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.

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Šlechtitelů 11 CZ 783 71 Olomouc Czech Republic and Department of Plant Physiology Faculty of Natural Sciences Comenius University in Bratislava Mlynská dolina B2 SK 842 15 Bratislava Slovakia

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Šlechtitelů 11 CZ 783 71 Olomouc Czech Republic and Department of Plant Physiology Faculty of Natural Sciences Comenius University in Bratislava Mlynská dolina B2 SK 842 15 Bratislava Slovakia Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Šlechtitelů 11 CZ 783 71 Olomouc Czech Republic and Department of Plant Physiology Faculty of Natural Sciences Comenius University in Bratislava Mlynská dolina B2 SK 842 15 Bratislava Slovakia

Zobrazit více v PubMed

Adamec L. 1997. Mineral nutrition of carnivorous plants – a review. Botanical Review 63: 273–299.

Adamec L. 2002. Leaf absorption of mineral nutrients in carnivorous plants stimulates root nutrient uptake. New Phytologist 155: 89–100. PubMed

Adamec L. 2003. Zero water flow in the carnivorous genus Genlisea. Carnivorous Plant Newsletter 32: 46–48.

Adamec L. 2006. Respiration and photosynthesis of bladders and leaves of aquatic Utricularia species. Plant Biology 8: 765–769. PubMed

Adamec L. 2007. Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae). Annals of Botany 100: 849–856. PubMed PMC

Adamec L. 2008. The influence of prey capture on photosynthetic rate in two aquatic carnivorous plant species. Aquatic Botany 89: 66–70.

Adamec L. 2010a. Dark respiration of leaves and traps of terrestrial carnivorous plants: are there greater energetic costs in traps? Central European Journal of Biology 5: 121–124.

Adamec L. 2010b. Ecophysiological look at organ respiration in carnivorous plants: a review. In: Osterhoudt G, Barhydt J, eds. Cell respiration and cell survival: processes, types and effects. New York: Nova Science Publishers, Inc., 225–235.

Adamec L. 2011. The comparison of mechanically stimulated and spontaneous firings in traps of aquatic carnivorous Utricularia species. Aquatic Botany 94: 44–49.

Adamec L. 2012. Firing and resetting characteristics of carnivorous Utricularia reflexa traps: physiological or only physical regulation of trap triggering? Phyton 52: 281–290.

Adamec L, Vrba J, Sirová D. 2011. Fluorescence tagging of phosphatase and chitinase activity on different structures of Utricularia traps. Carnivorous Plant Newsletter 40: 68–73.

Adlassnig W, Peroutka M, Lendl T. 2011. Traps of carnivorous plants as habitat: composition of the fluid, biodiversity and mutualistic activities. Annals of Botany 107: 181–194. PubMed PMC

Affolter JM, Olivo RF. 1975. Action potentials in Venus’s-flytraps: long term observations following the capture of prey. American Midland Naturalist 93: 443–445.

Albert VA, Williams SE, Chase MW. 1992. Carnivorous plants: phylogeny and structural evolution. Science 257: 1491–1495. PubMed

An C-I., Fukusaki E-I, Kobayashi A. 2001. Plasma-membrane H+-ATPases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco. Planta 212: 547–555. PubMed

Anderson B. 2005. Adaptations to foliar absorption of faeces: a pathway in plant carnivory. Annals of Botany 95: 757–761. PubMed PMC

Anderson B, Midgley JJ. 2003. Digestive mutualism, an alternate pathway in plant carnivory. Oikos 102: 221–224.

