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Organisms withstand normal ranges of environmental fluctuations by producing a set of phenotypes genetically programmed as a reaction norm; however, extreme conditions can expose a misregulation of phenotypes called a hidden reaction norm. Although an environment consists of multiple factors, how combinations of these factors influence a reaction norm is not well understood. To elucidate the combinatorial effects of environmental factors, we studied the leaf shape plasticity of the carnivorous pitcher plant Cephalotus follicularis . Clonally propagated plants were subjected to 12-week-long growth experiments in different conditions controlled by growth chambers. Here, we show that the dimorphic response of forming a photosynthetic flat leaf or an insect-trapping pitcher leaf is regulated by two covarying environmental cues: temperature and photoperiod. Even within the normal ranges of temperature and photoperiod, unusual combinations of the two induced the production of malformed leaves that were rarely observed under the environmentally typical combinations. We identified such cases in combinations of a summer temperature with a short-to-neutral day length, whose average frequency in the natural Cephalotus habitats corresponded to a once-in-a-lifetime event for this perennial species. Our results suggest that even if individual cues are within the range of natural fluctuations, a hidden reaction norm can be exposed under their discordant combinations. We anticipate that climate change may challenge organismal responses through not only extreme cues but also through uncommon combinations of benign cues.

Cephalotus follicularis is a carnivorous plant native to southwest Australia that belongs to the monospecific family Cephalotaceae. It forms both carnivorous pitcher leaves and non-carnivorous flat...

Around 75 years before Charles Darwin published his fundamental work on insectivorous plants, Scottish botanist Robert Brown observed that a small pitcher plant was an insect-catcher (Mithofer 2017). Six years later, Labillardiere described and named it as Cephalotus follicularis, the Albany pitcher plant, a species in its own genus and family, endemic to a small area in Southwest Australia (Cross et al. 2019).

BackgroundCarnivorous plants have been fascinating researchers with their unique characters and bioinspired applications. These include medicinal trait of some carnivorous plants with potentials for pharmaceutical industry.MethodsThis review will cover recent progress based on current studies on digestive enzymes secreted by different genera of carnivorous plants:Drosera(sundews),Dionaea(Venus flytrap), Nepenthes(tropical pitcher plants),Sarracenia(North American pitcher plants), Cephalotus(Australian pitcher plants), Genlisea(corkscrew plants),andUtricularia(bladderworts).ResultsSince the discovery of secreted protease nepenthesin inNepenthespitcher, digestive enzymes from carnivorous plants have been the focus of many studies. Recent genomics approaches have accelerated digestive enzyme discovery. Furthermore, the advancement in recombinant technology and protein purification helped in the identification and characterisation of enzymes in carnivorous plants.DiscussionThese different aspects will be described and discussed in this review with focus on the role of secreted plant proteases and their potential industrial applications.

Traps of several carnivorous plant species display characteristics commonly associated with attraction of pollinating insects. These may include a combination of color, scent, and a nectar reward for visitation (Chapter 12). This apparent similarity between carnivorous organs and arthropod-pollinated flowers led some authors to suggest that pitchers were examples of mimicry (e.g., Wiens 1978, Pasteur 1982). Juniper et al. (1989) devoted a chapter to this question, and concluded that convergent evolution of attractive traits, rather than mimicry, was responsible for the observed “floral” characteristics of pitcher traps. Moran (1996) reached a similar conclusion based on field studies of Nepenthes rafflesiana in Borneo. Juniper et al. (1989) developed their argument beyond merely refuting the idea of mimicry. Rather, they hypothesized that some interactions between invertebrates and carnivorous plants possessing extrafloral nectaries (EFNs in e.g., Sarracenia, Nepenthes, Cephalotus; Chapter 12) constituted not a predator–prey relationship, but a mutualism: an obligate or facultative interaction between species that is beneficial to both (Boucher et al. 1982). Within this broad definition, many mutualistic associations have been identified, including: resource/service (e.g., pollination of flowers by an animal for a nectar reward); service/service (e.g., ants protecting a host plant from herbivory in exchange for nesting space); and resource/resource or resource exchange (e.g., association between mycorrhizal fungi and green plants).Subsequent studies have provided support for the mutualistic hypothesis of Juniper et al. (1989). In this chapter, we review and synthesize the evidence for mutualistic associations between several animal taxa and members of the Nepenthaceae and Roridulaceae that facilitate nutrient acquisition by the plants via their trapping structures.

