Table 1.
Effects of the stressors, alone or combined, on physiological markers in drones.
| Physiological marker | Tissue | unit | Physiological functions | Physiological markers responses (Mean ± SD) | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Control | Nosema ceranae | Fipronil [0.1 µg.L−1] | Nos + Fip [0.1 µg.L−1] | ||||||||
| AChE | head | mUA.min−1.mg of tissue−1 | neural | 253.9 ± 30.2 | a | 235.9 ± 35.0 | ab | 221.2 ± 27.0 | b ↘ | 226.7 ± 15.8 | b ↘ |
| GOX | head | mUA.min−1.mg of tissue−1 | immune | 32.3 ± 14.6 | a | 32.1 ± 13.5 | a | 34.0 ± 18.7 | a | 30.5 ± 18.7 | a |
| GA3PDH | head | mUA.min−1.mg of tissue−1 | metabolic | 325.1 ± 54.3 | a | 334.5 ± 41.1 | ab | 336.7 ± 39.6 | ab | 391.8 ± 41.1 | b ↗ |
| LDH | head | mUA.min−1.mg of tissue−1 | metabolic | 46.5 ± 4.0 | a | 47.0 ± 3.8 | a | 52.5 ± 5.2 | b ↗ | 53.0 ± 3.4 | b ↗ |
| ATP | head | LI.mg of tissue−1 | metabolic | 11117.6 ± 1023.4 | a | 11779.7 ± 900.8 | ab | 11171.3 ± 587.7 | a | 12421.8 ± 823.2 | b ↗ |
| GST | head | mUA.min−1.mg of tissue−1 | metabolic. detoxification. antioxidant | 252.3 ± 26.5 | a | 253.2 ± 28.2 | a | 232.8 ± 23.0 | ab | 228.3 ± 15.2 | b ↘ |
| G6PDH | head | mUA.min−1.mg of tissue−1 | metabolic. antioxidant | 7.8 ± 0.7 | a | 7.1 ± 1.3 | a | 7.2 ± 1.0 | a | 7.1 ± 0.9 | a |
| CAT | head | mUA.min−1.mg of tissue−1 | antioxidant | 139.5 ± 51.9 | a | 164.3 ± 58.4 | ab | 158.1 ± 99.0 | ab | 244.9 ± 54.7 | b ↗ |
| GP | head | mUA.min−1.mg of tissue−1 | antioxidant | 24.9 ± 4.4 | a | 25.0 ± 4.4 | a | 31.01 ± 6.31 | b ↗ | 32.8 ± 5.2 | b ↗ |
| GR | head | mUA.min−1.mg of tissue−1 | antioxidant | 20.4 ± 5.6 | a | 21.6 ± 4.4 | a | 23.1 ± 3.9 | ab | 26.0 ± 4.9 | b ↗ |
| CaE-1 | abdomen | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 316.6 ± 66.4 | a | 275.5 ± 39.4 | a | 265.8 ± 32.8 | a | 294.4 ± 54.4 | a |
| CaE-2 | abdomen | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 518.9 ± 48.3 | a | 523.8 ± 29.4 | a | 501.8 ± 32.6 | a | 506.2 ± 24.5 | a |
| CaE-3 | abdomen | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 70.1 ± 14.8 | a | 66.9 ± 8.1 | a | 68.7 ± 9.5 | a | 72.6 ± 15.2 | a |
| POX | abdomen | mUA.min−1.mg of tissue−1 | immune | 2.1 ± 0.8 | a | 2.5 ± 1.0 | a | 3.3 ± 0.7 | b ↗ | 3.3 ± 0.6 | b↗ |
| CaE-1 | midgut | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 910.7 ± 172.3 | a | 913.2 ± 134.0 | a | 1003.0 ± 140.7 | a | 993.8 ± 115.5 | a |
| CaE-2 | midgut | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 536.5 ± 94.3 | ab | 521.5 ± 119.2 | a | 607.1 ± 61.8 | b | 577.8 ± 66.7 | ab |
| CaE-3 | midgut | mUA.min−1.mg of tissue−1 | metabolic. detoxification | 209.2 ± 49.3 | a | 211.6 ± 42.1 | a | 260.5 ± 45.2 | b↗ | 280.8 ± 37.4 | b ↗ |
| ALP | midgut | mUA.min−1.mg of tissue−1 | immune. metabolic | 19.4 ± 5.6 | ac | 14.0 ± 4.7 | b ↘ | 20.5 ± 6.4 | c | 16.0 ± 5.5 | ab |
| ATP | midgut | LI.mg of tissue−1 | metabolic | 23798.2 ± 7663.7 | a | 28557.6 ± 12897.7 | a | 22123.8 ± 9941.7 | a | 22613.4 ± 9276.1 | a |
| GST | midgut | mUA.min−1.mg of tissue−1 | metabolic. detoxification. antioxidant | 203.3 ± 39.7 | a | 204.4 ± 37.1 | a | 222.0 ± 25.0 | a | 254.3 ± 27.7 | b ↗ |
| CAT | midgut | mUA.min−1.mg of tissue−1 | antioxidant | 1154.8 ± 315.6 | a | 1414.8 ± 208.4 | bc ↗ | 1345.4 ± 330.8 | ab | 1606.4 ± 313.8 | c ↗ |
A multiple markers approach was performed to study the effects of the stressors in the head, midgut and abdomen of drones. Each marker was associated with one or more of the main physiological functions (neural, metabolic, immune, detoxification and antioxidant). The data represent the mean values ± standard deviations of the physiological markers responses expressed in milliUnits of Absorbance (mUA) or in Luminescence Intensity (LI) for ATP. Three samples of 6 drones were measured from each hive (n = 12 for each modality of treatment). For statistical analyses, a generalized linear mixed model was applied considering a random effect of the hives from which the drones came. Significant differences at P ≤ 0.05 between modalities are expressed with different letters. Case with the same letters indicate no significant difference between the groups. Arrows indicate the direction of the modulation relative to the control group.