Ecological fitting in a deceptive trap flower: Aristolochia gibertii recruits native drosophilid flies outside South America

Abstract

Deceptive pollination, in which plants lure pollinators without offering rewards, represents a sophisticated evolutionary strategy. The trap-flowers of Aristolochia provide an excellent system to study the coordinated evolution of floral morphology, chemistry, and phenology. However, the functional integration of these traits remains poorly understood, especially in introduced populations where pollinators differ from those in the native range. We investigated the reproductive ecology of the South American vine Aristolochia gibertii in an introduced population in southern China, combining floral anatomical, histochemical, and volatile analyses with visitor surveys and controlled bagging experiments. Flowers exhibit strict protogyny with a time-regulated trapping mechanism: erect retrorse trichomes confine dipteran visitors during the female phase, whereas trichome collapse during the male phase permits the pollen-laden visitors to escape. Concurrently, the gynostemium transitions in a coordinate fashion: stigmatic lobes elevate, split, and reflex downward upon male-phase entry, coinciding with anther dehiscence and stigma senescence, thereby preventing selfing. Volatile emissions shift markedly between phases: cis -β-ocimene dominates the female phase, while limonene and other terpenoids increase during the male phase; both phases emit fermentation-related volatiles (acetoin and 2,3-butanediol) that mimic yeast odors. Drosophilid flies, particularly Drosophila ficusphila , accounted for over 70% of visitors and served as the primary pollen vectors. Minute nectaries provide trace amounts of nectar, sustaining captives without offering a substantial reward. Bagging experiments confirmed an obligate outcrossing system, with no fruit set from autonomous self-pollination. Our findings demonstrate that A. gibertii achieves efficient pollination through tightly coordinated mechanical, temporal, and chemical traits that exploit drosophilid sensory biases. This system exemplifies ecological fitting, wherein an introduced plant recruits native generalist pollinators without a co-evolutionary history, and provides a mechanistic framework for understanding multi-trait integration in angiosperm deception strategies.