Natural enemies are more effective at controlling herbivores in diverse botanical ecosystems. Different chemical cues help to correspond in diversity of associations between prey and host plant species. Recent studies exhibited that the use of natural enemy is an ecofriendly measure to control pests. The Seven spotted ladybird beetle, Coccinella septempunctata play a prominent role in aphid management. It exploits several different cues released by plants to increase the efficiency of foraging. Aphid endoparasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) have an ability to locate itshosts by responding to odours from aphid hostplants or by visual searching.The treatments with different combinations of plant extracts and semiochemicals were used for natural enemypreference experiment. The experiment was conducted with seven treatments and five replications at Glass house situated in Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi field area during Feb-April, 2015. The Coccinella septempunctata were collected from wheat crop plants. They remained starved for two days before Olfactometer bioassays. For D. rapae, mummified aphidswere collected from wheat crop. Naive females were subjected to olfactometer tests. Seven different combined treatments of semiochemicals and plant extract were applied on filter paper strips at 3% concentration. The filter paper strips were placed in arms of olfactometer. The control arms were treated with n-hexane. Data pertaining to preference of C. septempunctata and D. rapae after treatment application were recorded and analysed statistically. It was found that T6 (β-pinene + E-β-Farnesene) exhibited highest mean number entries of C. septempunctata (6.13%) and highest mean time spend(6.23%) as compared to two other treatments applied. The results revealed that alarm pheromone component effective kairomone for aphid predatory beetles. It was found that T6 (β-pinene + E-β-Farnesene) exhibited highest mean number entries of D. rapae (7.50%) and highest mean time spend(6.39%) as compared to other treatments applied. The results revealed that release of insect derived semiochemicals can enhance visual searching and efficiency of parasitoid D. rapae.
Research Article · Volume 51, Issue 4, 7 May 2019 · Open Access
Behavioral Responses of Coccinella septempunctata and Diaeretiella rapae under the Influence of Semiochemicals and Plant Extract in Four Arm Olfactometer
· · ·
Affiliations & Notes ⌄
- 1Department of Entomology, PMAS-Arid Agriculture University, Rawalpindi 2Institute of Agricultural Sciences, University of the Punjab, Lahore , * Corresponding author: bushraentomologist@gmail.com
Article Info ⌄
- Journal:
- Pakistan Journal of Zoology
- Published:
- 7 May 2019
From the article
- Aphid cornicle secretions containing semiochemicals are attracting cues for C. septempunctata.
- It was found that plant extracts and oil have not exhibited mortality to C. septempunctata up to ten days after feeding the treated L. erysimi.
- The results revealed that T6 (β-pinene, E-β-Farnesene) exhibited highest mean number entries of C. septempunctata (6.13%) and highest mean time spend (6.23%) as compared to two other treatments applied.
- The time spent by D. rapae in EβF treated discs increased with increase in its concentration.
Selected from the article's own text.
Abstract
Introduction
The four arm olfactometer was designed by Pettersson (1970). It is a volatile based instrument having central arena with food source boxes which are connected with each other through connected tubes. It is designed to study the oviposition preference behavior of insect pest and its predator via screening experiments. Volatiles are emitted from the plant parts or body of prey. Insect pests or predators are confined in the central arena to test it for food preference .
The term ‘parasitoid’ for the first time was introduced by Reuter (1913). Parasitoids have the ability to respond plant odors . The volatile profile of plant odor also play a vital role to increase parasitoid attraction ; . It was found that volatiles released immediately from damaged plant attract parasitoids instantaneously ; .
Responses of natural enemies towards volatiles released from aphid infested plants are often specific in terms of plant species, plant developmental stage, herbivore species and developmental stage of herbivore ; . But sometimes, the host specificity is not universal ; .
Natural enemies including Coccinellid beetles, parasitoid wasps, lacewings, and hoverflies are attracted by plant volatiles which are induced by aphid attack . Endoparasitic wasps undergo obligatory development inside arthropod host. During the development phase, parasitoids can be influenced by chemical stimuli perceived from its host and the environment ; . It was found that experienced A. ervi and D. rapae exhibit a significant response to aphid induced plant volatiles as compared to naive individuals .
Natural enemies play a crucial role in pest management programs and ecological studies. Natural enemies are sensitive towards chemical cues released in multitrophic environment, with regard to host location ; . Predatory ladybeetle, Coccinella septempunctata (L.) is aphidiophagus and polyphagous ; . It is best known aphid predator. It can consume more than 100 aphids per day . It exploits the cues released by plants . The C. septempunctata has specialized olfactory cells in its compound eye . The olfactory and visual cues play an important role to locate aphids .
The alarm pheromone is released by many aphid species, but the subfamily Aphididae releases particularly sesquiterpene EβF . It is released when aphids are attacked by natural enemies. It induces avoidance behaviour among aphids and increase the foraging behaviour of parasitoids . It acts as kairomone for predators such as ladybirds ; . It acts as valuable tool in aphid pest-control strategies . Therefore, this experiment was carried out to study the behavioural responses of D. rapae under the influence of seven different combinations of semiochemicals and plant extract by using four arm olfactometer.
Different chemical cues are related to diverse associations between prey and its host plant. It was found that Coleomegilla maculate, Adalia bipuncata and C. septempuncata responses were related to semiochemicals released from aphid species and their host plants ; ; they use chemical cues to locate their preys. Alarm pheromone component EBF is an effective kairomone for aphid predators, i.e. two spotted ladybeetle .
Therefore, present study was carried out to see the olfactory responses of predatory beetles towards semiochemicals and plant extract. Al-Abassi et al (2000) found that the semiochemicals have been intensively studied for their use in insect biocontrol programs.
