) Total species Ixora pavetta Shannon’s diversity index (rarefied at 168 individuals) Dominance index Mean visitation per hour (total hours observed – 21.25) Total species Lepisanthes tetraphylla Shannon’s diversity index (rarefied at 127 individuals) Dominance index Mean visitation per hour (total hours observed – 15.6) Total species Memecylon umbellatum Shannon’s diversity index (rarefied at 116 individuals) Dominance index Mean visitation per hour (total hours observed-21.4) Total species Tarenna asiatica Shannon’s diversity index (rarefied at 376 individuals) Dominance index Mean visitation per hour (total hours observed – 5.75) Total species Walsura trifolia Shannon’s diversity index (rarefied at 177 individuals) Dominance index Mean visitation per hour (total hours observed – 17.6) Total species
Lake observed (rarefied)
Oorani observed (rarefied)
Pitchadikulam observed (rarefied)
Puthupet observed (rarefied)
2.54 (2.54)
2.63 (2.51)
Shakti observed (rarefied)
–
–
0.15 (0.15) 0.73
0.24 (0.24) 1.07
–
–
–
16
20
–
2.07 (2.07)
2.44
–
–
0.27 (0.27) 2.08
0.18 (0.19) 1.81
–
–
–
11
22
–
2.2 0.31 2.87
–
–
–
–
22
–
–
–
–
1.62 (1.62)
2.00 (2.00)
2.14 (2.13)
–
0.52 (0.52) 1.93
0.29 (0.29) 0.93
0.25(0.25) 1.50
–
9
10
12
–
2.12 (2.12)
2.10(2.08)
2.26 (2.22)
2.22(2.18)
0.34 (0.34) 1.35
0.37 (0.37) 0.96
0.23(0.23) 1.05
0.33(0.33) 1.53
13
16
19
17
2.56 (2.52)
2.31 (2.28)
2.30 (2.28)
2.64 (2.64)
0.17 (0.18) 1.21
0.313 (0.312) 0.87
0.139 (0.319) 0.99
0.20 (0.20) 1.37
25
21
27
1.84 (1.84)
1.98 (1.94)
2.39 (2.32)
0.25 (0.25) 4.096
0.43(0.43) 1.44
0.31 (0.31) 1.702
–
28
–
16
25
–
2.69 (2.6)
2.16 (2.16)
2.17 (2.12)
2.33 (2.26)
2.06 (2.05)
0.17 (0.18) 1.31
0.23 (0.23) 1.87
0.36 (0.36) 1.61
0.20 (0.22) 1.52
0.39 (0.39) 1.60
27
14
21
22
16 1.70 (1.70) 0.48 (0.48) 3.846
–
–
Nectarinia zeylanica Catopsilia pomona Euploea core Pachliopta hector Neptis hylas
Apis florea Trigona iridipennis Apis cerana Braunsapis picitariusCeratina (Pithitis) bigahmi
Trigona iridipennis Apis cerana Braunsapis picitarius Ceratina (Pithitis) bigahmi Apis dorsata
Trigona iridipennis Apis cerana Braunsapis picitarius Apis florea Eristalis quinquestriatus
Trigona iridipennis Braunsapis picitarius Apis cerana Apis florea Apis dorsata
–
–
Xylocopa sp. Amegilla zonata Catopsilia pomona Pachliopta hector Unidentified fly-2
Apis cerana Trigona iridipennis Megachile disjuncta Braunsapis picitarius Apis florea
12
–
Principal pollinators
–
–
17
2.65 (2.60)
2.44 (2.44)
2.78 (2.68)
0.27 (0.27) 0.87
0.18 (0.18) 0.64
2.23 (2.23) 2.16
30
17
45
Trigona iridipennis Apis cerana Braunsapis picitarius Apis dorsata Eristalis quinquestriatus
Apis dorsata Apis cerana Trigona iridipennis Euploea core (Common crow) Eristalis quinquestriatus
Braunsapis picitarius Trigona iridipennis Apis cerana Lycaenidae Scoliidae
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clog the stigma with heterospecific pollen sources (Westerkamp, 1991). However, considering their abundance and visitation frequencies they contribute significantly to pollination, especially in degraded habitats such as the TDEF fragments. Trees in a tropical lowland rain forest in Costa Rica were largely outcrossing (Bawa, 1974, 1979), whereas species in the cloud forests of Venezuela (Sobervilla and Arroyo, 1982), Cerrado savannas in Brazil (Saraiva et al., 1996), understory species in tropical montane forests in Costa Rica (Wesselingh et al., 1999), tree species in Blue Mountains of Jamaica (Tanner, 1982), and understory shrubs in a medium elevation forest in the southern Western Ghats of India (Devy and Davidar, 2006) had a higher proportion of selfcompatible species. In our study, we found evidence of both SC and SI breeding systems in TDEF. Of the ten species four were found to be obligate outcrossers, having very low ISI ratio, which included Capparis zeylanica, a bird-pollinated liana, Walsura trifolia, pollinated by diverse insects and dusk blooming Ixora pavetta, pollinated by moths and bees. Some of the species had high ISI ratio and significantly higher fruit set. Those species were Tarenna asiatica, pollinated by Apis dorsata, Memecylon umbellatum, pollinated by diverse insects, and Derris ovalifolia pollinated by many social bees. Short-lived flowers were found to be characteristics of tropical forests, with an average life-span of 1-day (Primack, 1985). In TDEF we also found that the majority of species had flower lifetime of 1day and the majority of flowers with short period of anthesis were insect-pollinated. Bird and butterfly-pollinated species such as Capparis brevispina and C. zeylanica, had flowers that were viable for 3 and 2 days, respectively. The bright-red colored stamens changed to cream color in C. zeylanica, and C. brevispina had white flowers with 1–2 bright-yellow petals which changed to brown before the flowers dried up (Fig. 1c). This may signal lack of rewards and that flowers were already pollinated. The majority of plants (77%) in TDEF were dispersed by birds and mammals (Davidar et al., 2007). Some bird species such as Whitebrowed bulbul and Red-vented bulbul were frequently seen feeding on fruits of Eugenia bracteata, Memecylon umbellatum, Lepisanthes tetraphylla, etc. However, in species like Walsura trifolia, fruits fall under the parent tree and saplings emerge around the parent tree (personal observation), suggesting lack of a dispersal agent in these highly degraded fragments. Small populations such as the ones investigated face increased short-term risk of extinction due to alteration in reproductive output caused by lack of interaction between species. Moreover, they are also less capable of adapting to environmental changes (Kéry et al., 2000) and may eventually be prone to genetic drift and inbreeding depression (Knight et al., 2005). Our earlier study in TDEFs showed many self-incompatible species were highly pollinatorlimited and had very low sapling recruitment (Nayak and Davidar, 2010). TDEFs are the only natural vegetation found along the coast of Pondicherry and south of Chennai, and are known to serve as refuge for migratory birds such as the Forest wagtail (Dendronanthus indicus) and the Blue-throated flycatcher (Cyornis rubeculoides). Conservation of these small forest patches dispersed in a heterogeneous landscape matrix is vital, for they may serve as refuges also for pollinating insects, important not only for wild plants but also for agricultural crops. Extinction of species from an ecosystem is easier to recognize than the extinction of mutualisms (Kearns and Inouye, 1997). Studying the functional processes could help in understanding large-scale processes involved in species persistence and rescuing endangered species through restoration programs (Ehrenfeld, 2000). Restoration of plant-pollinator mutualisms ensures the subsequent seed production, dispersal and seedling recruitment (Kaiser et al., 2008). Since many of the TDEFs species have generalist pollination modes, restoration efforts would probably be easier than with species that are highly specialized in terms of pollinators.
