Land Use	Classification	Area (0-3 km radius)	%	F	N
Built-up	Residential Area, Industrial Area, mixed pixels with built-up area	23.7	0.8
Open Area	Open lands, Quarries	212.1	7.5
Open Wetland	Aquaculture and wetlands	96.4	3.4
Water	River, Drainages	308.8	10.9
Agriculture	Agriculture Fields Current Fallow and Sown (Paddy)	709.3	25.1
Cashew	Cashew Plantations in scrub jungle	269.6	9.5	+	+
Forest	Evergreen forests, Deciduous and mixed Forests	123.7	4.4	+	+
Horticulture	Areca Gardens, Coconut plantations	349.2	12.3	+
Laterite	Laterite Quarry, Laterite Open lands	318.5	11.3	+
Laterite Acacia	Acacia auriculiformis plantation in laterite plateaus	193.8	6.9
Acacia	Acacia auriculiformis plantation	210.8	7.5
Vegetable Farm	Cucurbit varieties with inter crops like ladies finger	12.8	0.5	+
Total area (ha)		2,828.7	100

Note: N = Nesting habitats; F = Foraging habitats; + = present

Table 1 Elements of agricultural landscapes with beneficiary resource for pollinators

Male flowers opened earlier than the female ones in all species. In bitter gourd, cucumber and Mangalore gourd anthesis commenced before sunrise, in ridge gourd towards sunset and in snake gourd after sunset (Table 2).

Table 2 Anthesis time observed in cucurbits studied (in the monsoon months)

A total of 24 insect species (22 genera, 14 families, 4 orders), visited cucurbit flowers (Table 3). With 8 species of butterflies and 3 species of moths from 7 families, the Lepidopterans had the highest numbers of pollinators. Hymenopterans followed with 6 species of bees and 3 species of wasps. Bees were the most frequent flower visitors. The Dipterans (flies) and Coleopterans (beetles), with 2 species each, were infrequent visitors and had no notable role in pollination as specimen examination revealed general absence of pollen. Hymenopterans were observed as having the highest visitations on ridge gourd, followed by Mangalore gourd, cucumber and bitter gourd, respectively. Lepidopterans were dominant on snake gourd and frequent on bitter gourd. Bitter gourd was also visited by bees. Coleopterans and dipterans were infrequent on all cucurbits, except snake gourd.

Note: + = presence

Table 3 Insect species found on cucurbit flowers during the monsoon period

Crop-wise abundance of insect visitors is summarized in Figure 4. A. dorsata had the highest abundance of visits on ridge gourd (70.1%) followed by cucumber (66%), Mangalore gourd (56%) and bitter gourd (38%). A. dorsata was negligible on snake gourd. A. cerana was most abundant on Mangalore gourd (39.6%) and cucumber (31.6%). Ridge gourd and bitter gourd also had good dependence on A. cerana. Trigona sp. more frequently visited bitter gourd than others. Butterflies and moths were predominant on snake gourd. Beetles and flies were the least important pollinators on all crops and did not visit snake gourd.

Figure 4: Bar diagram of insect abundance on different cucurbit plants

In regards of pollinators visitation on Cucumis spp., 11 insect species visited C. pubescens and 10 species visited C. sativus (Table 3). A. dorsata was dominant visitor on Cucumis spp., 66% on Mangalore gourd and 56% on cucumber. A. cerana had 39.6% visitation on Mangalore gourd and 31.6% on cucumber. In Dharwad, neighboring district of Uttara Kannada, Prakash (2002) recorded 27 species of insects pollinated cucumber during post-monsoon season, where honeybees (A. dorsata, A. cerana and A. florea) as well as Trigona iridipennis Smith were the dominating visitors, validating our findings on honeybees as prime pollinators of Cucumis spp.

