- Top of page
- 1 INTRODUCTION
- 2 MATERIALS AND METHODS
- 3 RESULTS
- 4 Discussion
Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae), the potato tuberworm, is a key pest causing severe damage to potato, which, in turn, is a food crop of essential importance worldwide. The pest is indigenous to South America but at present is spreading in all the potato production areas in temperate and subtropical climatic regions. Gravid females can lay eggs on foliage and soil next to the host plant or directly near the eye buds of tubers exposed through soil cracks or when they are kept under storage. Larvae develop endophytically in leaves, stems and tubers and feed on different Solanaceae, with a preference for potato (Solanum tuberosum L.). In addition to direct damage, galleries inside tubers facilitate the entrance of pathogens responsible for further severe losses, which may reach up to 100% under inadequate storage conditions, as often happens in developing countries.
Until now, control of this pest has been carried out mainly using chemical insecticides, which are harmful to beneficial insects and cause pesticide resistance and environmental concerns.[2, 3] As for semiochemicals, the female sex pheromone of P. operculella has been identified as a mixture of (E,Z,Z)-4,7,10-tridecatrienil acetate [(E,Z,Z)-4,7,10-13:Ac] and (E,Z)-4,7-tridecadienil acetate [(E,Z)-4,7-13:Ac].[4-6] Sex pheromone has been successfully employed in integrated pest management programmes using traps for pest monitoring, whereas pheromone-based control techniques, such as mass trapping, attract-and-kill and mating disruption, are feasible[7-9] but not always satisfactory and not yet commercially viable. In spite of the great economic importance of P. operculella, little attention has been paid to the possible use of plant volatiles in control methods. Behavioural studies using plant material indicated that host plant recognition and selection by gravid females are mediated by chemical cues,[10-12] while roughness of tuber surface is considered to be an important factor affecting the subsequent choice of the oviposition site.[13, 14] Two electroantennographic (EAG) studies showed the capability of the peripheral olfactory system of potato tuberworm adults to perceive a broad range of volatiles identified from potato leaves and tubers.[11, 15] High EAG sensitivity to green-leaf volatiles, particularly aldehydes and alcohols, has been found, although there are some apparent inconsistencies in the rank order of EAG responses to either single compounds or classes of chemicals.[11, 15]
Long sensilla trichodea are the most abundant olfactory structures on the surface of both male and female antennae of the potato tuberworm and the pink bollworm, another important pest of the Gelechiidae family. However, no studies aimed at characterising male and female olfactory receptor neurons (ORNs) housed in the antennal sensilla trichodea of potato tuberworm have been carried out.
Hence, the goal of this study was to increase knowledge of the sensitivity of the P. operculella peripheral olfactory system to some electrophysiologically active host plant volatiles, previously identified, by single-cell recording (SCR) from sensilla trichodea ORNs of both sexes. Moreover, the effects of increasing concentrations of the most SCR-active compounds on the egg-laying behaviour of gravid females were assessed using a no-choice experimental design. Finally, the potential of one of the most bioactive compounds to disrupt potato tuberworm oviposition was evaluated in a traditional warehouse for potato storage.
- Top of page
- 1 INTRODUCTION
- 2 MATERIALS AND METHODS
- 3 RESULTS
- 4 Discussion
In potato tuberworm females, long sensilla trichodea apparently function as broad-spectrum sensors for a great number of odours ranging from plant volatiles to pheromone compounds. The authors could not with certainty distinguish responses of single olfactory cells, and therefore were unable to determine the degree of specificity of individual receptor neurons. However, the ability of females to detect their own sex pheromone has already been demonstrated with both electrophysiological and behavioural experiments in several species of Lepidoptera, i.e. Trichoplusia ni (Hübner), Choristoneura fumiferana (Clemens), Adoxophyes orana (Fischer von Röslerstamm), Spodoptera littoralis (Boisduval) and Spodoptera frugiperda (Smith),[23, 24] Euplagia (Panaxia) quadripunctaria (Poda), Cydia splendana (Hübner) and Cydia fagiglandana (Zeller) and Cydia pomonella (L.),[27, 28] and it has been proposed that this perception could play a role in the optimisation of pheromone production and in the spatial dispersion of calling females over the host plants.[21, 22, 29, 30]
Long sensilla trichodea located on the surface of male antennae mainly function as specific pheromone receptors. They house at least two different olfactory cells specialised to detect only one of the components of the female sex pheromone, as reported for other lepidopteran species.[26, 31, 32] It is worth noting that these specialised male receptor neurons occasionally but selectively respond to host plant compounds with chemical structures not related to those of pheromones, or that other neurons with different response specificities are possibly sometimes also present in these sensilla. Moreover, it cannot be ruled out that spikes from neighbouring sensilla have also been recorded. The possible existence of either sensilla or receptor cells responding both to plant volatiles and pheromone components might supply further interpretations concerning the reported ability of plant compounds to modulate the behavioural responses to pheromones in insect species. Host plant volatiles can indeed synergise the attractant power of a synthetic sex pheromone but can also have inhibitory or repellent effects that disrupt insect responses to pheromones.[34-42] Therefore, these interactions in odour perception at a peripheral level need to be carefully considered when setting up new semiochemically based monitoring or control methods.