Materials and methods
This experiment was conducted at Laboratories situated in Department of Entomology, Pir Mehr Ali Shah-Arid Agriculture University, Rawalpindi field area. The experiment was conducted comprising seven treatments with five replications.
Collection and rearing of insects
The C. septempunctata were collected from wheat crop plants. They were reared on 50% sugar solution. They remained starved for two days before Olfactometer bioassays.
Mummified aphids of D. rapae were collected from wheat crop in vials individually. On emergence, females were reared on 50% aqueous solution of honey for 2 days. Naive females were subjected to olfactometer tests.
Olfactometer bioassays
The behavioural responses of C. septempunctata and D. rapae under seven different treatments of plant extract and semiochemicals were determined by using a four-arm olfactometer ; ; . The bioassay consists a pairwise treatment comparison. All bioassays for predator response were performed at 20±2°C with 0.04 W / m2 light intensity .
Treatments were applied on filter paper strips at 3% concentration. The control arms were treated with n-hexane. Filter paper strips were placed in arms of olfactometer. Two arms are kept as control and rest of two arms are kept as treatment arms. These treatments are: T1, Turmeric; T2, β-pinene; T3, E-β-Farnesene; T4, Turmeric and β-pinene; T5, Turmeric and E-β-Farnesene; T6, β-pinene and E-β-Farnesene and T7, Turmeric, β-pinene and E-β-Farnesene.
Air was drawn in through the four orifices which passes in each quadrant by vacuum pump. Predator, C. septempunctata was released in central olfactometer chamber for 8 minutes and was allowed move freely within each region. Olfactometer was rotated at 90° after every two minutes interval. The number of entries and time spent by C. septempunctata in each region of olfactometer was recorded using Olfa software . After every 10 specimens, washed with Lipsol detergent (5% v/v; Bibby Sterilin Ltd., UK), rinsed with 80% ethanol and air dried. Data pertaining to number of entries and time spent by C. septempunctata in each region of olfactometer were recorded. Similar experiment was performed with D. rapae
Statistical analysis
Data pertaining to number of entries and time spent by C. septempunctata and D. rapae in each region of olfactometer was were analysed using Wilcoxon test. The HSD test at 5% level of significance to compare the difference between the means.
Table I.- Number of entries (Mean ± SEM) by male and female Coccinella septempunctata in control and treatment arm of olfactometer.
| Treatment | No of entries | Wilcoxon test (P-value) | |
| Control arm | Treatment arm | ||
| Male | |||
| T1 | 3.10 ± 0.23 | 4.90 ± 0.23 | 0.0004572 |
| T2 | 3.0 ± 0.26 | 5.90 ± 0.28 | 0.0001485 |
| T3 | 3.40 ± 0.22 | 6.80 ± 0.25 | 0.0001358 |
| T4 | 3.20 ± 0.25 | 5.40 ± 0.16 | 0.0001239 |
| T5 | 3.20 ± 0.25 | 5.80 ± 0.20 | 0.0001286 |
| T6 | 3.10 ± 0.23 | 7.20 ± 0.25 | 0.0001399 |
| T7 | 3.20 ± 0.25 | 6.0 ± 0.26 | 0.0001459 |
| Female | |||
| T1 | 3.20 ± 0.20 | 5.20 ± 0.25 | 0.0002962 |
| T2 | 3.30 ± 0.15 | 6.0 ± 0.26 | 0.000115 |
| T3 | 3.30 ± 0.26 | 6.60 ± 0.22 | 0.0001383 |
| T4 | 2.90 ± 0.23 | 5.50 ± 0.17 | 0.0001247 |
| T5 | 3.10 ± 0.23 | 6.0 ± 0.21 | 0.000127 |
| T6 | 3.40 ± 0.22 | 7.0 ± 0.26 | 0.0001383 |
| T7 | 3.30 ± 0.21 | 5.90 ± 0.28 | 0.0001383 |
***, P<0.001; **, P<0.01; *, P<0.05, P< 0.1 and P<1. C. septempunctata response was measured as (Mean±SEM) number of observations in the arms of four-way olfactometer. n=80 individuals tested in each treatment.
Results
Number of entries in arm of olfactometer
Male C. septempunctata
It was found that C. septempunctata exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. From Table I, it was found that male C. septempunctata exhibited the maximum significant preference towards treatment T6 (Wilcoxon’s test, T = 7.20; N = 80; P = 0.000139) as compared to other treatments applied. It was found that the treatment T4 (Wilcoxon’s test, T = 5.40; N = 80; P = 0.000127) was statistically similar to T5 (Wilcoxon’s test, T = 5.80; N = 80; P = 0.000128) which was statistically at par with T2 (Wilcoxon’s test, T = 5.90; N = 80; P = 0.000148). It was observed that C. septempunctata exhibited the minimum significant preference towards treatment T1 (Wilcoxon’s test, T = 4.90; N = 80; P = 0.024) as compared to other treatments applied. The preference of C. septempunctata towards treatment T7 was (Wilcoxon’s test, T = 6.0; N = 80; P = 0.000124) which was statistically similar to T3 (Wilcoxon’s test, T = 6.80; N = 80; P = 0.000138) (Table I).
