COMMENTARY COMMENTARY New evidence on the origin of carnivorous plants Thomas J. Givnish1 plants to open, infertile, moist sites, however, Department of Botany, University of Wisconsin-Madison, Madison, WI 53706 remained unexplained until modern cost- benefit models showed that carnivores are likely to obtain an advantage in growth rela- Carnivorous plants have fascinated scientists carnivorous plants in 20 genera, 12 families, tive to noncarnivores only on such sites, and the general public since the pioneering and 5 orders of flowering plants (Table 1). where nutrients and nutrients alone limit plant studies of Charles Darwin (1). No doubt Based on DNA sequence phylogenies, these growth, and where carnivory can accelerate part of their wide appeal is that carnivorous species represent at least nine independent plants have turned the evolutionary tables origins of the carnivorous habit per se, and photosynthesis and the conversion of photo- on animals, consuming them as prey, with at least six independent origins of pitfall synthate to new leaf tissue while decreasing the green predators often equipped with re- traps, five of sticky traps, two of snap traps, allocation to root tissue (2, 3, 5, 6). Wet soils markable lures, traps, stomachs, and—in and one of lobster-pot traps. To the extent and fire can favor carnivorous plants, by mak- a few cases—extraordinary speed of move- to which molecular phylogenies have been ing N more limiting for growth while making ment. To be considered carnivorous, a plant calibrated against the ages of fossils of other light and water less limiting (3). The wet, must be able to absorb nutrients from dead plants, these origins of carnivory appear to sandy, fireswept sites in fynbos occupied by bodies adjacent to its surfaces, obtain some have occurred between roughly 8 and 72 Roridula (6) should thus favor carnivory, advantage in growth or reproduction, and million years ago (Mya). In PNAS, Sadowski and indeed Roridula often grows in association have unequivocal adaptations for active et al. (4) contribute to our understanding with large numbers of carnivorous sundews. prey attraction, capture, and digestion (2, of the origins of plant carnivory by describ- Roridula, however, is in other respects 3). Some carnivorous species [e.g., Pinguicula ing the first fossilized trap of a carnivorous highly unusual as a carnivorous plant. Al- (butterworts), Philcoxia]lackobviousattrac- plant, a fragment of a tentacled leaf pre- though its glistening, glandular tentacles tants; some rely on passive pitfalls [e.g., served in Baltic amber from 35 to 47 do trap large numbers of insects, the secre- Cephalotus (Australian pitcher plant), Sarra- Mya, and allied to modern-day Roridula of tions are resinous rather than aqueous, and cenia (American pitcher plants)] rather than monogeneric Roridulaceae (Ericales) from so cannot support the activities of digestive active traps based on sticky tentacles [e.g., South Africa. enzymes. It does not secrete proteolytic en- Byblis, Drosera (sundews)] or snap traps As with most carnivorous plants, the two zymes; several authors thus argued that [e.g., Dionaea (Venus fly-trap), Utricularia living species of Roridula today grow on Roridula could not be carnivorous because (bladderworts)]; and some lack digestive open, extremely infertile, moist sites. The it could not digest prey or absorb the min- enzymes and instead depend on commensal occurrence of carnivorous plants on nutrient- erals released (7, 8). The resinous nature of microbes or insect larvae to break down poor substrates has been understood since Roridula secretions may be an adaptation to prey (e.g., Brocchinia, Darlingtonia,some Darwin showed that such plants augment the summer drought in the Mediterranean species of Sarracenia). Based on these crite- their supply of mineral nutrients through climate it now occupies, in that they do not ria, today we recognize at least 583 species of prey capture. The restriction of carnivorous lose volume or stickiness during long periods of drought; the secretions also do not dissolve during winter rains (9). It turns out that cer- Table 1. Currently recognized groups of carnivorous plants tain hemipterans (Pameridea)arecapableof Order Family or clade Genus/genera* No. of taxa negotiating the glandular leaves of Roridula without becoming entangled; they eat the Poales Bromeliaceae I BrocchiniaP 