In the no-choice behavioural bioassay the four most SCR-active volatiles from potato, hexanal, octanal, nonanal and 1-octen-3-ol strongly disrupted the oviposition site selection process by potato tuberworm females when individually applied at concentrations considerably above their production in intact and healthy plant tissues. This negative effect of unbalanced amounts of individual host plant volatiles on moth's egg-laying behaviour is consistent with the observation that in polyphagous insects the absolute and relative amounts of ubiquitous plant volatiles are critical factors in host selection.[43-46] Moreover, such a disruptive effect may be due to the insect's ability to avoid a source of toxic compounds. It is well known that the emission of green-leaf volatiles, including short-chained aliphatic aldehydes, alcohols and esters, dramatically increases when the plant tissues are wounded. These compounds are produced through the hydroperoxide lyase pathway of oxylipin metabolism in response to mechanical and herbivory damage and can play a major role in plant defence. For example, aliphatic aldehydes are known to possess fumigant and contact[49, 50] and repellent effects,[51, 52] depending on the dose, against various insect pests, including potato tuberworm females in laboratory oviposition bioassays. Moreover, some of them were found to inhibit pathogenic fungi[53, 54] and bacteria. Interestingly, synthetic plant volatiles, either corresponding (octanal and nonanal) or chemically related, (Z)-3-hexenol and (E)-2-hexenal, to those selected in the present study, were also shown to attract beneficial insects when deployed at high dosages in different agroecosystems.[56, 57] Moreover, potato tuberworm females are attracted to volatiles released by intact potato tubers but not to those from tubers damaged by conspecific larvae, which, in turn, orientate the natural enemy Orius insidiosus (Say).
In no-choice conditions, the olfactory cues from tubers were not able to enhance potato tuberworm oviposition in comparison with a control represented by an adequate physical substrate for oviposition, as demonstrated in previous studies,[13, 14] whereas the same odour has been shown to mediate female attraction to the plant at longer range.[11, 12] This suggests that potato tuberworm females probably use different cues for host plant recognition and oviposition site location respectively.
The experiments conducted under conventional storage conditions confirmed the results of laboratory assays. Octanal was preferred to hexanal because, even though slightly less effective, it has a lower volatility (octanal vapour pressure 1.2 mmHg at 20–25 °C, hexanal vapour pressure 11 mmHg at 20–25 °C) and hence is more suitable for a longer release duration in practical applications. In the warehouse, octanal elicited a strong decrease in the number of eggs laid compared with the untreated control, both when dispensers were directly deployed on potatoes and when tubers were 2.5 m apart from the treated side, probably as a result of a homogeneous dispersion of the compound in the surroundings. The present results therefore suggest the possibility of avoiding the direct contact of octanal with stored potatoes, and even of using a relatively low density of semiochemical-baited dispensers. In South-East Asia, repellent plant materials applied as dried leaves or powders just to cover stored-tuber bulks are reported to be an effective control strategy to prevent P. operculella infestation.[59-61]
In conclusion, this work has provided new information on the olfactory system of potato tuberworm, with particular attention to the perception of intra- and interspecific semiochemicals by long sensilla trichodea in both sexes. Moreover, laboratory and semi-field behavioural studies have shown that, among alternative botanical control means,[59, 62] the use of synthetic plant volatiles, i.e. common short- and straight-chained aldehydes and alcohols, as host recognition disruptant and/or oviposition deterrent for potato tuberworm appears to be feasible under potato storage conditions.
Further studies are now required to define large-scale application methods utilising these bioactive compounds against potato tuberworm.