Relating climatic factors to foraging behavior of honeybees (Apis mellifera) during blooming period of Guizotia abyssinica (L.F.)

Haftom Gebremedhn, Alemayehu Tadesse* and Tesfay Belay

Tigray Agricultural Research Institute, Mekelle Agricultural Research Center, Department of Apiculture and Sericulture,
P.O.Box 492, Mekelle, Tigray, Ethiopia
haftush@yahoo.com
* Mekelle University, Department of Animal, Rangeland and Wildlife Sciences,
PO Box 231, Mekelle, Tigray, Ethiopia

Abstract

 The present study was conducted at Mekelle Agricultural Research Center with the objective of determining the foraging behavior of local honeybees in relation to climatic factors. This was done during the blooming time of Guzotia abyssinica (LF). The data were collected during five observations at time intervals of: 8:30-3:30 AM, 10:30-11:30AM, 12:30-13:30PM, 14:30-15:30 PM and 16:30-17:30PM during one day. Each observation time was considered as a treatment. The collected data were analyzed using GLM repeated measurement analysis procedure using Genstat and SPSS software.

The highest numbers of honeybees were recorded at 8:30-9:30AM, while the least number of bees were recorded at 16:30-17:30PM. The number of bees that collected nectar had a positive association with air temperature (r=0.67; P=0.01) and negative relationship with relative humidity (r=-0.59; P=0.001). However, the number of bees that collected pollen had a positive correlation with relative humidity (r=+0.62; P=0.001) and a negative association with air temperature (r =-0.72; P=0.001). Thus honeybee activity was much higher during early morning hours. Honeybees also preferred a relatively higher air temperature for nectar than pollen collection, while they preferred a higher relative humidity for pollen than nectar collection. Honeybee and other insect pollinators can therefore be saved from pesticide hazards by not applying these chemicals at times when bee foraging activity is highest.

Key words: humidity, nectar, pollen, pollination, temperature

Introduction

Crop pollination is one of the most important economic outcomes of honeybee activities. Planned honeybee pollination is practiced widely to ensure maximum and high quality crop yield (Anita et al 2012). Many insect species assist the reproduction of plants through mediating pollen from flower to flower. Honeybees visit plants for its nectar and/or pollen (Lane and David 2006; Mattu et al 2012). However, foraging activities of social insects are influenced by climate (Tirado et al 2013) and unpredictable environmental variables in terms of timing and location of food (Biesmeijer and Ermers 1999; Lane and David 2006). Besides, the foraging behavior of bees is regulated by temperature, humidity, season, topography and availability of floral resources (Tripath 2011). All the daily activities and foraging patterns of honeybees are under the control and/or changed with weather conditions (Hossam et al 2012; Contreras et al 2013). Insects accordingly can alter their food preferences depending on environmental conditions (Tripath 2011; Contreras et al 2013).

However each species of social bee has a microclimate in which its foraging activity can be sustained (Contreras et al 2013). To predict whether a given honeybee race is worth using as a pollinator in a given climate, it is useful to know the foraging behavior of local honeybees and their response to the climatic factors. Moreover, there is limited information that pertaining the impact of climatic factors on the foraging patterns of local honeybees. Besides, their foraging behavior was not studied. This information is therefore important for protecting honeybees through rational pesticide use. Thus, this study was conducted to determine the foraging behavior of local honeybees (Apis mellifera) in relation to climatic factors during the blooming period of Guizotia abyssinica (LF). This would be helpful to synchronize the foraging behavior of bees with crop pest management practices, pollination and honeybee product utilization. Moreover this result can help to save pollinators by applying  pesticides when the activity of honeybees and other insect pollinators is reduced.

Material and methods

Description of study area

The study was carried out during 2013 cropping season at the farm of Mekelle Agricultural Research Center, Illala site. It is located Northeast of Mekelle at an elevation of 2015 m at N13031’21.2” latitude and E039030’14.7” longitude.

Foraging behavior of honeybees

This was done in four open plots planted to G.abyssinica. Each plot had 9m² area. The foraging behavior was studied during the blooming of G.abyssinica and ranged from 7 to 21 days of its flowering. The collected data included: foraging rate, time spent per flower, number of foragers, and honeybees association with other insects and timely pollen and/or nectar preference. For this purpose bees were coming from local backyards (within a radius of 300-500m from the observation plots).

