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Exploring the Best Native Pollinators for Pumpkin (Cucurbita pepo) Production in Punjab, Pakistan.

Byline: Mudssar Ali, Shafqat Saeed, Asif Sajjad and Muhammad Amjad Bashir

Abstract.- Pollination in pumpkin (Cucrubita pepo) largely depends on activity of native insect pollinators, especially the bees. In order to explore the pollinator diversity and the best native pollinators for pumpkin production, an experiment was performed at the research farm of the Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan. The visitation frequency of the bees across staminate and pistillate flowers, pattern of diurnal and seasonal visitation, efficiency in harvesting and depositing pollen and resultant fruit set per single visit were evaluated. The insect pollinator community was composed of 18 species in 3 orders and 6 families. Nomia sp., Apis dorsata and Halictus sp. were among the most abundant (189, 399, 117 respectively) and efficient pollinators in terms of number of pollen grains harvested (3121.50199.54, 2090.40139.03, 798.45109.39, respectively) and deposited (376.6023.01, 204.1520.63, 177.8516.31, respectively). The single visit fruit set percentage also revealed Nomia sp. (36.66) as the best pollinator followed by the A. dorsata (23.33) and Halictus sp. (20.0). Conserving and enhancing these bee species may boost pumpkin production in Pakistan.

Key words: Pumpkin, staminate and pistillate flowers, effective pollinators, single visit efficacy.

INTRODUCTION

Pollination is one of the essential ecosystem service provided by insects resulting in the sustainability of both natural and agro-ecosystems (Buchmann and Nabhan, 1996). The importance of pollinators to agro-ecosystems is high as 75% of the important crop species of the world depend on them for fruit or seed set (Klein et al., 2007). Pollinators contribute 35% to global food volume and provide essential nutrients for human subsistence (Gallai et al., 2009). Different crops vary in their pollination requirements and thus their dependence on insect pollinators (Morse and Calderone, 2000).Pumpkin (C. pepo) attracts a wide array of insect visitors due to its large, monoecious and showy flowers that open before sunrise and wilt or close by early afternoon (Hurd, 1964; McGregor,1976). The staminate flowers are more numerous than pistillate flowers, and produce both nectar and pollen, whereas pistillate flowers produce nectar only (Tepedino, 1981). The pollen grains in C. pepo are too large and sticky to be carried by the windand highly favour insect pollination (Hodges andBaxendale, 1995; Eischen, 2000).Honey bees are important pollinators of pumpkin (Nicodemo et al., 2009; Vidal et al., 2010) and their importance is more in areas where wild bees are absent or their number is unpredictable (Jaycox et al., 1975). Walters and Taylor (2006) have reported increased fruit set, size, weight and number of seeds per fruit in the presence of managed honey bee (A. mellifera) pollination. Apis dorsata and A. florea along with some solitary bees (Anthophoridae, XylCopidae, Megachilidae and Halictidae) have been dCumented visiting C. pepo flowers in India (Grewal and Sidhu, 1979; Girish,1981).However, a few studies have suggested that honeybees are less effective pollinators in pumpkin due to their inefficacy in harvesting pollen from the anthers (Linsley, 1961; Michelbacher et al., 1964) and uncertain visitation patterns in the presence of nearby competing crops (Westerkamp, 1991). The non Apis bees, particularly the squash bees, have been dCumented as more effective pollinators than the honey bees in a number of squash crops in Europe (Canto-Aguilar and ParraTabla, 2000; Sampson et al., 2007). These bees out compete honey bees in terms of visiting flowers anddepositing pollen to the conspecific stigmas (Ordway et al., 1987). Besides pollinating a number of other economically important crops in India and Pakistan (Kumar and Rao, 1991; Ali et al., 2011), bees from the family Halictidae have also been recognized as the most frequent and important pollinators of cucurbit crops (Melendez-Ramirez et al., 2002; Krug et al., 2010; Saeed et al., 2012 ).Determination of the pollination efficiency is the first step for the management and conservation of wild bee species (Primack, 1993). The efficiency of pollinators is measured in terms of different parameters such as visitation frequency, time spent per visit, pollen harvest and deposition and fruit and seed set in their single or multiple visits (NeEman et al., 2010). The computation of these diverse parameters, for instance, single-visit pollen deposition, floral preference (visits to pistillate and staminate flowers) and time spent per flower helps in measuring the overall performance of a pollinator to the reproductive success of a plant (Inouye et al.,1994; Harder and Wilson, 1998; NeEman et al.,2010).The bee fauna of cucurbit crops of Pakistan is still unexplored and consequently their role in crop pollination is poorly understood. Honey bees (A. mellifera) are considered as the important pollinators of cucurbit crops (Vidal et al., 2010; Saeed et al., 2012) and are used to provide the managed pollination services in many countries. In Pakistan, however, managed honey bees are not the successful pollinators in vegetable growing areas of Southern Punjab due to intensive use of pesticides and high temperature (Sajjad et al., 2008). Moreover, the vegetable growers lack sufficient resources to rent honey bees, therefore the services of wild pollinators may be of key importance (Kremen et al., 2007). The crop pollination efficiency of these wild native pollinators (in terms of fruit or seed set) should be evaluated (Primack,1993; Torchio, 1994) so that these may be protected and managed within the agricultural context (Kevan et al., 1990).The objectives of this study were todetermine the diversity of native floral visitors of C. pepo, their diurnal and seasonal dynamic pattern, and their single visit efficacy from the perspective of finding the best pollinators for futureconservation at Multan, Pakistan.