Acknowledgements We thank Mr. Prakash Patel, Mr. Joss Brooks, and Mr. Walter F. Gastmann for giving us permission to work in their restored forests: Lake Estate, Pitchandikulam, and Shakti, respectively. We are grateful to Dr. Viraktmat and Miss. Suma of University of Agricultural Sciences, GKVK, Bangalore for identifying the insect specimens.
References Aluri, J.S.R., 1990. Studies on pollination ecology in India: a review. Proc. Indian Nat. Sci. Acad. 4, 375–388. Appanah, S., 1993. Mass flowering of dipterocarp forests in the aseasonal tropics. J. Biosci. 18, 457–474. Bawa, K.S., 1974. Breeding systems of tree species of a lowland tropical community. Evolution 28, 85–92. Bawa, K.S., 1979. Breeding systems of trees in a tropical wet forest. N.Z. J. Bot. 17, 521–524. Bawa, K.S., 1990. Plant-pollinator interactions in tropical rain forests. Annu. Rev. Ecol. Syst. 21, 399–422. Bawa, K.S., Bullock, S.H., Perry, D.R., Coville, R.E., Grayum, M.H., 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Am. J. Bot 72, 346–356. Bond, W.J., 1993. Keystone species. In: Schulze, E.-D., Mooney, H.A. (Eds.), Biodiversity and Ecosystem Function. Springer, Berlin, pp. 237–253. Champion, H.G., Seth, S.K., 1968. Revised Survey of the Forest Types of India. Manager of Publications, New Delhi, p. 404. Davidar, P., 1985. Ecological interactions between mistletoes and their avian pollinators in South India. J. Bombay Nat. Hist. Soc. 82, 45–60. Davidar, P., Nayak, K.G., Dharmalingam, M., 2007. Effect of adult density on regeneration success of woody plants in natural and restored tropical dry evergreen forest fragments in Puducherry region, India. Curr. Sci. 92, 805–811. Devy, S.M., Davidar, P., 2003. Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. Am. J. Bot 90, 650–657. Devy, S.M., Davidar, P., 2006. Breeding systems and pollination modes of understorey shrubs in a medium elevation wet evergreen forest, southern Western Ghats, India. Curr. Sci. 90, 838–842. Ehrenfeld, J.G., 2000. Defining the limits of restoration: the need for realistic goals. Restor. Ecol. 8, 2–9. Gotelli, N.J., Entsminger, G.L., 2009. EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. http://garyentsminger.com/ecosim.htm. Kaiser, C.N., Hansen, D.M., Müller, C.B., 2008. Habitat structure affects reproductive success of the rare endemic tree Syzygium mamillatum (Myrtaceae) in restored and unrestored sites in Mauritius. Biotropica 40, 86–94. Kearns, C.A., Inouye, D.W., 1997. Pollinators, flowering plants, and conservation biology. BioScience 47, 297–306. Kearns, C.A., Inouye, D.W., Waser, N.M., 1998. Endangered mutualisms: the conservation of plant-pollinator interactions. Annu. Rev. Ecol. Syst. 29, 83–112. Kéry, K., Matthies, D., Spillmann, H-H., 2000. Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J. Ecol. 88, 17–30. Knight, T.M., et al., 2005. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36, 467–497. Kress, W.J., Beach, J.H., 1994. Flowering plants reproductive system. In: McDade, L.A., Bawa, K.S., Hespenheide, H.A., Hartshorn, G.S. (Eds.), La Selva, Ecology and Natural History of a Neotropical Rain Forest. University of Chicago Press, Chicago, pp. 161–182. Machado, I.C., Sazima, M., 2008. Pollination and breeding system of Melochia tomentosa L. (Malvaceae), a keystone floral resource in the Brazilian Caatinga. Flora 203, 484–490. Mani, S., Parthasarathy, N., 2006. Tree diversity and stand structure in inland and coastal tropical dry evergreen forests of peninsular India. Curr. Sci. 90, 1238–1246. Meher-Homiji, V.M., 1974. On the origin of the tropical dry evergreen forest in South India. Indian J. Ecol. Environ. Sci. 44, 19–39. Momose, K., et al., 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am. J. Bot. 85, 1477–1501. Nayak, K.G., Davidar, P., 2006. Vertebrate pollination in southern Indian forests. In: Annual Meeting of the Association for Tropical Biology and Conservation, XTBG, Kunming, China, 18–21 July, p. 2006. Nayak, K.G., Davidar, P., 2010. Pollinator limitation and the effect of breeding systems on plant reproduction in forest fragments. Acta Oecologica 36, 191–196. Parthasarathy, N., Selwyn, A.M., Udayakumar, M., 2008. Tropical dry evergreen forests of peninsular India: ecology and conservation significance. Trop. Conserv. Sci. 1, 89–110. Primack, B.P., 1985. Longevity of individual flowers. Annu. Rev. Ecol. Syst. 16, 15–37. Ramírez, N., 2004. Ecology of pollination in a tropical Venezuelan savanna. Plant Ecol. 173, 171–189. Saraiva, L.C., Cesar, O., Monteiro, R., 1996. Breeding systems of shrubs and trees of a Brazilian savanna. Arq. Biol. Technol. 39, 751–763.