Time spent per flower and foraging rate

Time spent by honeybee per flower was recorded using a stopwatch starting from landing on a flower to leaving that particular flower. Foraging rate was determined by counting the number of head flowers visited by a single honeybee per minute. This was done five times per day starting from 8:30AM to 17:30PM at two hours intervals for consecutive 15 days. Foraging rate and time spent per flower were recorded for a total of 12 honeybees at each recording time. This was done for honeybees that collected nectar and/ or pollen. Each observation time was therefore considered as a treatment.

Abundance of honeybees and other insects

The number of honeybees and other insects that visited the flowers of G.abyssinica were counted by visual observation starting from 8:30AM to 17:30PM at two hour intervals. This was done for consecutive 15 days starting from 7 days after flowering (24th September to 10th October, 2013). The number of honeybees and other insects in four sampling sites were counted per five plants/five minutes. For this purpose the plants were selected randomly.

Feed preference of honeybees

Timely feed preference of honeybees was investigated by counting the numbers of honeybees that collected pollen and/or nectar. This was done for 14 days starting 8 days after flowering (18th September to 3th October 2013). Foragers were categorized as nectar collectors when honeybees insert their head into the corolla of a floret and with no pollen loads on their legs; pollen collectors when honeybees had pollen loads on their legs. Pollen and nectar collectors were categorized when honeybees were collecting both nectar and pollen. This observation was done on twenty honeybee pollinators per plot in each observational period.

Abundance of honeybees and other insects in relation to flowering period of G.abyssinica

The foraging behavior of honeybees (abundance) across the flowering period of the plant in the four sampling sites were noted by considering the number of honeybees and other insects per five plants/five minutes from first to third weeks of the flowering period. Recording was done on only five days of the week.

Meteorological data

To see the effect of climatic factors on foraging behavior of honeybees during G. abyssinica pollination, temperature and relative humidity records were taken from Mekelle Agricultural Research Center Meteorological Station.

Data analysis

The collected data were analyzed using General Linear Model (GLM) repeated measures analysis procedure. Least significant difference (LSD) test was calculated to separate the treatment means whenever found significant. For all the indicated analysis and tests, GENSTAT statistical program (GENSTAT©, Version 13) was used. Spearman correlation test was also done with number of honeybees and other insects’ collected and meteorological data using SPSS version 16.

Result and Discussion

Abundance of honeybees and other insects

Time of the day had significant effect on the abundance of honeybees (Table1). The highest numbers of honeybees were recorded at 10:30-11:30AM, while the least number of honeybees was found at 16:30-17:30PM.The data revealed that abundance of honeybees declined gradually during the evening hours of the day. Similarly, in Egypt Mahfouz et al (2012) observed maximum number of honeybees during 9:00-11:00AM and numbers of bees were drastically reduced at 15:00-16:00PM. In India Neeraj and Ramashrit (2005) also found the maximum foragers (Apis species) at 11:00AM, while the least number was observed at 15:00PM. In Brazil Nascimento and Nascimento (2012) also reported 9:00AM and 13:00PM as period of high foraging activity for Apis mellifera adansonii.  

Time of the day had also significant effect on the abundance and diversity of insect pollinators (Table1 and Table 2). The maximum number of insects (12.1) was observed at 10:30-11:30AM, while the minimum was noted at 16:30-17:30PM (5.4) (Table 1). The highest insect diversity (4.95) was recorded at 14:30-15:30PM, whereas the least insect diversity was recorded at 16:30-17:30AM (Table 2). Murphy and Robertson (2000) also reported that abundance and diversity of insect pollinators varied considerably between observational periods. Other studies also illustrated that abundance of insect pollinators differed across the time of the day but increased around the midday (10:00AM - 12:00AM) (Semida and Elbanna 2006; Andrej and Anton 2006). On G.abyssinica Andrej and Anton (2006) observed differences in frequency of visits among the insect groups with respect to time of the day and reported the highest insect activity between 10:00AM and 11:00AM. In other studies also the maximum activity of insects was noticed at 10:00AM and 16:00PM, while a minimum being at 8:00AM and 18:00PM (Dhurve 2008).

As demonstrated in table 4, abundance of honeybees had shown negative association with the abundance of insects (r= -0.21). This might be due to the negative interaction between honeybees and other insects’ or competition with other pollinators. According to Garibaldi et al (2013), honeybees might displace wild insects (or vice versa) from flowers without any aggressive interactions. Awraris (2009) also reported interspecific exploitative competition between honeybees and wild pollinators.