Attaran E, Major IT, Cruz JA, Rosa BA, et al. 2014. Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiology 165: 1302–1314. PubMed PMC

Baldwin IT. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences, USA 95: 8113–8118. PubMed PMC

Bazile V, Le Moguédec G, Marshall DJ, Gaume L. 2015. Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Annals of Botany 115: 705–716. PubMed PMC

Bazile V, Moran JA, Moguédec GL, Marshall DJ, Gaume L. 2012. A carnivorous plant fed by its symbiont: a unique multi-faceted nutritional mutualism. PLoS One 7: e36179. PubMed PMC

Beilby MJ. 2007. Action potential in Charophytes. International Review of Cytology 257: 43–82. PubMed

Bohn HF, Federle W. 2004. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proceedings of the National Academy of Sciences, USA 101: 14138–14143. PubMed PMC

Bonhomme V, Gounand I, Alaux C, Jousselin E, Barthélémy D, Gaume L. 2011a. The plant-ant Camponotus schmitzi helps its carnivorous host-plant Nepenthes bicalcarata to catch its prey. Journal of Tropical Ecology 27: 15–24.

Bonhomme V, Pelloux-Prayer H, Jousselin E, Forterre Y, Labat J-J, Gaume L. 2011b. Slippery or sticky? Functional diversity in the trapping strategy of Nepenthes carnivorous plants. New Phytologist 191: 545–554. PubMed

Brittnacher J. 2011. Murderous plants. Carnivorous Plant Newsletter 40: 17–18.

Bruzzese BM, Bowler R, Massicotte HB, Fredeen AL. 2010. Photosynthetic light response in three carnivorous plant species: Drosera rotundifolia, D. capensis and Sarracenia leucophylla. Photosynthetica 48:103–109.

Chandler GE, Anderson JW. 1976. Studies on the nutrition and growth of Drosera species with reference to the carnivorous habit. New Phytologist 76: 129–141.

Chase MW, Christenhusz MJM, Sanders D, Fay MF. 2009. Murderous plants: Victorian Gothic, Darwin and modern insights into vegetable carnivory. Botanical Journal of the Linnean Society 161: 329–356.

Chia TF, Aung HH, Osipov AN, Goh NK, Chia LS. 2004. Carnivorous pitcher plant uses free radicals in the digestion of prey. Redox Report 9: 255–261. PubMed

Chin L, Moran JA, Clarke C. 2010. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytologist 186: 461–470. PubMed

Clarke CM. 1997. Nepenthes of Borneo. Kota Kinabalu, Malaysia: Natural History Publication.

Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA. 2009. Tree shrew lavatories: a novel sequestration strategy in a tropical pitcher plant. Biology Letters 5: 632–635. PubMed PMC

Clarke CM, Moran JA. 2001. Ecology. In: Clarke CM, ed. Nepenthes of Sumatra and Peninsular Malaysia. Kota Kinabalu, Malaysia: Natural History Publication, 29–75.

Cresswell JE. 1998. Morphological correlates of necromass accumulation in the traps of an Eastern tropical pitcher plant, Nepenthes ampullaria Jack, and observations on the pitcher infauna and its reconstitution following experimental removal. Oecologia 113: 383–390. PubMed

Darwin C. 1875. Insectivorous plants. London: John Murray.

Darwin F. 1878. Experiments on the nutritions of Drosera rotundifolia. Journal of Linnean Society – Botany 17: 17–32.

Dézerald O, Leroy C, Corbara B, et al. 2013. Food-web structure in relation to environmental gradients and predator–prey ratios in tank-bromeliad ecosystems. PLoS One 8: e71735. PubMed PMC

Dixon KW, Pate JS, Bailey WJ. 1980. Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. With special reference to catch of arthropod fauna by its glandular leaves. Australian Journal of Botany 28: 283–297.

Eilenberg H, Pnini-Cohen S, Schuster S, Movtchan A, Zilberstein A. 2006. Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. Journal of Experimental Botany 57: 2775–2784. PubMed

Ellison AM. 2006. Nutrient limitation and stoichiometry of carnivorous plants. Plant Biology 8: 740–747. PubMed

Ellison AM, Adamec L. 2011. Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120: 1721–1731.