MATERIALS AND METHODS

Study areaThe studies were conducted between August to November, 2011 at the research farm of Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan (30.255 N and 071.513 E) Pakistan. Pumpkin (Cucurbita pepo) was grown in an area of one hectare lCated at a distance of 1 km north of a 20 ha planted forest, dominated by perennial trees i.e., Acacia nilotica, Dalbergia sissoo etc. and different flowering weed species. The forest was a source of A. dorsata since there were many hives of this species lCated in it.The area has a subTropical climate with hotlong moist summer and short warm dry winter; the mean daily maximum and minimum temperatures range from 30 to 35C and 15 to 20C, respectively (Khan et al., 2010). The average annual rainfall of the area is 26 mm (Salma et al., 2012).Floral visitor censusWe conducted 15 minutes observations each for staminate and pistillate flowers. Observations were made on the hour at 07:00, 8:00, 9:00, 10:00 and 11:00 in seven-day intervals throughout the flowering season. During each observation, pollinator abundance (total visits) and the visitation frequency (number of visits per staminate or pistillate flowers per 15 minutes) were observed. A visit was only counted if an insect made a contact with either the anther or the stigma. The syrphid fly species were identified by a taxonomist (Acknowledgements) while the bee genera were identified to the lowest taxonomic level following Michener (2000). Most of the bees were not identified to species level due to lack of lCal taxonomic literature. Therefore, we maintained morphospecies based on their strong interactive morphological features. Voucher specimens were submitted to the Agricultural Museum of the Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan.

Foraging behaviorForaging behavior of the abundant pollinators was recorded in terms of visitation rate (number of flowers visited per min), time spent on pistillate and staminate flowers and their thrust for nectar and/or pollen. Since different insects had different diurnal and seasonal dynamics, observations were made with one hour interval from 07:00-11:00h on weekly basis.

Pollen harvestPollen harvest by a particular pollinatorspecies was estimated by caging buds 24 hours before they opened and uncaging them after they had opened fully. One pollinator species was allowed to visit which was subsequently captured and identified. To avoid overestimating the pollen harvest, this prCedure was executed early in the morning, when individuals arriving at flowers were beginning foraging activity. Pollen harvested by 50 individuals per pollinator species was calculated by using the Canto-Aguilar and ParraTabla (2000) method. Thirty flowers were caged for estimating total number of pollen grains produced.