K.G. Nayak, P. Davidar / Flora 205 (2010) 745–753 Selwyn, M.A., Parthasarathy, N., 2006. Reproductive traits and phenology of plants in tropical dry evergreen forest on the Coromandel coast of India. Biodivers. Conserv. 15, 3207–3234. Silberbauer-Gottsberger, I., Gottsberger, G., 1988. Über sphingophile Angiospermen Brasiliens. Plant Syst. Evol. 123, 157–164. Sobervilla, C., Arroyo, M.T.K., 1982. Breeding system in a montane tropical cloud forest in Venezuela. Plant Syst. Evol. 140, 19–37.
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Tanner, E.V.J., 1982. Species diversity and reproductive mechanisms in Jamaican trees. Biol. J. Linn. Soc. 18, 263–278. Wesselingh, R.A., Witteveldt, M., Morrissette, J., den Nijs, H.C.M., 1999. Reproductive ecology of understory species in a tropical montane forest in Costa Rica. Biotropica 31, 637–645. Westerkamp, C., 1991. Honeybees are poor pollinators—why? Plant Syst Evol. 177, 71–75.
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Pollination and breeding systems of woody plant species in tropical dry evergreen forests, southern India K. Geetha Nayak ∗ , Priya Davidar Department of Ecology and Environmental Sciences, School of Life Sciences, Pondicherry University, Kalapet, Pondicherry 605014, India
a r t i c l e
i n f o
Article history: Received 12 May 2009 Accepted 18 December 2009 Keywords: Breeding system Dry forest Habitat fragments Pollination mode Sexual system Reproductive phenology
a b s t r a c t Tropical dry evergreen forests (TDEF) are a unique forest type found along the east coast of India. They mostly occur as small, isolated fragments of varying sizes (0.5 to ≈10 ha) and are considered as endangered forests types in peninsular India. Although plant diversity is well documented in these forests, there is a paucity of ecological studies vital for conservation and for planning restoration activities. We studied reproductive biology of 13 woody species: four trees, six shrubs, and three lianas in fragments of TDEF in southern India. The phenology of reproduction, floral biology, anthesis and sexual system of each species were recorded. The pollination mode was assessed through observations of the visitation frequency of pollinators and from the floral characters. The breeding system was determined by handaugmented self- and cross-pollination experiments. The plants flowered during the dry season from January to July. Plants of nine species had both flowers and fruits at the same time. Twelve species were hermaphrodites and one was polygamo-dioecious. Flowers of 11 species opened at dawn and two at dusk. Four species were self-incompatible and six were self-compatible. Natural fruit set ranged from 10% to 56%, self-incompatible species having low fruit set. Cross-pollen augmentation increased fruit set, suggesting presence of outcrossing in all species. The majority of plants species (85%) had a generalized pollination system, receiving visits from diverse insects, such as social bees, solitary bees, wasps, moths and flies. However, only few of them were functionally important for the species. Two species namely: Capparis brevispina and C. zeylanica had butterflies and birds, respectively, as their main pollinators. Our data reveal that there is a predominance of outcrossing in plant species and a generalized pollination system in these forests. We suggest that restoration of TDEFs is crucial as habitats, not only for wild plants but also for pollinating insects. © 2010 Elsevier GmbH. All rights reserved.
Introduction Community wide studies on the reproductive biology of plants can provide information that is vital for the management of biodiversity (Bawa, 1990; Kearns and Inouye, 1997). Animals, primarily insects, are known to pollinate over 90% of plants in tropical forests, and a high proportion of plant species are obligate outcrossers (Bawa, 1990; Bawa et al., 1985). This high degree of dependence on animals for reproduction brings many tropical plants at risk from anthropogenic disturbance such as loss of habitats and changes in land-use patterns (Kearns et al., 1998). Pollination ecology of plant communities can provide information on whether some plants/pollinators are ‘keystone’ species, providing disproportionately important ecosystem services (Bond, 1993; Machado and Sazima, 2008).
∗ Corresponding author. E-mail addresses: [email protected] (K.G. Nayak), [email protected] (P. Davidar). 0367-2530/$ – see front matter © 2010 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2009.12.041
Community-level pollination and breeding system studies in tropical forests were first reported from Neotropics (Bawa et al., 1985; Kress and Beach, 1994), followed by Asia (Appanah, 1993; Devy and Davidar, 2003, 2006; Momose et al., 1998). Studies in India have focused on the pollination mode of species in the wet evergreen forests of the Western Ghats (Devy and Davidar, 2003, 2006), the dry forests of the Eastern Ghats (Aluri, 1990) and of particular taxa such as the Loranthaceae (Davidar, 1985). Here, we assessed the reproductive biology of 13 species of woody plants in small fragments of the tropical dry evergreen forest (TDEF), an endangered forest type in peninsular India that occurs along the coastal regions of south eastern India (Meher-Homiji, 1974). Of 75 TDEF patches surveyed, 149 woody plant species representing 102 trees and 47 lianas along with three native herbaceous species were recorded, with each patch having 25–40 species (Parthasarathy et al., 2008). Population sizes of over 50% of the adult plants in two patches were <10 individuals (Davidar et al., 2007). Based on floral characters, Selwyn and Parthasarathy (2006) predicted that bees could be the principal pollinators of many plant species in TDEF. However, quantitative field assessment of pollina-
Diverse insects Dawn Protandrous Nectar, pollen White Open-Cup/A 60 3 7 SI H Tree Meliaceae Walsura trifolia
dorsata)
Social bees (Apis Dusk Protandrous Shrub Rubiaceae Tarenna asiatica
H
SC
14.7
1
20
Short tubular/A
Pink, purple White Open-cup/A 40 2 8.6 SC Tree Melastomataceae Memecylon umbellatum
H
Cream White Cream Open-Cup/A Closed-Tubular/A Open-Cup/Z 25–40 15 33 1 1 2 9 21 6.9 SC SI SI Shrub Shrub Tree Rutaceae Rubiaceae Sapindaceae Glycosmis pentaphylla Ixora pavetta Lepisanthes tetraphylla
H H H&D
Pollen
Social Bees, wasps Dawn Protandrous
Diverse insects Moths, bees Social bees Dawn Dusk Dawn Protandrous Protandrous Protogynous
Social bees Bees Bees Dawn Dawn Dawn Protandrous – – Cream Yellow Cream Open-extrose/A Open-cup/A Open-cup/A 8–15 36 40 1 1 1 14 5.4 7.3 SC – – Shrub Shrub Tree Myrtaceae Flacourtiaceae Clusiaceae Eugenia bracteata Flacourtia ramontchi Garcinia spicata
H H H
Papilionaceous/A ∼10
Liana Fabaceae
H
SC
18
1
Open-Cup/A Open-extrose/A Open-extrose/A H H H
– SC SI
6.2 71 67
1 3 2
∼28 ∼45 ∼50
White
Nectar, Pollen Pollen Pollen Nectar, pollen Pollen Pollen Nectar, pollen Pollen
Protandrous
Dawn
Butterflies, bees Sunbirds, Flowerpeckers, Social bees, wasps
Dawn Dawn Dawn – Homogamous Homogamous Nectar Nectar
Anther/stigma maturation Reward Flower color Flower shape Fruit set to ripening (days) Flower longevity (days) Mean flower size (mm) Breeding system
Derris ovalifolia
Floral characteristics such as shape: actinomorphic/zygomorphic, size: measured using digital vernier calipers (150 mm with minimum of 0.05 mm), color, anthesis: dawn/dusk, and rewards: pollen, nectar or both, sexuality:
Shrub Liana Liana
Floral biology
Rubiaceae Capparaceae Capparaceae
About 195 individuals were studied in the five study sites. The number of individuals observed per species ranged from 2 to 10, some tree species were very few in certain sites (e.g., there were four trees of Walsura trifolia in Puthupet in 2003, subsequently reduced to three in 2005, and only two plants of Lepisanthes tetraphylla in Pitchandikulam). Weekly observations on flowering and fruiting were recorded for each of these species. Number of days taken for fruit maturation was also noted from tagged flowers.
