Testing Darwin’s Hypothesis about the Wonderful Venus Flytrap: Marginal Spikes Form a “Horrid Prison” for Moderate-Sized Insect Prey

Abstract

Botanical carnivory is a novel feeding strategy associated with numerous physiological and morphological adaptations. However, the benefits of these novel carnivorous traits are rarely tested. We used field observations, lab experiments, and a seminatural experiment to test prey capture function of the marginal spikes on snap traps of the Venus flytrap (Dionaea muscipula). Our field and laboratory results suggested inefficient capture success: fewer than one in four prey encounters led to prey capture. Removing the marginal spikes decreased the rate of prey capture success for moderate-sized cricket prey by 90%, but this effect disappeared for larger prey. The nonlinear benefit of spikes suggests that they provide a better cage for capturing more abundant insects of moderate and small sizes, but they may also provide a foothold for rare large prey to escape. Our observations support Darwin's hypothesis that the marginal spikes form a "horrid prison" that increases prey capture success for moderate-sized prey, but the decreasing benefit for larger prey is unexpected and previously undocumented. Thus, we find surprising complexity in the adaptive landscape for one of the most wonderful evolutionary innovations among all plants. These findings enrich understanding of the evolution and diversification of novel trap morphology in carnivorous plants.

Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

“…Determining how organisms use resources for the first time and occupy novel niches is an outstanding question in evolutionary ecology. Many changes accompany adaptation to a novel niche, and previous studies have investigated how shifts in behaviors (Bowman and Billeb, 1965;Tebbich et al, 2010;Curry and Anderson, 2012), morphologies (Ferry-Graham et al, 2001;Ferry-Graham, 2002;Hata et al, 2011;Davis et al, 2018), physiologies (Arias-Rodriguez et al, 2011;Tobler et al, 2015Tobler et al, , 2018 and kinematics (Janovetz, 2005;Patek et al, 2006;Cullen et al, 2013;McGee et al, 2013) can all facilitate this transition.…”

Prey capture analyses in the carnivorous aquatic waterwheel plant (Aldrovanda vesiculosa L., Droseraceae)

“…To what extent these field observations indeed reflect the efficiency of the snap-trapping mechanism and/or the efficiency of prey attraction is not yet clear and remains a promising subject for future studies. Interestingly, a low capture efficiency has also been reported for Venus flytraps ( D. muscipula ), the terrestrial sister of A. vesiculosa , in several field- and lab-based studies 20–22 .…”

“…However, as discussed for PCA 13, it may also happen that the trap rim glides off during the capture motion. In the closely related Venus flytrap ( D. muscipula ), where the teeth are much longer in relation to the overall trap dimension compared to A. vesiculosa , it has initially been hypothesized 32 and later found in a field- and lab-based study 22 that the teeth form a “prison” that increases prey capture success for moderate-sized prey. However, for larger prey a decreasing benefit was also found, which adds to the complexity of the adaptive landscape of the snap-trap system.…”

Functional organisation of the endomembrane network in the digestive gland of the Venus flytrap: revisiting an old story with a new microscopy toolbox

“…liquid versus solid; see also Scala et al ., 1969). Intensity or even quality of secretory events may also depend on the physiological state of the trap, performances of which will decrease with the number of cycles (mainly three, but exceptionally four cycles) (Davis et al ., 2019). It is also essential to stress that remodelling of the membrane system should probably be considered as a whole that is greater than the sum of its parts.…”

“…Prey digestion begins with the delivery of digestive enzymes from the hundreds of digestive glands in contact with the prey. After the immediate capture of the prey, the trap remains closed for 4–5 days before opening again to start a new cycle (Davis et al ., 2019). The description of the prey ‘digestive cycle’ established in the early 1980s (Robins & Juniper, 1980a,1980b,1980c,1980d) remains a solid foundation for today's research.…”