Elaeidobius kamerunicus Faust (Coleoptera: Curculionidae), the pollinating weevil, is the most efficient insect pollinator of oil palm, Elaeis guineensis Jacq. (Arecales: Arecaceae). In this experiment, the pollinating activity of E. kamerunicus was observed in an oil palm field in Hainan, China, in order to further understand the dynamics of the weevil's behavior on inflorescences. Both male and female inflorescences emitted an anise-like fragrance. Female inflorescences appeared to reward the weevils with copious nectar production, whereas male inflorescences appeared to do so with both nectar and pollen. The number of weevils visiting an inflorescence was assessed by the use of a sticky trap encircling it, and by counting the weevils present on samples of spikelets of inflorescences. The weevil population peaked on the 3rd day of anthesis on male inflorescences, and on the 2nd day of anthesis on female inflorescences. Weevil activity recorded on the day of highest abundance during anthesis revealed an inactive period during 07:00–08:00, substantial activity during 11:00–12:00, and peak activity during 17:30–18:00. The number of female adult weevils was always much greater than the number of males, both on male and on female inflorescences. Separation of anthesizing male inflorescences into 7 consecutive stages each 1 d long and use of sticky traps baited with anthesizing male flowers that were placed around inflorescences on the plant were optimal techniques for obtaining reliable data on the numbers of pollinating weevils. To increase the population of E. kamerunicus in Hainan, some steps should be taken including releases of adult weevils in oil palm plantations, and control of the weevil's predators and parasites, such as rats and harmful nematodes.
Elaeidobius kamerunicus Faust (Coleoptera: Curculionoidea) is identified as the most efficient insect pollinator of oil palm (Syed 1979; Ponnamma et al. 2006a). Elaeidobius kamerunicus was introduced from Africa into the oil palm growing regions of Asia and the Pacific in the early 1980s (Caudwell 2001) and into the oil palm plantations of India during 1985 (Ponnamma et al. 2006b). Introduction of the weevil into oil palm plantations increased fruit set and dramatically raised the yield of oil palm (Ponnamma 1999; Caudwell 2001). Also, the introduction of E. kamerunicus in Malaysia has increased pollination and fruit production (Syed 1982; Basri et al. 1983; Chiu et al. 1986). In general, the impact of the introduction of E. kamerunicus in Southeast Asia has been highly favorable (Corrado 1985; Donough & Law 1987; Wahid et al. 1987). The nematode Elaeolenchus parthenonema n. g., n. sp. (Nematoda: Sphaerularioidea: Anandranematidae n. fam.) is harmful to the weevil (Poinar et al. 2002), but the Bacillus thuringiensis products Lepcon-1, Bafog-1 (S), and Ecobac-1 (EC) have been proven innocuous to the weevil (Ahmad et al. 2012). The weevils prefer the inflorescence of oil palm (Elaeis guineensis Jacq.; Arecales: Arecaceae) for oviposition (Adaigbe et al. 2011), indicating they have a close relationship to this species. Females live longer than males (Allou 2004; Tuo et al. 2011), and this is significant for the artificial production of progeny. Climatic conditions have an obvious effect on the population dynamics and activity of E. kamerunicus (Chee & Chiu 1998). Therefore, we paid attention to climate as a factor in these experiments.
In the 1960s to 1980s, oil palm seeds were introduced from Malaysia and Papua New Guinea to China and planted mainly in Hainan, Yunnan, and Guangdong Provinces (Lin 2010). Currently, the planted oil palm area is about 42,000 ha on Hainan Island. In China, the pollinating curculionid E. kamerunicus was first recorded in oil palm plantations on Hainan Island. However, to date the population dynamics of E. kamerunicus in this part of China have not been studied in detail. This information is crucial to understand pollination efficiency of the weevils in relation to oil palm production. In the present paper, we report on the pollination activity of E. kamerunicus on oil palm on Hainan Island, China.
Materials and Methods
EXPERIMENTAL SITE
The experiment was conducted in an oil palm plot, located in Baodao Xincun of Danzhou City, Hainan Province, China (19.52°N, 109.46°E) in the years of 2012 to 2013. In Oct 2013, the average temperature was 25.3 °C in Danzhou (the maximum was 27.0 °C and the minimum was 22.5 °C based on Danzhou meteorological stations on Hainan Island). This site belongs to the Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences. The oil palm plantation, located on flat ground, is mainly used for scientific research. Nine-year-old oil palms were used for the experiment. The total plantation area was 50 ha, and the palms were triangle-planted with 10 m distance. The altitude of Danzhou is about 100–200 m. The soil is latosol. Danzhou has a tropical monsoon climate with an annual average temperature of 23.1 °C, rainfall of 1,486 mm, and sunshine for 2,072 h.