Female C. septempunctata
It was found that C. septempunctata exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. From Table I, it was found that female C. septempunctata exhibited the maximum significant preference towards treatment T6 (Wilcoxon’s test, T = 7.0; N = 80; P = 0.000138) as compared to other treatments applied. It was found that the treatment T2 (Wilcoxon’s test, T = 6.0; N = 80; P = 0.000138) was statistically similar to T5 (Wilcoxon’s test, T = 6.0; N = 80; P = 0.000127) which was statistically at par with T3 (Wilcoxon’s test, T = 6.60; N = 80; P = 0.000138). It was observed that C. septempunctata exhibited the minimum significant preference towards treatment T1 (Wilcoxon’s test, T = 5.20; N = 80; P = 0.024) as compared to other treatments applied. The preference of C. septempunctata towards treatment T4 was (Wilcoxon’s test, T = 5.50; N = 80; P = 0.000124) which was statistically similar to T7 (Wilcoxon’s test, T = 5.90; N = 80; P = 0.000138) (Table II).
Table II.- Number of entries (Mean ± SEM) by Diaeretiella rapae in control and treatment arm of olfactometer.
| Treatment 3% concentration | No. of entries | Wilcoxon test (P-value) | |
| Control arm | Treatment arm | ||
| T1 | 2.20 ± 0.25 | 3.90 ± 0.28 | 0.00109 |
| T2 | 2.30 ± 0.26 | 5.50 ± 0.34 | 0.0001494 |
| T3 | 2.40 ± 0.22 | 7.10 ± 0.28 | 0.0001383 |
| T4 | 2.50 ± 0.27 | 5.70 ± 0.21 | 0.0001086 |
| T5 | 2.10 ± 0.28 | 6.50 ± 0.17 | 0.0001301 |
| T6 | 2.60 ± 0.27 | 7.50 ± 0.18 | 0.0001254 |
| T7 | 2.0 ± 0.21 | 5.90 ± 0.23 | 0.000127 |
***, P<0.001; **, P<0.01; *, P<0.05; P< 0.1 and P<1. D. rapae response was measured as (Mean±SEM) number of observations in the arms of four-way olfactometer. n=80 individuals tested in each treatment.
Diaeretiella rapae
It was found that D. rapae exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. Among the seven treatments tested, D. rapae exhibited the maximum significant preference in treatment T6 (Wilcoxon’s test, T = 7.50, N = 80, p=0.00012), which was statistically at par with T3 (Wilcoxon’s test, T = 7.10, N = 80, p=0.00013). Whereas, the preference of D. rapae towards treatment T5 was (Wilcoxon’s test, T = 6.50; N = 80; P = 0.00013). It was found that the treatment T2 (Wilcoxon’s test, T = 5.50; N = 80; P = 0.00014) was statistically similar to T4 (Wilcoxon’s test, T = 5.70; N = 80; P = 0.00010) which was statistically at par with T7 (Wilcoxon’s test, T = 5.90; N = 80; P = 0.000148). Preference of D. rapae towards treatment T1 was minimum (Wilcoxon’s test, T = 3.90; N = 80; P = 0.00109) (Table II).
Time spent in arm of olfactometer
Male C. septempunctata
It was found that Coccinella septempunctata exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. From Table III, it was found that male C. septempunctata exhibited the maximum significant preference towards treatment T6 (Wilcoxon’s test, T = 6.13; N = 80; P = 1.083) as compared to other treatments applied. It was found that the treatment T6 was statistically similar to T3 (Wilcoxon’s test, T = 6.05; N = 80; P = 0.00018). It was observed that C. septempunctata exhibited the minimum significant preference towards treatment T1 (Wilcoxon’s test, T = 3.30; N = 80; P = 0.024) as compared to other treatments applied. The preference of C. septempunctata towards treatment T4 was (Wilcoxon’s test, T = 4.71; N = 80; P = 0.000179) which was statistically similar to T2 (Wilcoxon’s test, T = 4.55; N = 80; P = 0.00018). The preference of C. septempunctata towards treatment T7 was (Wilcoxon’s test, T = 5.21; N = 80; P = 0.000179) which was statistically similar to T5 (Wilcoxon’s test, T = 5.50; N = 80; P = 0.00018) (Table III).
Table III.- Time spent (Mean ± SEM) by male and female Coccinella septempunctata in control and treatment arm of olfactometer.
| Treatment | Time spent | Wilcoxon test (P-value) | |
| Control arm | Treatment arm | ||
| Male | |||
| T1 | 2.8 ± 0.15 | 3.30 ± 0.06 | 0.02479 |
| T2 | 2.52 ± 0.06 | 4.55 ± 0.11 | 0.0001806 |
| T3 | 1.38 ± 0.06 | 6.05 ± 0.09 | 0.0001806 |
| T4 | 2.65 ± 0.10 | 4.71 ± 0.11 | 0.0001796 |
| T5 | 1.89 ± 0.09 | 5.50 ± 0.09 | 0.0001817 |
| T6 | 2.37 ± 0.03 | 6.13 ± 0.03 | 1.083e-05 |
| T7 | 2.10 ± 0.07 | 5.21 ± 0.04 | 1.083e-05 |
| Female | |||
| T1 | 2.54 ± 0.17 | 3.69 ± 0.18 | 1.083e-05 |
| T2 | 2.21 ± 0.10 | 5.02 ± 0.16 | 0.0001817 |
| T3 | 1.34 ± 0.04 | 6.12 ± 0.1 | 0.0001806 |
| T4 | 2.33 ± 0.05 | 4.89 ± 0.2 | 1.083e-05 |
| T5 | 1.81 ± 0.09 | 5.02 ± 0.12 | 0.0001796 |
| T6 | 1.26 ± 0.04 | 6.23 ± 0.11 | 1.083e-05 |
| T7 | 1.67 ± 0.10 | 5.75 ± 0.13 | 0.0001806 |
***, P<0.001; **, P<0.01; *, P<0.05, P< 0.1 and P<1. C. septempunctata response was measured as (Mean±SEM) number of observations in the arms of four-way olfactometer. n=80 individuals tested in each treatment.