Ellison AM, Farnsworth EJ. 2005. The cost of carnivory for Darlingtonia californica (Sarraceniaceae): evidence from relationships among leaf traits. American Journal of Botany 92: 1085–1093. PubMed

Ellison AM, Gotelli NJ. 2001. Evolutionary ecology of carnivorous plants. Trends in Ecology and Evolution 16: 623–629.

Ellison AM, Gotelli NJ. 2002. Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. Proceedings of the National Academy of Sciences, USA 99: 4409–4412. PubMed PMC

Ellison AM, Gotelli NJ. 2009. Energetics and the evolution of carnivorous plants – Darwin’s ‘most wonderful plants in the world’. Journal of Experimental Botany 60: 19–42. PubMed

Escalante-Pérez M, Krol E, Stange A, et al. 2011. A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proceedings of the National Academy of Sciences, USA 108: 15492–15497. PubMed PMC

Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9–19. PubMed

Farnsworth EJ, Ellison AM. 2008. Prey availability directly affects physiology, growth, nutrient allocation and scaling relationships among leaf traits in 10 carnivorous plant species. Journal of Ecology 96: 213–221.

Feller U, Anders I, Mae T. 2008. Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. Journal of Experimental Botany 59: 1615–1624. PubMed

Fisahn J, Herde O, Willmitzer L, Peňa-Cortés H. 2004. Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. Plant and Cell Physiology 45: 456–459. PubMed

Frank JH, O’Meara GF. 1984. The bromeliad Catopsis berteroniana traps terrestrial arthropods but harbors Wyeomyia larvae (Diptera: Culicidae). Florida Entomologist 67: 418–424.

Fromm J, Lautner S. 2007. Electrical signals and their physiological significance in plants. Plant, Cell and Environment 30: 249–257. PubMed

Gallé A, Lautner S, Flexas J, Fromm J. 2015. Environmental stimuli and physiological responses: the current view on electrical signalling. Environmental and Experimental Botany 114: 15–21.

Gallie DR, Chang S-C. 1997. Signal transduction in the carnivorous plant Sarracenia purpurea: regulation of secretory hydrolase expression during development and in response to resources. Plant Physiology 115: 1461–1471. PubMed PMC

Galmés J, Kapralov MV, Andralojc PJ, et al. 2014. Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant, Cell and Environment 37: 1989–2001. PubMed

Gao P, Loeffler TS, Honsel A, et al. 2015. Integration of trap- and root-derived nitrogen nutrition of carnivorous Dionaea muscipula. New Phytologist 205: 1320–1329. PubMed

Gaume L, Forterre Y. 2007. A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS One 2: e1185. PubMed PMC

Gaume L, Perret P, Gorb E, Gorb S, Labat JJ, Rowe N. 2004. How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Structure and Development 33: 103–111. PubMed

Givnish TJ. 1989. Ecology and evolution of carnivorous plants. In: Abrahamson WG, ed. Plant–animal interactions. New York: McGraw-Hill, 243–290.

Givnish TJ, 2015. New evidence on the origin of carnivorous plants. Proceedings of the National Academy of Sciences, USA 112: 10–11. PubMed PMC

Givnish TJ, Barfuss MHJ, Van Ee B, et al. 2014. Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Molecular Phylogenetics and Evolution 71: 55–78. PubMed

Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD. 1984. Carnivory in the bromeliad Brocchinia reducta with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient poor habitats. American Naturalist 124: 479–497.

Givnish TJ, Sytsma KJ, Smith JF, Hahn WJ, Benzing DH, Burkhardt EM. 1997. Molecular evolution and adaptive radiation in Brocchinia (Bromeliaceae: Pitcairnioideae) atop tepuis of the Guayana Shield. In: Givnish TJ, Sytsma KJ, eds. Molecular evolution and adaptive radiation. New York: Cambridge University Press, 259–311.

