A novel insight into the cost-benefit model for the evolution of botanical carnivory

Abstract

Background: The cost-benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (AN) in the microsites inhabited by carnivorous plants.

Scope: This review summarizes results from the classical interpretation of the cost-benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost-benefit model.

Conclusions: Traps of carnivorous plants have lower AN than leaves, and the leaves have higher AN after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, RD) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.

Keywords: Action potential; Dionaea; Drosera; Nepenthes; Venus flytrap; botanical carnivory; carnivorous plant; cost–benefit; electrical signalling; jasmonates.

Fig. 1.

The carnivorous plants. (A) Cephalotus follicularis, (B) Darlingtonia californica, (C) Dionaea muscipula, (D) Nepenthes tentaculata, (E) Heliamphora nutans, (F) Sarracenia flava, (G) Drosera roraimae, (H) Pinguicula alpina, (I) Utricularia humboldtii.

Fig. 2.

Two related species of Brocchinia growing in the Guiana Highlands, Venezuela. (A) The non-carnivorous species Brocchinia tatei often grows in cloud forest and forms nearly horizontal rosette-forming green leaves. (B) The carnivorous species Brocchinia reducta grows in open vegetation and forms bright yellow-green leaves which are held vertically.

Fig. 3.

Classical interpretation of the cost–benefit model for evolution of botanical carnivory in the genus Nepenthes. Comparison of photosynthetic characteristics between the pitcher (the lid as a flat part of the pitcher) and lamina. (A) The leaf of Nepenthes truncata. (B) A/Ci response curve of photosynthesis. (C) Light response curve of photosynthesis. (D) Light response curve of effective photochemical quantum yield of photosystem II (ϕ_PSII). (E) Stomatal conductance (g_s). (F) Protein content and protein gel blot analysis (the same amount of protein was electrophoresed), leaf (1), digestive zone (2), peristome (3), lid (4). (G) Elemental composition of the leaf. (H) Pigment content and ratio. Data are means ± s.e. (n = 5); different letters denote significant differences among plant tissues (one-way ANOVA followed by Tukey’s test). For details of the methods, see the Supplementary Data.

Fig. 4.

A novel insight into the cost–benefit model in the Venus flytrap (Dionaea muscipula). (A) Spatio-temporal changes of chlorophyll a fluorescence in response to mechanical touches of trigger hairs (at time 660–670 s) and generation of action potentials, maximum quantum yield of photosystem II (F_v/F_m), effective photochemical quantum yield of photosystem II (ϕ_PSII), photochemical quenching (qP) and non-photochemical quenching (NPQ); for detailed explanations of the kinetics of chlorophyll a fluorescence in Venus flytrap see Pavlovič et al. (2011a). (B) Simultaneous measurement of gas exchange at a light intensity of 80 µmol m^–2 s^–1 PAR. (C) Measurement of gas exchange in the dark indicating the rate of respiration (R_D). (D) Action potentials in the trap in response to mechanical stimulation of trigger hairs. (E) Light response curve of photosynthesis in open control traps and traps in the digestive period 36 h after chemical stimulation with NH₄Cl. (D) The endogenous jasmonate level (JA, jasmonic acid; JA-Ile, isoleucine conjugate of jasmonic acid; cis-OPDA, cis-12-oxophytodienoic acid) in trap tissue 36 h after induction with NH₄Cl. Data are means ± s.e. (n = 5). For details of the methods, see the Supplementary Data.

Fig. 5.

Probable timed hierarchy of consecutive events detectable in carnivorous plants with the active trapping mechanism in response to prey capture adopted from plant defence mechanisms (Maffei et al., 2007). The earliest events measurable are action potentials generated by mechanical stimuli (Williams and Pickard, 1980; Hodick and Sievers, 1988; Krol et al., 2006; Escalante-Pérez et al., 2011) or chemical stimuli from prey (Scherzer et al., 2013), which trigger a cytosolic calcium increase (Escalante-Pérez et al., 2011) and generation of H₂O₂ (Chia et al., 2004; Ibarra-Laclette et al., 2011). Increased cytosolic Ca²⁺ is probably sensed by binding to calmodulin protein (CaM) or other calcium-sensing proteins, which can interact with mitogen-activated protein kinases (MAPKs; this part of the signaling pathway has not yet been documented in carnivorous plants). MAPKs regulate biosynthesis of jasmonates which trigger the expression of carnivory-related genes (Scherzer et al., 2013; Nakamura et al., 2013; Libiaková et al., 2014; Mithöfer et al., 2014; Paszota et al., 2014).

Fig. 6.

Unique nutrient sequestration strategies in three species of Nepenthes from Borneo. (A) Leaf litter utilization by N. ampullaria. (B) Pitcher plants N. lowii and N. rajah (C) have modified pitcher morphology for collecting faeces from the mountain tree shrew (Tupaia montana).