QUANTIFICATION OF WEEVIL ACTIVITY ON MALE AND FEMALE INFLORESCENCES
Experiments were conducted on male and female inflorescences of E. guineensis separately. Five plots were designed, and an inflorescence from each of palm in each plot was chosen. Experiments were repeated 5 times. The distance between plots was 30 m. The inflorescences were about 2 m above the ground.
We divided the period of anthesis of male inflorescences into 7 d. On the 1st day, about 25% of male flowers were fully open and functional, and this fraction increased to about 50% on the 2nd day and to 100% on the 3rd and subsequent days. This classification was based on the method of Chiu et al. (1986). However, we divided the period of anthesis of female inflorescences into 6 d, i.e., the 1st, 2nd, 3rd, 4th, 5th, and 6th day of anthesis. Sticky traps were applied for catching E. kamerunicus. The trap was 21.7 cm in diameter and 26.3 cm in height. It was folded into a cylinder surrounding an inflorescence with the outside surface coated with a sticky gel (Fig. 1). The traps were collected in individual plastic bags and brought to the laboratory. Elaeidobius kamerunicus adults were washed from these traps with xylene on the same day, and the numbers of males and females were counted.
NUMBERS OF WEEVILS THAT EMERGED PER SPIKELET DURING THE PERIOD OF ANTHESIS
On the male inflorescences, samples were collected from the field for assessing the adult weevil numbers. Five plots were designed, and an inflorescence from each palm in each plot was chosen. Six complete spikelets were subjected to stratified sampling from 6 sections of the male inflorescence. Experiments were repeated 5 times. The number of adults per spikelet was observed at monthly intervals. The insects from the month with the highest population density were chosen for other experimental purposes.
NUMBERS OF E. KAMERUNICUS VISITING MALE INFLORESCENCES DURING THE ANTHESIS PERIOD
To determine the number of weevils that visited male inflorescences during the anthesis period, we designed 5 plots. An inflorescence from each palm in each plot was chosen. Experiments were repeated 5 times. Sticky traps were installed at 09:00, and collected and replaced with a new one every 24 h until the male inflorescences had completely wilted.
NUMBERS OF E. KAMERUNICUS PER SPIKELET DURING THE ANTHESIS PERIOD
To determine the number of weevils per spikelet on the male inflorescence during the anthesis period, samples were taken at 11:00, and 6 complete spikelets were subjected to stratified sampling each from 6 sections of the male inflorescence. The selection of 6 spikelets per inflorescence was based in some part on the method of Chiu et al. (1986). Each collected spikelet was placed in an individual plastic bag, and the numbers of male and female weevils were counted. Collection of spikelets continued until the male inflorescences were completely wilted.
NUMBER OF E. KAMERUNICUS VISITING MALE INFLORESCENCES ON THE 3RD DAY OF ANTHESIS
To determine the number of E. kamerunicus visiting male inflorescences on the 3rd day of anthesis, sticky traps were installed at 06:00, and collected every hour (every half an hour during the active peak period of E. kamerunicus), and each trap was then replaced with a new one. Such collection continued until the end of the 3rd day of anthesis.
NUMBER OF E. KAMERUNICUS PER SPIKELET ON THE 3RD DAY OF ANTHESIS
To determine the number of E. kamerunicus per spikelet on the 3rd day of anthesis of male inflorescences, samples of spikelets were taken at 07:00, and 6 complete spikelets were subjected to stratified sampling every hour (every half an hour during the active peak period of E. kamerunicus) from 6 sections of the male inflorescence. The selection of 6 spikelets per inflorescence was based in part on the method of Chiu et al. (1986). The spikelets were collected in individual plastic bags, and the numbers of male and female weevils were counted. Such collection continued until the end of the 3rd day of anthesis .
NUMBER OF E. KAMERUNICUS VISITING FEMALE INFLORESCENCES DURING THE ANTHESIS PERIOD
To determine the number of E. kamerunicus visiting female inflorescences during anthesis, sticky traps were installed at 09:00, and collected after 24 h. A new trap to replace the old one was then installed around each inflorescence. Such collection continued until the female inflorescences had completely wilted.
NUMBER OF E. KAMERUNICUS VISITING FEMALE INFLORESCENCES ON THE 2ND DAY OF ANTHESIS
To determine the number of E. kamerunicus visiting female inflorescences on the 2nd day of anthesis, sticky traps were installed around the female inflorescences at 06:00 and collected every hour, but every half an hour during the active peak period of E. kamerunicus. A new trap to replace the old one was then installed around each inflorescence. Such collection continued until the end of the 2nd day of anthesis.
