How goats avoid ingesting noxious insects while feeding.

As mammalian herbivores feed, they often encounter noxious insects on plants. It is unknown how they handle such insects. We experimentally examined the behavioural responses of goats to the noxious spring-webworm (Ocnogyna loewii), and manipulated their sensory perception to reveal the process of insect detection. Goats did not avoid plants with webworms, demonstrating a remarkable ability to sort them apart from the plant (98% of webworms survived). Initial detection of webworms involved tactile stimulation, done by repeatedly touching the leaves with the muzzle. This enabled them to pick webworm-free leaves. If the goats picked up leaves with a webworm, they shook or discarded the leaf. They spat out webworms that entered their mouths, after detecting them by touch and taste. By using their keen senses and efficient behaviours, goats are able to feed while accurately excluding insects. These findings highlight the importance of direct interactions between mammalian herbivores and insects.

Turning in mid-air allows aphids that flee the plant to avoid reaching the risky ground.

When forced to drop from the plant, flightless arboreal insects can avoid reaching the risky ground by maneuvering their body through the air. When wingless pea aphids (Acyrthosiphon pisum) are threatened by natural enemies, they often drop off their host plant while assuming a stereotypic posture that rotates them in mid-air, aligning them with their feet pointing downwards. This position may increase their chances of re-clinging onto lower plant parts and avoid facing the dangers on the ground, although its effectiveness in realistic field conditions has not been tested. We performed both laboratory and outdoor experiments, in which we dropped aphids upon host plants to quantify clinging success in plants with different characteristics such as height and leaf size. Live aphids had twofold higher clinging rates than dead ones, indicating that clinging success is indeed affected by the active aerial-righting of dropping aphids. The ability to cling was positively dependent on the plants' foliage cover as viewed in vertical direction from above. Therefore, we released aphids in commercial alfalfa (Medicago sativa) fields with varying plant heights and foliage cover and induced them to drop. Most (up to 75%) of the aphids avoided reaching the ground in taller plants (65 cm), and 17% in shorter plants (21 cm), demonstrating the efficiency of the aphids' response in averting risks: both those of an approaching enemy on the plant and the plethora of new risks on the ground. Evidently, even in complex field environment, the aerial-righting mechanism can substantially reduce the possible risks following escape from a predator.

Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence, significance, and prospectus.

Mammalian herbivores induce changes in the chemical composition, phenology, distribution, and abundance of the plants they feed on. Consequently, invertebrate herbivores (predominantly insects) that depend on those plants, and the predators and parasitoids that are associated with them, may be affected. This plant-mediated indirect interaction between mammals and invertebrates has been extensively studied, but mammalian herbivores may also directly affect plant-dwelling invertebrates (PDI) by incidentally ingesting them while feeding. The ubiquity and small size of PDI render them highly susceptible to incidental ingestion, but as common as this interaction may intuitively seem, very little is known about its prevalence and ecological consequences. Nevertheless, cases of incidental ingestion of PDI and associated adaptations for avoiding it that have been sporadically documented in several invertebrate groups and life stages allow us to carefully extrapolate and conclude that it should be common in nature. Incidental ingestion may, therefore, bear significant consequences for PDI, but it may also affect the mammalian herbivores and the shared plants. Future research on incidental ingestion of PDI would have to overcome several technical difficulties to gain better insight into this understudied ecological interaction.

Anticipatory and reactive crouching of pea aphids in response to environmental perturbations.

Animals use different strategies to deal with changing environmental conditions. While standing and feeding on their host plant, aphids (Hemiptera: Aphididae) may be exposed to detrimental environmental perturbations, such as strong winds. If aphids are forcibly blown off the plant and spend time on the ground, they will face additional dangers by both ground-dwelling predators and detrimental soil temperature. It is therefore adaptive for aphids to behave in a way that lowers the risk of being removed from the plant. We observed that pea aphids (Acyrthosiphon pisum (Harris)) display a specific crouched body posture, previously undescribed, which reduces their chance of being carried off from the plant by sudden winds. We exposed aphids in the laboratory to different cues indicative of a windy environment: wind, plant vibration, and visual stimuli. We found that aphids crouch in two situations: 1) reactively, when they are being pulled by a continuous gust of wind threatening to dislodge them. 2) Anticipatorily, when environmental cues, such as plant vibration or continuous movement near their host plant, may signify that sudden wind gusts are expected. Crouching aphids were less likely to be dislodged by a sudden air stream or plant vibration than were aphids that did not crouch. Crouching thus improves the aphids' chances of remaining on their host plant under unfavorable environmental conditions.

The mono - and sesquiterpene content of aphid-induced galls on Pistacia palaestina is not a simple reflection of their composition in intact leaves.

Pistacia palaestina Boiss. (Anacardiaceae), a sibling species of P. terebinthus also known as turpentine tree or terebinth tree, is common in the Levant region. The aphid Baizongia pistaciae L. manipulates the leaves of the plant to form large galls, which provide both food and protection for its developing offspring. We analyzed the levels and composition of mono-and sesquiterpenes in both leaves and galls of ten naturally growing trees. Our results show that monoterpene hydrocarbons are the main constituents of P. palaestina leaves and galls, but terpene levels and composition vary among trees. Despite this inter-tree variation, terpene levels and compositions in galls from different trees resemble each other more than the patterns displayed by leaves from the same trees. Generally, galls contain 10 to 60 fold higher total terpene amounts than leaves, especially of the monoterpenes α-pinene and limonene. Conversely, the leaves generally accumulate more sesquiterpenes, in particular E-caryophyllene, germacrene D and δ-cadinene, in comparison to galls. Our results clearly show that the terpene pattern in the galls is not a simple reflection of that of the leaves and suggest that aphids have a strong impact on the metabolism of their host plant, possibly for their own defense.

When herbivores eat predators: predatory insects effectively avoid incidental ingestion by mammalian herbivores.

The direct trophic links between mammalian herbivores and plant-dwelling insects have been practically ignored. Insects are ubiquitous on plants consumed by mammalian herbivores and are thus likely to face the danger of being incidentally ingested by a grazing mammal. A few studies have shown that some herbivorous hemipterans are able to avoid this peril by dropping to the ground upon detecting the heat and humidity on the mammal's breath. We hypothesized that if this risk affects the entire plant-dwelling insect community, other insects that share this habitat are expected to develop similar escape mechanisms. We assessed the ability of three species (adults and larvae) of coccinellid beetles, important aphid predators, to avoid incidental ingestion. Both larvae and adults were able to avoid incidental ingestion effectively by goats by dropping to the ground, demonstrating the importance of this behavior in grazed habitats. Remarkably, all adult beetles escaped by dropping off the plant and none used their functional wings to fly away. In controlled laboratory experiments, we found that human breath caused 60-80% of the beetles to drop. The most important component of mammalian herbivore breath in inducing adult beetles and larvae to drop was the combination of heat and humidity. The fact that the mechanism of dropping in response to mammalian breath developed in distinct insect orders and disparate life stages accentuates the importance of the direct influence of mammalian herbivores on plant-dwelling insects. This direct interaction should be given its due place when discussing trophic interactions.