Flowering period had a significant influence on the abundance of honeybee and other insects (Table 1). The highest honeybees’ abundance (32.6) was recorded at the second week, while the least abundance of honeybees’ (5.9) was observed at the third week. Abundance of honeybees seems to decline gradually to the end of flowering period (Table 1). Abundance of honeybees might be related to the critical flowering period of G.abyssinica which in this case is in the second week. Mahfouz et al (2012) indicated that honeybee population decreased with diminishing of flowers per plant due to advancing age of the crops. Dhurve (2008) reported that the mean foraging activity of Apis dorsata was less (19.60 bees/m2/5min) at the first week of its flowering and increased to 50.06 bees/m2/5min on 5th day till 20th day after flowering. Then it decreased, with least (15.13 bees/m2/5minute) foraging activity on 25th day as the flowering period of G.abyssinica came to flag end. SimilarlyDhakal and Pandec (2003) reported that honeybees were most active towards middle of the flowering period when maximum numbers of plants were at bloom.

The abundance of other insects (outside honeybees) was the highest at the second and  third week. This might be due to reduced competition for floral resources from honeybees at the third week or the insects visiting the flowers might have some other mission outside pollen and nectar collection. Garibaldi et al (2013) mentioned that honeybees compete with other insect pollinators for floral resources.

The interaction effect between time of the day and flowering period also had a significant effect on the abundance of honeybees (Figure 1). The highest number of honeybees was recorded at 8:30-9:30AM (51.2) in the second week of the flowering period. The least number of honeybees was recorded at 16:30-17:30PM during the third week of the flowering period. However, the interaction effect between time of the day and flowering period had no effect on the abundance of insects (excluding honeybees) (Figure 1).

Figure 1: Abundance of honeybees and insects (exclude honeybees) across different time of the day and flowering period (Where A, 8:30-9:3AM; B, 10:30-11:3AM; C, 12:30-13:3PM; D, 14:30-15:30PM and E, 16:30-17:30PM)

 Honeybee foraging rate and time spent per flower

There were differences in the foraging rate of honeybees across the different times of the day (Table 2). A maximum foraging rate of 12.6 florets/minute was found at 12:30-13:30PM though it showed a decline towards the evening. Similarly, Rahman and Rahman (2000) revealed a gradual decline in the foraging activity of bees (Apis cerana indica) during the evening hours. The highest foraging rate of honeybees during 12:30-13:30PM might indicate the suitability of the climatic conditions. This specific time was also suitable to other insect pollinators as there is a positive association (r = 0.28; Table 4) of foraging rate with insect diversity. According to Garibaldi et al (2013) wild insects displaces honeybees (or vice versa) from flowers without any aggressive interactions and such a competition might cause honeybees to visit more flowers in a given time. Moreover, Awraris (2009) reported that interaction of honeybees with wild pollinators significantly increased the movement of honeybees among sunflower flower heads. Compared with Apis cerana (5-8 flowers/minute) the local bees (Apis mellifera) had higher foraging rate (Verma and Partap 2010).

Related to the time a bee spent on a flower head, differences were not observed between the different observation times (Table 2). Nderitu (2008) also indicated that the time of the day did not significantly influence the time a bee spent on a flower head. Compared with Apis cerana, the local bees (Apis mellifera) spent more time on a flower head. Apis cerana visits to individual flowers lasted from 4.3 to 6.7 seconds (Verma and Partap 2010).

Pollen and nectar preference of honeybees

Time of the day affected nectar and/or pollen preference of honeybees (Table 2). More honeybees collected nectar (Photo 1b) at 12:30-13:30PM than in the morning (8:30-9:30AM). Other studies demonstrated that weather greatly influenced whether bees collect pollen or nectar (Peat and Goulson 2005). According to Weiss (2000), a floret of G. abyssinica, which is the nectar source, emerges about midday and this gives chance for honeybees to collect nectar at midday. Junior et al (2010) also indicated that returning flights with nectar increased in frequency during the day at all seasons. Similarly, in Apis cerana, nectar collectors outnumbered pollen collectors in the afternoon (Verma and Partap 2010).