Contents Summary 1035 I. Introduction 1035 II. Evolution of the pitcher 1036 III. Convergent evolution 1036 IV. Divergent evolution 1038 V. Adaptive radiation and speciation 1040 VI. Conclusions and perspectives 1040 Acknowledgements 1040 References 1040 SUMMARY: The pitcher trap is a striking example of convergent evolution across unrelated carnivorous plant lineages. Convergent traits that have evolved across pitcher plant lineages are essential for trap function, suggesting that key selective pressures are in action. Recent studies have also revealed patterns of divergent evolution in functional pitcher morphology within genera. Adaptations to differences in local prey assemblages may drive such divergence and, ultimately, speciation. Here, we review recent research on convergent and divergent evolution in pitcher plant traps, with a focus on the genus Nepenthes, which we propose as a new model for research into adaptive radiation and speciation.

Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.

Cephalotus follicularis is an ecologically unique, taxonomically isolated and range-restricted carnivorous plant that occurs exclusively within vulnerable wetland habitats in coastal south-western Australia. Very little is known about the reproductive biology of this iconic plant species, particularly in relation to seed dormancy and the specific requirements for germination. This knowledge gap must be filled to facilitate the establishment of conservation and management initiatives for the species, as Cephalotus is increasingly impacted by habitat loss, alteration to natural hydrological and fire regimes and, in recent times, climatic change. This study aimed to determine the type of seed dormancy that the seeds of Cephalotus possess, determine the optimum conditions required for seed germination, and examine the storage behaviour of seeds. The seeds of Cephalotus are small (1.0 × 0.5 mm), lightweight (0.1 mg) and remain indehiscent within a wind-dispersed hairy achene. Results suggest that the seeds may exhibit some sensitivity to desiccation and appear to be short lived (

To establish a mass micropropagation procedure for Cephalotus follicularis, the effects of varying the strengths of solid Murashige and Skoog (MS) medium were investigated using subcultured shoot explants. After a 60-day primary culture from root mass, the regenerated shoot explants were subcultured every 60 days in solid MS medium. To facilitate shoot proliferation, liquid MS medium was applied with or without exogenous auxin and cytokinin. Our results demonstrate that shoot proliferation and survival of C. follicularis is most effective in modified MS (MMS) medium containing one-fifth or one-tenth strength macronutrients and full-strength micronutrients. Successful shoot proliferation and development of C. follicularis explants were obtained in one-fifth or one-tenth modified liquid MS medium without auxin and cytokinin or with addition of 5 μM indole 3-acetic acid/1 μM N6-benzyladenine for 45 days. The liquid medium consistently produced more explants than the solid medium and shortened the culturing time. Plantlets cultured in hormone-free one-fifth MMS medium developed greater root systems. Using the liquid culture we established, vigorous plants with extensive roots were obtained within 4 months. Plant survival in the greenhouse reached 100%.

Summary The present, third part of a series of studies on floral and extrafloral nectaries deals with auxiliary structures whose function is to conduct nectar from its source towards a more or less distant site of exposition. Ducts occur especially in plant groups that have a fixed conformation of floral organs and have been unable to dislocate the nectary towards a site more appropriate for pollination, such as spurs and narrow tubular containers. These drainage systems are concealed, preventing access to visitors. In all known cases, they run externally in capillary clefts between floral organs or in tubes 20–70 μm in diam., formed by invaginations of the cutinized but easily wettable epidermal surface with ± tightly connivent margins. The nectar flows along the ducts driven by capillary forces, secretion pressure and, in part, gravity. The Alliaceae, whose papillate septal nectaries principally bear their three primary outlets at the top of the superior ovary, only rarely discharge the fluid directly at these points, a case exemplified by Allium cernuum. In Brodiaea and Nothoscordum, cryptic ducts run along the external carpellary sutures towards the base of the ovary, where the nectar is released. In Triteleia and Dichelostemma, they continue proximally along an ovarial stipe that extends the distance between the source and the site of nectar deposition. An extreme is achieved in Milla, whose stipe is connate with the perigon tube by means of three septa; each of the three resulting separate nectar pipes is fed with nectar by ducts which run along the stipe over a distance of up to 13 cm, with apertures in the pipe's lower end The zygomorphic flowers of Wachendoifia (Haemodoraceae), with a semi-inferior, trilocular ovary, have only two nectariferous ovarial septa. These are sunken in the torus and drained by lateral, retroverse channels which conduct the fluid to a pair of external, spur-like auricles of the perigon segments. The nectar of Silene schafta and allies (Caryophyllaceae) collects at the bottom of an elongate, tubular calyx. Its source is a disk, borne a considerable distance away – as all remaining floral parts – by a long columnar stipe. The liquid flows within 10 cryptic channels along the stipe and is released at its base above the insertion of the calyx. In Capsicum (Solanaceae), nectar produced by an ovarial disk travels through concealed ducts from the inaccessible tubular part of the corolla towards five apertures which lie outside the staminal fascicle on the flat limb. Analogous drainage systems of the related genera Jaltomata and Physalis are illustrated. The spur of the zygomorphic corollas of Linaria and Kickxia (Scrophulariac.) is supplied with nectar by means of a single duct which descends from the disk and runs down along the dorsal wall to the spur's tip where the fluid is released into the main lumen of the spur. The Violaceae use different strategies to overcome the problem of supplying long spurs with the nectar they produce by distant connectival glands. In Corynostylis volubilis an internal furrow of the spur wall probably assumes this function, leading from the nectar scale to the spur's tip 5 cm away.

