host species [42, 69]. These herbivores live inside the plant tissue, either inside the
leaf lamina or in induced galls. Their endophytic lifestyle provides them with some
protection against biotic and abiotic factors such as UV irradiation and drought, and
in some cases probably also with protection against predaors or generalist parasitoids
[3, 70, 71] (but there are many specialized parasitoids of mining or galling herbivores (e.g., [70, 72])). The highly specialized nature of miners and gallers also
allows them to escape negative effects of certain defences of their hosts.
First, a miner larva living inside the leaf lamina does not have to deal with a tough
leaf surface and can preferentially feed on cells with high nutrition value [73].
Indeed, leaf toughness is an important predictor of food choice in leaf-chewing
insects, which cannot avoid chewing on the tough cuticle of the leaves [3, 74]. Some
plant groups such as palms or grasses, which contain high levels of silica-based
physical defences have especially tough leaves, which erode mandibular jaws of
chewing herbivores, significantly lowering their feeding efficiency [75, 76].
Second, their highly adapted nature allows gallers to manipulate their hosts to
form galls by using metabolites closely resembling or identical to phytohormones
[77, 78]. The ability of host manipulation was probably a key innovation in several
taxa of gall-forming herbivores because there have been repeated and often dramatic
radiations of gall-forming Arthropods including various insect orders and mites [79].
The radiations of several galler taxa have been characterized by associations with
key plant genera – e.g., radiation of Cynipidae wasps on Quercus, Pemphigidae
aphids on Pistacia, and Tenthredinidae sawflies on Salix [79]. A gall itself can have a
significantly different chemical profile than the rest of the plant tissue, and gallers
can control host plant defences, such as secondary metabolites [80]. Galls thus
can have lower content of defensive secondary metabolites, while they have higher
nutrient values than normal plant tissue (but note that increase of certain defensive metabolites in galls is also possible). Downregulation of host defences has been
recorded in many plant-galler systems as reviewed by Giron et al. [78] and include
downregulation of various phenolics, proteases, or volatile compounds (e.g.,
[80–83]). As suggested by Stone et al. [84] gallers “represent examples of an
alternative coevolutionary arms race paradigm, not between toxins and detoxification systems as in the Ehrlich and Raven model, but between host plant susceptibility
and gall inducer virulence.” This may lead to a situation when abundance or
diversity of gallers does not respond to host chemical defences [15]. This is quite
different from leaf chewers, which often show negative or positive correlation to the
secondary metabolite content of the host [13, 19]. Indeed, in some cases host
selection in gallers seems to focus on plant species with high nitrogen content
disregarding their defences, possibly as such hosts may be more easily manipulated
to contain even higher nutrient concentration [15]. Relatively recently, host manipulation toward higher nutrients and lower defences was also recorded in the case of
miners [78, 85], suggesting that some members of this guild can, to some extent,
ignore host defences as well.
Another example of a herbivore guild with a response to host plant defences
largely different from leaf-chewers are sucking herbivores. Sucking herbivores have
evolved specialized, so-called haustellate mouthparts. Such mouthparts evolved
4 Differential Response of Herbivores to Plant Defence
87
leaf lamina or in induced galls. Their endophytic lifestyle provides them with some
protection against biotic and abiotic factors such as UV irradiation and drought, and
in some cases probably also with protection against predaors or generalist parasitoids
[3, 70, 71] (but there are many specialized parasitoids of mining or galling herbivores (e.g., [70, 72])). The highly specialized nature of miners and gallers also
allows them to escape negative effects of certain defences of their hosts.
First, a miner larva living inside the leaf lamina does not have to deal with a tough
leaf surface and can preferentially feed on cells with high nutrition value [73].
Indeed, leaf toughness is an important predictor of food choice in leaf-chewing
insects, which cannot avoid chewing on the tough cuticle of the leaves [3, 74]. Some
plant groups such as palms or grasses, which contain high levels of silica-based
physical defences have especially tough leaves, which erode mandibular jaws of
chewing herbivores, significantly lowering their feeding efficiency [75, 76].
Second, their highly adapted nature allows gallers to manipulate their hosts to
form galls by using metabolites closely resembling or identical to phytohormones
[77, 78]. The ability of host manipulation was probably a key innovation in several
taxa of gall-forming herbivores because there have been repeated and often dramatic
radiations of gall-forming Arthropods including various insect orders and mites [79].
The radiations of several galler taxa have been characterized by associations with
key plant genera – e.g., radiation of Cynipidae wasps on Quercus, Pemphigidae
aphids on Pistacia, and Tenthredinidae sawflies on Salix [79]. A gall itself can have a
significantly different chemical profile than the rest of the plant tissue, and gallers
can control host plant defences, such as secondary metabolites [80]. Galls thus
can have lower content of defensive secondary metabolites, while they have higher
nutrient values than normal plant tissue (but note that increase of certain defensive metabolites in galls is also possible). Downregulation of host defences has been
recorded in many plant-galler systems as reviewed by Giron et al. [78] and include
downregulation of various phenolics, proteases, or volatile compounds (e.g.,
[80–83]). As suggested by Stone et al. [84] gallers “represent examples of an
alternative coevolutionary arms race paradigm, not between toxins and detoxification systems as in the Ehrlich and Raven model, but between host plant susceptibility
and gall inducer virulence.” This may lead to a situation when abundance or
diversity of gallers does not respond to host chemical defences [15]. This is quite
different from leaf chewers, which often show negative or positive correlation to the
secondary metabolite content of the host [13, 19]. Indeed, in some cases host
selection in gallers seems to focus on plant species with high nitrogen content
disregarding their defences, possibly as such hosts may be more easily manipulated
to contain even higher nutrient concentration [15]. Relatively recently, host manipulation toward higher nutrients and lower defences was also recorded in the case of
miners [78, 85], suggesting that some members of this guild can, to some extent,
ignore host defences as well.
Another example of a herbivore guild with a response to host plant defences
largely different from leaf-chewers are sucking herbivores. Sucking herbivores have
evolved specialized, so-called haustellate mouthparts. Such mouthparts evolved
4 Differential Response of Herbivores to Plant Defence
87