Pollen depositionFor estimating the pollen deposition on the floral stigma, floral buds were caged with muslin cloth bags 24 h before their opening. The flowers were un-caged during the peak activity period of pollinators (8:00 to 9:00) (Fig. 1) and stigmas were excised once the flowers had been visited by a particular pollinator species. The stigmas were then fixed in alcohol-acetic acid solution and stained with safranine, aniline blue and acetic acid (Dafni,1992). Pollen grains were counted by using thestereoscopic microscope at 40x magnification.

Single visit fruit setTo confirm the pollen deposition potential of different pollinators during a single visit, their effectiveness in terms of fruit set percentage was also calculated. For this purpose, we caged 30 other buds before they opened and re-caged them after a single visit was made by a particular pollinator species. Fruit set was evaluated 5-6 days after pollination when the difference in ovary swelling or abscission was obvious (Tepedino, 1981; Vidal et al., 2010). Fifty floral buds for both open-pollinated (unrestricted insect visitation) and caged (no insect visitation) were also maintained for the comparison.

Nectar production and sugar concentrationNectar produced by each flower type (staminate and pistillate) was measured at two hours interval during the anthesis period (07:00-11:00). Over two days, each of ten pistillate and staminate flowers was caged 24 hours before their opening. The nectar from these fresh flowers was extracted by using the graduated micropipette (10 l) and the volume calculated by using the Cruden and Hermann (1983) method. The sugar concentration of each flower was measured by placing a drop of five microliter of nectar in the hand held refractometer.

Data analysisThe data of time spent on staminate and pistillate flowers, visitation rate, pollen deposition and harvesting per pollinator species per visit and fruit set per single visit were analyzed by using analysis of variance (ANOVA). Means were compared by Fishers test at P= 0.05. Paired sample TTest was applied to check the differences in visitation frequencies of pollinator species, nectar volumes and sugar concentrations between the two floral types. The statistical analysis was performed on computer software XLSTAT (XLSTAT, 2012).

RESULTS

Pollinator communityThe pollinator community of C. pepo was composed of 12 bee species (Hymenoptera), 4 fly species (Diptera) and 2 butterfly species (Lepidoptera). Only 8 bee and 2 syrphid fly species were encountered during our systematic observations (Table I).Among the bees, A. dorsata, Nomia sp., Halictus sp., Lasioglossum sp.2, Lasioglossum sp.1, Ceratina sexmaculata, XylCopa sp., and Halictidae sp. came under systematic observations while Amegilla sp., Dieunomia sp., Agapostemon sp. and Megachile sp. were rarely seen. Halictidae was the dominant family with seven species followed by the Apidae with four species.Apis dorsata, Nomia sp. and Halictus sp.were the most frequent floral visitors with a total abundance of 399, 189 and 117 individuals respectively. Their average visitation frequency was also the highest among all the observed bee species, i.e. 3.33, 1.58 and 0.99 individuals per flower per minute respectively (Table I).Among the syrphid flies, Ischiodon scutellaris and Episyrphus balteatus were the Ccasional visitor and only recorded as a part ofpollinator community. The two butterfly species,Pieris brassicae (Pieridae) and Danaus chrysippus(Danadidae) were also rarely seen.

