Morphological plant defences

Trichomes

The first plant organs contacted during the preliminary stages of settling on a host are surface hairs or trichomes. Trichomes are epidermal appendages of diverse forms and structures, such as non-glandular hairs, scales, or pelt hairs. Trichomes affect the insect behaviour in general by providing a barrier that prevents small arthropods from landing directly on the plant surface and thereby interfering with movement and feeding. The densities of trichomes on the buds and leaf surface of some cultivars also deter feeding and sometimes oviposition.

Leaf trichome density and position may act as a physical obstacle to aphid feeding. The high trichome density on the leaf veins could prevent the aphid from finding a suitable feeding site (Oberholster 2002-2003).

Surface waxes

Plant leaves are protected against desiccation, insect predation and disease by a layer of surface waxes over the epicuticle. Epicuticular waxes affect the feeding behaviour of insects, particularly the settling of probing insects, acting as either phagostimulants or feeding deterrents. (Al-Ayedh 1997).

The chemistry of wax differs from plant to plant, but the most commonly occurring components are alkanes, primary and secondary alcohols and ketones, sometimes small amount of sugars and amino acids (Bernays and Chapman 1994).

Alkanes are amongst the commonest constituents of all plant waxes. Insects possess the sensory apparatus to detect these chemicals by contact or olfaction. (Al-Ayedh 1997).

2.2.2. Semiochemicals

Semiochemicals are molecular signals mediating interactions between organisms, either of the same species (pheromones) or between different species (allelochemicals) (Hooper and Pickett 2004).

Pheromones

Pheromones are important in the familiar mating response and they can affect insect behaviour as well (Hooper and Pickett 2004).

The main groups of aphid pheromones are:

 Sex pheromones

 Alarm pheromones

 Aggregation pheromones

Aphid sex pheromones are released by the sexual females to attract males and increase the success of mating. The pheromones are produced in glandular epidermal cells on the tibiae of the hind legs of the sexual females. The olfactory receptors are located on the third forth and sometimes on the fifth antennal segments of the male aphids (Hardie et al.

1999).

Aphid alarm pheromones are released when, for example, they are disturbed by a predator, and the response behaviour ranges from removal of mouthparts from the plant and moving away, to running, dropping off the plant and even attacking the predator with frontal horns, although not all aphids in a group respond. Nymphs in the early developmental stages do not respond to alarm pheromones because the risk of predation is lower than the risk involved in ceasing to feed and dropping from the plant.

Droplets secreted from the cornicles contain two types of material; a minor volatile, which rapidly vaporizes comprises the alarm pheromone and a rapidly setting waxy fraction, which is an irritant to predators and parasitoids and can interfere with moulting (Hardie et al. 1999).

Aggregation pheromones are behaviour modifying odours produced by winged aphids; it is attractive to other winged forms but repellent to wingless forms. Such behaviour may be due to host plant characteristics, which determine suitable feeding sites (Hardie et al.

1999).

Kairomones are aphid pheromones that are used by parasitoids and predators. For example, the aphid sex pheromones attracts not only males of certain aphid species, but also female parasitoid wasps and the alarm pheromone indicates the presence of aphids in the local area and stimulates searching behaviour in predators and parasitoids (Hardie et al.

1999).

Allelochemicals

The attraction of insects to plants and other organisms involves detection of specific semiochemicals or specific ratios of these usually volatile semiochemicals. The avoidance of unsuitable hosts can involve the detection of specific semiochemicals associated with non-host taxa (Pickett et al. 2005, Hooper and Pickett 2004).

An undamaged plant maintains a baseline level of volatile metabolites that are released from the surface of the leaf or from accumulated storage sites in the leaf. These chemicals reserves can include monoterpenes, sesquiterpenes and aromatics, which are stored in specialized glands or trichomes. Emissions of volatiles are often synchronized with the light cycle generally showing low emission at night and a high level during the periods of maximal photosynthesis. The volatiles released by an insect damaged plant are different from those of undamaged or mechanically damaged plants. Around the damaged area, systemic volatiles are synthesized and a mobile chemical messenger transmits information to the distal leaves and activates several defence responses in the host plant (Paré and Tumlison 1999). Semiochemicals are also used by parasitic insects and other predators of aphids to locate the host plants of their aphid prey. For example, Aphidius rhopalosiphi, the parasitoid wasp of cereal aphids, is attracted by wheat and this attraction is stronger if the plant is infested by R. padi (Gonzáles et al. 1999).