Gorb E, Kastner V, Peressadko A, et al. 2004. Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. Journal of Experimental Biology 207: 2947–2963. PubMed

Gowda DC, Reuter G, Schauer R. 1983. Structural studies of an acidic polysaccharide from the mucin secreted by Drosera capensis. Carbohydrate Research 113: 113–124.

Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7: 436–439. PubMed PMC

Greenwood M, Clarke C, Lee CC, Gunsalam A, Clarke RH. 2011. A unique resource mutualism between the giant Bornean pitcher plant, Nepenthes rajah, and members of a small mammal community. PLoS One 6: e21114. PubMed PMC

Hájek T, Adamec L. 2010. Photosynthesis and dark respiration of leaves of terrestrial carnivorous plants. Biologia 65: 69–74.

Harder R, Zemlin I. 1968. Blütenbildung von Pinguicula lusitanica in vitro durch Fütterung mit pollen. Planta 78: 72–78. PubMed

Hatano N, Hamada T. 2008. Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata. Journal of Proteome Research 7: 809–816. PubMed

Hatano N, Hamada T. 2012. Proteomic analysis of secreted protein induced by a component of prey in pitcher fluid of the carnivorous plant Nepenthes alata. Journal of Proteomics 75: 4844–4852. PubMed

He J, Zain A. 2012. Photosynthesis and nitrogen metabolism of Nepenthes alata in response to inorganic NO3– and organic prey N in the greenhouse. International Scholarly Research Network Botany ID 263270.

Heil M, Baldwin IT. 2002. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7: 61–67. PubMed

Herde O, Peña-Cortéz H, Willmitzer L, Fisahn J. 1997. Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wild-type and ABA-deficient tomato plants. Plant, Cell and Environment 20: 136–141.

Hlaváčková V, Krchňák P, Nauš J, Novák O, Špundová M, Strnad M. 2006. Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225: 235–244. PubMed

Hodick D, Sievers A. 1988. The action potential of Dionaea muscipula Ellis. Planta 174: 8–18. PubMed

Ibarra-Laclette E, Albert VA, Pérez-Torres CA, et al. 2011. Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome. BMC Plant Biology 11: 101. PubMed PMC

Inselsbacher E, Cambui CA, Richter A, Stange CF, Mercier H, Wanek W. 2007. Microbial activities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea. New Phytologist 175: 311–320. PubMed

Jaffé K, Michelangeli F, Gonzales JM, Miras B, Ruiy MC. 1992. Carnivory in pitcher plants of the genus Heliamphora (Sarraceniaceae). New Phytologist 122: 733–744.

Jaffe MJ. 1973. The role of ATP in mechanically stimulated rapid closure of Venus’s flytrap. Plant Physiology 51: 17–18. PubMed PMC

Jobson RW, Nielsen R, Laakkonen L, Wikström M, Albert VA. 2004. Adaptive evolution of cytochrome c oxidase: infrastructure for a carnivorous plant radiation. Proceedings of the National Academy of Sciences, USA 101: 18064–18068. PubMed PMC

Juniper BE, Robins RJ, Joel DM. 1989. The carnivorous plants. London: Academic Press.

Karagatzides JD, Ellison AM. 2009. Construction costs, payback times, and the leaf economics of carnivorous plants. American Journal of Botany 96: 1612–1619. PubMed

Karlsson PS, Pate JS. 1992. Contrasting effect of supplementary feeding of insects or mineral nutrients on the growth and nitrogen and phosphorous economy of pygmy species of Drosera. Oecologia 92: 8–13. PubMed

Knight SE. 1992. Costs of carnivory in the common bladderwort, Utricularia macrorhiza. Oecologia 89: 348–355. PubMed

Knight SE., Frost TM. 1991. Bladder control in Utricularia macrorhiza: lake specific variation in plant investment in carnivory. Ecology 72: 728–734.