Bitter gourd was visited by 13 species in which A. dorsata and Trigona sp. constituted 80.2%. Nidagundi and Sattagi (2005) recorded 10 insect visitors on bitter gourd in Dharwad i.e. 8 Hymenopterans and 2 Lepidopterans. Hymenopterans T. iridipennis, Halictus gutturosus Vachal and A. florea were important pollinators of bitter gourd (Subhakar et al. 2011). In Bangalore, 78.09% of pollinators on ridge gourd were bees, mainly A. cerana, A. florea and Tetragonula iridipennis (Kuberappa et al. 2008). In our study, the wild bee A. dorsata had the prime role as pollinator (70.1%). The rest of pollinators consisted of other bees, butterflies, flies, beetles and hawk moths.

4.2 Foraging dynamics

Insect forage is a collective process of individuals, as well as of the group (Traniello 1989). Crop-wise foraging times in our study (Trichosanthes excluded) by different insects are presented in Figures 5 to 8. A. dorsata and A. cerana, visited cucumbers from 06:30 to 16:30 hours, until the flowers wilted (Fig. 5).

Note: Straight line = Primary axis; Dot line = Secondary axis

Figure 5: Foraging pattern of diverse insect visitors on Cucumis sativus

Peak visit of A. dorsata was during 10:30 hours (18.87 visits/m2/5 minutes) and 11:30 hours (20 visits/m2/5 minutes). The visits were lesser earlier and later (0.2, 0.4 and 1.2 visits/m2/5 minutes at 07:30, 08:30 and 16:30 hours, respectively). Peak foraging by A. dorsata in a Dharwad study was between 11:00 to 12:00 hours (Pateel & Sattagi 2007). Conner-Michigan (1969) reported that 10:00 to 15:00 hours as the most effective for cucumber pollination in Ohio, in which a flower required at least 8 to 10 visits by bees for satisfactory fruit set. The maximum foraging activity of A. cerana in our study nearly overlapped with that of A. dorsata. Although the flowers bloomed at sunrise, the highest visitation frequency of A. cerana was at 9:30 hours (8.8 visits/m2/5 minuntes) and 10:30 hours (9.73 visits/m2/5 minutes). Visitations declined from 11:30 hours (7.71 visits/m2/5 minutes), reached minimum at 15:30 hours (0.13 visit/m2/5 minutes). Trigona sp. was only a minor forager of cucumber. Other infrequent visitors like butterflies, moths and beetles foraged mainly between 07:30 to 10:30 hours. Insect foragers on Mangalore gourd were observed from 06:30 to 17:30 hours (Fig. 6). The highest foraging frequency of 13.6 visits/m2/5 minutes was observed at 12:30 hours by Apis dorsata and the least was observed at 07:30 hours. Apis cerana had peak visitations at 13:30 hours (11.2 visits/m2/5 minutes), the lowest was at 08:30 and 17:30 hours (0.21visits/m2/5 minutes). Trigona sp. foraged maximum at 11:30 hours with 2.1 visits/m2/5 minutes and was not to be found from 15:30 hours.

Note: Straight line = Primary axis; Dot line = Secondary axis

Figure 6: Foraging patterns of diverse insect visitors on Cucumis pubescens

Insects foraged on bitter gourd (Momordica charantia) from 06:30 to 14:30 hours (Fig. 7). The stingless bee Trigona sp. as the major pollinator had peak visitations at 09:30 hours (6.88 visits/m2/5 minutes); lesser at 07:30 hours (6.75 visits/m2/5 minutes). By midday, Trigona sp. shifted to other cucurbits, mainly to Cucumis spp. Visitations of A. dorsata nearly overlapped with that of Trigona sp. in the morning, peaking at 07:30 hours (7 visits/m2/5 minutes) and 08:30 hours (6.88 visits/m2/5 minutes). A. cerana succeeded reaching maximum at 08:30 hours (3.14 visits/m2/5 minutes). The butterflies were infrequent on bitter gourd, the highest at 09:30 hours (1.75 visits/m2/5 minutes). As bitter gourd flowers bloomed very early in the morning, few moths could be found at 07:30 hours. Study of Subhakar et al. (2011) in Tirupati also showed that Trigona (iridipennis) was the most abundant and frequent visitor on bitter gourd (10.83 visits/m2/5 minutes).