Female C. septempunctata
It was found that Coccinella septempunctata exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. From Table III, it was found that female C. septempunctata exhibited the maximum significant preference towards treatment T6 (Wilcoxon’s test, T = 6.23; N = 80; P = 1.083) as compared to other treatments applied. It was found that the treatment T6 was statistically similar to T3 (Wilcoxon’s test, T = 6.12; N = 80; P = 0.00018). It was observed that C. septempunctata exhibited the minimum significant preference towards treatment T1 (Wilcoxon’s test, T = 3.69; N = 80; P = 1.083) as compared to other treatments applied. The preference of C. septempunctata towards treatment T4 was (Wilcoxon’s test, T = 4.89; N = 80; P = 1.083). The preference of C. septempunctata towards treatment T2 was (Wilcoxon’s test, T = 5.02; N = 80; P = 0.00018) which was statistically similar to T5 (Wilcoxon’s test, T = 5.02; N = 80; P = 0.000179) which was statistically at par with T7 (Wilcoxon’s test, T = 5.21; N = 80; P = 0.000181).
Table IV.- Time spent (Mean ± SEM) by Diaeretiella rapae in control and treatment arm of olfactometer.
| Treatment 3% concentration | Time spent | Wilcoxon Test (P-value) | |
| Control arm | Treatment arm | ||
| T1 | 2.07 ± 0.22 | 3.39 ± 0.14 | 0.0004943 |
| T2 | 1.99 ± 0.23 | 4.48 ± 0.25 | 0.0001806 |
| T3 | 1.31 ± 0.09 | 6.35 ± 0.08 | 0.0001817 |
| T4 | 2.21 ± 0.18 | 4.58 ± 0.14 | 1.083e-05 |
| T5 | 1.69 ± 0.13 | 5.68 ± 0.15 | 0.0001817 |
| T6 | 1.12 ± 0.03 | 6.39 ± 0.03 | 1.083e-05 |
| T7 | 1.93 ± 0.21 | 5.16 ± 0.3 | 1.083e-05 |
***, P<0.001; **, P<0.01; *, P<0.05; P< 0.1 and P<1. D. rapae response was measured as (Mean ± SEM) number of observations in the arms of four-way olfactometer. n = 80 individuals tested in each treatment.
Diaeretiella rapae
It was found that D. rapae exhibited a significant response to choose treatment arm over the control arm in all treatments tested in olfatometer bioassay. Among the seven treatments tested, D. rapae exhibited the maximum significant preference in treatment T6 (Wilcoxon’s test, T = 6.39, N = 80, P = 1.083), which was statistically at par with T3 (Wilcoxon’s test, T = 6.35, N = 80, P = 0.00018). It was found that the treatment T7 (Wilcoxon’s test, T = 5.16; N = 80; P = 1.083) was statistically similar to T5 (Wilcoxon’s test, T = 5.68; N = 80; P = 0.00018). It was observed that the treatment T2 (Wilcoxon’s test, T = 4.48; N = 80; P = 0.00014) which was statistically at par with T4 (Wilcoxon’s test, T = 4.58; N = 80; P = 0.000148). The preference of D. rapae towards treatment T1 was minimum (Wilcoxon’s test, T = 3.39; N = 80; P = 0.00049) (Table IV).
Discussion
Olfactory cues play an important role in foraging behaviour of natural enemies i.e. in ladybird foraging behaviour ; . Seagraves (2009) reported that C. septempunctata orient themselves towards prey using olfactory cues. Aphid cornicle secretions containing semiochemicals are attracting cues for C. septempunctata. Han and Chen (2002) found that seven spotted ladybird exhibited significant differences toward odor source when it was exposed to crushed 1200 tea aphids in a Y tube olfactometer. Seagraves (2009) reported that the attraction of coccinellids is related to prey density. Therefore, ladybird olfactory response by EBF is a dose dependent factor . Francis et al. (2004) found that coccinellids do not respond towards EBF when its amount is less than 2µg. Al-Abassi et al. (2000) found that attractivity of EBF for C. septempunctata decreases with increasing amount of α-caryophyllene.
Leroy et al. (2012) found that aphid associated semiochemicals, i.e., [E]-β-farnesene, α-pinene, β-pinene, Z,E-nepetalactone and (-)-β-caryophyllene are potential attractants for Harmonia axyridis. Alarm pheromone component (E)- β-farnesene, either emitted by aphids and plants is an attractant for coccinellids, C. septempunctata ; , Adalia bipunctata , Hippodamia convergens and H. axyridis ; . Aphid alarm pheromone (α-pinene and β-pinene formulated in paraffin oil) are attractants for the Asian lady beetle. It was found that alarm pheromone can attract 70.0% of tested females in the wind-tunnel experiments. The volatile α-pinene can significantly attract the H. axyridis .
It was found that (Z)-3-hexenol and (E)-2-hexenal act as a synomone for the coccinellids C. septempunctata . Alhmedi et al. (2010) found that H. axyridis do not show any behavourial response when (E)-β-farnesene, (Z)-3-hexenol and β-pinene is in amount of 5 μg in olfactory experiments.
Ladybirds can arrive in crop plants before aphid migrants via plant volatile chemicals (Honeˇk and Martinkova´, 2008; ; . The continuous emission of plant volatiles affect ladybird searching behaviour. This phenomenon contributes to broader ecological significance of induced plant responses towards biotic stress .