Canthium coromandelicum Capparis brevispina Capparis zeylanica
Reproductive phenology
Sexual system
Thirteen common species belonging to 10 families were selected. They include three liana species: Capparis brevispina DC., Capparis zeylanica L., Derris ovalifolia Benth., six shrub species: Canthium coromandelicum (Burm.f.) Alston, Eugenia bracteata Roxb., Flacourtia ramontchi L’Hér., Glycosmis pentaphylla (Retz.) DC., Ixora pavetta Andr., Tarenna asiatica (L.)., Kuntze ex K.Schum. four tree species: Garcinia spicata Kurz ex Talbot, Lepisanthes tetraphylla Radlk., Memecylon umbellatum Burm. f., Walsura trifolia (A. Juss.) Harms. A detailed study on their sexual system, breeding system and pollination ecology was conducted from 2003 to 2006 over three flowering seasons (Fig. 1 and Table 1).
Life form
Plant species
Family
Methods
Table 1 Details on life form, floral biology, plant sexual and breeding system (H, hermaphrodites; H&D, Polygamo dioecious; A, actinomorphic; Z, zygomorphic).
Tropical dry evergreen forests are distributed along the east coast of India and sometimes extend inland up to 50 km (Mani and Parthasarathy, 2006). These closed canopy forests have two distinct layers of tree species. The canopy is about 10–12 m in height, dominated by large trees such as Pterospermum canescens and Garcinia spicata, while the sub-canopy is composed of smaller trees such as Memecylon umbellatum and Canthium dicoccum (Champion and Seth, 1968). We selected five study sites in the Pondicherry region in southeastern India, at approximately 12◦ 04 N latitude and 79◦ 53 E longitude. Two of the sites were natural forests: Puthupet, about 8.8 ha in area, located 15 km north of Pondicherry town, and Oorani, about 1.5 ha, surrounded by village and agricultural land. Three of the sites were restored: Pitchandikulam and Shakti about 3–5 ha in area, located in the Auroville green belt, area surrounded by plantations and degraded areas and Lake Estate near Ousteri which is about 3 ha in area. The restored sites were originally dry arid land where almost all the vegetation and soil had been destroyed. Saplings of TDEF species were planted in the 1970s after soil conservation attempts such as contour bund constructions were undertaken. These sites were protected from the collection of minor forest products, livestock grazing and other human impact.
Flower anthesis
Study area
Cream White Red/Pink
Pollination mode
tion modes was lacking and the breeding and sexual system of these species has not yet been assessed. Davidar et al. (2007) found that many species regenerated poorly and there was a potential for the loss of rare tree species from these remnant patches. In this paper we report the sexual and breeding systems of 13 species commonly found in the TDEF.
Trigona sp.
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Fig. 1. Study sites and representation of TDEF species: (a) natural forest; (b) restored forest; (c) fly on Capparis brevispina; (d) Eristalis quinquestriatus on Ixora pavetta; (e) Lycaenidae on Lepisanthes tetraphylla; (f) Memecylon umbellatum.
hermaphroditic/dioecious/monoecious; flower longevity in days was recorded. Flowers were classified as open and closed based on the accessibility of nectar to the insect visitors.
Autogamy (isolated pollination) Flower buds were counted, tagged and covered by a mesh cloth to exclude pollinators and fruit set upon maturity recorded.
Breeding system About 2–8 plants per species were selected for breeding system experiments and assessment of natural fruit set. Inflorescences were selected randomly and the following treatments were assigned to each of the selected plants.
Hand-self-pollination Pollen collected from the anthers and transferred to stigma of the same individual.
Open/natural pollination (control) Hand-cross-pollination In order to monitor natural fruit set, flower buds were counted, tagged and left open for pollinator visits on each plant. The number of fruits upon maturity were noted.
Pollen collected from one to three plants and transferred to the stigma of a different individual.
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Fig. 2. The flowering and fruiting phenology of the study species.
Emasculation The anthers from the flowers were removed and bagged to test if flowers were apomictic. Index of self-incompatibility ISI was calculated to determine the breeding system in hermaphroditic plants. The ISI ratio was calculated between the percentage fruit set resulting from hand-self-pollination over that from hand-cross-pollination. Species with ratios <0.25 are considered self-incompatible and those with ratios >0.25 as selfcompatible (Bawa, 1974). Pollinator observation Pollinator observations were carried out over 125 h, spread across three flowering seasons (December–May) from 2003 to 2006. A branch with 3–5 inflorescences with open flowers was selected and all the insects/birds visiting the flowers were identified and recorded continuously for 5 min, with 2-min intervals between observation periods. Observations were carried out during peak flowering period of plant species in all study sites. Duration of time spent on pollinator observation per plant species is given in Table 4. Unknown pollinator species was collected and identified up to family level. The observations were mostly done during the day when pollinator activity was high. Night observations were made on plant species with white/cream-colored flowers (Ixora pavetta, Glycosmis pentaphylla, Lepisanthes tetraphylla and Walsura trifolia), in the year 2003 and 2006.
