Hierarchical metapopulation dynamics of two aphid species on a shared host plant.

We modeled hierarchical multiscale colonization-extinction dynamics of two aphid species living in a shared host plant. We parameterized the model with data collected at the level of individual ramets of the host plant, with the plants being organized as groups within islands. As expected, the extinction rates and per capita colonization rates decreased with increasing spatial scale. The per capita colonization rates were greater for winged than for unwinged individuals, but as the unwinged individuals were much more abundant, they actually performed most of the colonizations. Colonizations and extinctions were negatively correlated, so that when the colonization rate in a given island was high, the extinction rate in the same island was low. There was a clear indication of interspecific interaction, with the presence of one species increasing the extinction rate and decreasing the colonization rate of the other species. Further simulation results based on the parameterized model show a contrasting pattern between the two species, with Metopeurum fuscoviride (with relatively stable dynamics) being favored by a highly aggregated distribution of the ramets, whereas for Macrosiphoniella tanacetaria (with a high turnover rate), an equally high persistence time follows if the plants are distributed in a segregated manner over several islands.

Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection.

Complex biotic interactions shape ecological communities of plants, herbivores and their natural enemies. In studies of multi-trophic interactions, the presence of small, invisible micro-organisms associated with plants and those of a fourth above-ground trophic level have often been neglected. Incorporating these neglected factors improves our understanding of the processes within a multi-trophic network. Here, we ask whether the presence of a fungal endosymbiont, which alters plant quality by producing herbivore-toxic substances, trickles up the food chain and affects the performance and host-selection behaviour of aphid secondary parasitoids. We simultaneously offered hosts from endophyte-free and endophyte-infected environments to secondary parasitoids. Older and more experienced parasitoid females discriminated against hosts from the endophyte-infected environment. Developing in lower quality hosts from the endophyte-infected environment reduced the lifespan of secondary parasitoids. This indicates that aphid secondary parasitoids can perceive the disadvantage for their developing offspring in parasitoids from the endophyte environment and can learn to discriminate against them. In the field, this discrimination ability may shift the success of primary parasitoids to endophyte-infected plants, which co-occur with endophyte-free plants. Ultimately, the control of aphids depends on complex interactions between primary and secondary parasitoids and their relative sensitivity to endophytic fungi.

Trophic cascades initiated by fungal plant endosymbionts impair reproductive performance of parasitoids in the second generation.

Variation in plant quality can transmit up the food chain and may affect herbivores and their antagonists in the same direction. Fungal endosymbionts of grasses change the resource quality by producing toxins. We used an aphid-parasitoid model system to explore how endophyte effects cascade up the food chain and influence individual parasitoid performance. We show that the presence of an endophyte in the grass Lolium perenne has a much stronger negative impact on the performance of the parasitoid Aphidius ervi than on its aphid host Metopolophium festucae. Although the presence of endophytes did not influence the parasitism rate of endophyte-naïve parasitoids or their offspring's survival to adulthood, most parasitoids developing within aphids from endophyte-infected plants did not reproduce at all. This indicates a delayed but very strong effect of endophytes on parasitoid performance, which should ultimately affect plant performance negatively by releasing endophyte-tolerant herbivores from top-down limitations.

Natural enemies act faster than endophytic fungi in population control of cereal aphids.

1. Fast-growing populations of phytophagous insects can be limited by the presence of natural enemies and by alkaloids that are produced by symbiotic associations of many temperate grass species with endophytic fungi. It is unclear if and how acquired plant defences derived from endophytic fungi interact with natural enemies to affect phytophagous insect populations. 2. To assess the relative importance of endophytic fungi compared to that of natural enemies on the population dynamics of phytophagous insects, we carried out a fully factorial field experiment, in which the presence of natural enemies and the presence of endophytic fungi were manipulated simultaneously. Target colonies of aphids were monitored for 8 weeks starting from their natural appearance in the field to the end of the aphid season. 3. We show that on Lolium perenne increased natural enemy densities reduced the individual numbers of two common cereal aphids, Rhopalosiphum padi and Metopolophium festucae. 4. The presence of the endophytic fungi Neotyphodium lolii reduced the number of M. festucae but did not affect the number of R. padi. The reduction in R. padi numbers by predators and parasitoids was not influenced by the presence of endophytes. For adult M. festucae, however, the negative effects of natural enemies were significant only in the absence of endophytes. 5. Over the duration of the experiment, the effect of natural enemies on aphid colony growth was much stronger than the effect of the endophytic fungi N. lolii, presumably because predator and parasitoid action on aphid colonies is much faster than any effects of endophytes. 6. Our results demonstrate that with simultaneous action of acquired endosymbionts and natural enemies, both factors can control aphid colony growth but they generally act independently of each other.