Koller-Peroutka M, Lendl T, Watzka M, Adlassnig W. 2015. Capture of algae promotes growth and propagation in aquatic Utricularia. Annals of Botany 115: 227–236. PubMed PMC

Krol E, Dziubinska H, Stolarz M, Trebacz K. 2006. Effects of ion channel inibitors on cold- and electrically-induced action potentials in Dionaea muscipula. Biologia Plantarum 50: 411–416.

Król E, Plachno BJ, Adamec L, Stolarz M, Dziubinska H., Trebacsz K. 2012. Quite a few reasons for calling carnivores ‘the most wonderful plants in the world’. Annals of Botany 109: 47–64. PubMed PMC

Kruse J, Gao P, Honsel A, et al. 2014. Strategy of nitrogen acquisition and utilization by carnivorous Dionaea muscipula. Oecologia 174: 839–851. PubMed

Laakkonen L, Jobson RW, Albert VA. 2006. A new model for the evolution of carnivory in the bladderwort plant (Utricularia): adaptive changes in cytochrome c oxidase (COX) provide respiratory power. Plant Biology 8: 758–764. PubMed

Libiaková M, Floková K, Novák O, Slováková Ľ, Pavlovič A. 2014. Abundance of cysteine endopeptidase Dionain in digestive fluid of Venus flytrap (Dionaea muscipula Ellis) is regulated by different stimuli from prey through jasmonates. PLoS One 9: e104424. PubMed PMC

Maffei ME, Mithöffer A, Boland W. 2007. Before gene expression: early events in plant–insect interaction. Trends in Plant Science 12: 310–316. PubMed

Matušíková I, Salaj J, Moravčíková J, Mlynárová L, Nap JP, Libantová J. 2005. Tentacles of in vitro-grown round-leaf sundew (Drosera rotundifolia L.) show induction of chitinase activity upon mimicking the presence of prey. Planta 222: 1020–1027. PubMed

Meldau S, Ullman-Zeunert L, Govind G, Bartram S, Baldwin IT. 2012. MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biology 12: 213. PubMed PMC

Méndez M, Karlsson PS. 1999. Costs and benefits of carnivory in plants: insights from the photosynthetic performance of four carnivorous plants in a subarctic environment. Oikos 86: 105–112.

Mithöfer A, Reichelt M, Nakamura Y. 2014. Wound and insect-induced jasmonate accumulation in carnivorous Drosera capensis: two sides of the same coin. Plant Biology 5: 982–987. PubMed

Moran JA, Moran AJ. 1998. Foliar reflectance and vector analysis reveal nutrient stress in prey-deprived pitcher plants (Nepenthes rafflesiana). International Journal of Plant Sciences 159: 996–1001.

Moran JA, Clarke CM, Hawkins BJ. 2003. From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. International Journal of Plant Sciences 164: 635–639.

Moran JA, Clarke C, Greenwood M, Chin L. 2012. Tuning of color contrast signals to visual sensitivity maxima of tree shrews by three Bornean highland Nepenthes species. Plant Signaling and Behavior 7: 1267–1270. PubMed PMC

Moran JA, Hawkins BJ, Gowen BE, Robbins SL. 2010. Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. Journal of Experimental Botany 61: 1365–1374. PubMed PMC

Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. Glutamate receptor-like genes mediate leaf-to-leaf wound signals. Nature 500: 422–426. PubMed

Nabity PD, Zavala JA, DeLucia EH. 2013. Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata. Journal of Experimental Botany 64: 685–694. PubMed PMC

Nakamura Y, Reichelt M, Mayer VE, Mithöfer A. 2013. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proceedings of the Royal Society B: Biological Sciences 280: 20130228. PubMed PMC

Nishi AH, Vasconcellos-Neto J, Romero GQ. 2013. The role of multiple partners in a digestive mutualism with a protocarnivorous plant. Annals of Botany 111: 143–150. PubMed PMC

Nishimura E, Kawahara M, Kodaira R, et al. 2013. S-like ribonuclease gene expression in carnivorous plants. Planta 238: 955–967. PubMed