STATISTICAL ANALYSIS
Statistical analyses were performed using SAS 9.1 (SAS Institute, Cary, North Carolina, USA) as described by Ron (2007).
Results
NUMBERS OF WEEVILS THAT EMERGED PER SPIKELET DURING THE PERIOD OF ANTHESIS
Two high peaks of adult weevil emergence per spikelet occurred with 1 in Apr and 1 in Oct in both 2012 and 2013. The greatest values observed in various months were as follows: Oct > Nov > Apr (Fig. 2).
NUMBERS OF E. KAMERUNICUS VISITING MALE INFLORESCENCES DURING THE ANTHESIS PERIOD
Adult weevils (both females and males) were most abundant on male flowers on the 3rd day of anthesis when all the florets had opened. The number of female weevils was always greater than that of the males (Fig. 3). There were no weevils on the male inflorescences on the 1st day of anthesis when about 25% of the florets had opened. The number of adult weevils increased on the 2nd day when 50% of the florets had opened. On the 3rd day, the total number of the weevils reached a maximum of 599 adults. The number of adult weevils progressively declined on the male inflorescences on the 4th and 5th days to 420 and 95, respectively. Only one adult weevil was seen on the inflorescence on the 6th day. No weevils were collected on the 7th day. By this time, the male flowers had withered and a small fraction of the male spikelets were moldy.
NUMBERS OF E. KAMERUNICUS PER SPIKELET DURING THE ANTHESIS PERIOD
Adult weevils were most abundant on male spikelets on the 3rd day of anthesis when all the florets had opened, and the number of female weevils was always greater than that of the males (Fig. 4). There were few adult weevils on the male spikelets on the 1st day of anthesis when 25% of the florets had opened. The total number of adult weevils increased to 14 per spikelet on the 2nd day when 50% of the florets had opened. On the 3rd day, the weevils reached a maximum of 33 per spikelet, and the spikelets were covered with golden yellow pollen. The number of the adult weevils declined on the 4th and 5th days, and so did the amount of pollen. No adult weevils were caught on the 6th day, and by this time the spikelets had withered and the basal parts of the male spikelets were moldy.
NUMBER OF E. KAMERUNICUS VISITING MALE INFLORESCENCES ON THE 3RD DAY OF ANTHESIS
On the 3rd day of anthesis, the adult weevils were very active between both 11:00 and 12:00 and between 17:30 and 18:30, slightly active between 13:00 and 15:00, slightly active between 09:00 and 10:00 and between 16:00 and 17:30, and inactive between 07:00 and 08:00 (Fig. 5). The number of weevils visiting male inflorescences began to increase between 09:00 and 10:00. The total number of weevils reached a maximum of 515 at 11:30, of which 400 were females and 115 were males.
NUMBER OF E. KAMERUNICUS PER SPIKELET OF INFLORESCENCES ON THE 3RD DAY OF ANTHESIS
On the 3rd day of anthesis, the adult weevils were very active on spikelets between 17:00 and 18:00, active between 11:00 and 12:00, and inactive between 07:00 and 08:00 (Fig. 6). Only a few individuals visited the male spikelets between 09:00 and 10:00. The total number of weevils peaked at 17:30 with 36 adults per spikelet.
NUMBER OF E. KAMERUNICUS VISITING FEMALE INFLORESCENCES DURING THE ANTHESIS PERIOD
Adult weevils were most abundant on female flowers on the 2nd day of anthesis, and the number of adult females was always greater than that of males (Fig. 7). Twenty-eight adult weevils were found on the 1st day. On the 2nd day, when all the florets had opened, the total number of the weevils reached a maximum of 651. The number of adult weevils declined sharply during the 3rd, 4th, and 5th days. No weevils were seen on the 6th day, when the flowers had become black and a small number had become moldy.
NUMBER OF E. KAMERUNICUS VISITING FEMALE INFLORESCENCES DURING THE 2ND DAY OF ANTHESIS
Adult weevils were very active between 10:00 and 12:00, active between 17:00 and 18:30, and inactive between 07:00 and 09:00 on the 2nd day (Fig. 8). The total number of weevils peaked at 11:00, when it reached a maximum of 544. At 18:00, the number of individuals that visited female flowers was 298. The number of the weevils was less than 30 between 13:00 and 16:00. Only a few individuals visited female flowers between 07:00 and 09:00.