and hand-self- and cross-pollination. Data from all 3 years were used to calculate mean fruit set per treatment. Visitation rates from the 5-min observation periods were summarized for each plant species across all sites and years. An interaction matrix for plant species with all the pollinator visitation was generated (irrespective of the time spent on observation) and rarefaction simulation was performed by taking lowest number of visitors recorded for plant species in all years and sites using EcoSim software (Gotelli and Entsminger, 2009). Floral visitors which had highest visitation frequency in the matrix that resulted from rarefaction simulation were identified as the principal pollinators for each plant species. To determine the pool of frequent floral visitors, we used the species which had ≥15 visits after the rarefaction simulations. We performed linear regression to explore the relationship between ISI index and PE. Results Reproductive phenology Walsura trifolia commenced flowering in January followed by other species (Fig. 2). March–April was peak flowering with seven of the 13 species in flower. The time until fruit maturation ranged from eight to 60 days, with Eugenia bracteata and Ixora pavetta having the shortest time of 8 and 15 days, respectively. Capparis brevispina, Capparis zeylanica, Garcinia spicata and Walsura trifolia took about 45–60 days (Table 1). In nine species flowering and fruiting overlapped (Fig. 2). Floral biology and sexual system
Pollinator effectiveness index We calculated “pollinator effectiveness index” (PE) for each species of plants, which is the difference in the proportion of flower to fruit ratio from natural pollination (NP) to isolated pollination (IP). Isolated pollination data was not available for the year 2006. Hence, we used the data from 2004 and 2005 to calculate PE. PE = (NP − IP)
The flowers were mostly small (7 species with flowers <10 mm), white (10 species), open/cup shaped (10 species) with pollen and nectar easily accessible to the visitors, and hermaphroditic (12 species). Flowers of eight species lasted only for 1 day and 10 species opened flowers at dawn, two species Ixora pavetta and Tarenna asiarica at dusk. Seven species had protandrous flowers, and two were homogamous (Table 1). Breeding system
Data analyses Fruit set (percentage flowers that set fruit) was determined for each treatment: Natural pollination (control), isolated (bagged),
Of the ten species studied, six were self-compatible and four were self-incompatible. Hand-pollination experiments were not performed on three species namely Canthium coromandalicum, Fla-
Mean pollinator effectiveness index
– – 0.71 0.54 – – – 0.52 0.95 0.82 0.45 0.48 0.94
Mean ISI ratio
– 0.50 0.05 0.58 0.56 – – 0.56 0.06 0.08 0.59 0.52 0.07
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courtia ramontchii, Garcinia spicata, as the flower size was too small. Natural fruit set did not exceed 56% in all plant species (Table 2). Walsura trifolia and Lepisanthes tetraphylla had the lowest fruit set while Memecylon umbellatum and Tarenna asiatica had higher proportion of fruits (Table 2). Bagged flowers set fruits in all plant species, indicating that they could self-fertilize naturally. The mean fruit set from bagged pollination was lowest in self-incompatible species (Table 2). Emasculated flowers did not set fruit indicating that the flowers were not apomictic.
– 79.3 ± 19.5 70.7 ± 21.9 62.9 ± 17.1 67.8 ± 14 – – 66.3 ± 17 64.9 ± 23.7 67.6 ± 19.7 69.6 ± 21.1 84.8 ± 10.4 51.9 ± 20.9
Mean ± SD Mean ± SD
– 39.2 ± 29.5 4.6 ± 7.7 38.3 ± 17.2 36.3 ± 14.1 – – 37.4 ± 15.8 3.9 ± 4.6 6.2 ± 6.9 43.4 ± 21.8 44.2 ± 13.9 4.1 ± 5 13 46.7 ± 12.8 43.4 ± 16.4 38.8 ± 15.8 47.7 ± 15.4 18 10 ± 4 40.6 ± 14.8 38.1 ± 18.6 31.7 ± 14.5 47.7 ± 14.9 56.4 ± 8.6 13 ± 8.4
Mean ± SD
5.3 19.2 ± 12.1 4±6 23.8 ± 9.9 12.8 ± 10.9 6 1.5 28.7 ± 15.6 3.4 ± 10.2 10.8 ± 6.4 53.4 ± 18.4 32.7 ± 10.3 0.74
Mean ± SD
3 10 15 10 11 2 9 23 32 18 30 6 26 Canthium coromandelicum (Burm.f.) Alston Capparis brevispina DC. Capparis zeylanica L. Derris ovalifolia (Wight & Arn.) Benth. Eugenia bracteata (Willd.) Roxb.ex. DC. Flacourtia ramontchi Garcinia spicata Kurz ex Talbot Glycosmis pentaphylla (Retz.) DC. Ixora pavetta Andr. Lepisanthes tetraphylla (Vahl) Radlk. Memecylon umbellatum Burm. f. Tarenna asiatica (L.) Walsura trifolia (A. Juss.)
Natural fruit set (%) Bagged/isolated pollination (%) No. of plants (N) Plant species
Table 2 Results of pollination experiments and breeding systems.
