Insects Associated with Cucumbers ( Cucumis sativus L . ) at Bamunka-Ndop (North-West Region, Cameroon)

Studies on insects associated with cucumbers ( Cucumis sativus ) in Bamunka-ndop (North-West, Cameroon) under field conditions were conducted in 2017 and 2018 from April to July. The insect species diversity, the relative abundance, the frequency of visits and guilds were recorded on the plant from 7 am to 6 pm in a 2 hours time slots. Insects were found on the stem, leaves and flowers of cucumber. There were 10 insect species belonging to four Orders. Out of these, four species belonged to Hymenoptera (54.15%), whereas the Coleoptera (33.18%), the Orthoptera (7.83%) and the Diptera (4.84%) owned two species each. Formica sp. being the most represented insect (24.42%) followed by A. mellifera (21.66%). Nectarivorous, pollinivorous, stems and leaves feeders, flowers and leaves feeders were found on the crop. The peak of activities of all the insect species was situated between 10 am and 12 pm even though the temperature and the relative humidity of the study site appear not to affect their activities on the plant. These studies therefore indicated that the insects associated to cucumber should be exploited to work on their activities on cucumber and enhancing yield and quality of the fruits.


Introduction
Cucumber (Cucumis sativus L.) is a member of the Cucurbitaceae found in Asia and Africa (Renner et al., 2007). Today cucumbers are grown worldwide for salad and pickling . The fruit is commonly harvested while still green and are used as raw, cooked or pickled ( (Reshma & Hossain, 2011;Shah et al., 2015). Fresh cucumber is a good source of water, minerals, carbohydrates, protein, lipid, iron, vitamin, fibre and antioxidants (Rashid, 1999;Murad & Nyc, 2016).
Cucumber plant is usually monoecious vegetable where male and female flowers are present separately on the same plant (Tatlioglu, 1993;Shah et al., 2015). The male flowers appear first and in considerably larger number than the female flowers and those male flowers usually appear 10 days before the first female flower appears (Judson, 1929). Both flowers produce nectar that attracts pollinator insects Hossain et al., 2018). The female flowers produce higher volume of nectar as compared to male flowers, but sugar concentration is larger in male flowers of cucumber . The plant typically produces small amount of pollen which are sticky and suitable for pollination by bees (Hossain et al., 2018). The stigma is receptive during the day but much more receptive early in the morning (Collins, 2007).
One of the most important factors influencing the yield and quality of cucumber crop is insect activities (Connor, 1969). Some of the activities are destructive (Hernandez & Lemus, 1999) and others useful to the plant (McGegor, 1976). Insects like cucumber beetles feed on both the leaves and flowers (McGregor, 1976). They start to colonize cucumber plant after the species starts to form leaves and this persists till harvesting if not controlled (Connor & Martin, 1969;McGregor, 1976). Cucumbers is highly attacked by insect pests if pumpkins in the neighborhood (Kato & Nogueira-Couto, 2002). Insect pests on cucumber belong largely to the order Coleoptera (Pinero, 2018). Insects are also very important to cucumber plant mainly for pollination (Alderz, 1960). The flowers are not wind or self-pollinated and mainly insects are the major pollinators of cucumber flowers especially honey bees that visit a maximum number of flowers for nectar (Delaplane & Mayer, 2000;Nicodemo et al., 2009;Taha & Bayoumi, 2009). The dusted pollinators with pollen grains drop on the stigma causing gynoecious fertilization (McGregor, 1976). Pollinators are needed for efficient pollen transfer from one flower to other to have good fruit set . The major pollinators of cucumber belong mainly to the order Hymenoptera (Dorjav et al., 2017).When incomplete pollination occurs; fruits do not develop properly (Hodges & Baxendale, 1991). Therefore, inadequate pollination results in small or misshapen fruit and low yield of marketable fruits (Hossain et al., 2018).
Cucumber has tremendous economic and dietetic importance (Hossain et al., 2018). According to FAO (2018), Cameroon rank 17 th with a total production of 319.616 tons. The production is still low in Cameroon compared to that of other developing countries. In order to contribute to the improvement of the yields of this cucurbit, the present investigations were designed with a view to identify various types of insect associated with cucumber plant and their activities in Bamunka-Ndop. The information gained will help farmers to develop management plans that could increase the overall quality and quantity of cucumber yields.