Although the S-like ribonucleases (RNases) share sequence homology with the S-RNases involved in the self-incompatibility mechanism in plants, they are not associated with this mechanism. They usually function in stress responses in non-carnivorous plants and in carnivory in carnivorous plants. In this study, we clarified the structures of the S-like RNases of Aldrovanda vesiculosa, Nepenthes bicalcarata and Sarracenia leucophylla, and compared them with those of other plants. At ten positions, amino acid residues are conserved or almost conserved only for carnivorous plants (six in total). In contrast, two positions are specific to non-carnivorous plants. A phylogenetic analysis revealed that the S-like RNases of the carnivorous plants form a group beyond the phylogenetic relationships of the plants. We also prepared and characterized recombinant S-like RNases of Dionaea muscipula, Cephalotus follicularis, A. vesiculosa, N. bicalcarata and S. leucophylla, and RNS1 of Arabidopsis thaliana. The recombinant carnivorous plant enzymes showed optimum activities at about pH 4.0. Generally, poly(C) was digested less efficiently than poly(A), poly(I) and poly(U). The kinetic parameters of the recombinant D. muscipula enzyme (DM-I) and A. thaliana enzyme RNS1 were similar. The k cat/K m of recombinant RNS1 was the highest among the enzymes, followed closely by that of recombinant DM-I. On the other hand, the k cat/K m of the recombinant S. leucophylla enzyme was the lowest, and was ~1/30 of that for recombinant RNS1. The magnitudes of the k cat/K m values or k cat values for carnivorous plant S-like RNases seem to correlate negatively with the dependency on symbionts for prey digestion.

Functions of S-like ribonucleases (RNases) differ considerably from those of S-RNases that function in self-incompatibility. Expression of S-like RNases is usually induced by low nutrition, vermin damage or senescence. However, interestingly, an Australian carnivorous plant Drosera adelae (a sundew), which traps prey with a sticky digestive liquid, abundantly secretes an S-like RNase DA-I in the digestive liquid even in ordinary states. Here, using D. adelae, Dionaea muscipula (Venus flytrap) and Cephalotus follicularis (Australian pitcher plant), we show that carnivorous plants use S-like RNases for carnivory: the gene da-I encoding DA-I and its ortholog cf-I of C. follicularis are highly expressed and constitutively active in each trap/digestion organ, while the ortholog dm-I of D. muscipula becomes highly active after trapping insects. The da-I promoter is unmethylated only in its trap/digestion organ, glandular tentacles (which comprise a small percentage of the weight of the whole plant), but methylated in other organs, which explains the glandular tentacles-specific expression of the gene and indicates a very rare gene regulation system. In contrast, the promoters of dm-I, which shows induced expression, and cf-I, which has constitutive expression, were not methylated in any organs examined. Thus, it seems that the regulatory mechanisms of the da-I, dm-I and cf-I genes differ from each other and do not correlate with the phylogenetic relationship. The current study suggests that under environmental pressure in specific habitats carnivorous plants have managed to evolve their S-like RNase genes to function in carnivory.