Vekaria and Patel (2000) found that different treatments of neem extracts were less toxic towards D. rapae and C. septempunctata as compared to chemical insecticides. Halder et al. (2010) tested the efficacy of chloroform, methanol extracts and oils from nayantara, Vinca rosea and bottle brush against Lipaphis erysimi and C. septempunctata under laboratory condition. It was found that plant extracts and oil have not exhibited mortality to C. septempunctata up to ten days after feeding the treated L. erysimi. Chakraborty and Ghosh (2010) tested the toxicity of Bacillus thuringiensis, Beauveria bassiana, malathion and Neemactin and Avermectin on ladybeetle. It was found that Neemactin and Avermectin were least toxic as compared to six insecticide formulations tested.
The results revealed that T6 (β-pinene, E-β-Farnesene) exhibited highest mean number entries of C. septempunctata (6.13%) and highest mean time spend (6.23%) as compared to two other treatments applied. Results depicted that alarm pheromone is a promising biopesticide and attractant for several aphidophagous predators including C. septempunctata.
Hymenopteran parasitoids are important natural enemies in biological control programs of aphids in diverse crops . Previous studies revealed that parasitoids locate their hosts by semiochemicals emitted from their hosts and from the plants infested by their hosts . Wickremasinghe and van Emden (1992) and Vet and Dicke (1992) found that a number of aphid parasitoids respond and attract towards plant volatiles in olfactometer bioassays. Aphids themselves not attractive towards all parasitoids . Aphid release alarm pheromone from their cornicles when disturbed, which is attractive for some parasitoids .
Micha et al. (2000) found that the parasitoid orientation behavior in olfactometer bioassay is influenced by the odours emitted from infested plant baits. Some parasitoids respond to aphid induced plant volatiles and some remain unresponsive to odors of host plant ; . Heil (2008) reported that parasitoids have ability to distinguish between aphid infested and uninfested plants, and they can also distinguish between plants infested by different herbivores. Takemoto et al. (2009) found that volatiles released from Vicia faba infested by Acyrthosiphon pisum attract naive Aphidius ervi in a Y-tube olfactometer. Foster et al. (2005) reported that D. rapae spend up to 20 min time interval in the discs treated with EβF. The time spent by D. rapae in EβF treated discs increased with increase in its concentration. D. rapae can move towards high distances from untreated to EβF treated discs. Turlings et al. (2004) found that 90% of endoparasitoid Cotesia marginiventris females stay in odour treated arm. If no odour is offered in olfactometer bioassay, most of females stay in central chamber during 30 min duration. Wyckhuys and Heimpel (2007) found that response potential of aphid parasitoid Binodoxys communis towards certain stimuli was 59, 68, 67, 62, and 62% for odors from Aphis glycines, A. oestlundi, A. monardae, A. nerii, and A. asclepiadis, respectively. In olfactometer bioassays, both male and female A. ervi exhibited more significant time spent in air-stream containing β-phellandrene and caryophyllene as compared to controls .
Our study dipicted that T6 (β-pinene + E-β-Farnesene) exhibited highest mean number entries of D. rapae (7.50%) and highest mean time spend (6.39%) as compared to other treatments applied. Therefore, these semiochemicals are attractive to natural enemies, i.e., predatory beetles ; and parasitoids. Guerrieri et al. (1999) found that herbivore induced volatiles are released by plants is a systemic response. Cortesero et al. (2000) found that release of plant volatiles which attract parasitoid species should be enhanced through plant breeding.
Acknowledgements
The authors are thankful to research support of Dr. Tobby Bruce, Rhothmstat Research Institute, UK and Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi for providing an opportunity to carry out this study.
Statement of conflict of interest
The authors declare no conflict of interest.
References
- Acar, E.B., Medina, J.C., Lee, M.L. and Booth, G.M., 2001. Olfactory behaviour of convergent lady beetles (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Can. Entomol., 133: 389-397. https://doi.org/10.4039/Ent133389-3[CrossRef]
- Al-Abassi, S., Birkett, M.A., Petterson, J., Pickett, J.A., Wadhams, L.J. and Woodcock, C.M., 2000. Response of the seven-spot ladybird to an alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J. chem. Ecol., 26: 1765-1771. https://doi.org/10.1023/A:1005555300476[CrossRef]
- Alhmedi, A., Haubruge, E. and Francis, F., 2010. Intraguild interactions implicating invasive species: Harmonia axyridis as a model species. Biotech. Agron. Soc. Environ., 14: 187-201.
- Araya, J.E., Araya, M. and Guerrero, M.A., 2010. Effects of some insecticides applied in sublethal concentrations on the survival and longevity of Aphidius ervi (Haliday) (Hymenoptera: Aphidiidae) adults. Chilean J. agric. Res., 70: 221-227. https://doi.org/10.4067/S0718-58392010000200005[CrossRef]
- Bhasin, A., Mordue, A.J. and Mordue, W., 2000. Electrophysiological and behavioral identification of host kairomones as olfactory cues for Culicoides impuntatus and C. nubeculosis. Physiol. Ent., 25: 6-16. https://doi.org/10.1046/j.1365-3032.2000.00157.x[CrossRef]
- Bukovinszky, T., Gols, R., Posthumus, M.A., Vet, L.E.M. and van Lenteren, J.C., 2005. Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellén). J. chem. Ecol., 31: 461-480. https://doi.org/10.1007/s10886-005-2019-4[CrossRef]
- Capinera, J.L., 2008. Encyclopedia of entomology, 2nd ed. Springer, Germany, pp. 205. https://doi.org/10.1007/978-1-4020-6359-6[CrossRef]
- Chakraborty, K. and Ghosh, S.K., 2010. Incidence of Coccinella septempunctata in brinjal with some pesticides. Curr. Adv. agric. Sci., 2: 129-130.