Osunkoya OO, Daud SD, Di-Giusto B, Wimmer FL, Holige TM. 2007. Construction costs and physico-chemical properties of the assimilatory organs of Nepenthes species in northern Borneo. Annals of Botany 99: 895–906. PubMed PMC

Osunkoya OO, Daud SD, Wimmer FL. 2008. Longevity, lignin content and construction cost of the assimilatory organs of Nepenthes species. Annals of Botany 102: 845–853. PubMed PMC

Paszota P, Escalante-Perez M, Thomsen LR, et al. 2014. Secreted major Venus flytrap chitinase enables digestion of Arthropod prey. Biochimica et Biophysica Acta 1844: 374–383. PubMed

Pavlovič A. 2010. Spatio-temporal changes of photosynthesis in carnivorous plants in response to prey capture, retention and digestion. Plant Signaling and Behavior 5: 1325–1329. PubMed PMC

Pavlovič A. 2011. Photosynthetic characterization of Australian pitcher plant Cephalotus follicularis. Photosynthetica 49: 253–258.

Pavlovič A. 2012a. Adaptive radiation with regard to nutrient sequestration strategies in the carnivorous plants of the genus Nepenthes. Plant Signaling and Behavior 7: 295–297. PubMed PMC

Pavlovič A. 2012b. The effect of electrical signals on photosynthesis and respiration. In: Volkov A, ed. Plant electrophysiology – signaling and responses. Berlin: Springer-Verlag, 33–62.

Pavlovič A, Mancuso S. 2011. Electrical signaling and photosynthesis. Can they co-exist together? Plant Signaling and Behavior 6: 840–842. PubMed PMC

Pavlovič A, Masarovičová E, Hudák J. 2007. Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. Annals of Botany 100: 527–536. PubMed PMC

Pavlovič A, Singerová L, Demko V, Hudák J. 2009. Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis. Annals of Botany 104: 307–314. PubMed PMC

Pavlovič A, Demko V, Hudák J. 2010a. Trap closure and prey retention in Venus flytrap (Dionaea muscipula Ellis.) temporarily reduces photosynthesis and stimulates respiration. Annals of Botany 105: 37–44. PubMed PMC

Pavlovič A, Singerová L, Demko V, Šantrůček J, Hudák J. 2010b. Root nutrient uptake enhances photosynthetic assimilation in prey-deprived carnivorous pitcher plant Nepenthes talangensis. Photosynthetica 48: 227–233.

Pavlovič A, Slováková Ľ, Pandolfi C, Mancuso S. 2011a. On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis.). Journal of Experimental Botany 62: 1991–2000. PubMed PMC

Pavlovič A, Slováková Ľ, Šantrůček J. 2011b. Nutritional benefit from leaf litter utilization in the pitcher plants Nepenthes ampullaria. Plant, Cell and Environment 34: 1865–1873. PubMed

Pavlovič A, Krausko M, Libiaková M, Adamec L. 2014. Feeding on prey increases photosynthetic efficiency in the carnivorous sundew Drosera capensis. Annals of Botany 113: 69–78. PubMed PMC

Pereira CG, Almenara DP, Winter CE, Fritsch CE, Lambers H, Oliviera RS. 2012. Underground leaves of Philcoxia trap and digest nematodes. Proceedings of the National Academy of Sciences, USA 109: 1154–1158. PubMed PMC

Peroutka M, Adlassnig W, Volgger M, Lendl T, Url WG, Lichtscheidl IK. 2008. Utricularia: a vegetarian carnivorous plant? Plant Ecology 199: 153–162.

Plachno B, Adamec L, Huet H. 2009. Mineral nutrient uptake from prey and glandular phosphatase activity as a dual test of carnivory in semi-desert plants with glandular leaves suspected of carnivory. Annals of Botany 104: 649–654. PubMed PMC

Poppinga S, Hartmeyer SRH, Seidel R. 2012. Catapulting tentacles in a sticky carnivorous plant. PLoS One 7: e45735. PubMed PMC

Renner T, Specht CD. 2011. A sticky situation: assessing adaptations for plant carnivory in the Caryophyllales by means of stochastic character mapping. International Journal of Plant Sciences 172: 889–901.