Carnivorous plants have fascinated scientists and the general public since the pioneering studies of Charles Darwin (1). No doubt part of their wide appeal is that carnivorous plants have turned the evolutionary tables on animals, consuming them as prey, with the green predators often equipped with remarkable lures, traps, stomachs, and—in a few cases—extraordinary speed of movement. To be considered carnivorous, a plant must be able to absorb nutrients from dead bodies adjacent to its surfaces, obtain some advantage in growth or reproduction, and have unequivocal adaptations for active prey attraction, capture, and digestion (2, 3). Some carnivorous species [e.g., Pinguicula (butterworts), Philcoxia] lack obvious attractants; some rely on passive pitfalls [e.g., Cephalotus (Australian pitcher plant), Sarracenia (American pitcher plants)] rather than active traps based on sticky tentacles [e.g., Byblis, Drosera (sundews)] or snap traps [e.g., Dionaea (Venus fly-trap), Utricularia (bladderworts)]; and some lack digestive enzymes and instead depend on commensal microbes or insect larvae to break down prey (e.g., Brocchinia, Darlingtonia, some species of Sarracenia). Based on these criteria, today we recognize at least 583 species of carnivorous plants in 20 genera, 12 families, and 5 orders of flowering plants (Table 1). Based on DNA sequence phylogenies, these species represent at least nine independent origins of the carnivorous habit per se, and at least six independent origins of pitfall traps, five of sticky traps, two of snap traps, and one of lobster-pot traps. To the extent to which molecular phylogenies have been calibrated against the ages of fossils of other plants, these origins of carnivory appear to have occurred between roughly 8 and 72 million years ago (Mya). In PNAS, Sadowski et al. (4) contribute to our understanding of the origins of plant carnivory by describing the first fossilized trap of a carnivorous plant, a fragment of a tentacled leaf preserved in Baltic amber from 35 to 47 Mya, and allied to modern-day Roridula of monogeneric Roridulaceae (Ericales) from South Africa.

Morphology of the mature larvae and pupae of the apterous fly, Badisis ambulans McAlpine (Diptera: Micropezidae) are described and illustrated. In addition, the curious commensal habits of the larvae are described. Each spiracular plate of the mature larva is situated at the base of a small horn; similar horns have been described in other micropezid larvae. The posterior spiracles appear to be non-functional with depressions forming the vestiges of the spiracular openings. The larvae were found inside pitchers of the Albany pitcher plant, Cephalotus follicularis (Cephalotaceae) and have a commensal relationship with the plant. They feed on the decaying pitcher plant prey and leave the pitcher to pupate. It is likely that the larva obtains oxygen from the pitcher fluid. This is the first immature micropezid described from Australia.

Powdery mildew is reported for the first time on the Albany pitcher plant (Cephalotus follicularis). The plants originated from a nursery in Melbourne. The fungus was identified as Podosphaera xanthii using morphological characters and a rDNA ITS sequence. This is the first record of powdery mildew on the Cephalotaceae.

Summary A survey of u.v. patterns in the traps of carnivorous plants reveals that, similar to many flowers, certain traps show conspicuous u.v. patterns. These patterns are based on both u.v.-absorption by the plant surface itself and u.v.-absorption by nectar or pools of the digestive secretion. The results are discussed with respect to the possibility that u.v. patterns may attract prey to certain carnivorous plants.

The carnivorous pitcher plants of the Sarraceniaceae, Nepenthaceae and Cephalotaceae seem to have developed attraction and rewarding systems which resemble those of many flowers. Contrary to a previous view, Batcsian mimicry does not appear to apply to pitcher traps because: (a) there is no evidence of insects visiting traps by mistake, (b) no model is known for any one of the traps, (c) the duration of the trap activity and the structure of the plant community are not compatible with a deceptive mimetic status, (d) nectar which is a real reward is provided to visiting insects by the pitcher plants. It is suggested that these plants perform mutual rather than deceptive relations with the insect communities in their habitats. Insects benefit from nectar which is provided by pitchers and which serves for their nutrition in habitats where sources of floral nectar might be either uncommon or absent. At the same time the insects pay the plants in a small portion of their community which is ‘sacrificed’ as prey and consumed by the plants, which grow in nutrient deficient soils.