- Cortesero, A.M., Stapel, J.O. and Lewis, W.J., 2000. Understanding and manipulating plant attributes to enhance biological control. Biol. Contr., 17: 35-49. https://doi.org/10.1006/bcon.1999.0777[CrossRef]
- Desneux, N., Decourtye, A. and Delpuech, J.M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Ent., 52: 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440[CrossRef]
- Dicke, M., van Poecke, R.M.P. and de Boer, J.G., 2003. Inducible indirect defence of plants: From mechanisms to ecological functions. Basic appl. Ecol., 4: 27-42. https://doi.org/10.1078/1439-1791-00131[CrossRef]
- Foster, S.P., Denholm, I., Thompson, R., Poppy, G.M. and Powell, W., 2005. Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade off. Bull. entomol. Res., 95: 37-46. https://doi.org/10.1079/BER2004336[CrossRef]
- Francis, F., Lognay, G., Gaspar, C. and Haubruge, E., 2004. Olfactory responses to aphid and host plant volatile releases: (E)-b-farnesene an effective allomone for the predator Adalia bipunctata. J. chem. Ecol., 30: 741-755. https://doi.org/10.1023/B:JOEC.0000028429.13413.a2[CrossRef]
- Galvan, T.L., Koch, R.L. and Hutchison, W.D., 2005. Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biol. Contr., 34: 108-114. https://doi.org/10.1016/j.biocontrol.2005.04.005[CrossRef]
- George, D.R., King, L., Donkin, E., Jones, C.E, Croft, P. and Tilley, L.A.N., 2013. Dichotomy of male and female responses to hoverfly-driven cues and floral competition in the parasitoid wasp Aphidius ervi Haliday. Biol. Contr., 67: 539-547. https://doi.org/10.1016/j.biocontrol.2013.08.013[CrossRef]
- Gibson, R.W. and Pickett, J.A., 1983. Wild potato repels aphids by release of aphid alarm pheromone. Nature, 302: 608-609. https://doi.org/10.1038/302608a0[CrossRef]
- Girling, R.D., Hassall, M., Turner, J.G. and Poppy, G.M., 2006. Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae. Ent. Exp. Appl., 120: 1-9. https://doi.org/10.1111/j.1570-7458.2006.00423.x[CrossRef]
- Godfray, H.C.J., 1994. Parasitoids, behavioral and evolutionary ecology. Princeton University Press, Princeton, NJ, USA, pp. 83-210.
- Guerrieri, E., Poppy, G.M., Powell, W., Tremblay, E. and Pennacchio, F., 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J. chem. Ecol., 25: 1247-1261. https://doi.org/10.1023/A:1020914506782[CrossRef]
- Halder, J., Srivastava, C., Dhingra, S. and Dureja, P., 2010. Bioactivity of some plant extracts against mustard aphid, Lipaphis erysimi (Kalt.) and its predator Coccinella septempunctata (Linn.). Pestic. Res. J., 22: 174-176.
- Han, B. and Chen, Z., 2002. Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids, Toxoptera aurantii. J. chem. Ecol., 28: 2203-2220. https://doi.org/10.1023/A:1021045231501[CrossRef]
- Hatano, E., Kunert, G., Michaud, J.P. and Weisser, W.W., 2008. Chemical cues mediating aphid location by natural enemies. Eur. J. Ent., 105: 797-806. https://doi.org/10.14411/eje.2008.106[CrossRef]
- Heil, M., 2008. Indirect defence via tritrophic interactions. New Phytol., 178: 41-61. https://doi.org/10.1111/j.1469-8137.2007.02330.x[CrossRef]
- Hemptinne, J.L., Gaudin, M., Dixon, A.F.G. and Lognay, G., 2000. Social feeding in ladybird beetles: adaptive significance and mechanism. Chemoecology, 10: 149-152. https://doi.org/10.1007/PL00001817[CrossRef]
- Hoballah, M.E. and Turlings, T.C.J., 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. chem. Ecol., 31: 2003-2018. https://doi.org/10.1007/s10886-005-6074-7[CrossRef]
- Honek, A. and Martinkova, Z., 2008. Why is Coccinella septempunctata so successful (a point of view). Eur. J. Ent., 105: 1-12. https://doi.org/10.14411/eje.2008.001[CrossRef]
- Kalule, T. and Wright, D.J., 2004. The influence of cultivar and cultivar-aphid odours on the olfactory response of the parasitoid Aphidius colemani. J. appl. Ent., 128: 120-125.
- Leroy, P.D., Schillings, T., Farmakidis, J., Heuskin, S., Lognay, G., Verheggen, F.J., Brostaux, Y., Haubruge, E. and Francis, F., 2012. Testing semiochemicals from aphid, plant and conspecific: attraction of Harmonia axyridis. Insect Sci., 19: 372-382. https://doi.org/10.1111/j.1744-7917.2011.01449.x[CrossRef]
- Markovic, D., Glinwood, R., Olsson, U. and Ninkovic, V., 2014. Plant response to touch affects the behaviour of aphids and ladybirds. Arthropod-Pl. Interact., 8: 171-181. https://doi.org/10.1007/s11829-014-9303-6[CrossRef]
- Mattiacci, L., Rocca, B.A., Scascighini, N., D’Alessandro, M., Hern, A. and Dorn, S., 2001. Systemically induced plant volatiles emitted at the time of “danger”. J. chem. Ecol., 27: 2233-2252. https://doi.org/10.1023/A:1012278804105[CrossRef]
- Micha, S.G. and Wyss, U., 1995. The importance of plant odours for host searching of Aphidius uzbekistanicus (Hymenoptera, Aphidiidae), a parasitoid of the grain aphid (Sitobion avenae). Gesunde Pflanzen, 47: 300-307.