Population dynamicsThe diurnal dynamic pattern revealed that all the pollinators started their activity on or slightly before 07:00 h and the peak activity was observed between 8:00 to 09:00 h. Apis dorsata and Nomia sp. foraged throughout the observation period in both staminate and pistillate flowers while the activity of other pollinators largely ceased at 10:00 h in pistillate flowers (Fig.1A,B).The population dynamic pattern of pollinators during the full flowering season revealed A. dorsata and Nomia sp. as the most dominant and unevenly regular floral visitors of both staminate and pistillate flowers. In contrast, the abundance of syrphid flies was too low on pistillate flowers to conclude its seasonal Ccurrence (Fig. 2A,B).Visits to staminate and pistillate flowersStaminate flowers received more visits (117.7513.69) as compared to pistillate flowers (20.252.89) (F=48.52, df =1.0, p less than 0.0001). The t- test (Alpha=0.05) further confirmed that all the species were significantly higher on staminate flowers (Fig. 3).Apis dorsata visited a higher percentage of pistillate flowers (21%) compared to the other abundant bees i.e. Nomia (10%) and Halictus sp. (9%). Halictus sp. visited a higher percentage of staminate flowers (91%) followed by Nomia sp. (89%) and A. dorsata (78%).

Table I.- Insect species in Cucurbita pepo along with their abundance, visitation frequency and foraging behavior in staminate and pistillate flowers.

###Visitation###Visitation

###frequency###frequency

###Staminate###Pistillate###Foraging task

###Order###Family###Genus/Species###(Individuals/###(Individuals/

###abundance###abundance###(N/P)

###staminate###pistillate

###flower/minute)###flower/minute)

Hymenoptera###Apidae###Apis dorsata###399###3.33###107###0.89###N

###XylCopa sp.###09###0.08###0###0###N

###Ceratina sexmaculata###11###0.09###0###0###N/P

###Halictidae###Nomia sp.###189###1.58###22###0.18###N/P

###Halictidae sp.###13###0.11###3###0.03###N/P

###Lasioglossum sp.1###74###0.62###7###0.06###N/P

###Lasioglossum sp.2###97###0.81###10###0.08###N/P

###Halictus sp.###117###0.98###11###0.09###N/P

Diptera###Syrphidae###Eristalinus laetus###27###0.23###3###0.02###N/P

###Eristalinus aeneus###39###0.33###2###0.03###N/P

In C. pepo, pistillate flowers produced on an average almost twice the nectar volume (74.3519.33) than the staminate flowers (41.207.88) and also of higher sugar concentration (35.401.87: 32.102.02%). The paired sample t- test also revealed the significant differences in nectar volume (t = 2.47, p = 0.03) and sugar concentration (t = 2.54, p = 0.03) between the two flowering types.Foraging behaviorNectar and pollen were the primary foraging task of all the bee and syrphid fly species except XylCopa sp. and A. dorsata which fed on nectaralone (Table I).There was significant difference among thepollinators in terms of their stay time on both the staminate (F=51.31, df =6.0, p less than 0.0001) and pistillate (F=37.10, df =6.0, p less than 0.0001) types. Stay time was highest for Halictus on both floral types (90.876.81 for pistillate; 77.373.28 for staminate) followed by Lasioglossum sp.1 (79.844.56;63.312.84) and Lasioglossum sp.2 (71.364.64;54.292.87). It was lowest for E. aeneus(07.050.42; 17.561.30) (Table II). Pollinator species also varied significantly in terms of their visitation rate (F=147.93, df =6.0, p less than 0.0001). Nomia sp. visited the highest number offlowers (02.490.61) followed by A. dorsata(02.050.03) and Lasioglossum sp. 2 (01.560.05). Contrary to their highest stay time on both staminate and pistillate flowers, Halictus sp. (01.100.03) and visitation rate (Table II).

Pollination effectivenessPollen harvest differed statistically among the seven tested pollinator species (F=126.24, df =6.0, p less than 0.0001); Nomia sp. harvested the maximum number of pollen grains (3121.50199.54) comprising 9% of the average pollen production (336681970) followed by A. dorsata (2090.40139.03; 6%) and Halictus sp. (798.45109.39; 2%) (Table III).

Table II.- Pollination effectiveness of seven pollinators in terms of visitation rates and stay time.