2 P prey immobilized by the plant, and then Bromeliaceae II Catopsis 1 N from their excretions is absorbed by Eriocaulaceae PaepalanthusP 1 Caryophyllales DNDD clade Roridula (Fig. 1). This process substantially Droseraceae AldrovandaS, DionaeaS, DroseraT 115 augments the N supply to the plants, with Nepenthaceae NepenthesP 90 the plants obtaining 70% or more of their Drosophyllaceae DrosophyllumT 1 nitrogen supply in this fashion (7, 10). The Dioncophyllaceae TriphyophyllumT 1 mutualism appears stabilized by nonlinear Oxalidales Cephalotaceae CephalotusP 1 interactions: excess densities of Pameridea Ericales RS-Actinidiaceae clade turn counterproductive as the bugs switch Sarraceniaceae DarlingtoniaP, HeliamphoraP, SarraceniaP 32 to sap-sucking in the absence of prey, leading Roridulaceae RoridulaT 2 to negative impacts on Roridula and, ulti- T Lamiales Byblidaceae Byblis 6 mately, on the bugs themselves (11). Lentibulariaceae GenliseaL, PinguiculaT, UtriculariaS 330 Plantaginaceae PhilcoxiaT 1 Author contributions: T.J.G. wrote the paper. Taxa include all members of each genus, except for the monocot genera in order Poales, where the number of The author declares no conflict of interest. carnivorous species within the genus is listed. Independent origins of carnivory per se are indicated by boldface entries in the family/clade column. See companion article 10.1073/pnas.1414777111. *Trap types indicated by superscript: L, lobster-pot trap; P, pitfall; S, snap trap; T, sticky trap. 1Email: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1422278112 PNAS Early Edition | 1of2 Downloaded by guest on October 1, 2021 been a fossil insect egg (18). The remaining fossils considered legitimate remains of carniv- orous plants include one seed (now destroyed) of Byblis (Byblidaceae) from Australia (19), and palynomorphs possibly allied with Nepenthaceae (20). The last two fragments, however, do not demonstrate that the plants to which they belonged were, in fact, carniv- orous, which makes the find by Sadowski et al. (4) particularly important. The age of the am- ber Roridula,35–47 Mya, nicely brackets the divergence between Roridula and noncarnivo- rous Actinidiaceae roughly 39 Mya, as esti- mated from a calibrated DNA phylogeny (21). This result lends credence to the age estimates based on molecular data, and to the inference from phylogenetic reconstruc- tion that early Roridulaceae were carnivorous. The identity of the fossil Roridula appears to be beyond doubt. The former occurrence of Roridula around the Baltic—whereas its pres- ent-day distribution is restricted to the Cape Fig. 1. Growth form of Roridula gorgonias at Fernkloof Nature Reserve near Hermanus, showing glandular ten- FloristicProvinceofsouthwestSouthAfrica— tacles that immobilize insect prey. Close-up of leaves, showing a Pameridea bug (center) that eats immobilized prey impliesthatthisgroupwasoncefarmore and delivers nutrients to the plant via excreta. widespread. The distributions of families in the Clethraceae-Sarraceniaceae-Roridulaceae- Although the Roridula system is truly re- “apparent carnivorous plants,” in homage to Actinidiaceaecladesuggestthatitoriginated markable, similar kinds of complex digestive Holt’s concept of apparent competition (16). in southeastern North America or northern mutualisms may occur in other carnivorous The new fossil Roridula not only is the first South America. In the next few years, further plants. For example, Nepenthes bicalcarata fossil trap leaf uncovered, it is one of the very investigations of the Baltic amber might tell us provides domatia for ants, despite ants being few undoubted fossils of carnivorous plants what other plants grew in association with themostfrequentpreyofmanyNepenthes. of any kind. Archaeamphora from Chinese fossil Roridula, and thus the nature of the Givnish (5) and Hölldobler and Wilson (12) sediments 112 Mya was originally described vegetation in which fossil Roridula grew. proposed that the resident ants and plants as Sarraceniaceae, but now there is strong Based on cost-benefit models, the distribution might have a mutualistic relationship of some doubt that it was a member of that family of present-day Roridula, and the current dis- kind. In fact, the resident ant Camponotus or even a carnivorous plant; the unusual tributions of almost all other carnivorous schmitzi protects N. bicalcarata from weevils leaves may simply not have been traps (17). plants,itseemsmostunlikelythatfossil that attack their tendrils, and in addition Paleoaldrovanda, putatively a member of Dro- Roridula grew below a dense canopy of the facilitates the plant’s uptake of nutrients seraceae based on a “seed,” may actually have conifer forests that produced amber! (13).Theantscanswiminthepitcherfluid without adverse effect, retrieve large prey items, and excrete wastes into the pitcher, 1 Darwin C (1875) Insectivorous Plants (Appleton and Co., London). 