Edward B. Mondor

Predator-induced transgenerational phenotypic plasticity in the cotton aphid.

Transgenerational phenotypic changes, whereby offspring have an altered trait or a distinct alternate phenotype, frequently occur in response to increased maternal predation risk. The cotton aphid, Aphis gossypii (Glover), is unique, however, as offspring consist of four distinct phenotypes (“normal” light green apterae, “normal” dark green apterae, “dwarf” yellow apterae, and alatae), all with divergent life history patterns and resulting population dynamics. Here, we show that increased predation risk induces transgenerational phenotypic changes in cotton aphids. When exposed to search tracks from larval or adult convergent ladybird beetles, Hippodamia convergens Guérin-Méneville, cotton aphids produced greater numbers of winged offspring. In a subsequent experiment, apterous and alate individuals on clean plants were found to have primarily normal and dwarf offspring, respectively. We suggest that elevated predation risk may cause phenotypic changes in aphids over multiple generations, resulting in a more precipitous decline in herbivore populations than could be explained solely by increased predation rates.

Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum.

When attacked by a predator, an aphid may secrete a droplet of fluid from its cornicles containing a volatile alarm pheromone component, (E)-β-farnesene. This study investigated both qualitative and quantitative aspects of alarm pheromone production in the pea aphid, Acyrthosiphon pisum. The best predictor of cornicle droplet emission was reproductive phase, rather than instar, as prereproductive aphids were more likely to secrete cornicle droplets than either reproductive or postreproductive individuals. Analogously, alarm pheromone amounts were highest in prereproductive aphids. (E)-β-Farnesene quantities (mean ± SE) increased significantly from first instar (1.5 ± 0.6 ng) to second instar (11.2 ± 3.7 ng) and did not significantly change during third (12.8 ± 3.0 ng) or fourth instars (11.0 ± 3.7 ng). Alarm pheromone amounts then decreased significantly in adults (4.8 ± 2.3 ng). We suggest that prereproductive aphids have been selected to produce higher levels of pheromone because of their more clustered colony structure and higher levels of predation, as compared with adult aphids.

Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres

Environmental change is anticipated to negatively affect both plant and animal populations. As abiotic factors rapidly change habitat suitability, projections range from altered genetic diversity to wide-spread species loss. Here, we assess the degree to which changes in atmospheric composition associated with environmental change will influence not only the abundance, but also the genotypic/phenotypic diversity, of herbivore populations. Using free-air CO2 and O3 enrichment (FACE) technology, we assess numerical responses of pea aphids (Acyrthosiphon pisum) exhibiting a pink‐green genetic polymorphism and an environmentally determined wing polyphenism on broad bean plants (Vicia faba) under enriched CO2 and/or O3 atmospheres, over multiple generations. We show that these two greenhouse gases alter not only aphid population sizes, but also genotypic and phenotypic frequencies. As the green genotype was positively influenced by elevated CO2 levels, but the pink genotype was not, genotypic frequencies (pink morph:green morph) ranged from 1:1 to 9:1. These two genotypes also displayed marked differences in phenotypic frequencies. The pink genotype exhibited higher levels of wing induction under all atmospheric treatments, however, this polyphenism was negatively influenced by elevated O3 levels. Resultantly, frequencies of winged phenotypes (pink morph:green morph) varied from 10:1 to 332:1. Thus, atmospheric conditions associated with environmental change may alter not just overall population sizes, but also genotypic and phenotypic frequencies of herbivore populations, thereby influencing community and ecosystem functioning.

Inclusive fitness benefits of scent–marking predators

Because relatedness is high and dispersal is limited, one would expect to see higher levels of altruistic behaviour among clonal organisms than among animals of lesser relatedness. Enigmatically, however, parthenogenetic aphids do not emit alarm signals when a predator first enters a colony but only after being captured. Here, we report that an aphid smearing alarm pheromone directly onto a predator decreases the predation risk for clone–mates as the predator continues to search for additional prey. Adult multicoloured Asian ladybird beetles, Harmonia axyridis, daubed with alarm pheromone caused a greater proportion of aphids to drop off a plant and escape predation than did predators lacking pheromone droplets. Thus, along with direct fitness benefits of individual protection, aphid alarm signalling behaviour may have evolved through inclusive fitness benefits of protecting clone-mates by scent–marking predators.

Extrafloral nectary phenotypic plasticity is damage- and resource-dependent in Vicia faba

Phenotypic plasticity enables many damaged plants to increase nectar secretion rates from extrafloral nectaries (EFNs), or in the case of broad bean, Vicia faba L., to produce additional EFNs, to attract natural enemies of herbivores. While plants benefit greatly from these defensive mutualisms, the costs of producing EFNs are largely unknown. We hypothesized that if EFN production is costly, then damaged plants with high resource levels would be able to produce more EFNs than plants that are resource-limited. Here, we show that this indirect inducible defence does follow this general pattern. Vicia faba enriched with 6 or 12 g of 14 : 14 : 14 NPK fertilizer increased EFN numbers after leaf damage by 46 and 60%, respectively, compared with nutrient-poor plants. Thus, EFN production is both damage- and resource-dependent. Analogous to direct defences, production of EFNs may limit the overall loss of leaf tissue when risk of herbivory increases.

