REVIEW-ARTICLE |
Energetics and the evolution of carnivorous plants—Darwin's ‘most wonderful plants in the world’
1Harvard Forest, Harvard University, 324 North Main Street, Petersham, MA 01366, USA
2Department of Biology, University of Vermont, 120 Marsh Life Sciences Building, Burlington, VT 05405, USA
* To whom correspondence should be addressed. E-mail: aellison{at}fas.harvard.edu
Received 6 May 2008; Revised 5 June 2008 Accepted 16 June 2008
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Abstract |
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Carnivory has evolved independently at least six times in five angiosperm orders. In spite of these independent origins, there is a remarkable morphological convergence of carnivorous plant traps and physiological convergence of mechanisms for digesting and assimilating prey. These convergent traits have made carnivorous plants model systems for addressing questions in plant molecular genetics, physiology, and evolutionary ecology. New data show that carnivorous plant genera with morphologically complex traps have higher relative rates of gene substitutions than do those with simple sticky traps. This observation suggests two alternative mechanisms for the evolution and diversification of carnivorous plant lineages. The ‘energetics hypothesis’ posits rapid morphological evolution resulting from a few changes in regulatory genes responsible for meeting the high energetic demands of active traps. The ‘predictable prey capture hypothesis’ further posits that complex traps yield more predictable and frequent prey captures. To evaluate these hypotheses, available data on the tempo and mode of carnivorous plant evolution were reviewed; patterns of prey capture by carnivorous plants were analysed; and the energetic costs and benefits of botanical carnivory were re-evaluated. Collectively, the data are more supportive of the energetics hypothesis than the predictable prey capture hypothesis. The energetics hypothesis is consistent with a phenomenological cost–benefit model for the evolution of botanical carnivory, and also accounts for data suggesting that carnivorous plants have leaf construction costs and scaling relationships among leaf traits that are substantially different from those of non-carnivorous plants.
Key words: Carnivorous plants, competition, construction costs, cost–benefit model, Darwin, energetics, niche overlap, phylogeny, prey capture, universal spectrum of leaf traits
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Introduction |
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‘This plant, commonly called Venus’ fly-trap, from the rapidity and force of its movements, is one of the most wonderful in the world.’
(C. Darwin, Insectivorous plants, p. 231)1
Carnivorous plants have evolved multiple times among the angiosperms (Fig. 1), and the degree of morphological and physiological convergence across carnivorous taxa is remarkable. Molecular sequence data have revealed the phylogenetic history of the angiosperms (Stevens, 2007) and have yielded a better understanding of the patterns of evolution of carnivorous plants. The availability of reliable phylogenies, new observations and experiments, cost–benefit models (Givnish et al., 1984; Laakkonen et al., 2006), and contemporary statistical methods have allowed carnivorous plants to emerge as model systems that can be used to address a wide range of questions arising from plant molecular genetics to physiology and evolutionary ecology (Ellison and Gotelli, 2001; Ellison et al., 2003).
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Charles Darwin laid the foundation for modern research on carnivorous plants. In Insectivorous plants, Darwin (1875) applied his then relatively new conception of homology to illustrate evolutionary and functional convergence across seemingly unrelated taxa. He provided the first detailed descriptions of the structures by which eight genera of plants could entrap insects. With careful observations and clever experiments, Darwin determined for the first time that these plants directly dissolved animal protein using enzymes whose action was similar to pepsin and other proteases (see also Hepburn et al., 1919, 1927). He further showed that dissolved nutrients were directly absorbed by carnivorous plants and that captured prey contributes significantly to plant growth (Darwin, 1875).
Drawing on >125 years of subsequent research, this review surveys recent progress in three areas of inquiry that Darwin initiated in Insectivorous plants: (i) the tempo and mode of carnivorous plant evolution; (ii) patterns and processes of prey capture; and (iii) the energetic costs and benefits of botanical carnivory. These three research fronts are unified by stable phylogenetic placement of carnivorous taxa, new data on gene evolution in carnivorous plants (Jobson and Albert, 2002; Müller et al., 2004), and the refinement by Laakkonen et al. (2006) of the cost–benefit model for the evolution of botanical carnivory originally formulated by Givnish et al. (1984).
Current understanding of the phylogenetic placement of carnivorous plants re-affirms the occurrence of convergence in trapping mechanisms. Genomic data suggest biochemical, physiological, and ecological mechanisms that could have led to the rapid diversification of at least some carnivorous plant lineages. New analyses of published data on prey capture permit the evaluation of the degree of specialization among carnivorous plant genera and link evolutionarily convergent traits with the ecologically important process of predation. The use of carbon to measure both costs and benefits of carnivory allows carnivorous plants to be placed into the ‘universal spectrum of leaf traits’ (Wright et al., 2004, 2005) that reflects fundamental trade-offs associated with the allocation of carbon to structural tissues and photosynthesis (Shipley et al., 2006).
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The tempo and mode of carnivorous plant evolution |
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‘By comparing the structure of the leaves, their degree of complication, and their rudimentary parts in the six genera [Drosophyllum, Roridula, Byblis, Drosera, Dionaea, and Aldrovanda], we are led to infer that their common parent form partook of the characters of Drosophyllum, Roridula, and Byblis.’
(Insectivorous plants, p. 289)
‘It stands accordingly to reason that the carnivorous plants are quite as old as angiospermy, as an independent angiospermous group bound with still older groups eventually beyond the limits of angiospermy.’
(Croizat, 1960: 129)
In The origin of species, Darwin (1859) asserted the importance of homology—the similarity of traits resulting from shared ancestry—for understanding evolutionary relationships. Although the importance of homologous traits (including sequences of DNA, genes, and proteins) in reconstructing phylogenies is widely recognized, actually identifying them remains a challenge. Nowhere is this challenge more evident than in the history of the placement of carnivorous plants in angiosperm phylogenies (Juniper et al., 1989). A proper interpretation of patterns of prey capture, gene sequence data, and the evolution of carnivory all rely on firm knowledge of the phylogenetic placement of carnivorous plants and on stable nomenclature. Therefore, this review begins with a survey of current knowledge of carnivorous plant systematics, focused on how recent syntheses of molecular and morphological data illuminate the two most disparate hypotheses for the evolution and diversification of carnivorous plants: Darwin's (1875) hypothesis that the specialization and evolutionary novelty of carnivorous plants indicated convergence in independent lineages, and Croizat's (1960) hypothesis that carnivory evolved once near the base of the angiosperm lineage.
Darwin asserted that all of the species with sticky-leaf (or ‘flypaper’) traps in the genera Drosera, Byblis, Roridula, and Drosophyllum, along with the snap-trapping Venus’ fly-trap (Dionaea muscipula Ellis) and the water-wheel plant (Aldrovanda vesiculosa L.) were closely related (19th century botanists placed all six genera in the Droseraceae, the sundew family). In Insectivorous plants, he discussed in detail the apparent homology of the sessile glands that they use to digest prey. He also asserted that neither the butterworts (Pinguicula) (or the other Lentibulariaceae: Genlisea and Utricularia) nor the Asian pitcher plants (Nepenthes) were ‘at all related to the Droseraceae’ (Insectivorous plants, p. 292). Darwin appears to have had little familiarity with the American pitcher plants (Sarracenia, Darlingtonia, and Heliamphora), nor did he discuss the Australian pitcher plant Cephalotus follicularis Labill. (Cephalotaceae),2 but it is safe to say that he recognized at least three lineages of carnivorous plants: his ‘Droseraceae’, the Lentibulariaceae, and the (Asian) pitcher plants (Nepenthaceae).
In contrast to Darwin, Croizat (1960) asserted a common origin for all carnivorous plants and placed them close to the base of the entire angiosperm lineage.3 Croizat (1960) asserted that the Lentibulariaceae, and in particular Utricularia, was the basal angiosperm group, with morphological evolution proceeding from the relatively amorphous Utricularia with its vestigial leaves, stems, and roots that are barely distinguishable from one another, to plants with more differentiated characters including cladodes, shoots, and leaves. In Croizat's view, Nepenthes was derived directly from Utricularia.4 Although the scant fossil record of carnivorous plants does suggest a long evolutionary history for at least some taxa (Thanikaimoni and Vasanthy, 1974; Li, 2005; Heubl et al., 2006), modern phylogenetic analyses of molecular markers and DNA sequences suggest that carnivorous plants are highly derived, polyphyletic taxa. Contrary to Croizat's (1960) assertions, carnivorous plants do not represent a monophyletic ancestral Ur-angiosperm, nor are the vestigial structures of Utricularia evolutionary precursors to the more familiar morphological characters of higher plants.
Progress in resolving familial relationships
‘[C]onstructive discussion is out of the question, and attempts made at demonstrating, e.g., that Utricularia is "derivative" forthwith disqualify their proponents as essentially ill informed.’
(Croizat, 1960: 120)
Carnivorous plants can be found in four of the major angiosperm lineages (the Monocots, Core Eudicots, Rosids, and Asterids), and in five orders: Poales, Caryophyllales, Oxalidales, Ericales, and Lamiales (Fig. 1). Convergence of carnivorous plants and their traps is most apparent at the ordinal level, whereas gene sequences have distinguished between convergence and homology within orders, families, and genera.