A high population density of aphids (9 aphids/cm2) causes wheat seedlings to produce volatiles that have a repellent effect on apterous R. padi individuals (Quiroz et al.1997, Gonzáles et al. 1999).

Jasmonic acid

The plant stress hormone jasmonic acid activates many defence responses in the plant.

Jasmonic acid levels rise steeply in response to damage caused by a variety of herbivores and triggers the formation of many different kinds of plant defences besides proteinase inhibitors, including terpenes and alkaloids (Taiz and Zeiger 2002).

Jasmonic acid can act internally as a plant hormone associated with a damage/stress response, but, when methylated (methyl jasmonate), can be released by the plant and, whether naturally or not, will certainly have an effect on intact plants by up-regulating defence related and other genes (Pickett et al. 2006).

Cis-jasmone, which is also involved in the jasmonate pathway is a metabolic product of jasmonate and was thought originally to represents a sink for this pathway. Cis-jasmone affects plants by increasing attraction and searching by aphid predators (Pickett et al.

2005).

Salicylic acid

Methyl salicylate is biosynthetically related to salicylic acid, a signal molecule associated with systemically acquired resistance. This may indicate that the host plant defence pathways associated with hormonal activity of salicylate could present difficulties for colonization by aphids (Pickett et al. 2006). Methyl salicylate was found to deter aphids from colonizing plants and to increase foraging by parasitoids and predators attacking herbivorous insects and mites (Pickett and Poppy 2001). Prunus padus the winter host of R. padi releases a large amount of methyl salicylate, which stimulates the production of winged migrants on the winter host (Glinwood and Pettersson 2000).

Salicylic acid is also an internal stress signal (Pickett and Poppy 2001). Over 40 insect species from five separate Orders have been identified that have olfactory receptors for the methylated form methyl salicylate (Chamberlain et al. 2000, Pickett et al. 2003). The cereal aphids R. padi, S. avenae and Metopolophium dirhodum have a specific olfactory neuron on the sixth antennal segment to detect methyl salicylate (Pickett et al. 2006).

Ethylene (ET)

Ethylene is a plant hormone which plays an important role in plant defence. Ethylene biosynthesis is increased by stress conditions such as drought, flooding, chilling or mechanical wounding which triggers the stress responses such as abscission, senescence, wound healing and increased disease resistance. In combination with jasmonic acid is required for the activation of several plant defence genes (Taiz and Zeiger 2002). Insect herbivory is also known to stimulate an increase in ET emission. For example after Schizaphis graminum (biotype C) and Rhopalophum padi feeding on resistant barley a higher ET level was measured than in the susceptible barley (Argandona et al. 2001).

Harfouche et al. (2006) showed the armyworm larvae growth rate was significantly lower on ET producing maize plants than on plants treated with ET inhibitor which indicates ET is involved in the insect defence mechanism as well.

Abscisic acid (ABA)

ABA controls the resistance against pathogens and also plays a key role in the tolerance response to abiotic stress, and has been reported to act as a systemically transported signal from the roots to shoots (Erb et al. 2009). Above ground Diabrotica virgifera virgifera feeding induced the accumulation of abscisic acid in the above and below ground area of the plant which upregulated the hydroxamic acid pathway which resulted a higher level of DIMBOA in the shoot. Erb et al. (2009) concluded that D. virgifera induced production in the leaves is mediated by ABA.

Response to semiochemicals

Adult aphids can detect olfactory cues and use them for host location, escape responses and mate recognition. The olfactory receptor system of the host-alternating aphids is not only species- and sex-specific, but also morph-specific. The nymphal alatiform virginopara antenna is morphologically different to the adult’s antenna, which has three different types of olfactory receptor organs, proximal and distal primary rhinarium, and numerous secondary rhinaria. The primary rhinaria are presented in all developmental stages the

secondary rhinaria appear only in specific morphs of the adult stage and they become sex pheromone receptors in males.

The nymph’s olfactory system is not as developed as an adult because it does not require a specific sensory system for host selection (Park and Hardie 2003).

Aphids can detect semiochemicals with the primary rhinaria, which are on the fifth and sixth antennal segments (Pickett et al. 1997), and the contact chemosensory sensillae, which contact the plant surface during walking and are located at the tip of the antenna (Powell et al. 1999).