Discussion
Anthesizing male inflorescences were attractive to the weevils from day 1 to day 6 (Figs. 3 and 4). Adult weevils were most abundant on male flowers on the 3rd day of anthesis, when all the florets had opened. The number of females was always greater than the number of males on male inflorescences. Small numbers of E. kamerunicus gathered on the male inflorescences during the 1st and 5th days of anthesis, as had been reported previously by Dhileepan (1994). Ponnamma (1999) and Syed (1982) reported that the males of E .kamerunicus tended to aggregate and adult weevils were most abundant on male flowers on the 3rd day of anthesis. In this study, we conducted more detailed observations and obtained results similar to those reported by these earlier workers.
Fig. 7.
The number of Elaeidobius kamerunicus pollinating weevils visiting female inflorescences on each of the 6 d of the anthesis period of the female inflorescence of the African oil palm. Each data point in the figure is presented as the mean ± SE.
The density of the pollinating weevil per anthesizing male spikelet on Hainan Island was less than that in Cameroon (Syed 1982). This could be because E. kamerunicus on Hainan Island is adversely affected by natural enemies including spiders, mites, ants, nematodes, and rats. Previous studies reported that the weevil population was affected by predators. Rats and ants are known to feed on the larvae of the pollinating weevil (Liau 1984; Saúl et al. 1998; Ponnamma et al. 2006a). During this study, we occasionally caught spiders, ants, and rats on the sticky traps. In the laboratory, we observed infestation of the weevils by mites and nematodes. To increase the population of E. kamerunicus in Hainan Island, measures to control natural enemies, i.e., mites, ants, nematodes, and rats, must be addressed.
We demonstrated that adult weevils were most abundant on the female flowers on the 2nd day of anthesis. This finding is similar to that of Hala et al. (2012) but differs from the results of Syed (1979, 1982), who reported that the adult weevil population increased to a maximum on the female inflorescences during the 2nd and 3rd days of anthesis. The differences between our observations and those reported by Syed (1979, 1982) could perhaps be due to differences in climate and location.
Elaeidobius kamerunicus was more abundant on male inflorescences than female inflorescences, and this is similar to the results of Hala et al. (2012). Our examinations were more detailed than those of Tuo et al. (2011). Adult weevils were more likely to stay on the spikelets for mating and oviposition at dusk, and this finding agrees with that of Tuo et al. (2011). We noted that the male flowers released a distinct anise-like odor, which seemed to be strongest on the 3rd day of anthesis. Female flowers also emitted a distinct anise-like odor, which seemed strongest on the 2nd day of anthesis. Perhaps the anise-like odor attracted the adult weevils. The number of adult weevils at 11:00 was 1.8 times greater than at 18:00, possibly because the adult weevils were feeding on the nectar in the flowers. We found that female flowers had much nectar at 11:00. Our experimental results demonstrate that the adult weevils were active between 11:00 and 12:00 and between 17:30 and 18:00, and inactive between 07:00 and 08:00, irrespective of whether they were present on male or female inflorescences. Other workers reported that the activity of the oil palm pollinating weevil was substantial between 16:00 and 18:00, and the number of E. kamerunicus was greatest between 12:30 and 14:30 and smallest around noon (Chiu 1984; Chinchilla et al. 1991; Ponnamma 1999). Their results differ from our findings reported in this study. These differences might be due to differences either in the behavior of E. kamerunicus or in the physiology of the African oil palm under the influence of climatic factors that differ in the various countries where this crop is produced.
In this study, we discovered that E. kamerunicus weevils aggregated on male inflorescences during the 1st to 6th day of anthesis, and on the female inflorescences during the 1st to 5th day of anthesis. Weevil abundance peaked on the 3rd day of anthesis on male inflorescences when all florets were open, and on the 2nd day of anthesis on female inflorescences. Activity of the weevils recorded on the day of highest abundance during anthesis showed an inactive period between 07:00 and 08:00, and consistent activity occurred between 11:00 and 12:00 and between 17:30 and 18:00. In this study, we conducted much more detailed observations than have been reported previously. Sticky traps incorporating anthesizing male flowers as bait or sampling weevil-covered spikelets of the anthesizing male inflorescence are 2 sampling methods for estimating the weevil population. The 2nd method was reported by Chiu et al. (1986) to be more reliable than the 1st method. In this study, we found that the separation of anthesizing male inflorescences into 7 stages and encircling the inflorescences with sticky traps was an optimal procedure for obtaining reliable data.
Acknowledgments
This work was supported by the Specialized Fund for the Basic Research Operating Expenses Program of the Central Public Welfare Scientific Research Institute funds (No. 1630022011037) and 211 Project for Hainan University. We are grateful to RRI-CATAS for providing the oil palm plantation for the experiment.