Revill MJW, Stanley S, Hibberd JM. 2005. Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. Journal of Experimental Botany 56: 2477–2486. PubMed

Rice BM. 2011. What exactly is a carnivorous plant? Carnivorous Plant Newsletter 40: 19–22.

Riedel M, Eichner A, Jetter R. 2003. Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers. Planta 218: 87–97. PubMed

Rischer H, Hamm A, Bringmann G. 2002. Nepenthes insignis uses a C2-portion of the carbon skeleton of l-alanine acquired via its carnivorous organs, to build up the allelochemical plumbagin. Phytochemistry 59: 603–609. PubMed

Robins RJ, Juniper BE. 1980. The secretory cycle of Dionaea muscipula Ellis. I. The fine structure and the effect of stimulation on the fine structure of the digestive gland cells. New Phytologist 86: 279–296.

Romero GQ, Mazzafera P, Vasconcellos-Neto J, Trivelin PCO. 2006. Bromeliad-living spiders improve host plant nutrition and growth. Ecology 87: 803–808. PubMed

Rottloff S, Stieber R, Maischak H, Turini FG, Heubl G, Mithöfer A. 2011. Functional characterization of a class III acid endochitinase from the traps of the carnivorous pitcher plant genus, Nepenthes. Journal of Experimental Botany 62: 4639–4647. PubMed PMC

Rottloff S, Mithöfer A, Müller U, Kilper R. 2013. Isolation of viable multicellular glands from tissue of the carnivorous plant, Nepenthes. Journal of Visualized Experiments 82: e50993. PubMed PMC

Sadowski E-M, Seyfullaha LJ, Sadowski F, Fleischmann A, Behling H, Schmidt AR. 2015. Carnivorous leaves from Baltic amber. Proceedings of the National Academy of Sciences, USA 112: 190–195. PubMed PMC

Scharmann M, Grafe TU. 2013. Reinstatement of Nepenthes hemsleyana (Nepenthaceae), an endemic pitcher plant from Borneo, with a discussion of associated Nepenthes taxa. Blumea 58: 8–12.

Scherzer S, Krol E, Kreuzer I, et al. 2013. The Dionaea muscipula ammonium channel DmAMT1 provides NH4+ uptake associated with Venus flytrap’s prey digestion. Current Biology 23: 1649–1657. PubMed

Schulze W, Frommer WB, Ward JM. 1999. Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. The Plant Journal 17: 637–646. PubMed

Sirová D, Adamec L, Vrba J. 2003. Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytologist 159: 669–675. PubMed

Sirová D, Borovec J, Šantrůčková H, Šantrůček J, Vrba J, Adamec L. 2010. Utricularia carnivory revisited: plants supply photosynthetic carbon to traps. Journal of Experimental Botany 61: 99–103. PubMed

Sirová D, Borovec J, Picek T, Adamec L, Nedbalová L, Vrba J. 2011. Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants. Functional Plant Biology 38:583–593. PubMed

Sydenham PH, Findlay GP. 1975. Transport of solutes and water by resetting bladders of Utricularia. Australian Journal of Plant Physiology 2: 335–351.

Thorén LM, Karlsson S. 1998. Effects of supplementary feeding on growth and reproduction of three carnivorous plant species in subarctic environment. Journal of Ecology 86: 501–510.

Thorén LM, Tuomi J, Kämäräinen T, Laine K. 2003. Resource availability affects investment in carnivory in Drosera rotundifolia. New Phytologist 159: 507–511. PubMed

Thornham DG, Smith JM, Grafe TU, Federle W. 2012. Setting the trap: cleaning behaviour of Camponotus schmitzi ants increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata. Functional Ecology 26:11–19.

