Why Are Plants Carnivorous?

1 ECOPHYSIOLOGICAL LOOK AT PLANT CARNIVORY: Why are plants carnivorous? LUBOMÍR ADAMEC Institute of Botany, Section of Plant Ecology Dukelská 135, CZ-379 82 T řebo ň, Czech Republic 1. Introduction About 650 species of vascular carnivorous (Latin: carnis – flesh, vorare – to swallow) plants occur throughout the world (e.g., Rice, 2006) out of the total of about 300,000 species of vascular plants. Carnivorous plants belong to 15-18 genera of 8-9 botanical families and 5 orders (Givnish, 1989; Juniper et al., 1989; Müller et al., 2004; Heubl et al., 2006; Porembski and Barthlott, 2006; Studni čka, 2006). Due to many remarkable and striking morphological, anatomical, physiological, and ecological features, carnivorous plants have always attracted considerable interest of both researchers and gardeners. Nevertheless, the degree and extent of knowledge of the main disciplines studying this particular ecological functional plant group has always considerably lagged behind the study of non-carnivorous plants. However, similar to the dynamically growing knowledge of non-carnivorous plants, the study of carnivorous plants has developed very rapidly and progressively within the last decade, mainly due to the use of modern molecular taxonomic approaches. Also, modern ecophysiological research of carnivorous plants has progressed considerably within the last decade and has elucidated most of the particulars of carnivorous plants. Thus we are increasingly more able to discuss to what extent carnivorous plants are unique from or common with “normal” non-carnivorous plants. The aim of this paper is to classify and review recent experimental results and concepts concerning plant carnivory from an ecophysiological point of view, with an emphasis on mineral nutrition, growth characteristics, and comparison of aquatic and terrestrial carnivorous plants. The latter two subjects have often been neglected in previous reviews (cf. Juniper et al., 1989). The present review is focused on mineral nutrition as it is believed that mineral nutrition represents the key processes and the main benefit of carnivory for these plants (Adamec, 1997a; Ellison and Gotelli, 2001). A new model of “nutritional” cost-benefit relationships is presented. However, there are several other remarkable ecological phenomena associated with carnivory, e.g., prey- pollinator conflict (Zamora, 1999), prey attraction (Givnish, 1989), prey selectivity (Harms, 1999), competition between carnivorous and non-carnivorous plants (Brewer, 1999a,b), and relationships within inquiline communities in pitcher traps (Gray et al. 2006). Most of these phenomena were thoroughly reviewed by Ellison et al. (2003) and will not be mentioned in this study. The present review follows from previous review publications in this field. Undoubtedly, Darwin (1875) was the first who summarized multilateral research on carnivorous plants, even though the main focus of his book was aimed at his studying 2 the irritability of Drosera tentacles. He was the first to prove digestion of prey and to reveal that carnivorous plants showed enhanced growth if fed on insects and/or animal proteins. Darwin’s book greatly influenced and inspired several generations of botanists and physiologists studying carnivorous plants. About 70 years after Darwin, the knowledge of carnivorous plants, based on literature items, were comprehensively reviewed in a monograph by Lloyd (1942). Physiological investigations on carnivorous plants, focusing on mineral and organic nutrition, trap excitation and movement, and digestive enzyme secretion were reviewed by Lüttge (1983). Evolution and ecological cost-benefit relationships of carnivorous plants were discussed thoroughly by Givnish (1989) in his review. Carnivorous plant biology, with an emphasis on cytology, anatomy, biochemistry, and physiology, was reviewed in detail in an excellent monograph by Juniper et al. (1989). This review includes all literature sources published before 1987-1988, and serves as a reference list of literature. In the decade after this monograph appeared, the mineral nutrition of carnivorous plants has been studied intensively. The subjects of mineral and organic nutrition of carnivorous plants as key ecophysiological processes associated with carnivory were classified and thoroughly reviewed by Adamec (1997a), who separately analyzed processes in field- and greenhouse-grown plants and also in terrestrial and aquatic carnivorous plants. Modern trends in studying carnivorous plants with an emphasis on phylogenetic diversity and cost-benefit relationships were reviewed in a well-arranged way by Ellison and Gotelli (2001). Selected ecological phenomena and processes associated with carnivory were reviewed in details by Ellison et al. (2003). Proceedings of a special Session on “Biology of Carnivorous Plants,” at the International Botanical Congress held in Vienna, Austria, in 2005, were published in a special issue of Plant Biology 8(6) in 2006 (for comments see Porembski and Barthlott, 2006). In this special issue, Ellison (2006) reviewed ecophysiological subjects of nutrient limitations in carnivorous plants and identified modern directions for this research. Finally, Guisande et al. (2007) have recently published a detailed review on the bladderwort ( Utricularia ) genus which includes also some ecophysiological points. 