Carnivorous Plants Physiology, ecology, and evolution

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Fleischmann, A., Systematics and evolution of Lentibulariaceae: II. Genlisea. ..... between genome size and morphology, habitat, or life history (annual vs. peren-.
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Systematics and evolution of Lentibulariaceae: II. Genlisea Andreas Fleischmann

7.1  Life history and morphology Genlisea comprises 30 species (Fleischmann 2012a, Fleischmann et al. 2017; Appendix) of entirely rootless, rosette-forming, hygrophilous carnivorous herbs. Ten species are (facultative or obligate annual) therophytes, 19 are evergreen perennials, and one species, Genlisea tuberosa, is a tuberous geophyte (Fleischmann 2012a, Rivadavia et al. 2013). Genlisea grows in habitats similar to the majority of carnivorous plants (Chapter 2): open, exposed, nutrient-poor, and at least seasonally moist to very wet habitats, usually on soils flushed by seeping to swiftly moving water. They grow in and around springs, seeps, and ephemeral flushes of granitic inselbergs, sandstone plateaus (tepuis), ferricretes, in clearings of wet savanna vegetation, and on wet quarzitic sand fields (Fleischmann 2012a). All species are strict calcifuges that occur only on acidic to neutral soils.

7.1.1 Leaves All species of Genlisea are strictly heterophyllous, producing two contrastingly different types of leaves. Both types of leaves are arranged alternately and with alternate (spiral) phyllotaxis along short, condensed stems (29 species), or on long, prostrate, stolon-like, horizontally creeping subterraneous stems with prolonged internodes (Genlisea repens; Figure 7.1). The first type of leaf is photosynthetic, bifacial, flat, foliar, petiolate with spatulate or oblong to lanceolate lamina, arranged in dense or lax rosettes that are appressed to the ground.

The second type of leaf is the so-called rhizophyll (“root-leaf”): a subterranean, tubular, hollow organ of inverted Y-shape, which functionally replaces the absent roots by anchoring the plants to the soil and taking up nutrients (Adamec 2008c). The rhizophylls are the complex, carnivorous eel traps unique to the genus (Figure 7.2; Chapters 12, 13, 15). They are of epiascidiate ontogeny (as are the pitcher leaves of pitcher plants; Chapters 3, 9) and exhibit positive geotropic growth (Kilian 1951, J­ uniper et  al.  1989, Fleischmann 2012a). Each rhizophyll (“trap”) consists of a solid stalk that widens at its distal end into a globose to ovoid or spindle-shaped, hollow chamber (the trap vesicle or digestive chamber, often compared to a “stomach”). At the opposite end, the vesicle opens into a terete, hollow “tubular neck.” The tubular neck widens and bifurcates at its end into two hollow, helically twisted trap arms (of opposite rotation; Fleischmann 2012a). The interior of the helical arms and tubular neck is lined with serial rows of stiff, retrorse bristles (the numerous “bows” of the eel trap), the vesicle interior surface is covered with quadrifid digestive glands (Figure 7.2), and the rhizophyll external surface is sparsely covered with sessile glands. Traps are ≈1–20 cm in overall length (including the stalk), with the tubular neck part ≈0.1–0.5 mm in diameter (Fleischmann 2012a). Species from the phylogenetically early-­ branching G. subg. Tayloria and G. sect. Africanae (§7.3) develop just a single monomorphic type of rhizophyll, whereas plants of G. sects. Recurvatae and Genlisea have dimorphic traps: comparatively short, thick, and wide (inner diameter) “surface

Fleischmann, A., Systematics and evolution of Lentibulariaceae: II. Genlisea. In: Carnivorous Plants: Physiology, ecology, and evolution. Edited by Aaron M. Ellison and Lubomír Adamec: Oxford University Press (2018). © Oxford University Press. DOI: 10.1093/oso/9780198779841.003.0007

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Figure 7.1  (Plate 7 on page P6) Vegetative and generative morphology of Genlisea. (a, d) Genlisea flexuosa (G. subg. Tayloria), with monomorphic traps. (b, e) G. margaretae (G. sect. Recurvatae) with dimorphic traps (note the short, thick surface traps and the longer, filiform deep-soil traps). (c, f) G. repens (G. sect. Genlisea), the sole species with a prostrate stoloniferous habit. (g) the unique multiple-circumscissile capsule dehiscence pattern of G. subg. Genlisea, illustrated here by G. hispidula. Photographs by Andreas Fleischmann.

traps” just beneath the soil surface; and comparatively long-stalked, thin and filiform “deep-soil traps” that grow vertically downward, reaching into deeper soil layers (Fleischmann 2012a; Figure 7.1). This trap dimorphism might serve to exploit different soil organisms from different soil strata.