Study site, experimental plot and biological material
The experiment was carried out twice, April to July 2017 and 2018 in Bamunka-Ndop, North-West Region of Cameroon. Ndop Plain is a highland intermountain plain within the Bamenda High Lava Plateau; it opens out to the South-East through which the river Noun flows; it is located between Latitude 5°40' and 6°10' North of the Equator and between Longitude 10°15' and 10°50' East; the relief of this plain varies and, consequently, the orographic conditions have an effect on precipitation. The average altitude is 1200 m above sea level and it has a humid tropical climate with the annual rainfall ranging from 1500 to 2000 mm, the wet season lasts from mid-March to mid-November; the rest of the months are dry. The annual average temperature is 21.3°C; large water deficits are experienced from the months of December to February (Babungo Agriculture Post, 2015). The experimental plot was 10 m long and 5 m wide (50 m²) and was bounded by various spontaneous and cultivated plants. The biological material was represented by insects naturally present in the environment. Seeds of cucumber were purchased from an agrishop in Ndop market.

Sowing and weeding
The experimental plot was divided into four beds (10 m long x 1 m wide each). The sowing was done the 10 th April, 2017 and 18 th April, 2018, on one line per bed, the line has nine holes and in each hole, two seeds were placed. The space was 1 m between holes. Weeding was performed manually as necessary to maintain ridge weeds-free. Sowing was done using fowls manures and fertilizers NPK (20:10:10) first after two weeks of germination and secondly at four weeks of growth.

Study of the of insects behavior on cucumber plant
The frequency of insects in the cucumber was determined based on observations on the stem, leaves and open flowers every day, during each of the following daily time frame, from 17 th May to 30 th June 2017 and from 25 th May to30 th June 2018: 7-9 am, 10 am-12 pm, 1-3 pm and 4-6 pm. In a slow walk along all plants, the identity of all insects that visited C. sativus was recorded. Specimens of all insect taxa were caught with an insect net. For each species, two to five insect specimens were captured. These insects were conserved in 70% ethanol for subsequent taxonomy determination except for Lepidoptera which were conserved in wrapper following Borror & White (1991) recommendations. All insects encountered on stem, leaves and flowers were registered and the cumulated results expressed in number of visits to determine their relative frequency in the entomofauna of cucumber plant.
In addition to the determination of insect's frequency, direct observations of the feeding behavior on cucumber plant were made on insect fauna in the experimental field. The plant products harvested by insects during each visit were registered based on the foraging behavior. On a flower, nectar foragers were seen extending their proboscis to the base of the corolla while pollen gatherers scratched anthers with the mandibles or the legs; on the stem and the leaves, stem feeders and leave feeders were seen eating those parts of the plant.
During each daily period of observations, the temperature and the relative humidity of the station were registered using a mobile thermo-hygrometer, every one hour.

Data analysis
Data were analyzed using descriptive statistics, correlation coefficient (r) for the study of the association between two variables, chi-square (χ 2 ) test for the comparison of two percentages using SPSS statistical software (version 19.0; SPSS, Inc., Chicago, Illinois, USA) and Microsoft Excel 2010.

Insects found on the cucumber plant
Many insect species visited cucumber plant in different way. The percentage of insects visitors was higher on the flowers (64%), followed by the leaves (32%) and finally on the stem (4%) (Fig. 1).

Figure 1: Distribution of insect visitors on the different parts of cucumber plant at Bamunka-Ndop in 2017 and 2018
In total, 10 insect's species belonging to six Families under four Orders visiting the cucumber plant were recorded during the two studied period (table 1). Out of these, four species belonged to Hymenoptera (54.15%), two to Coleoptera (33.18%), Orthoptera (7.83%) and Diptera (4.84%) respectively. The Hymenopterans were mostly found on the flowers (table 1). This result is similar of that of Sajjanar et al. (2004) in India. Among the hymenopteran species, Formica sp. was the most frequent (24.42%) insect visitor followed by Apis mellifera (21.66%). Acalymma vittatum and Galerucina sp. (Coleoptera) were found feeding actively on both leaves and flowers (table 1) of cucumber plant. Order Orthoptera represented by Zonocerus variegatus and Acanthacris ruficornis were found only when the plant germinated till when the plant produced strong stem and broad leaves. They actively cut the stem and leaves of cucumber plant up to about three weeks of germination where the stem became stronger to be cut and leaves strong and broad. The Dipterans represented by Episyrphus balteatus and Musca domestica species were found only on the cucumber flowers (table 1).

Apis mellifera
Nectar gathering on flowers Ceratina sp.

Acalymma vittatum
Consumption of leaves and floral pieces Galerucina sp.

Relative abundance of insect visitors in the entomofauna of cucumber
The relative abundance of insects (table 3) revealed that 241 and 193 visits of 10 and 8 insect species were found on the different part of the plant respectively. Formica sp. was the most represented insect with 106 visits (24.42%) followed by A. mellifera with 94 visits (21.66%); A. vittatum with 79 visits (18.20%) and Galerucina sp. with 65 visits (14.98%). The other insect species have a percentage less than 6%.