Pollinator

###(n=100)###Rate

###No. of flowers

###species

###Staminate###Pistillate###visited/min

###(N=100)

Apis dorsata###30.022.39 d###67.114.67 cd###02.050.03 b

Nomia sp.###49.502.99 c###58.204.29 d###02.490.05 a

Lasioglossum###63.312.84 b###79.844.56 ab###01.310.04 d

sp.1

Lasioglossum###54.292.87 c###71.364.64 bc###01.560.05 c

sp.2

Halictus sp.###77.373.28 a###90.876.81 a###01.100.03 e

Eristalinus###23.371.51 de###10.550.60 e###01.390.05 d

laetus

Eristalinus###17.561.30 e###07.050.42 e###01.240.05 de

aeneus

Pollen deposition followed a similar pattern as pollen harvest (F=42.23, df =6.0, p less than 0.0001). Nomia sp. proved the best pollen depositor (376.60 23.01) followed by A. dorsata and Halictus sp. (204.1520.63 and 177.8516.31, respectively).

Syrphid flies did not prove to be efficient pollen harvesters and depositors (Table III).Single visit efficacy in terms of fruit setpercentage (F=47.99, df =8.0, p less than 0.0001) revealedNomia sp. as the best pollinator (36.66) followed by A. dorsata (23.33) and Halictus sp. (20.0) while the remaining pollinator species were statistically non- significant. All the flowering buds receiving unrestricted insect visitation set fruit while no fruitset at all resulted from caged buds due to flowerabortion (Table III).

DISCUSSION

The large and monoecious flowers of pumpkin (C. pepo) produce copious nectar and pollen and attract a wide array of insect visitors, particularly bees (Canto-Aguilar and ParraTabla,2000; Nicodemo et al., 2009). In this study 18 floral visitor species from 3 insect orders and 6 families were observed foraging in our single experimental plot.The diurnal dynamic pattern revealed the peak activity of pollinators between 08.00 and 09.00 h. Apis dorsata and Nomia sp. foraged throughoutthe observation period in both staminate and pistillate flowers while the activity of otherpollinators largely ceased at 10:00 h in pistillateflowers. In Indian Punjab, the foraging activity of insect visitors in C. pepo has been dCumented from07:00 to 10:30 a.m. when the flowers began to close(Atwal, 1970). Several factors have beendCumented to influence the foraging activity of thepollinators including the temperature light levels,wind speed and relative humidity (Primack andInouye, 1993) and these can alter the most abundantand effective pollinators of a crop (Kremen et al.,2002).

Table III.- Pollination effectiveness of seven pollinators in terms of pollen harvest and deposition along with fruit set per single visit.

###Number of###Single

###Pollen###pollen grains###visit

Pollinator

###harvesting###deposited/###fruit set

species

###(n=50)###stigma/visit###(%)

###(n=30)###(n=30)

