Phytochemistry-mediated disruption of ant-aphid interactions by root-feeding nematodes

Plants link interactions between aboveground and belowground organisms.
Herbivore-induced changes in plant chemistry are hypothesized to impact
entire food webs by changing the strength of trophic cascades. Yet few
studies have explored how belowground herbivores affect the behaviors of
generalist predators, nor how such changes may act through diverse changes
to the plant metabolome. Using a factorial experiment, we tested whether
herbivory by root-knot nematodes (Meloidogyne incognita) affected the
aboveground interaction among milkweed plants (Asclepias fascicularis or
Asclepias speciosa), oleander aphids (Aphis nerii), and aphid-tending ants
(Linepithema humile). We quantified the behaviors of aphid-tending ants,
and we measured the effects of herbivore treatments on aphid densities and
on phytochemistry. Unexpectedly, ants tended aphids primarily on the
leaves of uninfected plants, whereas ants tended aphids primarily at the
base of the stem of nematode-infected plants. In nematode-infected plants,
aphids excreted more sugar per capita in their ant-attracting honeydew.
Additionally, although plant chemistry was species-specific, nematode
infection generally decreased the richness of plant secondary metabolites
while acting as a protein sink in the roots. Path analysis indicated that
the ants’ behavioral change was driven in part by indirect effects of
nematodes acting through changes in plant chemistry. We conclude that
belowground herbivores can affect the behaviors of aboveground generalist
ant predators by multiple paths, including changes in phytochemistry,
which may affect the attractiveness of aphid honeydew rewards.