Over 95% of the >600 species of carnivorous plants are currently placed within the Caryophyllales and Lamiales (Fig. 1). New combined analyses based on sequences of the trnK intron and its associated matK gene, additional chloroplast genes (atpB, rbcL), and nuclear 18S rDNA have clarified relationships among carnivorous families within the Caryophyllales (Heubl et al., 2006). These analyses simultaneously confirm one of Darwin's notions of homology,5 but dispel another:6 Aldrovanda vesiculosa and Dionaea muscipula are sister taxa, and this clade of snap-trappers is a sister group to the sundews (Drosera) with their sticky leaves (Cameron et al., 2002; Rivadavia et al., 2003).
Three other carnivorous families—Nepenthaceae, Drosophyllaceae, and Dioncophyllaceae—are also clearly rooted within the Caryophyllales (Fig. 1). All three of these families are in a large clade linked to the Droseraceae by a common ancestor, presumably one with flypaper traps. Contrary to Darwin's hypothesis that Nepenthes was ‘not at all related to the Droseraceae’ (Insectivorous plants, p. 292), this genus (i.e. its monogeneric family, the Nepenthaceae) is the sister group of the Droseraceae (Fig. 1). The dewy pine Drosophyllum lusitanicum Link is now firmly established in its own family (Drosophyllaceae), and carnivory appears to have been re-derived in the Dioncophyllaceae by the flypaper-trapping Triphyophyllum peltatum (Hutch. & Dalz.) Airy Shaw (Cuenoud et al., 2002; Heubl et al., 2006).
Carnivory also had more than one independent origin in the Lamiales (Müller et al., 2004, 2006; Fig. 1). As in the Caryophyllales, evolution of the trap structure in carnivorous Lamiales has proceeded from flypaper traps in Pinguicula to the more complex, unidirectionally twisted ‘eel’ traps in Genlisea and the bladder traps of Utricularia with their unique suction mechanism (Lloyd, 1942; Guisande et al., 2007). At least half of all described carnivorous species are in these three genera, which historically were linked based on shared floral characters (Taylor, 1989). Contemporary molecular analysis unites them based on shared sequences in the trnL and rps16 introns, rbcL, the functional coxI and matK genes, and 5.8S rDNA (Jobson and Albert, 2002; Jobson et al., 2003; Müller et al., 2004, 2006; Cieslak et al., 2005). Despite Croizat's posthumous protestations to the contrary, both genetic and morphological data support the monophyly of the Lentibulariaceae, with Pinguicula sister to a Genlisea–Utricularia clade. However, contrary to Albert et al. (1992), it is clear that the other carnivorous family in this order, the Byblidaceae (fide P
achno et al., 2006), is neither directly ancestral to the Lentibulariaceae nor even closely related to it (Fig. 1).
The three remaining carnivorous dicot families—Roridulaceae, Sarraceniaceae, and Cephalotaceae—illustrate variations on the convergent theme of trap evolution. Based on rbcL and 18S rDNA analyses, the African endemic Roridulaceae (two species) was considered to be the sister to the American Sarraceniaceae (three genera, 27 species) in the Ericales (Albert et al., 1992; Conran and Dowd, 1993). However, the current placement of these two families in the overall angiosperm phylogeny (Stevens, 2007) reverses this, and has the Sarraceniaceae with its pitcher traps sister to a clade containing the sticky-leaved Roridulaceae and the non-carnivorous Actinidicaceae. If this placement is confirmed, it would represent one instance among carnivorous plant lineages of morphologically more complex traps (here, pitchers) being ancestral to simpler sticky traps. Similarly, the Australian endemic Cephalotus follicularis (Cephalotaceae) has no apparent sticky-leaved ancestor (Fig. 1).
Within the monocots, carnivory has also evolved at least twice in the Bromeliaceae genera Brocchinia (B. hectioides Mez, B. reducta Baker, and possibly B. tatei L.B. Smith) (Givnish, et al., 1984; Benzing et al., 1985) and Catopsis berteroniana (Schultes & Schultes) Mez (Frank and O'Meara, 1984). As with Cephalotus, there is no apparent sticky-leaved sister group to these bromeliads with pitcher traps.
Progress in resolving generic and subgeneric relationships
‘...at the present moment, I care more about Drosera than the origin of all the species in the world.’
(Darwin 1860, in a letter to Charles Lyell7)
As the ordinal placement and systematics of carnivorous plant families have stabilized, attention has turned to resolving relationships among the genera and to resolving subgeneric relationships in the most speciose carnivorous genera—Drosera, Nepenthes, Pinguicula, Genlisea, Utricularia, and Sarracenia. In most cases, phylogenetic patterns based only on inferred homologous morphological traits have been misleading. However, when morphological data have been combined with molecular analyses, novel insights into the evolution and biogeography of these carnivorous plant genera have emerged.
Drosera:
As mentioned above, Drosera, Dionaea, and Aldrovanda form a well-supported clade, with snap-trapping having evolved only once in the clade consisting of Dionaea and Aldrovanda (Cameron et al., 2002; Rivadavia et al., 2003). The infrageneric classification of Drosera, on the other hand, has gone through many revisions. All data point to the basal position of D. regia Stephens, a South African narrow endemic, in the monophyletic Drosera clade. Beyond that conclusion, however, there is little concordance among different proposed phylogenies and subgeneric classifications.
Seine and Barthlott (1994) proposed a morphology-based classification of Drosera consisting of three subgenera and 11 sections, but this classification is not congruent with phylogenies based on molecular data alone (Rivadavia et al., 2003; Williams et al., 2004) or on combining molecular and morphological data (Rivadavia et al., 2003). Further, different statistical analyses of rbcL data (e.g. using MacClade in Rivadavia et al., 2003 and PAUP in Williams et al., 1994) do not concur. For example, Williams et al. (1994) identified a ‘capensis’ clade consisting of South African and non-Australian temperate species, but this clade was not clearly identified by Rivadavia et al. (2003), who sequenced many more species than did Williams et al. (1994). Rivadavia et al. (2003) hypothesized that Drosera originated in southern Africa or in Australia; that South American species arose by dispersal from Australia; and that African species other than D. regia and D. indica L. were subsequently derived from South American ancestors. While shades of Croizat and Gondwanan vicariance could be inferred from this analysis, a Gondwanan origin of Drosera is not supported by the recent evolution of the Droseraceae (Rivadavia et al., 2003). Clearly much more work remains to be done in this genus.
Nepenthes:
About 90 species of Nepenthes, the sister group to the Droseraceae, occur throughout southeast Asia, with many endemics on Borneo and Sumatra. Biogeographic outliers (disjuncts) occur in India (N. khasiana Hook. f.), Sri Lanka (N. distillatoria L.), the Seychelles (N. pervillei Blume), and Madagascar (N. madagascarensis Poir. and N. masoalensis Schmid-Hollinger) (Meimberg et al., 2001; Meimberg and Heubl, 2006). Morphology has been of limited use in resolving systematic relationships in this genus (Jebb and Cheek, 1997), but phylogenetic analysis of Nepenthes has improved dramatically as molecular data have accrued (Meimberg et al., 2001; Meimberg and Heubl, 2006). Both chloroplast (trnK intron and matK gene) and nuclear (PRT1 along with a non-plastid, translocated copy of trnK) genes have been used in phylogenetic reconstruction (Meimberg et al., 2001; Meimberg and Heubl, 2006). These results suggest that the five western, biogeographically disjunct species listed above are ancestral to three clades consisting of the Indo-Malayan species. The relatedness and, more importantly, the biogeographic origins of these latter species suggest repeated colonizations and radiations by Nepenthes within the Indonesian islands throughout the Tertiary (Meimberg and Heubl, 2006).
Pinguicula:
As with studies of Drosera and Nepenthes, the new cladistic analyses of Pinguicula do not agree with historical subgeneric classifications (Casper, 1966; Legendre, 2000). Based on sequencing of trnK/matK and morphological analysis of 46 of the 
80 species of Pinguicula, Cieslak et al. (2005) found high levels of support for five discrete, geographically bounded lineages. This fundamental result supplanted and simplified earlier subgeneric and sectional classifications (three subgenera and 12 sections; Casper, 1966; Legendre, 2000). In Cieslak et al.’s (2005) new classification, the basal lineage appears to be tropical, with successive branchings of clades consisting of Eurasian species, East Asian species, the Eurasian P. alpina L., and a Central American/Mexican/Caribbean group (Cieslak et al., 2005; Müller et al., 2006). However, phylogenetic reconstruction based on sequencing nrITS1 and nrITS2 of 29 species of Pinguicula offered a different picture (Degtjareva et al., 2006). Although both phylogenies found some support for a derived Central American/Mexican/Caribbean clade, and the nrITS-based phylogeny was reasonably congruent with Casper's (1966) morphological classification, the remaining clades identified by the nrITS-based phylogeny were polyphyletic in the trnK-based phylogeny (Cieslak et al., 2005). Resolving the infrageneric phylogeny of Pinguicula requires clearer definition of informative morphological and molecular characters as well as sequence data from a wider range of species.
Genlisea and Utricularia:
In contrast to the ongoing systematic confusion in Pinguicula, sequence data from matK, trnK, rbcL, rps16, and trnL-F (Jobson et al., 2003; Müller et al., 2004, 2006) generally have supported the infrageneric grouping of the 21 species of Genlisea based on differences in the way capsules dehisce (Fischer et al., 2000). The South American subgenus Tayloria is sister to a clade consisting of three African species and five additional South American species. The African species do not form a natural clade, as the East African/Madagascan species G. margaretae Hutchinson is more closely related to the South American species than it is to the remaining African species (Fischer et al., 2000; Müller et al., 2006).