Note: Straight line = Primary axis; Dot line = Secondary axis

Figure 7: Foraging patterns of diverse insect visitors on M. charantia

Ridge gourd Luffa acutangula is an important vegetable in coastal Uttara Kannada. Foraging was observed from 17:30 to 22:30 hours (Fig. 8). Honeybees were major foragers. A. dorsata made 13.67 visits/m2/5 minutes at 18:30 hours, while A. cerana had 4.67 visits/m2/5 minutes at 17:30 hours. Beetles, wasps and other bees were rare visitors. A. cerana, A. florea and Tetragonula iridipennis were reported as main pollinators of Luffa sp. in Bangalore (Kuberappa et al. 2008). Shrivastava (1991) reported sphingid moth as an important pollinator of Luffa sp., an evening bloomer. For snake gourd, a night bloomer with white flowers, moths were the main visitors during night, while butterflies frequented after daybreak. The bee-hawk moth had the highest visitations between 20:30 and 22:30 hours. The rainy nights of Southwest Monsoon hampered further observation in the midnight hours.

Note: Straight line = Primary axis; Dot line = Secondary axis

Figure 8 Foraging patterns of diverse insect visitors on Luffa acutangula

4.3 Elements of the landscape

Insect pollinators are known to rely on diverse elements of landscapes (habitats) for resources like nectar, pollen, nesting materials and species-specific nesting sites. Landscape element analysis of the study area (with 3 km buffer) was done using remote-sensing data and field data (Fig. 9).

Figure 9 Land use elements in the landscape (with 3 km radius surrounding)

Forests provide nesting and foraging sites for insect pollinators, ensuring their permanence in the landscape. High proportions of natural or semi-natural habitats close to agricultural area are known to benefit bee diversity, mutualistic interactions and insect foraging movements (Hagen & Kraemer 2010). In the 3 km radius around the vegetable growing area, there were forest, cashew trees (in scrub jungle), horticulture, laterite plateaus and vegetable farm, which provided food for the insects. Only forest and cashew trees in scrub jungle were the main nesting areas for the insects. The presence of almost 100 ha forest patch, within the 3 km radius from the Halkar Village, was of high significance, especially in the vicinity of Kumta, a municipal town. The forest has been under careful protection by the village community for generations and is acclaimed as one of the best examples of community managed forests in India (Chandran 2001). The low laterite plateaus characteristic of Uttara Kannada is the key role in providing foraging resources for honeybees and lepidopterans (Balachandran et al. 2014). The forests and scrub on laterite hills provided habitats for A. dorsata. Changes in landscape structure are considered to be the primary cause of limitation in pollination services in agricultural systems (Viana et al. 2012).

In retrospect, plants can escape competition by utilizing different pollinator species or guilds, due to species-specific floral morphology and blooming times, favoring resource partitioning, conferring mutual benefits to both hosts and pollinators (Pleasants 1980; Schoonhoven et al. 2005). Bees are prominent among cucurbit pollinators. The foraging schedules on any given species showed minimal overlapping between different foragers. A. dorsata, took advantage of the early morning blooming of bitter gourd, congregated on it from 06:30 to 09:30 hours, and shifted to cucumber and Mangalore gourd as the day progresses, although it continued to forage in lesser frequencies until the flowers ceased by midday. After completing their visits on Cucumis spp. during the rest of the day, A. dorsata extended their foraging activity into the night on ridge gourd, although in lesser frequencies, up to 22:30 hours. The knowledge on foraging activity and local climate is important for carrying out multi-species cropping of gourds and cucumbers to obtain maximum crop production.