Apis dorsata###2090.40139.03b###204.1520.63 b###23.33 bc

Nomia sp.###3121.50199.54a###376.6023.01 a###36.66 b

Lasioglossum###324.0533.36de###116.0014.11 d###10.0 cde

sp.1

Lasioglossum###582.8080.22cd###138.4513.05 cd###13.33cde

sp.2

Halictus sp.###798.45109.39c###177.8516.31 bc###20.0 cd

Eristalinus###153.5512.74e###99.1009.14 de###6.66 de

laetus

Eristalinus###106.6512.56e###70.9507.64 e###6.66 de

aeneus

Open###-###-###100.0 a

pollinated

Caged###-###-###0.00 e

pollinated

A. dorsata visited a significantly higher percentage of pistillate flowers among all the observed pollinators. This is because Apis bees preferentially collect nectar rather than pollen from C. pepo (Michelbacher et al., 1964) and a two fold greater nectar volume along with higher sugar concentration was available in pistillate than in staminate flowers in our studies. Similar preference of A. mellifera for pistillate flowers has also been dCumented by Artz and Nault (2011). In contrast, the lower number of visits to pistillate flowers by the other bee species in this study might be due totheir dependence on pollen required for larval development and adult maintenance (Michener,2000) which is a limiting factor in pistillate flowers.These perhaps only visit pistillate flowers when the nectar rewards in staminate flowers become limiting.The attractiveness of pollinators to the C.pepo depends upon the nectar quantity and sugar concentration in its flowers (Karp et al., 2004). The higher nectar volume prolongs the time spent by the pollinators on a flower and increases the chances of pollen deposition and successful pollination (Manetas and Petropoulou, 2000). The increased time spent by the bees on pistillate flowers in our study could be due to their two fold higher nectar volume and sugar concentration than the staminate flowers. However, Girish (1981) did not find any significant difference between the time spent by the bees on both floral types probably because the staminate flowers had slightly more nectar than the pistillate ones but of similar sugar concentration.Nomia sp. visited higher numbers of flowers than did A. dorsata. The solitary bee (Peponapis pruinosa) has been reported foraging faster than honey bees A. mellifera (Tepedino, 1981). Visitation rate is an important measure used in many pollination studies (PrCtor et al., 1996) and it is generally considered that the more visits made the more efficient is the pollinator. However, this depends upon the amount of pollen transferred by a pollinator per visit to the pistillate flowers (Herrera,1989).Pollen harvest and deposition per single visit revealed Nomia sp. as the best pollinator followed by A. dorsata and Halictus sp. The squash bee (female P. limitaris) and bumble bee (Bombus impatiens) have also been dCumented as better pollinators than the managed honey bee species (A. mellifera) in terms of harvesting and depositing pollen per single visit (Canto-Aguilar and Parra- Tabla, 2000; Artz and Nault, 2011). The high quantity of pollen harvested by the Nomia sp. in our studies could be due to its dependence on the cucurbit pollen and it could serve as a pollen source for its larval cells as has been previously reported for P. limitaris (Willis and Kevan, 1995). In general, the magnitude of pollen removal and its deposition may vary with the behaviour of the pollinator (either collecting nectar or collecting pollen) at flowers(Goodell and Thomson, 1996; Freitas and Paxton,1998; Williams and Thomson, 2003) and the degreeof grooming pollen from their bodies (Rademaker et al., 1997). The fruit and seed quality in C. pepo has been found to increase with the pollen load size (Melendez-Ramirez et al., 2000).The previous studies on pollination biology of pumpkin suggest that percent fruit set increased with the increase in number of visits (Nicodemo et al., 2009; Vidal et al., 2010). Therefore, we fCused on single visit efficacy of different pollinator species aiming to determine the best pollinator in terms of fruit set percentage. Nomia sp. proved the best pollinator with the highest fruit set (35%) followed by A. dorsata (22%) and Halictus sp (19%). However, Tepedino (1981) found 22% fruit set in either the single visit of the squash bee, P. pruinosa or the honey bee, A. mellifera. The increased fruit set by the Nomia sp. in our studies could be due to its higher pollen deposition (376) per single visit compared to the pollen deposition (200) of P. pruinosa in the Tepedino study. The high pollen depositing ability resulting in increased fruit set has also been previously reported for B. impatiens by Artz and Nault (2011).In conclusion, Nomia sp., A. dorsata andHalictus sp. proved to be the best pollinators for C. pepo production. Conserving and enhancing these native pollinators may boost C. pepo production in Pakistan. Future studies should evaluate the effectiveness of these native pollinators for other cucurbit crops together with basic studies on their biology such as nesting site lCations and alternate nectar resources.

ACKNOWLEDGEMENTS

The study was funded by Higher Education Commission of Pakistan. We are grateful to Dr. Claus Claussen (Twedter Holz 12 D-24944Flensburg, Germany) for his help in identification of syrphid fly species.

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Author:Ali, Mudssar; Saeed, Shafqat; Sajjad, Asif; Bashir, Muhammad Amjad
Publication:Pakistan Journal of Zoology
Article Type:Report
Geographic Code:9PAKI
Date:Apr 30, 2014
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