The super-host Mimosa gemmulata Barneby (Fabaceae) and the implications of the life cycles of Lopesia spp. (Cecidomyiidae) on gall developmental processes

Abstract

The genus Mimosa L. (Fabaceae) has 21 host species, in which 35 gall morphospecies are reported for the Brazilian flora. Mimosa gemmulata Barneby stands out as a super-host of six gall morphospecies, of which four are bivalve-shaped: the lenticular (LG), the green lanceolate (GLG), the brown lanceolate (BLG) and the globoid (GG) galls. Peculiarly, on M. gemmulata, the four bivalve-shaped galls are induced on the pinna-rachis by four species of Lopesia Rübsaamen 1908 (Cecidomyiidae). Phenological, anatomical, cytometric, histochemical and immunocytochemical studies reveal that differences among the bivalve-shaped galls associated with M. gemmulata relate to the lifespans of the Lopesia spp., and consequently, to their galls. The constant leaf flushing in M. gemmulata supports the asynchrony of the multivoltine life cycles of Lopesia spp. and the non-overlapping of gall induction periods. The LG life cycle lasts two months, the GLM and the GLV life cycles last three months, and the GG life cycle lasts four months. This variation of 1 to 2 months in the gall lifespans determines the highest structural and nutritional support in the cell walls and protoplasm of the GG tissues, when compared to the other galls. During the development of the bivalve-shaped galls, the types of leaf trichomes of M. gemmulata are conserved, but their size, cell number and distribution are differently altered in each gall. The parenchyma cells recruited from the pinna-rachis redifferentiate into the storage, sclerenchyma cells, and vascular cells of the four bivalveshaped galls, but the highest stimuli-induced responses in all host plant cell lineages occur in the GG. In this gall, the typical nutritive tissue has mixed origin, from epidermal and parenchyma cells. The sites of spatial and temporal detection of auxins and cytokinins determine the patterns of cell division and elongation during the ontogenesis of each bivalve-shaped gall. The highest cell and tissue dynamics in responses to plant hormones is related to the longest life cycle of the Lopesia sp. associated to the GG. The entrance of the ectoparasitoid Torymus sp. and the endoparasitoid Platygastridae in M. gemmulataLopesia GG system impacts the feeding behavior of the gall-inducing Lopesia larvae, resulting in precocious gall senescence. Thus, we conclude that the differences among the bivalve-shaped galls associated with M. gemmulata are determined by the time that each Lopesia sp. stimulates the development of its specific gall, with the highest potential of responses in the GG, which has the longest lifespan.