Hand-self-pollination (%)
Hand-cross-pollination (%)
Insect visitors and pollinators We recorded 6070 individuals of 83 floral visitor species during 1494 5-min observations. About 39 floral visitor species from five orders had more than 15 visits during the observation period. Hymenoptera, the social and solitary bees, were the commonest floral visitors, followed by Lepidoptera (butterflies and moths), and Diptera (Table 3). Social bees such as Apis cerana, Apis dorsata, Trigona iridipennis and Braunsapis picitarius visited about eight to ten species of plants studied and had higher proportion of visits. Among the Lepidoptera Euploea core (Indian common crow) were found abundantly in sites and made frequent visits to the plants. A syrphid fly, Eristalis quinquestriatus, had the highest visitation frequency among the Dipterans and visited nine species of plants. Ixora pavetta flowers opened at dusk and were visited by moths such as Syntomis sp., Maraca testularis, and some other species of the family Pyralidae, in addition to Eristalis quinquestriatus and social bees during the day. Capparis zeylanica attracted bird species such as Nectarinia asiatica (Purple sunbird), Nectarinia zeylanica (Purple-rumped sunbird) and Dicaeum erythrorhynchos (Tickell’s flowerpecker) (Table 3). The plants were visited by insects belonging to three orders: Hymenoptera (both bees and wasps), Diptera, Lepidoptera, and only flowers of one species (Capparis zeylanica) were birdpollinated. Five principal pollinators arranged according to descending order of their visitation rates for all plant species are given in Table 4. No species was exclusively visited by only one group of pollinators. However, bees were the dominant pollinators both in visitation frequency and abundance. Flowers with dawn anthesis were mainly visited by social bees, wasps and butterflies (Tables 1 and 3). Most of the diurnal visitations were by Apis cerana, Apis dorsata, Braunsapis picitarius, Trigona sp. (Table 3). Apis cerana visited all the 13 plant species, Trigona iridipennis, a stingless bee, visited eight species. Xylocopa sp. erratically visited many plants. However, their visitation rates to the plants were very low, except for Capparis brevispina where it incessantly hovered on the flowers and had copious pollen on the abdomen after several visits. Even species such as Ixora pavetta that opened at dusk were visited during the day by bees and flies. Species richness of floral visitor for plant species varied, Ixora pavetta, Memecylon umbellatum, Walsura trifolia, had >20 species of insect visitors and similar visitation diversity (Table 4). Relationship between ISI and PE All the plant species studied display some degree of pollinator dependence for the fruit set. However, SC species relied less on the pollinators (Fig. 3). ISI was negatively related to pollination effectiveness index (PE) (y = −1.093x + 1.277, df = 24, R2 = 0.706, p < 0.0001). This indicates that a significant proportion of fruit set in self-incompatible species is achieved by pollinator visitation. Discussion Our study shows that the reproductive activity in the tropical dry evergreen forests is concentrated in the dry season from Jan-
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Table 3 The percentage of visits by frequent visitor species and the number of plant species visited. Order
Species
Birds
Nectarinia asiatica Dicaeum erythrorhynchos Nectarinia zeylanica
0.3 0.4 1.0
2 5 3
Diptera
Bombylidae Platypezidae Unidentified fly Eristalis quinquestriatus
0.3 0.4 1.1 5.3
5 4 8 9
Hymenoptera-bees
Amegilla sp. Megachile hera Coelioxys confusus Megachile disjuncta Ceratina hieroglyphica Megachile sp. Amegilla zonata Nomia sp. Megachile lanata Xylocopa sp. Ceratina (Pithitis) bigahmi Apis florea Apis dorsata Braunsapis picitarius Apis cerana Trigona iridipennis
0.3 0.3 0.6 0.9 0.9 1.1 1.7 1.8 1.9 2.6 3.4 7.2 7.9 12.5 12.8 21.9
3 3 6 6 4 8 7 9 6 8 6 8 8 8 10 8
Hymenoptera-wasp
Scoliidae-3 Vespidae Sphecidae Scoliidae-2 Scoliidae
0.3 0.3 0.5 0.8 2.3
1 5 4 1 7
Lepidoptera
Hesperidae Pyralidae Delias eucharis Acraea violae Neptis hylas Tirumala limniace Jamides celeno Catopsilia pomona Pachliopta hector Lycaenidae Euploea core
0.3 0.3 0.4 0.4 0.4 0.5 0.7 0.8 1.0 1.9 2.5
4 1 6 6 5 7 8 4 7 6 8
uary to May. Flowering progressed sequentially with one species flowering after another, the peak being observed in the dry period (March) (Selwyn and Parthasarathy, 2006). This sequential flowering probably prevents clogging of stigma with heterospecific pollen. Fruiting followed flowering very quickly in many species and fruits and flowers were available on the plant at the same time. Social bees such as Apis cerana and Trigona iridepennis had the highest visitation rates and were found abundantly in all the sites. They were the most common visitors to flowering plants. Selwyn and Parthasarathy (2006) assessed the reproductive traits of 84 species in TDEF based on floral morphology, descriptions in
Fig. 3. Relationship between index of self-incompatibility and pollinator effectiveness index (PE) (y = −1.093x + 1.277, df = 24, R2 = 0.706, p < 0.0001).
% Visits
Number of plants species visited
literature and casual observations, reported four categories of pollination. However they did not note that many of the species were generalists in terms of pollinators. Vertebrate pollination was uncommon compared to other South Indian forests (Nayak and Davidar, 2006), and only Capparis zeylanica was visited by sunbirds and flowerpeckers. Ixora pavetta and Tarenna asiatica displayed a moth-pollinator syndrome, having dusk anthesis but were visited during the day by honeybees and syrphid fly. The diversity of pollination modes was low compared with undisturbed tropical wet forests. Twelve pollination modes were recorded in the lowland rainforests of Malaysia (Momose et al., 1998), 11 in Costa Rica (Kress and Beach, 1994), and 9 in Brazil (Silberbauer-Gottsberger and Gottsberger, 1988). Devy and Davidar (2006) reported seven in wet evergreen forests in India. However, we did not find any species exclusively confined to one group of pollinators (except Capparis brevispina and Capparis zeylanica, butterfly- and bird-pollinated species, respectively). The number of pollination modes present in a forest can vary with degree of disturbance in a habitat (Ramírez, 2004). TDEFs are mostly isolated and have a highly degraded vegetation. Probably there have been losses within the local pollinator pool and many species may receive pollination services from secondary and generalist pollinators such as honey bees. The number of solitary bees was much lower than that of social bees (not quantified but qualitative observations). Honeybees are known to be less efficient pollinators compared to other bee species, as they are more generalist and collect pollen from various floral resources, which may
K.G. Nayak, P. Davidar / Flora 205 (2010) 745–753
751
Table 4 Visitation diversity and frequency of all insect visitors and principal pollinators in descending order of their visitation rates. Species/site