7.1.2  Inflorescences and flowers The inflorescences of Genlisea are bracteose racemes; the scape can be glabrous, covered with eglandular or glandular hairs, or a mixture of both types of hairs. The species-specific indumentum often is a reliable taxonomic character. Each flower is subtended by a basifixed bract and two lateral bracteoles. The flowers of Genlisea follow the general design of Lentibulariaceae: they are zygomorphic, hermaphroditic, pentamerous, and tetracyclic, with a personnate, spurred, bilabiate

corolla, two bithecate stamens and a superior, subglobose ovary with persistent bilabiate style and free central placentation. The corolla throat of all but one species (G. exhibitionista) is covered by a gibbose, upwardly arching swelling of the corolla lower lip that creates a “masked flower.” The calyx consists of five spreading, basally adnate sepals and is persistent in fruit. The corolla is bilabiate: the upper lip is made up of two petals which can be fused only to the base, with two free lobes spreading (G. subg. Tayloria), or entirely fused (G.  subg. Genlisea). The lower lip of the corolla consists of three fused petals, which also make up the corolla throat and spur. The spur either parallels the pedicel (spreading from the corolla lobes; G. subg. Tayloria) or the corolla lower lip (G. subg. Genlisea; Fleischmann et al. 2010, Fleischmann 2012a). This results in two different flower types. Flowers of G. subg. Tayloria (most notably in G. violacea, less expressed in some other species) are

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trap stalk

digestive chamber tubular trap part, interior lined with retrorse bristles

digestive glands

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serial rows of stiff retrorse bristles

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helically twisted trap arms with numerous entrances

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Figure 7.2 The Genlisea rhizophyll. Overview of trap on the left (G. repens shown); SEM details of digestive chamber (G. violacea); tubular neck (G. repens); and trap entrance (G. flexuosa). Photographs by Andreas Fleischmann (reproduced in part from Fleischmann 2012a).

salverform: the spreading corolla lobes create a landing platform, and only the pollinators’ proboscis or mouthparts can be inserted into the abruptly narrowed corolla tube and spur. Members of G. subg. Genlisea display masked flowers of the snapdragon type, with an upwardly arching gibbose palate that seals the entrance to the corolla throat: to enter the corolla tube to reach the nectar secreted inside the spur, the pollinator has to push down the lower lip of the corolla (Fleischmann 2012a).

7.1.3  Fruits and seeds The capsules are (sub)globose, often lined with species-specific indumentum, and either held ­

upright in fruit (G. sects. Africanae and Genlisea) or on a downward-curving pedicel (G. subg. Tayloria and G. sect. Recurvatae). Ripe Genlisea capsules display two contrasting dehiscence types, which correspond to the two subgenera: in G. subg. Tayloria the capsules are longitudinally bivalvate, whereas in G.  subg. Genlisea they are circumscissile with a single or multiple ring-like dehiscence lines, or display a spiral dehiscence unique among angiosperms (Figure 7.1). The numerously produced seeds are globose to prismatic. Their size, shape, and testa ornamentation differ among the different sections: G. subg. Tayloria: prismatic and dorsiventrally compressed, with reticulate or papillate testa; G. sects. Africanae

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and Recurvatae: both ovoid to globose with very regular, isodiametric reticulation, but of different size classes; G. sect. Genlisea: pyramidal to angulate-ovoid, with smooth testa (Fleischmann ­ 2012a).