The 220 species of Utricularia have been organized into three subgenera and 21 sections. Analysis of trnL-F, rps16, and trnK sequence data (Jobson et al., 2003; Müller and Borsch, 2005) suggested a refinement of the three subgenera Polypompholyx, Bivalvia, and Utricularia. Taylor's (1989) 34 sections based on morphology were, with three exceptions (sections Iperua, Setiscapella, and Psyllosperma), upheld as monophyletic. Current analysis suggests a single terrestrial origin for bladderworts in South America; the aquatic and epiphytic habits of Utricularia species appear to have been re-derived multiple times within the genus (Jobson et al., 2003; Müller and Borsch, 2005; Müller et al., 2006).
Greilhuber et al. (2006) reported the remarkable result that many species of Genlisea and Utricularia have very small nuclear genome sizes. In fact, they found that Genlisea margaretae (C-value = 63 Mbp), G. aurea St. Hil. (64 Mbp), Utricularia gibba L. (88 Mbp), U. blanchetii A.DC. (135 Mbp), and U. parthenopipes P. Taylor (140 Mbp) have smaller C-values than that found for the previous record holder for the smallest angiosperm genome, Arabidopsis thaliana (L.) Heynh. (157 Mbp). Neither the functional significance nor the potential role in evolutionary diversification of this apparent genome simplification in Genlisea and Utricularia is known.
Sarracenia:
Recent genetic analyses have revealed perhaps the most taxonomic surprises in the American pitcher plants (Sarraceniaceae). Three sets of phylogenetic reconstructions, one based only on the chloroplast rbcL gene (Albert et al., 1992), another that used rbcL along with two nuclear ITS regions of rDNA (Bayer et al., 1996), and a third that used ITS-2 along with the 26S rRNA gene (Neyland and Merchant, 2006), have all supported the monophyly of the Sarraceniaceae. Older analyses of biogeographical (Croizat, 1960; McDaniel, 1971; Maguire, 1978), palynological (Thanikaimoni and Vasanthy, 1972), and morphological (Macfarlane, 1893; deBuhr, 1977; Maguire, 1978; Juniper et al., 1989) data have traditionally grouped the North American genera Sarracenia and Darlingtonia together and posited that the South American genus Heliamphora was either sister to, or derived from, a Sarracenia–Darlingtonia clade. In contrast, all of the molecular data suggest that Darlingtonia is sister to a derived Sarracenia–Heliamphora clade. This result is concordant with Renner's (1989) hypothesis that modern-day Sarraceniaceae are derived from a widespread common ancestor (or ancestral stock).
These results do not settle the long-standing debate about whether the common ancestor of modern Sarraceniacae was Neotropical (South America) or subtropical (southeast North America) (Bayer et al., 1996; Neyland and Merchant, 2006). However, these results do help in resolving species-level relationships within the genus Sarracenia. Three distinct clades now seem plausible in this genus: one consisting of S. psittacina Michx., S. minor Walt., and S. flava L.; another consisting of S. rubra Walt. (sensu lato), S. alata Wood, S. oreophila (Kearney) Wherry, and S. leucophylla Raf.; and a third consisting of S. purpurea L. (sensu lato).
Neither Bayer et al. (1996) nor Neyland and Merchant (2006) provide support for separation of the S. rubra complex into the separate species and subspecies S. jonesii Wherry, S. alabamensis Case & Case, S. rubra ssp. gulfensis Schnell, S. rubra ssp. wherryi (Case & Case) Schnell, and S. rubra ssp. rubra Walt. (Case and Case, 1974, 1976; Schnell, 1977, 1979b; Godt and Hamrick, 1998). Although the S. rubra complex is clearly derived within the genus (Romeo et al., 1977), the molecular data provide no apparent discrimination among them. The repeated failure to distinguish them as distinct taxa raises questions about the separate listing of S. jonesii and S. alabamensis as endangered species in the USA.
In contrast to the lack of taxonomic differentiation within S. rubra, there do appear to be significant differences among named taxa within S. purpurea. This species was divided by Gleason and Cronquist (1991) into two varieties (considered to be subspecies by Schnell, 2002), S. purpurea purpurea (Raf.) Wherry and S. purpurea venosa (Raf.) Wherry; the latter has been further subdivided into three varieties: venosa (Raf.) Fernald; montana Schnell & Determann; and burkii Schnell (Schnell, 1979a, 1993; Schnell and Determann, 1997) or two varieties (venosa, montana) and the separate species S. rosea Naczi, Case & Case (Naczi et al., 1999). The ITS-2 and 26S rRNA analyses confirmed an earlier study based on allozymes (Godt and Hamrick, 1999); all data clearly separate S. purpurea venosa var. burkii from the other named varieties of S. purpurea venosa and S. purpurea purpurea, and support its elevation to S. rosea (Neyland and Merchant, 2006). Because S. rosea is endemic to the Florida panhandle, additional data on its distribution, demography, and threats to its persistence are immediately needed to determine if it should be a candidate for listing as threatened or endangered at either the state or federal level.
Furthermore, both the allozyme work (Godt and Hamrick, 1999) and the molecular analysis (Neyland and Merchant, 2006) linked the two varieties of S. purpurea venosa more closely to each other than to S. purpurea purpurea; and the three taxa diverge from each other by about as much as S. rosea diverges from the S. purpurea clade (Neyland and Merchant, 2006). Thus, either the three other subspecies/varieties of S. purpurea each should be raised to species status (as tentatively suggested by Neyland and Merchant, 2006), or they should be considered as a single species with broad geographic variability (as suggested by Gleason and Cronquist, 1991; Ellison et al., 2004).
Rates of genetic change and new hypotheses arising from carnivorous plant genomics
As phylogenetic hypotheses have stabilized and as more gene sequence data have accrued for carnivorous plant species, comparative analyses of evolutionary rates of the different taxa have become possible. Initial attention has focused on the Lentibulariaceae because of the extreme specialization in trap morphology within the derived genera Utricularia and Genlisea. Jobson and Albert (2002) found that relative rates of nucleotide substitutions (based on RRTree computations: Robinson-Rachavi and Huchon, 2000) in seven loci (trnL/matK intron, trnL second exon, trnL-F spacer, rps16 intron, cox1, and 5.8S RNA) occurred 4–14 times faster in Utricularia than in Pinguicula. Similarly, Müller et al. (2004) reported that Genlisea and Utricularia have relative rates of nucleotide substitutions (relative to an Amborella+Nymphaeales outgroup) in matK that are 63% higher than they are in Pinguicula.8 Müller et al. (2004) also found that substitution rates of Genlisea and Utricularia were higher than those of 292 other angiosperm taxa, and that four other carnivorous plant genera—Pinguicula, Drosera, Nepenthes, and Sarracenia—had substitution rates more in line with those of other angiosperms (Fig. 2).
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, where CPi is the relative substitution rate of carnivorous plant species i (see text footnote 8 for caveats in using this estimator). Figure reprinted from Müller (2004) with permission of the author and the publisher, Georg Thieme Verlag KG.Two hypotheses have been suggested to account for the high rates of molecular evolution observed in Utricularia and Genlisea. First, Jobson and Albert (2002) hypothesized that a single or small number of changes in regulatory genes could have led to rapid morphological evolution in Utricularia. In particular, Jobson et al. (2004) focused on the coxI subunit of cytochrome c oxidase. They showed that a unique motif of two contiguous cysteine residues in coxI has been subject to strong selection, and this novel structure of coxI in Utricularia could help to provide the additional metabolic energy required to reset Utricularia traps.
As Darwin and Croizat both noted, Utricularia shows little differentiation between stems, shoots, and leaves. Such ‘relaxed’ morphology is often observed in aquatic and epiphytic habitats, where neutral buoyancy (in the water) or other supporting structures (for epiphytes) obviate the need for structural tissues (such as large stems or wood). Thus, the combination of a unique molecular mutation in a key metabolic pathway and the relaxed morphological requirements of aquatic and epiphytic habitats has been hypothesized to be the driver of morphological diversity in this genus (Jobson et al., 2004; Laakkonen et al., 2006). We refer to this hypothesis as the ‘energetics hypothesis’.
Alternatively, Müller et al. (2004) pointed to the extreme specialization of the traps in Genlisea and Utricularia relative to the sticky leaves of Pinguicula and Drosera and the pitfalls of Nepenthes and Sarracenia as paralleling the differences in genetic substitution rates (Fig. 2). Like Jobson et al. (2004), Müller et al. (2004) suggested that high mutation rates in Utricularia and Genlisea are related to relaxed morphological constraints. However, Müller et al. (2004) further argued that morphological evolution in carnivorous plants was achievable because they can directly take up large biosynthetic building blocks, such as amino acids, peptides, and nucleotides, that the plants obtain from capturing and dissolving prey. Importantly, Müller et al. (2004) suggested that Utricularia and Genlisea have more predictable and frequent captures of prey in their habitats relative to the other carnivorous genera, and that there is a positive feedback between this reliable supply of prey and further morphological evolution. We refer to this hypothesis as the ‘predictable prey capture hypothesis’.
These two hypotheses were formulated for carnivorous Lentibulariaceae (Genlisea and Utricularia relative to Pinguicula), but the general pattern of complex traps being derived relative to simple (sticky-leaf) traps (Fig. 1) suggests that these hypotheses could apply across carnivorous plant lineages. Although the broader application of these hypotheses to other carnivorous plant lineages is necessarily speculative, testing between the energetics and predictable prey capture hypotheses nonetheless could provide further insights into factors driving the evolution of carnivorous plants. These analyses are the focus of the subsequent sections of this paper.