- Micha, S.G. and Wyss, U., 1996. Aphid alarm pheromone (E)-beta-farnesene: A host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology, 7: 132-139. https://doi.org/10.1007/BF01245965[CrossRef]
- Micha, S.G., Kistenmacher, S., Mölck, G. and Wyss, U., 2000. Tritrophic interactions between cereals, aphids and parasitoids: discrimination of different plant-host complexes by Aphidius rhopalosiphi (Hymenoptera: Aphidiidae). Eur. J. Ent., 97: 539-543. https://doi.org/10.14411/eje.2000.083[CrossRef]
- Mondor, E. and Roitberg, B., 2000. Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior? J. Insect Behav., 3: 321-329. https://doi.org/10.1023/A:1007754000862[CrossRef]
- Moraes, M.C.B., Laumann, R., Sujii, E.R., Pires, C. and Borges, M., 2005. Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi. Ent. Exp. Appl., 115: 227-237. https://doi.org/10.1111/j.1570-7458.2005.00290.x[CrossRef]
- Nazzi, F., 1996. Olfa. A computer program for collecting and analyzing behavioral data with the four-armed olfactometer. Exeter Software, Setauket, New York.
- Ninkovic, V., Abassi, S.A. and Petterson, J., 2001. The influence of aphid-induced plant volatiles in ladybird beetle searching behavior. Biol. Contr., 21: 191-195. https://doi.org/10.1006/bcon.2001.0935[CrossRef]
- Ninkovic, V., Al Abassi, S., Ahmed, E., Glinwood, R. and Pettersson, J., 2011. Effect of within-species plant genotype mixing on habitat preference of a polyphagous insect predator. Oecologia, 166: 391-400. https://doi.org/10.1007/s00442-010-1839-2[CrossRef]
- Ninkovic, V. and Pettersson, J., 2003. Searching behaviour of the seven spotted ladybird, Coccinella septempunctata-effects of plant odour interaction. Oikos, 100: 65-70. https://doi.org/10.1034/j.1600-0706.2003.11994.x[CrossRef]
- Osawa, N., 2000. Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul. Ecol., 42: 115-127. https://doi.org/10.1007/PL00011990[CrossRef]
- Pettersson, J., Ninkovic, V., Glinwood, R., Abassi, S.A., Birkett, M., Pickett, J. and Wadhams, L., 2008. Chemical stimuli supporting foraging behaviour of Coccinella septempunctata L. (Coleoptera: Coccinellidae): volatiles and allelobiosis. Appl. Ent. Zool., 43: 315-321. https://doi.org/10.1303/aez.2008.315[CrossRef]
- Pettersson, J., Ninkovic, V., Glinwood, R., Birkett, M.A. and Pickett, J.A., 2005. Foraging in complex environment-semiochemicals support searching behaviour of the seven spot ladybird. Eur. J. Ent., 102: 365-370. https://doi.org/10.14411/eje.2005.053[CrossRef]
- Pettersson, J., 1970. An aphid sex attractant in biological studies. Ent. Scand., 1: 63-73. https://doi.org/10.1163/187631270X00357[CrossRef]
- Pickett, J.A., Wadhams, L.J. and Woodcock, C.M., 1998. Insect supersense: Mate and host location by insects as model systems for exploiting olfactory interactions. The Biochemist, 20: 8-13.
- Pickett, J.A. and Griffith, D.C., 1980. Composition of aphid alarm pheromones. J. chem. Ecol., 6: 349-360. https://doi.org/10.1007/BF01402913[CrossRef]
- Poppy, G.M., 1997. Tritrophic interactions: Improving ecological understanding and biological control. Endeavour, 21: 61-65. https://doi.org/10.1016/S0160-9327(97)01042-9[CrossRef]
- Rahmani, S. and Bandani, A.R., 2013. Sublethal concentrations of thiamethoxam adversely affect life table parameters of the aphid predator, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Crop. Prot., 54: 168-175. https://doi.org/10.1016/j.cropro.2013.08.002[CrossRef]
- Reuter, O.M., 1913. Habits and instincts of insects. Friedlander, Berlin, pp. 1-20.
- Riddick, E.W., Aldrich, J.R., Deand, M.A. and Davis, J.C., 2000. Potential for modifying the behavior of the multicolored asian lady beetle (Coleoptera: Coccinellidae) with plant-derived natural products. Annls. entomol. Soc. Am., 93: 1314-1321. https://doi.org/10.1603/0013-8746(2000)093[1314:PFMTBO]2.0.CO;2[CrossRef]
- Roditakis, E., Couzin, I.D., Barlow, K., Franks, N.R. and Charnley, A.K., 2000. Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour. Ann. appl. Biol., 137: 329-335. https://doi.org/10.1111/j.1744-7348.2000.tb00074.x[CrossRef]
- Röse, U.S.R., Lewis, W.J. and Tumlinson, J.H., 1998. Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps. J. chem. Ecol., 24: 303-319. https://doi.org/10.1023/A:1022584409323[CrossRef]
- Sabelis, M., Takabayashi, J., Janssen, A., Kant, M., van Wijk, M., Sznajder, B., Aratchige, N., Lesna, I., Belliure, B. and Schuurink, R., 2007. Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities. In: Ecological communities: Plant mediation in indirect interaction webs (eds. T. Ohgushi, T. Craig and P. Price). Cambridge University Press, Cambridge, pp. 188-217. https://doi.org/10.1017/CBO9780511542701.010[CrossRef]
- Seagraves, M.P., 2009. Lady beetle oviposition behavior in response to the trophic environment. Biol. Contr., 51: 313-322. https://doi.org/10.1016/j.biocontrol.2009.05.015[CrossRef]
- Sengonca, C. and Liu, B., 1994. Responses of the different instar predator, Coccinella septempunctata L. (Coleoptera: Coccinellidae), to the kairomones produced by the prey and non-prey insects as well as the predator itself. Z. Pflanzenk. Pflanzen., 101: 173-177.