2. Plant carnivorous syndrome All plants considered carnivorous have to fulfill several criteria to separate them from other ecological plant groups (e.g. saprophytes). Nevertheless, due to a great diversity of ecological and functional plant traits, these criteria are still partly ambiguous (cf. Juniper et al., 1989; Adamec, 1997a). Thus, what is really crucial for a working definition of “plant carnivory”? Considering that the main ecophysiological benefit and consequence of carnivory is the uptake of growth-limiting mineral nutrients from prey, the criteria for the carnivorous syndrome (i.e. cluster of characters) may be as follows: a) capturing or trapping prey in specialized traps, b) absorption of metabolites (nutrients) from killed prey, and c) utilization of these metabolites for plant growth and development (Lloyd, 1942; Givnish 1989; Juniper et al., 1989; Adamec, 1997a). As all plants are able to absorb organic substances from soil (e.g. from dead animals), the criterion of capturing prey in traps, which actively kill prey, separates carnivorous from saprophytic plants. Moreover, Juniper et al. (1989) and many later authors state two 3 other criteria such as prey attraction and digestion. However, on the basis of recent knowledge of this issue, it is possible to conclude that these additional criteria are not indispensable for functioning of carnivorous plants. First, the ability to attract prey has only been studied and confirmed in a part of carnivorous plants yet and it is not clear whether or not it occurs in very abundant genera of carnivorous plants such as Utricularia and Genlisea (Givnish, 1989; Guisande et al., 2007; Płachno et al., unpubl.). Moreover, the study on north European Pinguicula species (Karlsson et al., 1987) did not reveal prey attraction in P. alpina , in contrast with other species, without the plant being limited by prey capture. Second, it is generally accepted that carnivorous plants can also digest prey without secreting their own hydrolytic digestive enzymes in traps, relying only on enzyme secretion by trap commensals (e.g. Givnish., 1989; Jaffe et al., 1992; Butler et al., 2008). Thus, these two additional criteria – prey attraction and digestion – may rather be considered technical details which can only improve the efficiency of carnivory but are not indispensable for carnivory as such. In an analogy with parasitic plants (holoparasites and hemiparasites), Joel (2002) proposed the term “holocarnivory” for carnivorous plants secreting their own digestive enzymes (e.g. Dionaea, Drosera, Drosophyllum, Pinguicula, Nepenthes ) and “hemicarnivory” for those plants which do not (e.g. Brocchinia , Roridula ). However, the diversity of ecological relationships concerning prey digestion is evidently wider and an additional classification can be based on the way by use of which carnivorous plants gain nutrients from prey, regardless of secretion of own enzymes. All carnivorous plants except for Roridula can gain nutrients from prey carcasses more-or-less directly and such a type of carnivory can be termed as “direct”. Two Roridula species, however, capture prolific prey but they usually do not digest it. The captured prey are grazed by kleptoparasitic hemipteran bugs Pameridea which are found only on the Roridula plants and which defecate on its surface; the plants absorb nutrients through specialized cuticular gaps (Ellis and Midgley, 1996; Midgley and Stock, 1998; Anderson et al. 2003; Anderson 2005). Thus, mineral nutrients from prey are gained indirectly , through excrements of the bugs as mediator, and this type of carnivory can be termed as “indirect”. Discussing the carnivorous syndrome, one can make a physiological look at plant carnivory and question to what extent carnivorous plants are physiologically unique within the plant kingdom. In line with Juniper et al. (1989, p. 10-11), it is possible to point out five physiological key processes which are typical and common for plant carnivory: a) rapid movements of traps; b) their electrophysiological regulation; c) hydrolytic enzyme secretion; d) foliar uptake of nutrients; e) stimulation of root nutrient uptake by foliar nutrient uptake. Yet, all

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