There were differences in the number of honeybees collecting pollen (Photo 1a) in the different times of the day. More honeybees were collecting pollen in the morning (8:30-9:30AM) and few collected pollen in the late afternoon. According to Weiss (2000), the floret of G. abyssinica opens and liberates pollen early in the morning. More honeybees visited the plants on the morning (8:30-9:30AM) for collecting both pollen and nectar (Photo 1b). So for G.Abyssinica plant, honeybees prefer to collect pollen in the morning. Other authors also pointed out that pollen collection had a significant variation with relation to the time of day (Nascimento and Nascimento 2012). Verma and Partap (2010) also reported that pollen collectors outnumbered nectar collectors during the morning.

Photos 1a,b,c. Honeybee collecting pollen (a), nectar (b) and pollen and nectar (c) from G.abyssinica flowers (left to right)

Effect of temperature and relative humidity on honeybee foraging behavior

There were differences in mean temperature and relative humidity during the observation times (Table 3). The time period of 12:30-13:30 PM had the highest temperature, while 12:30-13:30 PM and 8:30-9:30AM had the lowest relative humidity and temperature.

There was no correlation of air temperature and relative humidity with the frequency of foragers’ exiting, foraging rate and time honeybees spent per flower (Table 4). Abundance of insects tended to be positively correlated with mean air temperature (r= +0.42), while there was a negative tendency with relative humidity (r = -0.22). Abundance of honeybees had positive relationship with relative humidity (r = + 0.20), while there was negative trend with air temperature (r= -0.30). Omoloye and Akinsola (2006) also indicated negative correlation between the intensity of visitation by honeybees and temperature. Foraging rate of bees tended to be positively associated with air temperature (r= +0.21), while there was a negative tendency with relative humidity (r= -0.19). Similarly, Peat and Goulson (2005) revealed that temperature did not significantly influence foraging rate of bees.

Temperature and relative humidity had significant effect on the pollen and nectar preference of honeybees (Table 4). The number of bees that collected nectar had a positive association with air temperature (r=0.67; P=0.01) and negative relationship with relative humidity (r=-0.59; P=0.001). However, the number of bees that collected pollen had a positive correlation with relative humidity (r=0.62; P=0.001) and negative association with air temperature (r =-0.72; P=0.001).This might be the reason why honeybees were collecting more nectar starting from 12:30 to 13:30PM in which high temperature was recorded (Table 3). Peat and Goulson (2005) also revealed that weather had a great influence on whether bees collected pollen or nectar. In stingless bees the number of pollen loads increased as relative humidity rose (r = 0.40), while high temperatures had negative influence on the number of pollen loads collected (r = -0.23); and the number of nectar loads was also positively correlated with air temperature (r = 0.24) (Fidalgo and Kleinert 2010).

Conclusions and recommendations

• Time of the day had a significant effect on the foraging behavior of honeybees and abundance and diversity of insect pollinators.
  
  
• The observation time of 8:30-9:30AM and 10:30-11:30AM had the highest abundance of honeybees and others insects, respectively.
  
  
• Abundance of honeybees declined towards the evening hours of the day.
  
  
• Flowering period had a significant effect on the abundance of insect visitors. Honeybees’ abundance was the highest in the second week and declined towards the end of flowering period.
  
  
• Temperature and relative humidity had significant influence on whether honeybees collected pollen and/or nectar. The number of pollen loads increased as relative humidity rose, while high temperatures had a strong negative influence on the number of honeybees that collected pollen. Air temperature was positively correlated with the number of honeybees collecting nectar, while relative humidity was negatively correlated with nectar collection.
  
  
• There is need to harmonize agricultural practices like pest control operations with pollination and honeybee product utilization in such a way that it saves honeybees and other insect pollinators. Such operations should be applied at times when honeybees and other insect pollinators’ activities are very much reduced.

Acknowledgements

We are grateful for the financial and material support provided by the Mekelle Agricultural Research Center of the Tigray Agricultural Research Institute. We are also very grateful to the livestock and crop researchers of Mekelle Agricultural Research Center, Kinfe Mezgebe of Mekelle Agricultural Research Center coordinator and Embza Kasa and Eyerus Meles from Mekelle agricultural research center, Alemat Embaye researcher of Axum Agricultural Research Center and Teklay Gerezgabhear for their very great support throughout the study.

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Received 11 December 2013; Accepted 24 February 2014; Published 5 April 2014

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