Corresponding author: Javaid Iqbal (
Academic editor: Jack Neff
Honey production gains are needed to deal with high demand in Saudi Arabia. The honey bee races are facing stressful hot-arid weather conditions that can affect different aspects of physiology and behavior. The hypopharyngeal glands (
Ali H, Alqarni AS, Iqbal J, Owayss AA, Raweh HS, Smith BH (2019) Effect of season and behavioral activity on the hypopharyngeal glands of three honey bee
Beekeeping has been practiced in the Arabian Peninsula for centuries. It is an important aspect in the agriculture sector of Saudi Arabia with an additional objective to increase the income of Saudi beekeepers (
Hypopharyngeal glands (
The activity of the
Lipofuscin are undegradable lipid-protein granules enclosed in a single membrane in the
Beekeepers in Saudi Arabia are spending large amounts of money for importing exotic bee races because the population of indigenous bees is too scarce and honey production is too low to meet the increasing demands of the local market (
The bee colonies of the indigenous race
The selected colonies of each race were of equal estimated colony strengths containing 5 frame bees, 3 frame brood and 2 frame of food. The plenty of flora and flowers of different plants such as
Fifty newly emerged bees of each race from cells were marked with different paint colors of Uni-Paint® (yellow and white) to determine their ages at the time of collection. Direct marking was done to keep the new emerged bees in their natural environment, no cages were used. Nurse bees were collected at 11 days, whereas foragers were collected 25 days after emergence. The separate experiments were performed during the peak summer (later June: 27–40 °C, 9.5–10% relative humidity) and winter (December: 15–20 °C, 35–38% relative humidity) seasons. A thermo-hygrometer (HANNA, HI93640N, Europe) was used to record the meteorological factors.
The heads of ten marked nurse or forager bees were dissected with a sharp blade in the Melittology Research Lab,
The morphological measurements and images of the acini size were recorded from mounted specimens using a 10× objective on a stereomicroscope (M165C, Leica, Germany) with a camera (DP71, Olympus). The maximum length (L) and width (W) of ten acini per slide were taken from different image locations for each individual bee (
Acinal surface area = π × ((a × b) / 2),
where a = maximum length, b = maximum width, and π = 3.14.
Microscopic measurement of acini length and width in the hypopharyngeal glands of honey bees.
Lipofuscin was identified by its granular appearance in the acini of
Data were examined for normality and homogeneity using the Kolmogorov-Smirnov test and Levene’s test, respectively. The means were tested using an analysis of variance and subsequently separated using the LSD test at
Selected images of the acini of the nurses and foragers of the three bee races are shown in Figure
Acini in the hypopharyngeal glands of the nurse and forager bees.
Figure
The mean acini measurements in the
Acini sizes (length, width, and surface area) of nurse and forager bees.
Inter-race comparison of acini size (length, width, and surface area) among the
Measurements of acini size and lipofuscin accumulation percentages in the hypopharyngeal glands of honey bees.
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Summer |
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0.162±0.005 | 0.101±0.005 | 0.128±0.005 | 0.071±0.009 | 0.033±0.001 | 0.011±0.002 | 12.33 | 45.43 |
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0.190±0.011 | 0.121±0.013 | 0.143±0.012 | 0.083±0.007 | 0.043±0.006 | 0.016±0.002 | 14.13 | 56.27 | |
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0.199±0.012 | 0.124±0.013 | 0.147±0.013 | 0.088±0.015 | 0.046±0.006 | 0.017±0.005 | 15.57 | 58.23 | |
Winter |
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0.151±0.014 | 0.101±0.012 | 0.111±0.012 | 0.062±0.015 | 0.027±0.005 | 0.012±0.003 | 11.10 | 40.50 |
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0.178±0.008 | 0.132±0.008 | 0.129±0.007 | 0.095±0.009 | 0.036±0.003 | 0.020±0.004 | 12.20 | 46.00 | |
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0.179±0.016 | 0.134±0.012 | 0.136±0.001 | 0.098±0.015 | 0.039±0.006 | 0.020±0.004 | 14.80 | 46.33 |
The microscopic lipofuscin accumulation granules in the
Lipofuscin accumulation (black granular structures: arrows) in the hypopharyngeal glands of nurse and forager bees
Comparisons between nurse and forager bees in the accumulation of lipofuscin in hypopharyngeal glands.
The comparison among indigenous (
In summer, the lipofuscin accumulation values in the nurse bees were
The acini size and lipofuscin accumulation were inversely correlated with each other in the nurses and foragers of all bee races. The larger acini size in the nurse bees was correlated with a lower lipofuscin accumulation, and the smaller acini sizes in the foragers was correlated with higher lipofuscin accumulation (Table
Inter-race comparison of lipofuscin accumulation
Seasonal variations in lipofuscin accumulation between summer and winter bees of the same race. Asterisks (*) in the graph represent significant differences between the groups (LSD test at p ≤ 0.05).
Summary table for the inverse correlation between acini size and lipofuscin accumulation in the three bee races. Larger acini corresponded to lower lipofuscin accumulation and vice versa.
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Nurses | ↑ | ↓ | |
Foragers | ↓ | ↑ |
Our results showed that acini size is linked with honey bee age-specific tasks. Nurse bees have significantly larger acini (L, W, and
Acini size is positively correlated with HPG activity and its secretion. The larger acini in young nurses corresponds to higher HPG activity because of the production of royal jelly (
Furthermore, the acini size (L, W, and
Many factors, such as bee race, body size, brood pheromones, ecological factors, starvation, heat stress, Varroa infestation, diseases, and pesticides could play an important role in acini size in bee races (
In the present study, cellular senescence was observed by measuring the difference in lipofuscin accumulation in
Lipofuscin accumulation is also known to be related to the onset of senescence and is dependent on foraging age (
Furthermore, indigenous bees (
This study suggests the need to further investigate the association of
Collectively, nurse bees presented significantly larger acini and less lipofuscin accumulation than foragers. Consequently, a strong inverse correlation was observed between acini size and lipofuscin accumulation. Inter-race comparisons showed that indigenous bees possess smaller acini and less lipofuscin accumulation in the
The authors extend their appreciation to the Deanship of Scientific Research at the King Saud University for funding the work through the research group project No. RGP-189.