7.2 Carnivory Warming (1874) first studied and illustrated the morphology and anatomy of the rhizophylls, and Darwin (1875) first considered Genlisea to be a carnivorous plant. He was also the first to understand the trapping principle of the peculiar rhizophyll, and compared it with an eel trap or bow net. ­ Heslop-Harrison (1975) documented that proteolytic digestive enzymes are secreted from the trap interior glands, and Barthlott et  al. (1998) used radioisotope traces to demonstrate that Genlisea takes up nutrients from prey. Captured animals are probably killed inside the traps by anoxia (­Adamec 2007b) and subsequently digested by a pool of continuously secreted proteolytic enzymes that are released from the quadrifid glands that line the vesicle and upper neck region of the rhizophyll interior (Heslop-Harrison 1975, Barthlott et al. 1998, Płachno et al. 2006, 2007a). Genlisea apparently unselectively catches a diversity of soil organisms that are small enough to fit the trap entrance. Barthlott et  al. (1998) hypothesized that Genlisea specializes on protozoa, but all other data suggest that its prey spectrum is broader than is known for any other carnivorous plant (Darwin 1875, Goebel 1891b, 1893, Kuhlmann 1938, Lloyd 1942, Heslop-Harrison 1975, Studnička 1996, 2003a, Płachno et  al.  2005a, 2008, Płachno & Wołowski 2008, Fleischmann 2012a). Trap contents include cyanobacteria and non-photosynthetic eubacteria, protozoa (ciliates, flagellates, and thecate amoebae), and large numbers of nematodes, small soil crustaceans (especially copepods), collembola, mites, and various unicellular “algae” (diatoms, desmids, chrysophytes, euglenophytes, and singlecelled green algae). Some of the trapped microorganisms apparently are able to survive within the traps (Płachno and Wołowski 2008), and some non-trophic interactions between Genlisea and trap-­ inhabiting microbes may occur (Caravieri et al. 2014, Cao et al. 2015).

7.3  Phylogeny and evolution Genlisea and Utricularia (Chapter  8) are sister genera (Figure 7.3; Jobson et al. 2003, Müller et al. 2004, Fleischmann et al. 2010); the rhizophylls of Genlisea and the bladder traps of Utricularia are homologous to one another, as both are to the sticky traps of their common sister genus Pinguicula (Fleischmann 2012a; Chapter 3), and to the common foliar leaves of plants. The traps of Genlisea are epiascidiate (§7.2.1), and a likely scenario for their evolution is a continued inward folding and final fusion of the lateral margins of adhesive leaves of the presumed common ancestor (Chapter 3).

7.3.1  Infrageneric classification Two subgenera (Fromm-Trinta 1977, Fischer et  al.  2000) and four sections (Fleischmann et al. 2010) have been proposed. The two subgenera, G. subg. Tayloria and G. subg. Genlisea, were circumscribed based on capsule dehiscence (Fromm-Trinta 1977, Fischer et  al.  2000), and these are supported further by flower morphology and seed ultrastructure (Fleischmann 2012a), and by phylogeny and cytology (Fleischmann et al. 2010, 2014).

7.3.2 Phylogeography Genlisea is likely to have originated in the Neotropics, like its sister genus Utricularia (Jobson et al. 2003), and the highest extant species diversity of Genlisea occurs in the southeastern Brazilian highlands (Fleischmann et al. 2011a, Fleischmann 2012a; Figure 7.4). Phylogenetic reconstructions of Genlisea (Jobson et al. 2003, Müller et al. 2004, ­Fleischmann et  al.  2010, 2014) have revealed two major sister clades within the genus, which correspond to the two subgenera Tayloria and Genlisea. Within the Brazilian G. subg. Tayloria, the large, perennial species (G. uncinata, G. oligophylla, G.  ­metallica, G. flexuosa) represent early-­branching lineages, whereas the more derived species are annuals or short-lived polycarpic species (G. ­violacea, G. lobata, G. nebulicola, G. exhibitionista; ­Fleischmann et  al.  2010, 2011a). Subgenus Genlisea comprises three clades, two of them exclusively African—G.  sects. Africanae and Recurvatae—and

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tropical Africa (3 species) + Madagascar (1 species)

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Subg. Genlisea [22]

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Neotropics (Brazil 10 species, Guyana Highlands 10 species, Central America 1 species, Caribbean 1 species)

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eastern Brazilian highlands

Utricularia Pinguicula

Figure 7.3  Simplified phylogeny of Genlisea, topology based on Fleischmann et al. (2010).

one exclusively Neotropical—G. sect. Genlisea (­Fleischmann et al. 2010; Figure 7.3). All extant Neotropical species of G. subg. ­Genlisea share a common ancestor with the African G. sect. Recurvatae. In contrast to the paraphyletic African species, the derived Neotropical species in G. sect. Genlisea form a monophyletic group, implying a single colonization event of G. subg. Genlisea in South America via trans-Atlantic long-distance dispersal (Fleischmann et al. 2010; Fleischmann 2012a). ­Genlisea thus has colonized South America twice: first by a radiation of G. subg. Tayloria, and later following recolonization from Africa by derived members of G. subg. Genlisea (Fleischmann et al. 2010). The two subgenera are immediate sister groups in phylogenetic reconstructions (Fleischmann

