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TREE November 2001.Qxd Review TRENDS in Ecology & Evolution Vol.16 No.11 November 2001 623 Evolutionary ecology of carnivorous plants Aaron M. Ellison and Nicholas J. Gotelli After more than a century of being regarded as botanical oddities, carnivorous populations, elucidating how changes in fitness affect plants have emerged as model systems that are appropriate for addressing a population dynamics. As with other groups of plants, wide array of ecological and evolutionary questions. Now that reliable such as mangroves7 and alpine plants8 that exhibit molecular phylogenies are available for many carnivorous plants, they can be broad evolutionary convergence because of strong used to study convergences and divergences in ecophysiology and life-history selection in stressful habitats, detailed investigations strategies. Cost–benefit models and demographic analysis can provide insight of carnivorous plants at multiple biological scales can into the selective forces promoting carnivory. Important areas for future illustrate clearly the importance of ecological research include the assessment of the interaction between nutrient processes in determining evolutionary patterns. availability and drought tolerance among carnivorous plants, as well as measurements of spatial and temporal variability in microhabitat Phylogenetic diversity among carnivorous plants characteristics that might constrain plant growth and fitness. In addition to Phylogenetic relationships among carnivorous plants addressing evolutionary convergence, such studies must take into account have been obscured by reliance on morphological the evolutionary diversity of carnivorous plants and their wide variety of life characters1 that show a high degree of similarity and forms and habitats. Finally, carnivorous plants have suffered from historical evolutionary convergence among carnivorous taxa9 overcollection, and their habitats are vanishing rapidly. A major focus of future (Fig. 1). For example, flypaper (sticky) traps have research on this exciting group of plants should be directed towards strategies evolved independently in five eudicot families for their conservation and management. (Lentibulariaceae, Roridulaceae, Byblidaceae, Droseraceae and Dioncophyllaceae), and pitfall traps Carnivorous plants have fascinated evolutionary have arisen in three eudicot families (Sarraceniaceae, ecologists, botanists and horticulturists for centuries. Nepenthaceae and Cephalotaceae) and one monocot Early investigators were reluctant to accept that family (Bromeliaceae). Most researchers have plants could consume insects and other small followed Darwin’s lead in considering the flypaper invertebrates1; Darwin2 provided the first detailed traps of Roridula, Byblis and the Droseraceae (sensu experimental evidence for carnivory in several stricto) to be homologous2. As recently as the late genera. Since then, approximately 600 species of 1980s, researchers thought that all extant carnivorous carnivorous plants have been identified in plants were derived from a common ancestor1. six angiosperm subclasses, including both However, modern molecular data support multiple, monocotyledons and eudicotyledons3,4. Twentieth- polyphyletic origins of the carnivorous plants, and century botanists focused on describing the even flypaper traps within the traditionally anatomical specializations and physiological recognized family Droseraceae (including the sundew mechanisms associated with botanical carnivory1,5 genera Drosera and Drosophyllum) appear to be and identifying commonalities among the homoplasic. Phylogenetic analysis based on sequences carnivorous plants. In the mid-1980s, Givnish6 of the chloroplast MatK gene suggest that Droseraceae proposed a general cost–benefit model to explain the is polyphyletic and that Drosophyllum should be restriction of most carnivorous plants to well-lit, moved into its own family10. nutrient-poor, waterlogged habitats. Although Current placements of carnivorous families common ecological factors have led to some within broader angiosperm phylogenies have been evolutionary convergence, focus on ecological determined using chloroplast rbcL (Refs 3,11,12), similarities has obscured important evolutionary MatK (Ref. 10) and ORF2280 (Ref. 13) sequences, differences. Recent research on carnivorous plants nuclear ribosomal 18S RNA (Ref. 14) and internal Aaron M. Ellison* has highlighted these differences, which illustrate transcribed spacer (ITS) sequences11. For Dept of Biological the richness of ecological and evolutionary questions carnivorous taxa in three families within the Sciences, Mount Holyoke College, South Hadley, that can be approached with these plants. New Caryophyllidae, phylogenetic analyses suggest a MA 