Conflicting Dynamics of Galling and Pollination: Arastichus gallicola (Hymenoptera, Eulophidae), a Specialized Parasitic Galler in Pistillate Flowers of Thaumatophyllum bipinnatifidum (Araceae)

Abstract

In the complex dynamics of plant-insect interactions, the specialized galling of reproductive structures presents unique evolutionary adaptations. This study investigates the parasitic relationship between Arastichus gallicola (Hymenoptera, Eulophidae), an ovary-galling wasp, and the inflorescences of Thaumatophyllum bipinnatifidum (Araceae). We employed field experiments and histological analyses to investigate the mechanisms driving this interaction. We reveal that ovule fertilization is not required for gall formation; however, pollination substantially enhances gall retention by reducing inflorescence abscission. Inflorescences exposed solely to galling presented a 64% abscission rate, whereas those with both galling and pollination experienced 33% abscission, underscoring pollination's role in mitigating inflorescence loss. Detailed observations of A. gallicola oviposition and larval development reveal the intricate gall formation process characterized by progressive tissue hypertrophy surrounding the larva. Galling and seed development were mutually exclusive, with only 9% of fruits containing both. This mutual exclusivity suggests a competitive interaction for developmental resources within the ovary. Our findings underscore the specialized larval biology of galling chalcid wasps, illustrating how interactions between gall formation and host reproductive strategies shape the evolution of gall induction in floral tissues. Our study advances the understanding of ovary-galling adaptations and the selective pressures shaping antagonistic and mutualistic interactions in plant reproductive structures.

Keywords: Chalcidoidea; gall development; gall-inducing insects; insect–plant interactions.

Figure 1

Oviposition in Thaumatophyllum bipinnatifidum flowers and early developmental stages of Arastichus gallicola. (a) Close-up of female wasp during oviposition; (b,c) ovipositor insertion sites: (b) through the flower stigma and (c) through the ovary wall; (d) detail of egg placement, with arrows indicating two eggs attached to the ovule base, each anchored to the funicle by a long peduncle; (e) position of the first larval instar (arrow) near the ovule funicle; (f) close-up of the first larval instar. Abbreviations: fun = ovule funicle, ov = plant ovule.

Figure 2

Immature stages of Arastichus gallicola. (a) Egg with peduncle; (b) first larval instar at 7 days; (c) first larval instar at 17 days; (d) second larval instar at 25 days; (e) third larval instar at 37 days.

Figure 3

Longitudinal sections of Thaumatophyllum bipinnatifidum ovules showing early developmental stages of Arastichus gallicola. (a,b) Position of the wasp egg (arrows) relative to the ovule; (c–f) position of the first-instar larva (arrow) relative to the ovule; (e) detail of the larva near elements of the ovule funicle; (f) close-up of the larva. Abbreviations: end = endothelium, es = embryo sac, fun = funicle, it = inner integument, l = larva, loc = ovarian locule, nu = nucellus.

Figure 4

Longitudinal sections of Thaumatophyllum bipinnatifidum ovaries, showing an ovule undergoing gall formation and an unaffected ovule (ov), 20–25 days after oviposition. (a) Pistillate flower with affected (dotted rectangle) and unaffected ovules; (b) close-up of the affected ovule, showing the ovule elements; (c) close-up of the dotted area in (b), highlighting hypertrophied cells surrounding the larva, indicative of gall formation. Abbreviations: inu = induced nucellus, it = inner integument, loc = ovarian locule, ov = unaffected ovule.

Figure 5

Longitudinal sections of a Thaumatophyllum bipinnatifidum ovary with galled ovules containing larvae (arrows). (a) Overview showing three larvae within ovule galls; (b) close-up of the dotted area in (a), detailing the affected ovule and parenchyma; (c) close-up of the dotted area in (b), illustrating hypertrophied cells throughout the tissue surrounding the larva. Abbreviations: iov = induced ovary tissue, ipa = induced parenchymal elements, l = larva.

Figure 6

Longitudinal sections of fully developed galls of Arastichus gallicola in Thaumatophyllum bipinnatifidum ovary. (a) Section showing a galled ovary with two galls, each containing a larva; (b) close-up of the dotted area in (a), highlighting induced parenchymal elements. Abbreviations: ind = induced parenchymal elements, l = larva.