et al. 2010), and there is as yet no evidence supporting either clade as the last common ancestor. However, species within G. subg. Tayloria share several floral characters with Pinguicula, and these can thus be considered plesiomorphic in Genlisea: bivalvate capsule dehiscence, a corolla with bilobed upper lip, and a spur that spreads from the corolla lower lip (paralleling the pedicel). In contrast, species of G. subg. Genlisea, share certain floral characters with the common sister genus Utricularia: an entire upper corolla lip and the spur paralleling the lower corolla lobe. In Utricularia (including U. sects. C ­ alpidisca, Setiscapella, and Utricularia; ­Chapter 8) and in G. subg. Genlisea, there is a switch from ­lilac-blue to yellow flower color in derived lineages. This switch certainly evolved in parallel

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in both genera and in all sections, given their continentally disjunct ranges, different habitats, but it could have a common genetic basis and might be an adaptation to similar pollinator guilds.

7.3.3  Chromosome numbers Species within G. subg. Tayloria have a common chromosome number of 2n = 16 and comparatively large chromosome size (Fleischmann et  al.  2014). Within G. subg. Genlisea, a large reduction in chromosome size and an increase of chromosome number has occurred. In G. sect. Africanae, chromosome numbers of 2n = 32 and 40 have been reported for G. hispidula (Fleischmann et al. 2014, Vu et al. 2015), whereas G. margaretae, in the consecutive sister group, G. sect. Recurvatae, has 2n = 38 (Fleischmann et  al.  2014, Tran et  al.  2016). Species in G. sect. Genlisea have large numbers of minute chromosomes (Greilhuber et al. 2006; Fleischmann et al. 2014, Vu et al. 2015). This pattern is accompanied by an evolutionary genome size reduction.

7.3.4  Genome size Genome size among Genlisea species varies 25-fold (Greilhuber et al. 2006, Fleischmann et al. 2014, Vu et al. 2015, Tran et al. 2015b); this huge range is exceeded by very few other plant genera (e.g., a 68-fold variation between the largest and smallest known genome sizes has been found within the parasitic plant genus Cuscuta; I. Leitch unpublished data). Some members of Genlisea have the smallest genome sizes currently known among angiosperms, with holoploid genomes of only 61 Mbp (Genlisea tuberosa) or 64 Mbp (Genlisea aurea), respectively (Greilhuber at al. 2006, Fleischmann et al. 2014). At the same time, the largest genomes known in Lentibulariaceae also occur in Genlisea. Genome sizes of the immediate sister genus Utricularia and the common sister of both, Pinguicula, all fall in between the largest and smallest ­Genlisea genomes (­Greilhuber et  al.  2006, Fleischmann et al. 2014, Veleba et al. 2014). In Genlisea, genome size appears to reflect chromosome size (and to a lesser degree karyotype) and phylogenetic affinity (Fleischmann et al. 2014). Fleischmann et  al. (2014) therefore postulated an evolutionary trend in genome reduction from an

ancestor with large genomes (still present in extant members of G. subg. Tayloria and G. sect. Africanae) to the ultra-small genomes observed in extant members of the derived G. sect. Genlisea. However, Vu et al. (2015) found the genome size in Genlisea to be of no evolutionary significance, and hypothesized that the contemporary variation in genome size evolved from a common ancestor with mediumsized genomes, leading to the comparatively large genomes of G. subg. Tayloria and G. sect. A ­ fricanae on the one hand, and very small to ultra-small genomes in G. sects. Recurvatae and Genlisea on the other side. Genlisea species with large and ultra-small genomes can have similar or identical chromosome numbers, but differ greatly in chromosome structure and cell size (Tran et  al.  2015b), and in DNA composition of telomere and centromere regions (Tran et al. 2015a). Genome size appears to have little effect on morphology or physiology in Genlisea, and no association has been found between genome size and morphology, habitat, or life history (annual vs. perennial) (Fleischmann et al. 2014, Vu et al. 2015). On the other hand, genome size does appear to be related to rate of evolutionary diversification: the 16-species clade with ultra-small genomes (G. sects. G ­ enlisea and Recurvatae; Figure 7.3) is more species rich than its immediate sister, G. sect. Africanae, a clade of six species with large genomes. In a few other plant lineages, including Veronica (Lamiales), a similar scenario of significant genome downsizing preceding increased diversification has been observed (Meudt et al. 2015). However, a causal relationship between genome size and diversification is unknown.