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Pattern and process in prey capture by carnivorous plants |
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TopAbstractIntroductionThe tempo and mode...Pattern and process in...What do they do...Conclusions and directions for...References |
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‘Now it would manifestly be a great disadvantage to the plant [Dionaea muscipula] to waste many days in remaining clasped over a minute insect, and several additional days or weeks in afterwards recovering its sensibility; inasmuch as a minute insect would afford but little nutriment. It would be far better for the plant to wait for a time until a moderately large insect was captured, and to allow all the little ones to escape; and this advantage is secured by the slowly intercrossing marginal spikes, which act like the large meshes of a fishing-net, allowing the small and useless fry to escape.’
(Insectivorous plants, pp. 251–252).
The available phylogenetic data suggest that in all carnivorous lineages except perhaps the Sarraceniaceae/Roridulaceae clade (Fig. 1), complex traps (pitchers, eel traps, bladders) are derived relative to sticky-leaved, flypaper traps (Ellison and Gotelli, 2001). Müller et al. (2004) hypothesized that carnivorous genera with rapidly evolving genomes (Genlisea and Utricularia) have more predictable and frequent captures of prey than do genera with more slowly evolving genomes; by extension it could be hypothesized that, in general, carnivorous plants with more complex traps should have more predictable and frequent captures of prey than do those with relatively simple traps. Increases in predictability and frequency of prey capture could be achieved by evolving more elaborate mechanisms for attracting prey, by specializing on particular types of prey, or, as Darwin suggested, by specializing on particular (e.g., large) sizes of prey. In all cases, one would expect that prey actually captured would not be a random sample of the available prey. Furthermore, when multiple species of carnivorous plants co-occur, one would predict, again following Darwin,9 that interspecific competition would lead to specialization on particular kinds of prey.
The accumulated contents of carnivorous plant traps can provide an aggregate record of the prey that have been successfully ‘sampled’ by the plant. Over the past 80 years, many naturalists, botanists, and ecologists have gathered data on prey contents of carnivorous plants from around the world. Such samples can be used to begin to test the hypothesis that carnivorous plant genera differ in prey composition and to look for evidence of specialization in prey capture. Here these data are summarized and synthesized in a meta-analysis to test for differences in prey composition among carnivorous plant genera, and to look for evidence of specialization in prey capture.
The data
Prey capture data were gathered from 30 studies that were published (in the literature or in otherwise unpublished MSc and PhD theses) between 1923 and 2007. These studies encompass 87 records of prey capture for 46 species of carnivorous plants in eight genera: Drosera (13 species), Dionaea (one species), Triphyophyllum (one species), Nepenthes (11 species), Pinguicula (seven species), Utricularia (five species), Sarracenia (seven species), and Brocchinia (one species). The geographic scope of these data is similarly broad, encompassing all continents on which carnivorous plants occur. Each record (prey composition of a single plant taxon at a single locality) was treated as an independent observation, and no distinction was made in terms of within- and between-species variability within each plant genus. Most studies contained from dozens to thousands of individual prey items; the one record of Drosera rotundifolia measured by Judd (1969) in southwestern Ontario, Canada that contained only six individual prey items was excluded from the analysis. Using designations in the original publications, prey were classified into 43 taxonomic groups. For insects, these taxonomic groups were usually orders, although virtually all authors distinguished ants from other Hymenoptera, and this distinction was retained in the analysis. There were a few coarser classifications (e.g. ‘Other insects’, ‘Mollusca’), but prey in these categories were very rare.
In the majority of the studies, the original data consisted of counts of individual prey, usually pooled from traps of several plants. Some studies of Pinguicula and other sticky-leaved plants recorded the number of prey per leaf area, whereas others summarized data as percentages of captures per trap or as numbers of individuals per trap. For the purposes of the present analyses, all of the observations were converted to the proportion of prey collected for each species within a study. Most carnivorous plants consume a wide range of prey; a notable documented exception is Nepenthes albomarginata Lobb ex Lindl., which, based on field observations (Kato et al., 1993; Merbach et al., 2002) and stable isotope analysis (Moran et al., 2001), appears to prey almost exclusively on termites. Among other terrestrial carnivorous plants, captured prey is dominated by ants and flies (Fig. 3), whereas captured prey of aquatic Utricularia spp. is dominated by Cladocera (mean=37% of prey) and cyclopoid copepods (mean=36% of prey).10
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Do different carnivorous plant genera specialize on particular prey?
Methods of data analysis
The first question considered was whether there was any indication of specialization by different carnivorous plant genera. A specialist would be one whose prey consisted of many individuals of only a few prey taxon, whereas a generalist predator would have prey consisting of relatively few individuals spread among many different prey taxon. A useful index of specialization is Hurlbert's (1971) probability of an interspecific encounter (PIE):
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In this analysis, PIE has a simple and direct statistical interpretation: if an investigator randomly sampled two individual prey items from the same trap (or set of traps that are pooled for a species in a site), what are the chances that they represented two different prey taxa? A value of PIE close to 1 implies that the carnivorous plant genus was not a prey specialist because any two randomly sampled prey items would probably be from different prey taxa. In contrast, a value of PIE close to 0 implies specialization on a single prey taxon because any two randomly sampled prey items would probably be the same. Note that the value of PIE contains no information about the identity of the prey taxa, only the numbers of prey taxa and the relative distribution of individuals among them. Thus, two carnivorous plant genera might have identical values of PIE, but share no prey taxa in common.
In addition to PIE, the proportion of prey items represented by ants (Formicidae) and the proportion represented by flies and mosquitoes (Diptera), two of the most important prey taxa for most carnivorous plants, were also analysed. PIE and the proportion of ants and flies were arcsine-square root transformed prior to analysis (Gotelli and Ellison 2004). A one-way ANOVA was used to compare the response variables among the different genera of carnivorous plants, without distinguishing among within- and between-species variation within a genus. Statistical analyses were conducted using R version 2.6.1.11
Results:
The analysis of prey capture spectra using PIE suggests that different carnivorous plant genera differ significantly in their relative degree of taxonomic specialization, at least at the ordinal level of prey diversity (F7,79=2.03, P=0.009). The analysis included a low outlier for Drosera erythrorhiza Lindl. (Watson et al., 1982) in which 10 826 of 10 911 prey items counted (99.2%) were Collembola (PIE=0.015), and only one sample for the genus Triphyophyllum (Green et al., 1979), the most generalist taxa measured (PIE=0.802). However, removal of these two taxa from the analysis did not alter the qualitative conclusion; PIE still differed among genera (F6,78=3.84, P=0.002). The most specialized carnivorous plant genera in the analysis were the pitcher plants Brocchinia (PIE=0.189), Nepenthes (PIE=0.452), and Sarracenia (PIE=0.491), and the most generalized genera were Triphyophyllum (PIE=0.802) and Utricularia (PIE=0.713; Fig. 4A).
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Differences among genera in the capture of particular prey taxa were also very strong. Genera differed dramatically in the proportion of ants and flies captured (ants, F7.79=36.01, P < 10–15; flies, F7,79=8.29, P=1.5x10–7). The pitcher plants Brocchinia, Nepenthes, and Sarracenia had the highest proportions of ants in their diets (90, 73, and 55%, respectively), reflecting their higher specialization values (low PIE). Captures of ants were much less frequent for the sticky traps of Drosera (3.4%) and Pinguicula (0.5%), and for the aquatic, bladder-trapping Utricularia (0%). Flies predominated in the diets of Drosera (44%) and Pinguicula (52%) (Fig. 4C), but were uncommon prey for Utricularia (3%) and Sarracenia (14%). A notable outlier was a single study of Sarracenia purpurea by Judd (1959), in which 690 of 1095 prey (63%) were Diptera (not identified to suborders or families by Judd, 1959).
Collectively, these results illustrate that different genera of carnivorous plants do indeed selectively capture different prey taxa. In some cases, the differences simply reflect habitat differences: ants and adult flies are unavailable to aquatic Utricularia or terrestrial Utricularia with subterranean traps. However, the statistical significance of differences in captures of flies and ants by pitchers (Sarracenia and Nepenthes) and sticky traps (Drosera and Pinguicula) is not dependent on the inclusion of Utricularia in the analysis, but rather do appear to reflect the different morphological specializations in these genera.
Are they really specialists? Comparisons of captured prey and available prey
Although the frequencies of prey collected in carnivorous plant traps are rarely equiprobable, a predominance of a single prey taxon, such as ants, need not indicate specialization because some taxa simply may be more abundant than others. In five published studies (Watson et al., 1982; Zamora 1990, 1995; Antor and García, 1994; Harms 1999), the investigators not only collected prey from carnivorous plants but also used passive traps in the habitat to sample available prey. Watson et al. (1982) used life-sized and -shaped cardboard models of Drosera erythrorhiza coated with Hyvis 10 (a tacky inert compound based on polymerized butane) to assess prey available to Drosera erythrorhiza in the field. Zamora (1990) used life-sized and -shaped paper or wooden models to assess prey available to Pinguicula nevadense (Lindbg.) and P. vallisneriifolia Webb., respectively. Antor and García (1994) used sticky cards in one year (1990) and sticky, life-sized, leaf-shaped models in another year (1991) to assess prey available to Pinguicula longifolia Ram. ex. DC ssp. longifolia. Harms (1999) used grab samples to determine prey available to Utricularia intermedia Hayne, U. minor L. and U. vulgaris L.