- Shiojiri, K., Takabayashi, J., Yano, S. and Takafuji, A., 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol., 43: 23-29. https://doi.org/10.1007/PL00012011[CrossRef]
- Storeck, A., Poppy, G.M., van Emden, H.F. and Powell, W., 2000. The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Ent. Exp. Appl., 97: 41-46. https://doi.org/10.1046/j.1570-7458.2000.00714.x[CrossRef]
- Takemoto, H., Powell, W., Pickett, J., Kainoh, Y. and Takabayashi, J., 2009. Learning is involved in the response of parasitic wasps Aphidius ervi (Haliday) (Hymenoptera: Braconidae) to volatiles from a broad bean plant, Vicia faba (Fabaceae), infested by aphids Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Appl. Ent. Zool., 44: 23-28. https://doi.org/10.1303/aez.2009.23[CrossRef]
- Turlings, T.C.J., Wackers, F., Vet L.E.M., Lewis, W.J. and Tumlinson, J.H., 1993. Learning of host finding cues by hymenopterous parasitoids. In: Insect learning: Ecological and evolutionary perspectives (eds. D.R. Papaj and A.C. Lewis). Chapman & Hall, NY, pp. 51-78. https://doi.org/10.1007/978-1-4615-2814-2_3[CrossRef]
- Turlings, T.J., Davison, A.C. and Tamo, C., 2004. A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol. Ent., 29: 45-55. https://doi.org/10.1111/j.1365-3032.2004.0362.x[CrossRef]
- van Poecke, R.M., Roosjen, M., Pumarino, L. and Dicke, M., 2003. Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species. Ent. Exp. Appl., 107: 229-236. https://doi.org/10.1046/j.1570-7458.2003.00060.x[CrossRef]
- Vekaria, M.V. and Patel, G.M., 2000. Bioeffficacy of botanicals and certain chemical insecticides and their combinations against the mustard aphid, Lipaphis erysimi. Ind. J. Ent., 62: 150-158.
- Verheggen, F.J., Fagel, Q., Heuskin, S., Lognay, G., Francis, F. and Haubruge, E., 2007. Electrophysiological and behavioral responses of the multicolored Asian lady beetle, Harmonia axyridis Pallas, to sesquiterpene semiochemicals. J. chem. Ecol., 33: 2148-2155. https://doi.org/10.1007/s10886-007-9370-6[CrossRef]
- Vet, L.E.M. and Dicke, M., 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Ent., 37: 141-172. https://doi.org/10.1146/annurev.en.37.010192.001041[CrossRef]
- Wabale, A.S. and Kharde, M.N., 2010. Bioefficacy of plant extracts against sugarcane woolly aphid (Ceratovacuna lanigera Zehntener). Asian J. exp. biol. Sci., 1: 592-595.
- Webster, B., Bruce, T., Pickett, J. and Hardie, J., 2010. Volatiles functioning as host cues in a blend become non host cues when presented alone to the black bean aphid. Anim. Behav., 79: 451-457. https://doi.org/10.1016/j.anbehav.2009.11.028[CrossRef]
- Wickremasinghe, M.G.V. and van Emden, H.F., 1992. Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiol. Ent., 17: 297-304. https://doi.org/10.1111/j.1365-3032.1992.tb01025.x[CrossRef]
- Wyckhuys, K.A.G. and Heimpel, G.E., 2007. Response of the soybean aphid parasitoid Binodoxys communis to olfactory cues from target and non-target host-plant complexes. Ent. Exp. Appl., 123: 149-158. https://doi.org/10.1111/j.1570-7458.2007.00532.x[CrossRef]
- Xue, J., He, J. and Xie, Y., 2008. Attractive effect of plant volatiles on Harmonia axyridis (Pallas). Chinese J. appl. environ. Biol., 4: 494-498.
- Young, S., David, C.T. and Gibson, G., 1987. Light measurement for entomology in the field and laboratory. Physiol. Ent., 12: 373-379. https://doi.org/10.1111/j.1365-3032.1987.tb00763.x[CrossRef]
- Zhu, J., Cossé, A.A., Obrycki, J.J., Boo, K.S. and Baker, T.C., 1999. Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata and the green lacewing, Chrysoperla carnea to semiochemicals released from their prey and host plant: electroantennogram and behavioral responses. J. chem. Ecol., 25: 1163-1177. https://doi.org/10.1023/A:1020846212465[CrossRef]
- Zhu, J.W. and Park, K.C., 2005. Methyl salicylate, a soybean aphid induced plant volatile attractive to the predator Coccinella septempunctata. J. chem. Ecol., 31: 1733-1746. https://doi.org/10.1007/s10886-005-5923-8[CrossRef]
- Zhu, J.J., Obrycki, J., Ochieng, S.A., Baker T.C., Pickett, J.A. and Smiley, D., 2005. Attraction of two lacewing species to volatiles produced by host plants and aphid prey. Naturwissenschaften, 92: 277-281. https://doi.org/10.1007/s00114-005-0624-2[CrossRef]
Services
Article usage statistics
Loading…