7.4 Distribution 7.4.1  Global patterns of diversity Genlisea shows an interesting amphi-Atlantic distribution pattern, with 21 species in the Neotropics (South to Central America, and Cuba in the ­Caribbean) and nine in tropical Africa including Madagascar (Figure  7.4). The genus is almost exclusively tropical; only G. hispidula extends into subtropical latitudes in southern Africa, whereas G. aurea and G. repens cross the tropic of Capricorn in South ­ America (Fleischmann 2012a). Genlisea

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Figure 7.4  Global distribution of Genlisea, with species numbers indicated (from data in Fleischmann et al. 2010, Fleischmann 2012a).

species grow from sea level to ≈2800 m a.s.l., but the majority are found between 600 and 1500 m a.s.l. (­Fleischmann 2012a). Not a single species of Genlisea occurs on both South America and Africa (Fleischmann et al. 2010, 2017, Fleischmann 2012a). The areas with greatest species numbers and diversity in South America are the central Brazilian highlands and the Guyana Shield, and just a single, widespread, annual species (G. filiformis) extends the range of the genus to the north, with isolated populations in Cuba, Belize, Nicaragua, and southern México (Fleischmann 2012a; Figure 7.4).

7.4.2  Brazil: the center of diversity All but three of the 18 Neotropical species (and 60% of all Genlisea species) occur in Brazil; the three others, G. glabra, G. sanariapoana, and G. pulchella, are endemic to the Guyana Highlands. At least ten of

the Brazilian species are endemic to the country (Fleischmann 2012a, Fleischmann et  al. 2017). The eight species of G. subg. Tayloria all are Brazilian endemics, occupying a small area in the highlands of eastern Brazil, mainly in the Serra do Espinhaço (Fleischmann et  al.  2011a). Of the three Guyana Highland endemics, G. glabra and G. roraimensis are confined to the summits of the tepuis, whereas G. sanariapoana is a lowland species endemic to the llanos plains along the Upper and Middle Orinoco River (Fleischmann 2012a).

7.4.3  African species The nine African species grow in tropical West and East Africa; G. margaretae extends this overall range into central Madagascar, where it occurs in a few outlying populations (Figure 7.4). The centers of diversity in Africa are on the Angolan and ­Zambian Plateaus, from where G. hispidula has spread to

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form several disjunct populations in Afromontane regions. In parallel with the widespread Neotropical annual, G. filiformis, the small annual G. stapfii has the widest range of distribution among the ­African species, extending from Senegal southwest (absent in the dry areas of the Ghana Dry Zone and the Dahomey Gap) to the Central African Republic in the west and the Republic of Congo (Congo-­ Brazzaville) in the south (Fischer et  al.  2000; Fleischmann 2012a).

7.5  Future research Although the small genus Genlisea is taxonomically, morphologically, anatomically, and phylogenetically relatively well-studied, the exact functioning of its rhizophyll traps, especially regarding prey attraction, is still not fully understood. The basic functional mechanism and anatomy of these eel traps long has been known (Warming 1874, Darwin 1875), but it is still unclear whether the rhizophylls are purely passive traps that lure prey to their interior by some kind of attractant or if they actively create a water current that sucks small soil organisms into the traps. There is published evidence to support both theories. Studies with detached traps found no evidence for a water current in Genlisea rhizophylls (Adamec 2003b, Płachno et  al.  2005a,

2008). On the other hand, immobile prey items and soil particles frequently are present in the traps, bifid glands similar to those which work as water pumps in Utricularia traps occur on the rhizophylls, and ink tracers in vivo together suggest an active trap (Juniper et  al.  1989, Meyers-Rice 1994, Studnička 1996, 2003a, Fleischmann 2012a). Although Barthlott et  al. (1998) hypothesized chemotactic attraction of prey by Genlisea, no chemical attractant yet has been detected from Genlisea traps (Płachno et al. 2008). Other hypothesized attractants include secreted mucilage as bait (Goebel 1891b, Lloyd 1942) and rhizophyll entrances acting as deceptive soil shelters (Studnička 2003a). Both Studnička (2003a) and Adamec (2007b) hypothesized that oxygen released from the traps could attract prey in otherwise anaerobic soils. This hypothesis seems more likely for the deep-soil traps in species with rhizophyll dimorphism than in most species that form traps just beneath the soil surface, where aerobic conditions prevail (Fleischmann 2012a). Last, the basic ecology of Genlisea, including population dynamics and interspecific interactions (prey spectrum, associated biota, and pollination biology) barely has been explored, although the first pollinator observations were reported by ­Fleischmann (2012a) and Aranguren Díaz (2016).