The appropriate null hypothesis is that the carnivorous plant is a passive trap: the relative abundance of the different prey categories does not differ from the relative abundance of prey in the environment. The alternative hypothesis is that some prey taxa are selectively attracted or captured by the plant. Under the alternative hypothesis, there should be a significant difference in the relative proportions of prey caught and the relative proportions of prey available.
Methods of data analysis:
To quantify the similarity of the prey captured by plants to the prey collected in passive traps, we used the Jaccard index, J (Jaccard, 1901):
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Results:
In all cases, JChao was close to 1.0, indicating a very high similarity between prey captured by the plants and prey captured by inert traps or taken in a grab sample (Fig. 5). For each pairwise comparison (captures by plants versus prey available), the confidence interval bracketed 1.0 (Fig. 5), so the null hypothesis that these carnivorous plants were behaving as passive sampling traps could not be rejected. The occasional observations of mass captures of locally abundant insects (Oliver, 1944; Evans et al., 2002) are in line with this conclusion, as is Folkerts's (1992) observation that the majority of ants captured by Sarracenia minor, S. flava, and S. purpurea in the southeast USA are the very abundant, non-native fire ant Solenopsis invicta Buren. These results do not necessarily imply that carnivorous plants are not ‘specialized’ in their diets. Rather, the observed degree of specialization is similar to that of a simple passive trap of similar size and shape. Unique coloration (e.g. Schaefer and Ruxton, 2008) or chemical attractants (e.g. Jaffe et al., 1995; Moran, 1996) of some carnivorous plant genera do not appear to contribute much to the composition of captured prey. Rather, selectivity of a trap can be understood largely based on the simple geometry of its size, shape, and orientation. As a caveat, note that the majority of these results are for genera (Pinguicula, Sarracenia) that have traps that have relatively passive mechanisms for attracting prey.
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Niche overlap among co-occurring carnivorous plants
Darwin (1859) speculated that competition between species is more severe within a genus. If this is true, co-occurring congeners should partition important ecological resources, such as space, food, or time (Schoener, 1974). Such partitioning should be reflected in relatively low niche overlap between pairs of species. For carnivorous plants, this question can be phrased as whether co-occurring congeners show any evidence of partitioning or specialization on different categories of prey. Folkerts (1992) provided prey utilization data on five Sarracenia species that co-occur in the southeastern USA. Porch (1989), Thum (1986), van Achterberg (1973), and Verbeek and Boasson (1993) provided data on co-occurring species of Drosera in, respectively, the southeastern USA, Germany, The Netherlands, and southwestern Australia. These same data were part of the prey utilization analyses described above, but here these data are isolated for more detailed analysis of niche overlap.
Methods of data analysis:
How much niche overlap would be expected by chance, in the absence of any competition? The EcoSim software (Gotelli and Entsminger, 2007) was used to quantify niche overlap using Pianka's (1973) index of overlap in resource use:
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Results:
For the most species-rich assemblages [five species of Sarracenia (Folkerts, 1992) and five species of Drosera (Verbeek and Boasson, 1993)], niche segregation was not observed (Table 1). In the Sarracenia assemblage, the highest observed niche overlap was between Sarracenia flava and Sarracenia purpurea (overlap = 0.99), and the lowest overlap was between Sarracenia leucophylla and Sarracenia psittacina (overlap=0.26). The average overlap for all 10 unique pairs was 0.637 (Table 1), which is about midway between complete segregation (0.0) and complete overlap (1.0). However, in the simulated ‘null assemblages’, the average niche overlap was only 0.197, and the observed overlap in the real Sarracenia community was larger than that found in 998 out of 1000 simulation trials. Thus, the real five-species Sarracenia assemblage (and all pairwise comparisons) showed significantly more niche overlap than expected by chance (P=0.002), directly contradicting the hypothesis of niche segregation in sympatry.
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Similar results were found for five species of co-occurring Drosera at the Fitzgerald River site in southwestern Australia (Verbeek and Boasson, 1993). Observed pairwise niche overlaps ranged from 0.65 (D. menziesii versus D. paleacea) to 0.92 (D. glanduligera versus D. paleacea). The average overlap for the pooled assemblage was 0.534, >96% of the 1000 simulations (Table 1). This result again suggested significantly more niche overlap than expected by chance (P=0.04).
The high overlap in both cases was clear from an inspection of the raw data. Except for S. leucophylla, which favoured Diptera, all co-occurring Sarracenia primarily captured ants (Folkerts 1992). The relatively modest morphological differences between co-existing species of Sarracenia did not translate into appreciable differences in composition of prey captured, suggesting that competition for limiting resources was not regulating species co-existence. Similarly, among co-occurring Drosera at Fitzgerald River, prey composition was dominated by Collembola, Homoptera, and Diptera (Verbeek and Boasson, 1993).
No evidence of interspecific competition was found among the Sarracenia assemblages composed of two or three species (Folkerts, 1992), or among the two- or three-species assemblages of Drosera in the southeastern USA, Germany, The Netherlands, and at Murdoch University (van Achterberg, 1973; Thum, 1986; Porch, 1989; Verbeek and Boasson, 1993) (Table 1). In all cases, the observed niche overlap was significantly greater than expected (Table 1), which was the opposite of the pattern that would be predicted by competitive segregation of prey.
The two caveats to these results are that prey were identified only to orders and that the analysis assumed that all prey categories were equally abundant. Finer taxonomic resolution of prey could reveal less overlap among prey. If the assumption of equal abundance of prey categories is violated, the analytic method used tends to overestimate the amount of niche overlap because the results are dominated by common taxa. In contrast, when independent estimates of prey abundance are available, values of prey actually used can be rescaled to downweight the importance of common prey (for further discussion of statistical issues associated with measures of niche overlap, see Gotelli and Graves, 1996). Unfortunately, the studies used here for assessing niche overlap did not include independent estimates of prey availability.
Rates and efficiency of prey capture by pitcher plants and bladderworts
‘From an examination which I made to-day on a leaf of the S. flava about half grown, I am led to suspect that the surface, where the fly stands so unsteadily, and from which it finally drops down to the bottom of the tube, is either covered with an impalpable and loose powder, or that the extremely attenuated pubescence is loose. This surface gives to the touch the sensation of the most perfect smoothness. The use of a good microscope will determine this point.’
The statistical analysis of the prey spectra (Figs 3 and 4) revealed that at relatively coarse taxonomic resolution (genera of plants, orders of prey), carnivorous plants act as opportunistic sit-and-wait predators, capturing prey in proportion to their availability (Fig. 5), and rarely competing with co-occurring congeners (Table 1). Additional evidence from several species of pitcher plants and bladderworts, however, suggests that these taxa do have some adaptations to increase the rates and efficiency of capture of specific prey items, at least under certain environmental conditions.
Detailed observations of Sarracenia purpurea using video cameras (Newell and Nastase, 1998) and of Darlingtonia californica Torrey using multiple observers (Dixon et al., 2005) found that fewer than 2% of ants visiting S. purpurea or wasps visiting D. californica were successfully captured by the plants. These observations were made under sunny and relatively dry field conditions. Similar rates of ant captures by Nepenthes rafflesiana Jack. (Bohn and Federle, 2004; Bauer et al., 2008) were observed under sunny and dry conditions. However, when the pitcher lip (peristome) of N. rafflesiana was wetted by rain, condensation, or secretion of nectar by the extrafloral nectaries lining the peristome, it became, like that of Macbride's (1818) Sarracenia flava, a nearly frictionless surface. Foraging ants that contacted the wetted peristome ‘aquaplaned’ and slipped into the pitcher in very large numbers (Bauer et al., 2008); capture rates by N. rafflesiana under humid or wet conditions often reached 100% of foraging ants (Bauer et al., 2008). As the other pitcher plants—Cephalotus and all the Sarraceniaceae—also have extrafloral nectaries ringing the peristome (Vogel, 1998; Pachno et al., 2007), it is not unreasonable to hypothesize that these taxa also have peristomes that could be wetted to increase prey capture rates. Hopefully, we will not have to wait another 200 years for a good microscopist to test this hypothesis for the other groups of pitcher plants!
Adaptations to enhance prey capture by bladderworts have also been postulated. The suction trap (described in detail by Lloyd, 1942; Guisande et al., 2007) of Utricularia is a highly specialized structure that is activated when a passing animal touches a trigger hair (Lloyd, 1942 illustrated it as a ‘better mousetrap’). When triggered, the trap opens inward, the prey is sucked in to the water-filled trap, the door closes, and the prey is digested and absorbed. Finally, the water is pumped out and the trap is reset. This energy-intensive process appears to be facilitated by the evolutionary change in coxI described above (Jobson et al., 2004).
Beginning with Darwin (1875) investigators have hypothesized that periphyton growing on the hairs and bristles surrounding the trap attract zooplankton that graze their way down to the trigger hairs. This hypothesis was verified experimentally for U. vulgaris by Meyers and Strickler (1979) and for U. foliosa L. (Díaz-Olarte et al., 2007). However, the presence and species composition of periphyton on hairs and bristles of Utricularia appear to depend on local environmental conditions (Díaz-Olarte et al., 2007), not on a direct facilitation of periphyton growth by Utricularia (cf. Ulanowicz, 1995). Determining causal relationships between environmental conditions, morphological structures, and prey capture rates and efficiency by Utricularia remains an active area of research.
Do fly-traps really catch only large prey?