Has the Attraction of Predatory Coccinellids to Cornicle Droplets Constrained Aphid Alarm Signaling Behavior

When attacked by a predator, aphids of many species secrete cornicle droplets, containing an alarm pheromone, that results in the dispersal of nearby conspecifics. As females are parthenogenetic, alarm signaling functions to enhance the survival of clone-mates. Enigmatically, however, aphids are physically able to, but usually do not emit alarm pheromone when initially detecting a predator, but rather signal only when captured by a predator. We hypothesized that cornicle droplets may be attractive to natural enemies and result in an increased risk of predation for the signaler, thereby selecting for prudent alarm signalers. We tested this hypothesis by investigating the olfactory cues that the multicolored Asian ladybird beetle, Harmonia axyridis Pallas, uses to locate pea aphids, Acyrthosiphon pisum. In choice tests, H. axyridis were attracted to odors from pea aphid colonies, whether feeding or not feeding on a host plant leaf, but were not attracted to cornicle droplets containing alarm pheromone. Further, individual pea aphids emitting cornicle droplets were not located more often or in a shorter period of time by beetles than aphids not emitting cornicle droplets. Thus, the cost of emitting early alarm signals is not prohibitively high in regards to the attraction of predators such as H. axyridis.

Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands.

Species introductions into novel habitats, especially island ecosystems, can have devastating effects on ecosystem function and stability. Though none are native, at least 96 aphid species can now be found on one or more of the Hawaiian Islands. As aphids cause direct feeding damage and transmit plant viruses, it is important to identify the traits that have enabled these particular species to successfully colonize the archipelago. To address this question, nine morphological and ecological traits that may contribute to successful colonization were assessed for aphids present in Hawaii. As a comparative null model, we assessed the same traits for heterospecific congeners which are not present in the archipelago, but are present elsewhere in the world. Here we report that traits with higher frequencies among colonizing aphid species are: small apterae size, broad host range, anholocycly (i.e., permanent parthenogenesis), and presence in continental USA. Small aphids arriving from the mainland US and capable of feeding on numerous plant species may be intercepted less often by plant protection agents. It is also likely that asexually reproducing species are well suited to the Hawaiian subtropical climate, thereby eliminating the need for sexual phases and egg-laying for overwintering. By understanding the traits that enable aphids to successfully colonize remote islands, it is our hope that plant protection efforts may be enhanced, thereby reducing damage to native ecosystems.

Do exaptations facilitate mutualistic associations between invasive and native species

As invasive species are key threats to ecosystem structure and function, it is essential to understand the factors underlying their success. Enigmatically, mutualistic organisms are often successful in colonizing novel environments even though they commonly persist only through intricate relationships with other species. Mutualistic ants, for example, protect aphids from natural enemies while collecting carbohydrate–rich honeydew. To facilitate this interaction, ants have evolved aggressive responses to aphid alarm pheromone emissions. As invasive and native mutualists have not evolved together, however, it is unclear if this form of cross-species communication exists between these two parties thereby facilitating these novel interactions. We address this hypothesis by assessing whether the invasive Argentine ant, Linepithema humile, responds to native poplar aphid, Chaitophorus populicola, alarm signals. Here, we show that interspecific signalling does exist in this newly established mutualistic interaction. Argentine ant workers exhibit increased aggression and double the number of visits to an aphid colony after an aphid alarm signal is emitted. We suggest that pre-adaptations may facilitate the emergence of mutualistic associations between many invasive and native species.

Invasive aphids attack native Hawaiian plants

Invasive species have had devastating impacts on the fauna and flora of the Hawaiian Islands. While the negative effects of some invasive species are obvious, other species are less visible, though no less important. Aphids (Homoptera: Aphididae) are not native to Hawai’i but have thoroughly invaded the Island chain, largely as a result of anthropogenic influences. As aphids cause both direct plant feeding damage and transmit numerous pathogenic viruses, it is important to document aphid distributions and ranges throughout the archipelago. On the basis of an extensive survey of aphid diversity on the five largest Hawaiian Islands (Hawai’i, Kaua’i, O’ahu, Maui, and Moloka’i), we provide the first evidence that invasive aphids feed not just on agricultural crops, but also on native Hawaiian plants. To date, aphids have been observed feeding and reproducing on 64 native Hawaiian plants (16 indigenous species and 48 endemic species) in 32 families. As the majority of these plants are endangered, invasive aphids may have profound impacts on the island flora. To help protect unique island ecosystems, we propose that border vigilance be enhanced to prevent the incursion of new aphids, and that biological control efforts be renewed to mitigate the impact of existing species.

Transgenerational Behavioral Plasticity in a Parthenogenetic Insect in Response to Increased Predation Risk

Reliable cues of increased predation risk can induce phenotypic changes in an organism’s offspring (i.e. transgenerational phenotypic plasticity). While induction of defensive morphologies in naïve offspring in response to maternal predation risk is widespread, little is known about transgenerational changes in offspring behavior. Here we provide evidence for transgenerational behavioral plasticity in the pea aphid, Acyrthosiphon pisum. When pre-reproductive individuals of two genotypes (“pink” and “green”) were exposed to the alarm pheromone (E)-β-Farnesene (EBF), a reliable cue of increased predation risk, next-generation offspring altered their feeding site choices relative to the location of the maternal aphids. Offspring of EBF-treated aphids occupied “safer” feeding sites: green offspring occupied “safer” feeding sites in the natal colony, while pink offspring dispersed to occupy sites on neighboring plant leaves.