11 Anderson B, Midgley JJ (2007) Density-dependent accelerating nutrient uptake; ant wastes ac- 2 Givnish TJ, Burkhardt EL, Happel RE, Weintraub JW (1984) outcomes in a digestive mutualism between carnivorous count for 42–76% of total N uptake and ants Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit Roridula plants and their associated hemipterans. Oecologia prolong pitcher lifetimes (13). In other sys- model for the general restriction of carnivorous plants to sunny, 152(1):115–120. moist, nutrient-poor habitats. Am Nat 124(4):479–497. 12 Hölldobler B, Wilson EO (1990) The Ants (Springer, Berlin). tems, the prey processed by a digestive mu- 3 Ellison M, Adamec L (2011) Ecophysiological traits of terrestrial 13 Bazile V, Moran JA, Le Moguédec G, Marshall DJ, Gaume L tualist may not even be captured by the and aquatic carnivorous plants: Are the costs and benefits the same? (2012) A carnivorous plant fed by its ant symbiont: A unique multi- plant’sowntraps.Nepenthes lowii attracts Oikos 120(11):1721–1731. faceted nutritional mutualism. PLoS ONE 7(5):e36179. 14 tree shrews (Tupaia montana) to their excep- 4 Sadowski E-M, et al. (2014) Carnivorous leaves from Baltic amber. Clarke CM, et al. (2009) Tree shrew lavatories: A novel nitrogen Proc Natl Acad Sci USA, 10.1073/pnas.1414777111. sequestration strategy in a tropical pitcher plant. Biol Lett 5(5): – tionally large, broad traps with secreted 5 Givnish TJ (1989) Ecology and evolution of carnivorous plants. 632 635. 15 Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG (2011) A rewards, and they defecate into the pitcher Plant–Animal Interactions, ed Abrahamson WG (McGraw-Hill, New novel resource-service mutualism between bats and pitcher plants. York), pp 243–290. while marking it as their territory. Their feces Biol Lett 7(3):436–439. 6 Ellison AM, Gotelli NJ (2009) Energetics and the evolution of account for 57–100% of all leaf N (14). 16 Holt RD (1977) Predation, apparent competition, and the carnivorous plants—Darwin’s ‘most wonderful plants in the world’ structure of prey communities. Theor Popul Biol 12(2):197–229. Nepenthes rafflesiana var. elongata, with J Exp Bot 60(1):19–42. 17 Brittnacher J (2013) Phylogeny and biogeography of the 7 Ellis AG, Midgley JJ (1996) A new plant-animal mutualism involving smaller but elongate traps, provides a roost Sarraceniaceae. Carniv Plant Newsletter 42(3):99–106. for a small bat and obtains nutrients from a plant with sticky leaves and a resident hemipteran. Oecologia 18 Hermanová Z, Kvacekˇ J (2010) Late Cretaceous – its feces (15). Whether these systems are best 106(4):478 481. Palaeoaldrovanda, not seeds of a carnivorous plant but eggs of an 8 Juniper BE, Robias RJ, Joel DM (1989) The Carnivorous Plants viewed as coprophagy or indirect forms of insect. J Natur Hist Mus (Prague) 179(9):105–118. (McGraw-Hill, New York). 19 Conran J, Christophel D (2004) A fossil Byblidaceae seed from 9 carnivory involving digestive mutualists that Voigt D, Gorb S (2010) Desiccation resistance of adhesive Eocene South Australia. Int J Plant Sci 165(4):691–694. deliver the remains of prey is worth debating. secretion in the protocarnivorous plant Roridula gorgonias as an 20 Kumar M (1995) Pollen tetrads from Palaeocene sediments of Clearly, however, both plants benefit from adaptation to periodically dry environment. Planta 232(6): Meghalaya, India: Comments on their morphology, botanical affinity 1511–1515. and geological records. Palaeobot 43(1):68–81. animals whose death results in their acquisi- 10 Anderson B, Midgley JJ (2003) Digestive mutualism, an alternative 21 Ellison AM, et al. (2012) Phylogeny and biogeography of tion of nutrients; we might consider them pathway in plant carnivory. Oikos 102(1):221–223. the carnivorous plant family Sarraceniaceae. PLoS ONE 7(6):e39291.

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