[Of 14 Dionaea leaves sent to Darwin by William M. Canby], ‘[f]our of these had caught rather small insects, viz. three of them ants, and the fourth a rather small fly, but the other ten had all caught large insects, namely five elaters, two chrysomelas, a curculio, a thick and broad spider, and a scolopendra....But what most concerns us is the size of the ten larger insects. Their average length from head to tail was 0.256 of an inch, the lobes of the leaves being on average 0.53 of an inch in length, so that the insects were very nearly half as long as the leaves within which they were enclosed. Only a few of these leaves, therefore, had wasted their powers by capturing small prey, though it is probable that many small insects had crawled over them and been caught, but had then escaped through the bars.’
(Insectivorous plants, p. 252)
Our analyses suggest that carnivorous plants are not selective predators with respect to prey composition. However, is there any evidence that, as Darwin hypothesized, they capture only relatively large prey? Here the data are limited to two small collections of prey contents of the Venus’ fly-trap, Dionaea muscipula (Darwin, 1875; Jones, 1923). In both cases, some assumptions had to be made to reconstruct the data and test the hypothesis that Dionaea prey are unusually large.
Darwin (1875) provided the average size of only the 10 largest prey (0.256 inch=6.5 mm); the sizes of the four smaller prey items (three ants and a fly) were not reported. Jones (1923) gave a bit more detail for 50 dissected Dionaea leaves, each with one prey item: of the 50 prey items recovered, ‘only one was less than 5 mm in length, and only seven, less than 6 mm; ten were 10mm or more in length, with a maximum of 30 mm’ (Jones 1923: 593). Jones also reported that the average length of the prey was 8.6 mm, and the normal minimum observed was 6.4 mm (approximately the average length of Darwin's subsample).
Based on Jones's (1923) reported size intervals, prey size distributions were simulated using R version 2.6.1 as being drawn from a mixture of three normal distributions [N(5.5, 0.25), N(20, 5), and N(8, 1)]12, with sample sizes respectively equal to 7 (‘less than 6 mm’, but more than 5 mm), 10 (‘10mm or more in length, with a maximum of 30 mm’), and 32 (the remainder, unenumerated by Jones, but by inference being between 6 and 10 mm long), plus one outlier (4 mm), corresponding to the one ‘less than 5 mm in length’). This mixture gave a skewed distribution of prey sizes with mean=9.3 mm, and a median=7.6 mm. Darwin's distribution of prey was similarly simulated as a mixture of two normals: N(6.5, 1) and N(5.5, 0.25) with sample sizes of 10 and 4, respectively. Because Darwin gave no information on the size of the four small prey items, the sample of small prey sizes in this mixture was drawn from the same distribution as Jones's small prey. This mixture gave a skewed distribution of prey sizes with mean=6.0 mm and a median=5.8 mm. The two distributions are shown in Fig. 6.
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The relevant question is whether either of these data sets support the hypothesis that the average size of prey that Dionaea captures is at least half the length of a 13.5 mm leaf (Darwin's ‘0.53 of an inch’). A plausible way to determine this is to create replicate bootstrapped samples (i.e. with replacement) of the available data and use these bootstrapped samples to estimate the population mean and confidence intervals (Efron, 1982).
The sample function in R was used to create 10 000 bootstrapped samples of both Darwin's and Jones's prey size data. The estimated mean of the small population from which Darwin drew his sample was 6 mm (95% CI=5.70–6.38), which fails to support the hypothesis that Dionaea catches prey that is on average half as large as the trap (6.75 mm). In contrast, the estimated population mean of Jones's larger sample was 9.3 mm (95% CI=7.92–10.86), a result that is more in line with Darwin's expectation.
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What do they do with all that prey? The energetics of botanical carnivory |
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TopAbstractIntroductionThe tempo and mode...Pattern and process in...What do they do...Conclusions and directions for...References |
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‘Ordinary plants...procure the requisite inorganic elements from the soil by means of their roots....[T]here is a class of plants which digest and afterwards absorb the animal matter, namely, all the Droseraceae, Pinguicula, and, as discovered by Dr. Hooker, Nepenthes.’
(Insectivorous plants, p. 365)
Based on his detailed observations of feeding behaviour and nutrient absorption, Darwin discussed how carnivorous structures might have evolved in plants. Later authors (e.g. Lloyd, 1942; Juniper et al., 1989) generally followed his lead. Little attention was paid to why botanical carnivory might evolve until Givnish et al. (1984) proposed a cost–benefit model to explain why carnivorous plants are most common in habitats that are bright and wet but very low in nutrients. Givnish et al.’s (1984) model postulated a trade-off between the nutrients gained by capturing animals and the energy foregone by constructing photosynthetically inefficient traps instead of leaves. Givnish et al. (1984) asserted that carnivory would be expected to evolve if the increased nutrients provided by carnivory gave plants possessing carnivorous structure an energetic advantage relative to co-occurring non-carnivorous plants. This model was elaborated by Benzing (2000), who additionally considered decaying litter as a nutrient source and a third axis of selection. Both models were initially derived from studies of carnivorous bromeliads, but the cost–benefit framework has been used to interpret results from a wide range of observational and experimental studies on many carnivorous plant species (reviewed by Ellison and Gotelli, 2001; Ellison, 2006).
The benefits of carnivory
Givnish et al. (1984) identified three ways in which nutrients acquired through carnivory could result in energetic benefits to the plants. First, photosynthesis could increase with increasing nutrient uptake (following prey capture and digestion). This photosynthetic benefit could be realized through either an increase in the total mass of leaves the plant can support or an increased Amass. Secondly, the excess nutrients derived from carnivory could be disproportionately allocated to reproduction. This allocation to reproduction should be measurable either as a positive relationship between prey captured and seeds produced or as an increase in nutrient content within the seeds. Thirdly, if carnivorous plants could extract carbon from prey, they could bypass photosynthesis as a means of producing sugars. This last benefit could be most important for aquatic carnivorous plants, as CO2 used for photosynthesis is often limiting because it must be obtained by diffusion from the surrounding water (Adamec, 1997a, 1997b, 2006).
Most studies on the benefits of carnivory have found that plants significantly increase growth (in terms of leaf mass or total biomass) in response to prey additions (see Table 1 of Ellison, 2006). However, detailed measurements of photosynthesis of carnivorous plants in response to prey or nutrient additions—the primary measure of the first hypothesized benefit of carnivory—have generated more equivocal results. Méndez and Karlsson (1999) reported no significant increase in photosynthetic rates of Pinguicula villosa L., P. vulgaris L., or Drosera rotundifolia when they were provided supplemental prey. Adamec (2008) found that the photosynthetic rate of Aldrovanda vesiculosa increased following prey additions, but that of Utricularia australis decreased following prey additions. However, for both species, supplemental prey caused an increase in growth rates (Adamec, 2008). Wakefield et al. (2005) also reported no significant change in photosynthetic rates of Sarracenia purpurea pitchers fed additional prey in a field study, although tissue N and P concentrations did increase with feeding level. Nutrient storage in new Sarracenia pitchers (Butler and Ellison, 2007) or reproductive structures (see below) are alternative sinks for excess nutrients derived from prey captured by existing pitchers. For example, in a greenhouse study of prey addition to 10 species of Sarracenia, Amass increased in new pitchers, and photosystem II stress (as measured by fluorescence) decreased with prey additions (Farnsworth and Ellison, 2008).
The second postulated benefit of carnivory has also been demonstrated. Temperate-zone Pinguicula species, which exhibit reproductive pre-formation (buds set in year y flower and produce seeds in year y+1; Worley and Harder, 1999), increased vegetative reproduction in the year of prey additions and also increased sexual reproduction in subsequent years (Thorén and Karlsson, 1998; Worley and Harder, 1999). In P. vallisneriifolia, neither flower set nor fruit set changed with prey additions, but seed set (measured as seed:ovule ratio) did increase (Zamora et al., 1997). A similar increase in seed:ovule ratio in response to prey availability and inorganic nutrient addition was observed in Sarracenia purpurea (Ne'eman et al., 2006), which also makes pre-formed buds (Shreve, 1906). Three other Pinguicula species (P. alpina, P. villosa, and P. vulgaris) all preferentially allocated nitrogen to reproductive structures (Eckstein and Karlsson, 2001). Both fruit set and seed set of Drosera intermedia and D. rotundifolia were positively correlated with prey captured (Thum, 1989; Stewart and Nilsen, 1992). Experimental prey additions subsequently confirmed these correlative results (Thum, 1988).
In summary, increases in plant growth, nutrient storage, and reproduction in response to increased prey have been documented in a number of carnivorous plant species, although evidence for elevated photosynthetic rates is weak. To date, there is only scant evidence for Givnish et al.’s (1984) third prediction, that of heterotrophic uptake of C from prey. Fabian-Galan and Savageanu (1968) found that 14C from labelled Daphnia fed to both Aldrovanda vesiculosa and Drosera capensis L. was incorporated into leaf and stem tissues and into new growing tips of these carnivorous plants. Similarly, Drosera erythrorhiza stored 14C from labelled flies in new growth (Dixon et al., 1980). Additional evidence for facultative heterotrophy in carnivorous plants is most likely to be found in aquatic carnivorous plants (Adamec, 1997a, 1997b, 2006), as dissolved CO2 can limit photosynthetic rates in submerged plants.