Frequency of insect visits
The frequency of insect visiting the cucumber depends on the part of the plant visited and the time slots for observation. On the leaves (table 4), all the insects have their peak of activity between 10 am and 12 pm with a frequency of visits of 34.75%. Formica sp. was constant along the day till 2 pm when their number started decreasing.  (table 5), all the insects have their peak of activity between 10 am and 12 pm with a frequency of visits of 41.73%. n: cumulated number of visits of an insect during the two seasons on the flowers; P: percentage of visits = (n / 278) x 100; A: total number of visit Table 6 shows that A. ruficornis and Z. variegatus present on the stem have their peak of activity between 10 am and 12 pm with a frequency of visits of 40%.    For the two cumulated years, fig. 3 shows that in the morning (7-9 am), the number of visits is low. The temperature is low and the relative humidity is high; during the peak of insect activities, the relative humidity decreases and the temperature increases. In the evening (4-6 pm), the number of visits decreases, the temperature decreases and the relative humidity increases.
The beetles species found in cucumber crop during the experiment were found on both leaves and flowers of the plant. This is attributed to the fact that they are herbivores and eats away the tender tissues of the plant as reported Malerbo et al. (1999) and Brandt (2012). These authors supported that A. vittatum, Diabrotica vittata and Galerucina species always found feeding on leaves and flowers of cucumber plant from germination till fruit formation if not treated. A. vittatum is a serious insect pest of fresh market cucurbits (Ellers-Kirk & Fleischer, 2006) with those feeding modes that result in severe defoliation. A. vittatum shows a strong preference for plants in the family Cucurbitaceae. The cotyledons of seedlings and wilting plants are particularly attractive to A. vittatum since they contain a high concentration of cucurbitacins, the metabolites produced by the plants in response to herbivorous attack. This is an example of coevolution between A. vittatum and cucurbits, whereby a repellent defense evolved by the host plant has been adopted as a feeding stimulant by the herbivorous beetle (Hoffmann & Zitter, 1994). When feeding on cucurbits, adult male A. vittatum produce an aggregation pheromone, which attracts more individuals into the area (Boucher, 2003). . In Philippines, on C. sativus, it was documented that the intense morning activity of bee species is synchronized with the higher nectar secretion which occurs 2 to 3 hours after flowers opening at dawn (Cervancia & Bergonia, 1990). However, in the evening, the number of insect visitors on the flowers is low due to the reduction in volume of pollen and nectar. Similar observations were made on cucumber by Sattigi et al. (1996) who noted that in general foraging activity of honey bees was noticed throughout the day with a peak of activity between 8am and 12pm depending of the different season and the foraging activity was low during other hours of the day. In the same vein, some bee species such as A. mellifera species are primary visitors and pollinators of most members of Cucurbitaceae (Free, 1993 ., 2014). These bees get pollen and nectar as their reward (Nicodemo et al., 2009), which is similar to our findings. Bees depend on the pollen and nectar produced by Cucurbita flowers for their survival (Hurd et al., 1971) and this is important in helping to transfer pollen from the male to female flowers.
Coleoptera, Orthoptera and Diptera species of the experimental field were also found in abundance in the morning hours (10 am-12 pm) and few in the evening (4-6 pm). This is attributed to the fact that the environmental conditions in the morning (Fig. 3) allow good activity on the plant and as reported Khan et al. (2015), cucumber pests mostly beetles are very active at low temperature, high humidity and low precipitation.
The temperature and the relative humidity of the study site seem not to influence insect activities on cucumber crop. Bramel et al. (2004) and Tuell & Isaacs (2010) reported that the weather during bloom affects abundance and foraging of insect pollinators. Moreover flowering insects preferred warm or sunny days for the good floral activity (Kasper et al., 2008). Globally, Free (1993), Cervancia & Bergonia (1990), Chen (1996) and Sajjanar et al. (2004) reported that ants, beetles, flies and bees are insects visiting mostly cucurbits in the morning hours which correspond to the flower opening and stigma receptivity.

Conclusion
In Bamunka-Ndop, cucumber is a plant species that attracted a wide range of insect species found on the stem, leaves and flowers of the plant. They belong to orders Hymenoptera, Coleoptera, Orthoptera and Diptera with the hymenopterans predominant. Among the hymenopterans, ants and honeybees were the major visitor insects found. Based on their feeding strategies, four guilds associated with cucumber plant were noted: The guild of pollinivorous, the guild of nectarivorous, the guild of stem and leaves feeders and the guild of flowers and leaves feeders. During the experiment, the insect species recorded were present on the plant from7 am to 6 pm, with a peak of visits between 10 am and 12 pm. Moreover, the temperature and the relative humidity of the study site seem not to influence their activities on cucumber crop. These studies therefore indicated that the insects associated to cucumber should be exploited to work on their activities on the plant and enhancing yield and quality of the fruits as the crop is an important fruit vegetable since its cultivation and consumption have recently increased.