Quantitative differences detected in the histology of galls induced by the same aphid species in different varieties of the same host

Abstract

Plant galls are abnormal growths caused by an inducer that determines their morphology and anatomy. We qualitatively and quantitatively compared the histological anatomy of five aphid species (Paracletus cimiciformis, Forda marginata, Forda formicaria, Baizongia pistaciae and Geoica wertheimae) that induce galls in Pistacia terebinthus shrubs growing in Israel. We also quantitatively compared these galls to those that the aphids create on the same host in Spain. Histological study was conducted following methods described previously by the authors. Quantitative differences among the galls were found in five of 12 common anatomical traits: gall thickness, stomatal number in the epidermis-air, size of vascular bundles, distance of phloem ducts from the lumen and number of intraphloematic schizogenous ducts. Other structures were particular to one or some species: number of cracks in the epidermis-lumen, a sclereid layer, trichomes and microcrystal inclusions. Fisher's tests of combined probabilities showed that the galls induced in Israel were statistically different from those in Spain. In particular, the number of intraphloematic schizogenous ducts was higher in the galls induced in P. terebinthus in Israel. Such differences were also found in other traits related to defence of the gall inhabitant. In conclusion, while the gall shape and size are determined mainly by the cecidogenic insect, it seems that the host plant also plays an important role in determining the number/size of quantitative traits, in this case mainly protective structures.

Experimental validation of the soil fertility hypothesis in a natural Mediterranean tri‐trophic system

“…The anti‐insect properties of the wall in galls induced by aphids have been demonstrated, as has the importance of the permeability of the gall wall to non‐polar volatile compounds for the survival of the aphids inside the gall cavity (Martinez, 2010). The richness of protective structures found in the same galls was histologically described by Àlvarez and colleagues (Álvarez et al, 2009, 2016; Àlvarez, 2012; Martinez et al, 2018), and it is admitted that these structures are avoided by the gall inducers (Wool, 2005).…”

“…Galling insects profit from the gall tissue as a nutrient source (via phloem ducts for example Wool, 2012;Martinez et al, 2018), as a physical barrier (wall thickness, sclereids, schizogenous ducts of sticky resins - Alvarez et al, 2009;Martinez et al, 2018), and through chemical protection (resins rich in terpenoids - Rand et al, 2014). Galls are created by the host plant as a means of anti-herbivore defense (Hanley et al, 2007), but manipulated by the gall inducer for its own advantage (Price & Pschorn-Walcher, 1988;Martinez et al, 2018). At the end of the second growing season, we effectively measured longer current-year apical shoots and internodes in fertilized trees than in control trees, in accordance with SFH, and than was demonstrated in the past (e.g., Dardeau et al, 2015).…”

“…These last two trends should be the result of more enemy attacks on galls developing in fertilized trees, leading to a lower percentage of gall survival, as a consequence of lower concentrations of protective secondary metabolites in gall tissues on fertilized trees (Fernandes & Price, 1991). Galling insects profit from the gall tissue as a nutrient source (via phloem ducts for example – Inbar et al, 1995; Wool, 2012; Martinez et al, 2018), as a physical barrier (wall thickness, sclereids, schizogenous ducts of sticky resins – Alvarez et al, 2009; Martinez et al, 2018), and through chemical protection (resins rich in terpenoids – Rand et al, 2014). Galls are created by the host plant as a means of anti‐herbivore defense (Hanley et al, 2007), but manipulated by the gall inducer for its own advantage (Price & Pschorn‐Walcher, 1988; Martinez et al, 2018).…”

“…On the other hand, the accumulation of defensive products could be toxic to the gall inducers themselves, although galling aphids, as endophagous insects, are able to manipulate their host plants to enhance their food sources, from a qualitative (Rand et al, 2014(Rand et al, , 2017 and quantitative point of view (e.g., Aloni et al, 1989). Gallinducing insects also manipulate the defenses of the host plant for their own protection (Wool, 2005;Martinez, 2010;Rost as et al, 2013;Rand et al, 2017;Martinez et al, 2018). One could think that there are no differences between the PSH and the SFH, both claiming that stressed plants are more susceptible to herbivores.…”

A study on the effect of host plants on Chinese gallnut morphogenesis

“…Gall abundance on Mangifera indica leaves was found to be higher in the upper than the lower zone of the plant canopy, which on its turn was higher than in the inner zone [ 20 ]. In a type of aphidic gall, the number/size of the gall is different when a kind of aphid feeding on the different site of the same host [ 21 ]. In addition to size and number, the host plant also affects the morphogenesis of galls.…”