The costs of carnivory
The costs of carnivory have been assessed much less frequently than the benefits, perhaps because measuring energy foregone is more difficult than measuring increased growth, photosynthetic rates, or seed set. However, the existing measurements do suggest that the costs can be substantial. Among carnivorous plants with flypaper traps, carbon and nutrients (in proteins) must be allocated to construction of specialized leaf glands, sticky mucilage, and digestive enzymes. Pate (unpublished data, as cited in Pate, 1986, p. 320) reported that Australian Drosera spp. allocated 3–6% of net photosynthate to the production of mucilage for leaf glands. In shaded conditions when light levels fell well below photosynthetic saturation, Pinguicula vallisneriifolia reduced its mucilage production, presumably because it lacked sufficient carbon (Zamora et al., 1998). At the opposite extreme, when nutrients were added to the soil, Drosera rotundifolia reduced its mucus gland production (Thorén et al., 2003). This result was attributable to the avoidance of the costs of carnivory when nutrients were obtained at a lower carbon cost.
Similar plasticity has been observed in Utricularia spp. and Sarracenia spp. When prey or dissolved nutrients were plentiful, the number of carnivorous bladders declined significantly in U. macrorhiza Le Conte (Knight and Frost, 1991), U. vulgaris (Friday, 1992), and U. foliosa (Guisande et al., 2000, 2004). Bladder traps are photosynthetically inefficient, and Knight (1992) calculated that U. macrorhiza of a given mass without bladders would grow 1.2–4.7x faster than U. macrorhiza of the same mass with bladders. Likewise, Sarracenia purpurea produced non-carnivorous leaves (phyllodia) when inorganic nutrients were added to levels comparable with atmospheric inputs from anthropogenic sources, and these phyllodia photosynthesized 25% faster than did carnivorous pitchers (Ellison and Gotelli, 2002). Similar results were obtained for S. purpurea and eight other species of Sarracenia fed supplemental prey (Farnsworth and Ellison, 2008). The related Darlingtonia californica had absolute levels of Amass of carnivorous plants that were 30–50% lower than predicted from scaling relationships between leaf nitrogen content and Amass of non-carnivorous plants (Ellison and Farnsworth, 2005), and similar departures from the universal spectrum of leaf traits have been observed for other species of Sarracenia (Farnsworth and Ellison, 2008).
Photosystems of carnivorous plants do appear to be nutrient limited. Fluorescence measurements of greenhousegrown Sarracenia species suggested significant ‘stress’ of photosystem II at low levels of prey capture, and this stress was alleviated by prey additions (Farnsworth and Ellison, 2008). Observations of spectral reflectance also implied low chlorophyll content and similar photosystem stress in Nepenthes rafflesiana in the field (Moran and Moran, 1998). Overall photosynthetic nitrogen use efficiency (µmol CO2 mol N s–1; Aerts and Chapin, 2000) is 50% lower for carnivorous plants than for non-carnivorous plants (P=1.3x10–14, t-test; Fig. 7); and photosynthetic phosphorus use efficiency is 60% lower for carnivorous plants than for non-carnivorous plants (P=5.5x10–7, t-test; Fig. 7). These data on photosynthetic nutrient use efficiency further support the hypothesis that carnivorous plants are outliers with respect to scaling relationships between tissue nutrient content and Amass that have been compiled for thousands of non-carnivorous species (Wright et al., 2004, 2005). However, the data for non-carnivorous plants come from a wide range of habitats and plant life-forms. It is not known whether carnivorous plants have higher photosynthetic nutrient use efficiencies than co-occurring non-carnivorous plants. However, there is no evidence to suggest that carnivorous plants and non-carnivorous plants are actually competing for nutrients (Brewer, 1999a, 1999b, 2003).
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Can carnivorous plants escape Hobson's Choice?
Where to elect there is but one,‘Tis Hobson's choice—take that, or none.
(from England's reformation, by Thomas Ward; 1710)
The observations that carnivory appears to be energetically costly, that excess nutrients do not lead directly to increasing photosynthetic rates in existing leaves or traps, and that photosynthetic nutrient use efficiency of carnivorous plants is extremely low led Ellison and Farnsworth (2005) to suggest that botanical carnivory is an evolutionary Hobson's Choice—the last resort when nutrients are scarcely available from the soil. Two new lines of evidence challenge this interpretation, however.
First, two recent studies have shown that the actual energetic costs of constructing carnivorous traps are significantly lower than the energetic costs of constructing phyllodia of carnivorous plants (Osunkoya et al., 2007; Karagatzides and Ellison, 2009) or leaves of non-carnivorous plants (Fig. 8). These data include not only ‘passive’ traps (flypaper traps of Drosera, pitfall traps of Nepenthes and Sarracenia) but also the ‘active’ snap-traps of Dionaea. Thus, carnivorous traps are relatively inexpensive structures that provide substantial nutrient gain for little energetic cost; thus, it would take very little photosynthetic gain to yield a substantial marginal benefit13 from a small investment in carnivory.
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Not all active traps are equally active, however. The snap-trap of the Venus’ fly-trap uses a mechanical trigger (the mechanism of which is still poorly understood) passively to release elastic energy stored in the fully hydrated leaf (Forterre et al., 2005). This relatively cheap trap is rarely reset; rather, after one (rarely two or three) captures, the trap senesces (Darwin, 1875). In contrast, Utricularia’s suction trap is used multiple times, and must be reset after it captures prey (Lloyd, 1942). Pumping out water is an energetically expensive process, and how Utricularia bears this cost has come to light only recently.
Jobson et al. (2004) found that the coxI gene in Utricularia has a markedly different structure—with two contiguous cysteines—from that seen in 99.9% of coxI sequences recorded from Archaea, bacteria, or eukaryotes. This dicysteine motif causes a conformational change that at least partly decouples this protein's electron transport function from its proton pumping function. Laakkonen et al. (2006) estimated that this conformational change optimizes power output when the bladder trap is reset. Although there is an associated respiratory cost to this change, this cost ought to be offset by gains due to carnivory. Laakkonen et al. (2006) modified Givnish et al.’s (1984) original cost–benefit model to replace photosynthetic costs with respiratory costs. The rapid rate of gene substitution rates in Utricularia (Müller et al., 2004; see Fig. 2) further suggests that once this mutation arose in coxI, selective pressures on Utricularia were relaxed and ‘runaway’ morphological evolution occurred in this genus. Whereas this mutation in coxI has been completely or partially lost in Genlisea, its rapid rate of evolution has been attributed to the smaller energetic costs of the passive, albeit morphologically complex, eel traps in that genus (Jobson et al., 2004). Measurements of construction costs of traps in Pinguicula, Genlisea, and Utricularia would shed additional light on the generality of this hypothesis.
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Conclusions and directions for future research |
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The integration of three research areas—the tempo and mode of carnivorous plant evolution as revealed through molecular analysis; the dynamics of prey capture illuminated with rigorous statistical analysis; and the physiological energetics of botanical carnivory in the context of cost–benefit models—has dramatically improved our understanding of many of the questions that Darwin first raised in Insectivorous plants. This integration also permits the evaluation of existing hypotheses that may explain the evolution of carnivorous plants and the convergence of trap structures in a wide range of angiosperm lineages. The well-documented restriction of carnivorous plants to low-nutrient, high-light, and wet environments was explained phenomenologically by a cost–benefit model (Givnish et al., 1984). Molecular data have revealed novel mutations and accelerated mutation rates in carnivorous plants, suggesting plausible alternative mechanisms underlying this phenomenological model (Jobson et al., 2004; Müller et al., 2004; Laakkonen et al., 2006). Analyses of carnivorous plant nutrient physiology, trap and leaf construction costs, and overall physiological energetics support the hypothesis that mutations in coxI provide an energetic boost in the Genlisea–Utricularia clade. Statistical analyses support the hypotheses that carnivorous plants have evolved varying degrees of prey specialization (Fig. 4), although there is no evidence for niche partitioning among co-existing congeners (Table 1).
This review also raises unanswered questions and highlights research needs in the areas of carnivorous plant systematics and taxonomy, dynamics of prey capture, and physiological energetics. Priority areas include the following.
Systematics and taxonomy
- By identifying a key configurational change in coxI, Jobson et al. (2004) found a plausible molecular and physiological pathway to botanical carnivory. Are there alternative pathways that overcome the energetic costs of carnivory in other carnivorous plant lineages, including others within unrelated carnivorous groups within the Lamiales?
- Molecular data have strongly supported infrageneric morphology-based classification systems for the speciose carnivorous genera of Utricularia and Genlisea, but do not agree with morphological-based classifications of Drosera, Pinguicula, or Sarracenia. Better integration of morphological and molecular data (cf. Williams et al., 1994), along with full genomic sequences of representative carnivorous plant species, could help to resolve phylogenies of many groups of carnivorous plants
- Complete genomic data also would allow for less biased estimates of mutation rates in carnivorous plants relative to non-carnivorous plants, and could provide an explanation for the remarkably low C-values found in Utricularia and Genlisea (Greilhuber et al., 2006). C-values are well known to be correlated with cell size (Gregory, 2001), which in turn may be correlated with bladder size. Further analysis of the relationship between trap size (and prey capture rates; see, for example, Sanabria-Aranda et al., 2006), cell size, and C-values of Utricularia would be illuminating.
- The genetic analyses to date have suggested some biogeographical anomalies. Examples include repeated transoceanic dispersal events in Drosera; repeated colonizations of the Indonesian islands by Nepenthes; and evidence that Darlingtonia is sister to a Sarracenia–Heliamphora clade. As better distributional data and genetic data become available, these should be explicitly linked (using tools such as GeoPhyloBuilder14) to create formal phylogeographic hypotheses regarding the origin and diversification of carnivorous plants.