Capparis brevispina Shannon’s diversty Index (rarefied at 38 individuals) Dominance index Mean visitation per hour (total hours observed – 3.9) Total species Capparis zeylanica Shannon’s diversty index (rarefied at 96) Dominance index Mean visitation per hou r (total hours observed – 5.25) Total species Derris ovalifolia Shannon’s diversity index Dominance index Mean visitation per hour (total hours observed – 7) Total species Eugenia bracteata Shannon’s diversity index (rarefied at 57 individuals) Dominance index Mean visitation per hour (total hours observed – 8) Total species Glycosmis pentaphylla Shannon’s diversity Iindex (rarefied at 110) Dominance index Mean visitation per hour (total hours observed – 18.4) Total species Ixora pavetta Shannon’s diversity index (rarefied at 168 individuals) Dominance index Mean visitation per hour (total hours observed – 21.25) Total species Lepisanthes tetraphylla Shannon’s diversity index (rarefied at 127 individuals) Dominance index Mean visitation per hour (total hours observed – 15.6) Total species Memecylon umbellatum Shannon’s diversity index (rarefied at 116 individuals) Dominance index Mean visitation per hour (total hours observed-21.4) Total species Tarenna asiatica Shannon’s diversity index (rarefied at 376 individuals) Dominance index Mean visitation per hour (total hours observed – 5.75) Total species Walsura trifolia Shannon’s diversity index (rarefied at 177 individuals) Dominance index Mean visitation per hour (total hours observed – 17.6) Total species
Lake observed (rarefied)
Oorani observed (rarefied)
Pitchadikulam observed (rarefied)
Puthupet observed (rarefied)
2.54 (2.54)
2.63 (2.51)
Shakti observed (rarefied)
–
–
0.15 (0.15) 0.73
0.24 (0.24) 1.07
–
–
–
16
20
–
2.07 (2.07)
2.44
–
–
0.27 (0.27) 2.08
0.18 (0.19) 1.81
–
–
–
11
22
–
2.2 0.31 2.87
–
–
–
–
22
–
–
–
–
1.62 (1.62)
2.00 (2.00)
2.14 (2.13)
–
0.52 (0.52) 1.93
0.29 (0.29) 0.93
0.25(0.25) 1.50
–
9
10
12
–
2.12 (2.12)
2.10(2.08)
2.26 (2.22)
2.22(2.18)
0.34 (0.34) 1.35
0.37 (0.37) 0.96
0.23(0.23) 1.05
0.33(0.33) 1.53
13
16
19
17
2.56 (2.52)
2.31 (2.28)
2.30 (2.28)
2.64 (2.64)
0.17 (0.18) 1.21
0.313 (0.312) 0.87
0.139 (0.319) 0.99
0.20 (0.20) 1.37
25
21
27
1.84 (1.84)
1.98 (1.94)
2.39 (2.32)
0.25 (0.25) 4.096
0.43(0.43) 1.44
0.31 (0.31) 1.702
–
28
–
16
25
–
2.69 (2.6)
2.16 (2.16)
2.17 (2.12)
2.33 (2.26)
2.06 (2.05)
0.17 (0.18) 1.31
0.23 (0.23) 1.87
0.36 (0.36) 1.61
0.20 (0.22) 1.52
0.39 (0.39) 1.60
27
14
21
22
16 1.70 (1.70) 0.48 (0.48) 3.846
–
–
Nectarinia zeylanica Catopsilia pomona Euploea core Pachliopta hector Neptis hylas
Apis florea Trigona iridipennis Apis cerana Braunsapis picitariusCeratina (Pithitis) bigahmi
Trigona iridipennis Apis cerana Braunsapis picitarius Ceratina (Pithitis) bigahmi Apis dorsata
Trigona iridipennis Apis cerana Braunsapis picitarius Apis florea Eristalis quinquestriatus
Trigona iridipennis Braunsapis picitarius Apis cerana Apis florea Apis dorsata
–
–
Xylocopa sp. Amegilla zonata Catopsilia pomona Pachliopta hector Unidentified fly-2
Apis cerana Trigona iridipennis Megachile disjuncta Braunsapis picitarius Apis florea
12
–
Principal pollinators
–
–
17
2.65 (2.60)
2.44 (2.44)
2.78 (2.68)
0.27 (0.27) 0.87
0.18 (0.18) 0.64
2.23 (2.23) 2.16
30
17
45
Trigona iridipennis Apis cerana Braunsapis picitarius Apis dorsata Eristalis quinquestriatus
Apis dorsata Apis cerana Trigona iridipennis Euploea core (Common crow) Eristalis quinquestriatus
Braunsapis picitarius Trigona iridipennis Apis cerana Lycaenidae Scoliidae
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K.G. Nayak, P. Davidar / Flora 205 (2010) 745–753
clog the stigma with heterospecific pollen sources (Westerkamp, 1991). However, considering their abundance and visitation frequencies they contribute significantly to pollination, especially in degraded habitats such as the TDEF fragments. Trees in a tropical lowland rain forest in Costa Rica were largely outcrossing (Bawa, 1974, 1979), whereas species in the cloud forests of Venezuela (Sobervilla and Arroyo, 1982), Cerrado savannas in Brazil (Saraiva et al., 1996), understory species in tropical montane forests in Costa Rica (Wesselingh et al., 1999), tree species in Blue Mountains of Jamaica (Tanner, 1982), and understory shrubs in a medium elevation forest in the southern Western Ghats of India (Devy and Davidar, 2006) had a higher proportion of selfcompatible species. In our study, we found evidence of both SC and SI breeding systems in TDEF. Of the ten species four were found to be obligate outcrossers, having very low ISI ratio, which included Capparis zeylanica, a bird-pollinated liana, Walsura trifolia, pollinated by diverse insects and dusk blooming Ixora pavetta, pollinated by moths and bees. Some of the species had high ISI ratio and significantly higher fruit set. Those species were Tarenna asiatica, pollinated by Apis dorsata, Memecylon umbellatum, pollinated by diverse insects, and Derris ovalifolia pollinated by many social bees. Short-lived flowers were found to be characteristics of tropical forests, with an average life-span of 1-day (Primack, 1985). In TDEF we also found that the majority of species had flower lifetime of 1day and the majority of flowers with short period of anthesis were insect-pollinated. Bird and butterfly-pollinated species such as Capparis brevispina and C. zeylanica, had flowers that were viable for 3 and 2 days, respectively. The bright-red colored stamens changed to cream color in C. zeylanica, and C. brevispina had white flowers with 1–2 bright-yellow petals which changed to brown before the flowers dried up (Fig. 1c). This may signal lack of rewards and that flowers were already pollinated. The majority of plants (77%) in TDEF were dispersed by birds and mammals (Davidar et al., 2007). Some bird species such as Whitebrowed bulbul and Red-vented bulbul were frequently seen feeding on fruits of Eugenia bracteata, Memecylon umbellatum, Lepisanthes tetraphylla, etc. However, in species like Walsura trifolia, fruits fall under the parent tree and saplings emerge around the parent tree (personal observation), suggesting lack of a dispersal agent in these highly degraded fragments. Small populations such as the ones investigated face increased short-term risk of extinction due to alteration in reproductive output caused by lack of interaction between species. Moreover, they are also less capable of adapting to environmental changes (Kéry et al., 2000) and may eventually be prone to genetic drift and inbreeding depression (Knight et al., 2005). Our earlier study in TDEFs showed many self-incompatible species were highly pollinatorlimited and had very low sapling recruitment (Nayak and Davidar, 2010). TDEFs are the only natural vegetation found along the coast of Pondicherry and south of Chennai, and are known to serve as refuge for migratory birds such as the Forest wagtail (Dendronanthus indicus) and the Blue-throated flycatcher (Cyornis rubeculoides). Conservation of these small forest patches dispersed in a heterogeneous landscape matrix is vital, for they may serve as refuges also for pollinating insects, important not only for wild plants but also for agricultural crops. Extinction of species from an ecosystem is easier to recognize than the extinction of mutualisms (Kearns and Inouye, 1997). Studying the functional processes could help in understanding large-scale processes involved in species persistence and rescuing endangered species through restoration programs (Ehrenfeld, 2000). Restoration of plant-pollinator mutualisms ensures the subsequent seed production, dispersal and seedling recruitment (Kaiser et al., 2008). Since many of the TDEFs species have generalist pollination modes, restoration efforts would probably be easier than with species that are highly specialized in terms of pollinators.