Vadassery J, Reichelt M, Jimenez-Aleman GH, Boland W, Mithöfer A. 2014. Neomycin inhibition of (+)-7-iso-lasmonoyl-l-isoleucine accumulation and signaling. Journal of Chemical Ecology 40: 676–686. PubMed

Vincent O, Roditchev I, Marmottant P. 2011a. Spontaneous firings of carnivorous aquatic Utricularia traps: temporal patterns and mechanical oscillations. PLoS One 6: e20205. PubMed PMC

Vincent O, Weißkopf C, Poppinga S, et al. 2011b. Ultra-fast underwater suction traps. Proceedings of the Royal Society B: Biological Sciences 278: 2909–2914. PubMed PMC

Volkov AG, Adesina T, Jovanov E. 2007. Closing of Venus flytrap by electrical stimulation of motor cells. Plant Signaling and Behavior 2: 139–145. PubMed PMC

Volkov AG, Adesina T, Markin VS, Jovanov E. 2008. Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiology 146: 694–702. PubMed PMC

Vos IA, Pieterse CMJ, van Wees SCM. 2013. Costs and benefits of hormone-regulated plant defences. Plant Pathology 62: 43–55.

Vredenberg W, Pavlovič A. 2013. Chlorophyll a fluorescence induction (Kautsky curve) in a Venus flytrap (Dionaea muscipula) leaf after mechanical trigger hair irritation. Journal of Plant Physiology 170: 242–250. PubMed

Wakefield AE, Gotelli NJ, Wittman SE, Ellison AM. 2005. Prey addition alters nutrient stoichiometry of the carnivorous plant Sarracenia purpurea. Ecology 86: 1737–1743.

Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111: 1024–1058. PubMed PMC

Wells K, Lakim MB, Schulz S, Ayasse M. 2011. Pitchers of Nepenthes rajah collect faecal droppings from both diurnal and nocturnal small mammals and emit fruity odour. Journal of Tropical Ecology 27:347–353.

Wicke S, Schäferhoff B, dePamphilis CW, Müller KF. 2014. Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. Molecular Biology and Evolution 31: 529–545. PubMed

Williams SE, Bennett AB. 1982. Leaf closure in the Venus flytrap: an acid growth response. Science 218: 1120–1121. PubMed

Williams SE, Pickard BG. 1972a. Receptor potentials and action potentials in Drosera tentacles. Planta 103: 193–221. PubMed

Williams SE, Pickard BG. 1972b. Properties of action potentials in Drosera tentacles. Planta 103: 222–240. PubMed

Williams SE, Pickard BG. 1980. The role of action potentials in the control of capture movements of Drosera and Dionaea. In: Skoog F, ed. Plant growth substances. Berlin: Springer, 470–480.

Zamora R, Gómez JM, Hódar JA. 1998. Fitness responses of a carnivorous plant in contrasting ecological scenarios. Ecology 79: 1630–1644.

Is the co-option of jasmonate signalling for botanical carnivory a universal trait for all carnivorous plants?

Water Cannot Activate Traps of the Carnivorous Sundew Plant Drosera capensis: On the Trail of Darwin's 150-Years-Old Mystery

First record of functional underground traps in a pitcher plant: Nepenthespudica (Nepenthaceae), a new species from North Kalimantan, Borneo

Alternative oxidase (AOX) in the carnivorous pitcher plants of the genus Nepenthes: what is it good for?

Recent ecophysiological, biochemical and evolutional insights into plant carnivory

Jasmonate-independent regulation of digestive enzyme activity in the carnivorous butterwort Pinguicula × Tina

Biochemical and mesophyll diffusional limits to photosynthesis are determined by prey and root nutrient uptake in the carnivorous pitcher plant Nepenthes × ventrata

Anaesthesia with diethyl ether impairs jasmonate signalling in the carnivorous plant Venus flytrap (Dionaea muscipula)