Dynamics of prey capture
- Prey capture data should be better resolved taxonomically; existing, ordinal data clearly are quite coarse, but family- (and lower) level data are harder to come by. Specialization and niche segregation may become more apparent if prey are sorted to finer taxonomic levels.
- Measures of specialization, niche overlap, capture rate, and capture efficiency are all potentially biased without parallel measurements of available prey (cf. Gotelli and Graves, 1996) and prey size. Future studies of prey capture by carnivorous plants should also measure the relative abundance of potential prey in the surrounding habitat.
- The dichotomy between ‘passive’ and ‘active’ traps needs to be rethought. Darwin observed movement by the tentacular glands in Drosera and hypothesized selectivity in size of prey captured by Dionaea. Macbride (1818) proposed the existence of a frictionless peristome in Sarracenia, and Federle and his colleagues (Bohn and Federle, 2004; Bauer et al., 2008) found such frictionless surfaces in Nepenthes. The amount of friction, however, can be controlled either by environmental conditions (rain, fog) or by the plant itself (nectar secretion). Because hypotheses regarding the evolution and diversification of carnivorous plants depend, at least in part, on mechanisms and rates of prey capture, renewed attention should be focused on the activity of ‘passive’ traps, especially in the pitcher plants and in Genlisea.
- Similarly, better assessment of the relative importance of environmental control and direct control by the plant itself of periphyton abundance on Utricularia traps and its role in prey capture will help to clarify exactly how active these traps are (Lloyd, 1942; Meyers, 1982). Such studies will also expand the focus of research on prey capture by carnivorous plants beyond simple predator–prey models (cf. Ulanowicz, 1995; Díaz-Olarte et al., 2007).
Carnivorous plant energetics
- The benefits of botanical carnivory are well established (Ellison, 2006). More importantly, an assessment of the relationship (or lack thereof) between changes in growth rate and underlying ecophysiological processes such as photosynthesis and respiration or tissue nutrient content and stoichiometry (see Shipley, 2006) would unify the currently discordant data on responses of carnivorous plants to experimental prey and nutrient additions.
- Available data indicate that most responses to prey addition do not occur in the fed traps, but in traps and leaves that are subsequently produced (Butler and Ellison, 2007; Farnsworth and Ellison, 2008). Therefore, not only should future studies assess changes in Amass in leaves produced subsequently to feeding, but they should also better delineate where nutrients are stored and how they are subsequently remobilized in current and future growing seasons. Stable isotopes can be used effectively for such studies (Butler and Ellison, 2007; Butler et al., 2008).
- Measurements of the costs of carnivorous structures have lagged well behind measurements of the benefits. Estimates of trap construction costs in the Lentibulariaceae and other carnivorous Lamiales are needed to complement existing data on Sarraceniaceae and carnivorous Caryophyllales.
- Many derived lineages of carnivorous plants have separated traps from photosynthetic structures: phyllodia of Nepenthes, Cephalotus, and Sarracenia; leaves of Utricularia and Genlisea; and loss of carnivory in Triphyophyllum as the plant matures (Green et al., 1979). Detailed analysis of construction costs of traps and photosynthetic structures in these genera will provide additional insights into the true costs of botanical carnivory.
- How is the carbon derived from prey used by carnivorous plants? This last question is perhaps the most vexing and hearkens back to Darwin:
‘Most, however, of the plants belonging to these four classes [carnivorous plants that directly and indirectly digest prey, those that derive nutrients only from decaying litter, and parasitic plants] obtain part of their carbon [emphasis added] like ordinary species, from the atmosphere. Such are the diversified means, as far as at present known [emphasis added], by which higher plants gain their subsistence.’
(Insectivorous plants, p. 367)
Since Darwin's seminal publication, carnivorous plants have continued to provide general insights into the evolution and biogeography of plant lineages, the physiological ecology of nutrient uptake and use, and the evolution of leaf form. There is much yet to learn about these most wonderful plants in the world.
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Acknowledgements |
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Since 1997, our research on carnivorous plants has been supported by the US National Science Foundation (awards 98-05722, 98-08504, 00-83617, 02-34710, 02-35128, 03-01361, 03-30605, 04-00759, 04-52254, 05-41680, 05-41936 to AME and/or NJG); and NSF/EPSCOR (award 008297 to NJG). We thank our colleagues Leszek B
dzki, Jessica Butler, Elizabeth Farnsworth, Clarisse Hart, and Jim Karagatzides for fruitful discussions and collaborations in the field and lab as these ideas have evolved, and the dozens of undergraduates who have worked with us on a variety of carnivorous plant projects. Elizabeth Farnsworth drew the traps shown in Fig. 1. Kai Müller provided us with a detailed explanation of Fig. 2 which is reprinted from his 2004 paper with permission from him and from the publisher of Plant Biology, Georg Thieme Verlag KG, Stuttgart, Germany. The final version of the manuscript also reflects helpful comments from Lubomir Adamec, Elizabeth Farnsworth, Matt Fitzpatrick, Clarisse Hart, Stan Rachootin, and an anonymous referee. |
Footnotes |
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1 All quotations from Darwin's Insectivorous plants are from the second (1898) edition.
2 Sarracenia is mentioned in passing only on the penultimate page of Insectivorous plants. In a letter to W Thiselton-Dyer (letter 724 in F Darwin, 1903), he refers to Asa Gray's examination of Sarracenia. In a letter to JD Hooker (letter 726 in F Darwin, 1903), he writes of hoping that Hooker will resume work on Cephalotus and Sarracenia and provide comparative data for Darwin's ongoing studies of Utricularia.
3 ‘The "carnivorous ancestor" can of course be figured, as I have, in function of a morphogenetic and phylogenetic average quantified to fit everything – by tendency – between the Podostemonaceae/Lentibulariaceae and the Sarraceniaceae/Dioncophyllaceae.’ (Croizat, 1960: 256).
4 ‘The difference in all these regards between Nepenthes, and Utricularia and other lentibulariaceous genera is in every respect one of degree, not at all one of kind. The "runner" which in the latter aggregate becomes by easy steps under our own eyes "cladode" and "leaf" (cf., e.g., U. alpina/Pinguicula vulgaris) is by now fully fixed as "foliage" in Nepenthes. ...the interrelations between "foliage" and "stem" turn out to be far more complicated in Nepenthes than they are in the simplest forms of the Lentibulariaceae [i.e., Utricularia].’ (Croizat, 1960: 181-182).
5 ‘these octofid projections [of the footstalk, backs of leaves, and spikes of Dionaea] are no doubt homologous with the papillae on the leaves of Drosera rotundifolia’ (Insectivorous plants, p. 233).
6 ‘The circumferential part of the leaf of Aldrovanda thus differs greatly from that of Dionaea; nor can the points on the rim be considered as homologous with the spikes round the leaves of Dionaea, as these latter are prolongations of the blade, and not mere epidermic productions. They appear also to serve for a widely different purpose.’ (Insectivorous plants, p. 263).
7 Page 492 of the 1911 edition of The life and letters of Charles Darwin, edited by F Darwin.
8 This percentage comparison assumes similar molecular clocks and may be biased by using the basal angiosperm (Amborella+Nymphaeales) as the outgroup in the analysis (Kai Müller, personal communication to A Ellison, 5 March 2008).
9 ‘As species of the same genus have usually, though by no means invariably, some similarity in habits and constitution, and always in structure, the struggle will generally be more severe between species of the same genus, when they come into competition with each other, than species of distinct genera.’ [The origin of species, p. 64, 1996 Oxford University Press printing of the 2nd edition (1859)].
10 The raw data and complete list of studies from which the data were drawn are available as data set HF-111 from the Harvard Forest data archive: http://harvardforest.fas.harvard.edu/data/p11/hf111/hf111.html.
12 The notation N(µ, 
) means a normal distribution with mean = µ and standard deviation = . We used the R function rnorm(...) to generate our size distributions.
13 The marginal benefit is the difference between the total photosynthetic increase resulting from nutrients gained from producing a new trap and the total photosynthetic cost of producing a trap as opposed to a phyllode or other photosynthetically more efficient structure.)
14 https://www.nescent.org/wg_EvoViz/GeoPhyloBuilder.
15 Data available from the Harvard Forest Data Archive, dataset HF-112: http://harvardforest.fas.harvard.edu/data/p11/hfX112/hf112.html.
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Abbreviations |
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Amass, mass-based photosynthetic rate in nmol CO2 g–1 s–1; ANOVA, analysis of variance; atpB, chloroplast gene encoding the β chain of membrane-bound ATP synthase; C-value, amount of DNA in a haploid nucleus [in millions of base pairs (Mbp)]; coxI, mitochondrial gene encoding subunit 1 of cyctochrome c oxidase; ITS, internal transcribed spacer; JChao, the Chao–Jaccard abundance-weighted index of similarity; nrITS, nuclear ribosomal ITS; matK, chloroplast gene believed to encode a maturase, it is located within the trnK intron; PIE, probability of interspecific encounter, used here as a measure of specialization on prey by carnivorous plants; PRT1, nuclear gene encoding peptide transferase 1; rbcL, chloroplast gene encoding ribulose-bisphosphate carboxylase; rps16, a non-coding chloroplast intron; RRTree, software for comparing sequence divergence rates among related lineages (by extension, it has also come to mean the statistical relative-rate test between groups of sequences on a phylogenetic tree); trnK, a non-coding chloroplast intron; it includes the matK exon; trnF and trnL, two other non-coding chloroplast introns; trnL-F, intergenic spacer between the trnL and trnF introns.
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