Acknowledgements We thank Mr. Prakash Patel, Mr. Joss Brooks, and Mr. Walter F. Gastmann for giving us permission to work in their restored forests: Lake Estate, Pitchandikulam, and Shakti, respectively. We are grateful to Dr. Viraktmat and Miss. Suma of University of Agricultural Sciences, GKVK, Bangalore for identifying the insect specimens.
References Aluri, J.S.R., 1990. Studies on pollination ecology in India: a review. Proc. Indian Nat. Sci. Acad. 4, 375–388. Appanah, S., 1993. Mass flowering of dipterocarp forests in the aseasonal tropics. J. Biosci. 18, 457–474. Bawa, K.S., 1974. Breeding systems of tree species of a lowland tropical community. Evolution 28, 85–92. Bawa, K.S., 1979. Breeding systems of trees in a tropical wet forest. N.Z. J. Bot. 17, 521–524. Bawa, K.S., 1990. Plant-pollinator interactions in tropical rain forests. Annu. Rev. Ecol. Syst. 21, 399–422. Bawa, K.S., Bullock, S.H., Perry, D.R., Coville, R.E., Grayum, M.H., 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Am. J. Bot 72, 346–356. Bond, W.J., 1993. Keystone species. In: Schulze, E.-D., Mooney, H.A. (Eds.), Biodiversity and Ecosystem Function. Springer, Berlin, pp. 237–253. Champion, H.G., Seth, S.K., 1968. Revised Survey of the Forest Types of India. Manager of Publications, New Delhi, p. 404. Davidar, P., 1985. Ecological interactions between mistletoes and their avian pollinators in South India. J. Bombay Nat. Hist. Soc. 82, 45–60. Davidar, P., Nayak, K.G., Dharmalingam, M., 2007. Effect of adult density on regeneration success of woody plants in natural and restored tropical dry evergreen forest fragments in Puducherry region, India. Curr. Sci. 92, 805–811. Devy, S.M., Davidar, P., 2003. Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. Am. J. Bot 90, 650–657. Devy, S.M., Davidar, P., 2006. Breeding systems and pollination modes of understorey shrubs in a medium elevation wet evergreen forest, southern Western Ghats, India. Curr. Sci. 90, 838–842. Ehrenfeld, J.G., 2000. Defining the limits of restoration: the need for realistic goals. Restor. Ecol. 8, 2–9. Gotelli, N.J., Entsminger, G.L., 2009. EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. http://garyentsminger.com/ecosim.htm. Kaiser, C.N., Hansen, D.M., Müller, C.B., 2008. Habitat structure affects reproductive success of the rare endemic tree Syzygium mamillatum (Myrtaceae) in restored and unrestored sites in Mauritius. Biotropica 40, 86–94. Kearns, C.A., Inouye, D.W., 1997. Pollinators, flowering plants, and conservation biology. BioScience 47, 297–306. Kearns, C.A., Inouye, D.W., Waser, N.M., 1998. Endangered mutualisms: the conservation of plant-pollinator interactions. Annu. Rev. Ecol. Syst. 29, 83–112. Kéry, K., Matthies, D., Spillmann, H-H., 2000. Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J. Ecol. 88, 17–30. Knight, T.M., et al., 2005. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36, 467–497. Kress, W.J., Beach, J.H., 1994. Flowering plants reproductive system. In: McDade, L.A., Bawa, K.S., Hespenheide, H.A., Hartshorn, G.S. (Eds.), La Selva, Ecology and Natural History of a Neotropical Rain Forest. University of Chicago Press, Chicago, pp. 161–182. Machado, I.C., Sazima, M., 2008. Pollination and breeding system of Melochia tomentosa L. (Malvaceae), a keystone floral resource in the Brazilian Caatinga. Flora 203, 484–490. Mani, S., Parthasarathy, N., 2006. Tree diversity and stand structure in inland and coastal tropical dry evergreen forests of peninsular India. Curr. Sci. 90, 1238–1246. Meher-Homiji, V.M., 1974. On the origin of the tropical dry evergreen forest in South India. Indian J. Ecol. Environ. Sci. 44, 19–39. Momose, K., et al., 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am. J. Bot. 85, 1477–1501. Nayak, K.G., Davidar, P., 2006. Vertebrate pollination in southern Indian forests. In: Annual Meeting of the Association for Tropical Biology and Conservation, XTBG, Kunming, China, 18–21 July, p. 2006. Nayak, K.G., Davidar, P., 2010. Pollinator limitation and the effect of breeding systems on plant reproduction in forest fragments. Acta Oecologica 36, 191–196. Parthasarathy, N., Selwyn, A.M., Udayakumar, M., 2008. Tropical dry evergreen forests of peninsular India: ecology and conservation significance. Trop. Conserv. Sci. 1, 89–110. Primack, B.P., 1985. Longevity of individual flowers. Annu. Rev. Ecol. Syst. 16, 15–37. Ramírez, N., 2004. Ecology of pollination in a tropical Venezuelan savanna. Plant Ecol. 173, 171–189. Saraiva, L.C., Cesar, O., Monteiro, R., 1996. Breeding systems of shrubs and trees of a Brazilian savanna. Arq. Biol. Technol. 39, 751–763.
K.G. Nayak, P. Davidar / Flora 205 (2010) 745–753 Selwyn, M.A., Parthasarathy, N., 2006. Reproductive traits and phenology of plants in tropical dry evergreen forest on the Coromandel coast of India. Biodivers. Conserv. 15, 3207–3234. Silberbauer-Gottsberger, I., Gottsberger, G., 1988. Über sphingophile Angiospermen Brasiliens. Plant Syst. Evol. 123, 157–164. Sobervilla, C., Arroyo, M.T.K., 1982. Breeding system in a montane tropical cloud forest in Venezuela. Plant Syst. Evol. 140, 19–37.
753
Tanner, E.V.J., 1982. Species diversity and reproductive mechanisms in Jamaican trees. Biol. J. Linn. Soc. 18, 263–278. Wesselingh, R.A., Witteveldt, M., Morrissette, J., den Nijs, H.C.M., 1999. Reproductive ecology of understory species in a tropical montane forest in Costa Rica. Biotropica 31, 637–645. Westerkamp, C., 1991. Honeybees are poor pollinators—why? Plant Syst Evol. 177, 71–75.