01075-6418, USA. research on carnivorous plant phylogeny informs monophyletic origin (Fig. 2)10. Molecular techniques *e-mail: aellison@ interpretations of cost–benefit analyses for the have also resolved relationships among the mtholyoke.edu evolution of carnivory in plants, use of captured prey, Sarraceniaceae, Roridulaceae and Byblidaceae, Nicholas J. Gotelli tradeoffs between attracting pollinators versus prey, which had been grouped on the basis of Dept of Biology, and overall ecological effects of the carnivorous morphological analyses as sister taxa within the University of Vermont, 1 14 Burlington, VT 05405, syndrome . Recent studies also have successfully Rosidae . The consensus tree based on rbcL, ITS and USA. modeled the demography of some carnivorous plant 18S RNA sequences places the Sarraceniaceae and http://tree.trends.com 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02269-8 624 Review TRENDS in Ecology & Evolution Vol.16 No.11 November 2001 (a) (c) structures, such as bladders and pitfalls, also evolved from ancestors possessing simpler, flypaper type traps [i.e. Roridula (flypaper) – Sarraceniaceae (pitfall; Fig. 1d); Drosera (flypaper) – Nepenthes (pitfall); Byblis (flypaper; Fig. 1c); and the butterworts Pinguicula (flypaper; Fig. 1e) – Utricularia (bladder; Fig. 1f)]3. The adaptive value of carnivory The multiple, independent evolution of carnivory in diverse plant families suggests that it is an (d) adaptation to the low nutrient, bright, waterlogged habitats in which carnivorous plants occur6. Thus, the nutritional benefits of carnivory have been a traditional focus of research16. Givnish6 proposed a cost–benefit model that predicts that carnivory is adaptive only in nutrient-poor environments that are well lit and moist (Box 1). This model requires (b) both high light and wet conditions, because the photosynthetic costs to carnivory are thought to exceed the benefits in either shady or dry habitats. Benzing17 recently extended this model by allowing (e) for explicit tradeoffs between light, moisture and nutrient availability through litter (Box 1). Benzing’s model can provide a synthetic framework for recent data showing that carnivorous taxa vary in the amount of nutrients obtained through carnivory and in the production of carnivorous structures. Testing these models requires detailed measurements of the contribution of carnivory to the nutrient budget of (f) the plant, photosynthetic rates of carnivorous and noncarnivorous organs, the relationship between nutrient uptake and photosynthesis, and production rates of carnivorous organs. Nutritional benefits of carnivory Schulze et al.18 used δ15 nitrogen (N) (Ref. 19) of soil and insects to show that carnivorous species differ significantly in their reliance on insect-derived nutrients (Table 1). In general, reliance on insect- derived N increases as carnivorous structures become Fig. 1. Photographs of Roridula as sister taxa closely related to the more elaborate (from sticky leaves of Drosera spp. to carnivorous plant taxa, Ericales3,11,14, but locates Byblis near the Solanaceae the >1 m tall pitchers of the cobra lily Darlingtonia illustrating evolution within the Asteridae14. This conclusion supports californica); the northern pitcher plant Sarracenia within clades and 20 convergent characters recent morphological analysis of the phylogenetic purpurea being a notable exception to this pattern . across clades. (a) Drosera position of Byblis based on its embryology15. The two Plants themselves vary through time in the relative binata; (b) Nepenthes remaining eudicot families of carnivorous plants, contribution of insect-derived N to total plant rafflesiana; (c) Byblis filifolia; (d) Sarracenia Lentibulariaceae and Cephalotaceae, have been N content. In the four genera of pitcher plants purpurea; (e) Pinguicula placed respectively in the Lamiidae and Geraniales, (Cephalotus, Darlingtonia, Nepenthes and vulgaris; (f) Utricularia based on rbcL sequences3. Sarracenia), juveniles have nonfunctional pitchers, radiata. All photographs Sequence data also provide insights into the origins and derive their N from the soil and from insects by Aaron M. Ellison. and evolution of carnivorous structures, with some captured by older pitchers18. By contrast, young surprises. Although carnivory has long been considered functional pitchers that capture insects retain to be a highly derived character9, within the virtually all the nutrients that they derive from prey carnivorous clade of the Caryophyllidae (Fig. 2) and do not shunt nutrients to nonfunctional carnivory is a basal trait within the Droseraceae pitchers18. Similarly, new bladders of the aquatic (flypaper traps; Fig. 1a) that is retained in the common bladderwort Utricularia vulgaris
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