A B S T R A C T Scanning electron microscopy was used to observe features of representative species of the five carnivorous pitcher plant genera which allow them to lure, capture, and digest insects. Nepenthes rafflesiana, Sarracenia purpurea, Darlingtonia californica, Heliamphora heterodoxa, and Cephalotus follicularis were studied. The many morphological similarities observed in the phylogenetically unrelated plants show evidence supporting the concept of their convergent evolution. Several previously undescribed features of some plants were resolved which help elucidate their insect trapping mechanisms. THE SCANNING ELECTRON microscope (SEM) has been used to observe many features of the actively insectivorous Venus's fly trap [Dionaea muscipula Ellis (Droseraceae)] which allow it to lure, capture, and digest insects (Mozingo, et al., 1970). However, few such observations have been made of the analogous features of the passively insectivorous pitcher plants, other than Sarracenia (Panessa and Gennaro, 1972; Barckhaus and Weinert, 1974; Panessa, et al., 1976). The five genera of pitcher plants [Nepenthes (Nepenthaceae); Sarracenia, Darlingtonia, Heliamphora (Sarraceniaceae); Cephalatus (Cephalotaceae)] trap insects passively by means of hollow leaves or leaf appendages termed "pitchers." At the top of the pitcher are nectar glands which attract insects to the pitcher. The structure of the pitcher and gland placement induce attracted insects to enter the pitcher, and once inside this "pitfall" trap (Lloyd, 1942), the insect is prevented from escaping by various features of the pitcher. Captured insects drown in the liquid contained at the bottom of the pitcher and are digested by bacteria, or in some cases by a pepsin-like enzyme secreted by digestive glands.

(1832). LVIII. Remarks on the structure and affinities of Cephalotus. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science: Vol. 1, No. 4, pp. 314-317.

(1883). On the Morphology of the Pitcher of Cephalotus follicularis. Transactions of the Botanical Society of Edinburgh: Vol. 14, No. 1-4, pp. 172-181.

THE four genera of pitchered insectivorous plants at present in general cultivation are Nepenthes, Sarracenia, Darlingtonia, and Cephalotus. Attention was drawn to the minute structure and physiological action of the first three of these by Sir J. Hooker in his celebrated presidential address to the British Association in 1874, while the structure and morphology of the last was treated of by my master, Prof. Dickson (Journal of Botany, 1878, 1881). Both observers pointed out an attractive surface studded with honey-glands, which constituted the lid part, a conducting surface, either of an exceedingly smooth nature (Nepenthes), or beset with small downward-directed hairs (Sarracenia, Darlingtonia, Cephalotus), and in most cases a glandular surface (Nepenthes, S. purpurea and Cephalotus), the secretion from which directly or indirectly assisted in digestion of animal products. In Sarracenia and Darlingtonia there was found in addition a detentive surface, covered with long deflected hairs.

In an attempt to encourage the filling of gaps in the chromosome record for higher plants, Raven (1975) listed families for which no chromosome information was available; 44 from Cronquist (1968) and 49 from Thorne (1968) and Takhtajan (1969). A few of these mainly monotypic families are represented in the living collections at Kew and two have now been studied: Akaniaceae and Cephalotaceae; but it was subsequently discovered that a count for Cephalotusfollicularis Labill., the only member of the latter family, had previously been published by Kondo (1969). Voucher material of the plants studied has been placed in the Kew Herbarium and permanent slide preparations are retained in the Cytology Section, Jodrell Laboratory.

Growth, size and mortality of pitchers, and volume of their fluid contents were examined in the endemic Albany pitcher plant Cephalotus follicularis in relation to exposure, and age of the pitchers, and the time of year. C. follicularis had its growth season in spring and summer, between late October and February. Mortality was greatest in 'Year 2 or Older' pitchers, and greater in exposed pitchers in both age classes. The highest mortality was recorded between December and February. The pitchers opened when growth had finished, and their size was independent of age and year. There was no difference in size between sheltered localities, but one exposed locality had pitchers that were significantly larger than those of other localities. The pitchers contained fluid during development while the lid was closed which suggested that, initially, the fluid was a plant secretion. There was a significant difference in fluid volumes between shaded and exposed pitchers in late summer but these differences did not exist in spring following the winter rains.

The West Australian pitcher plant Cephalotus follicularis has adaptive structures for carnivory including modified leaves as pitfall containers, specialized surface microtopography to reduce adhesion of insect footpads and the development of gland tissue that secretes digestive enzymes. Gland masses on the lateral pitcher walls are made up of unspecialized mesophyll cells supporting two different types of gland. Cephalotus is geographically and taxonomically isolated from other pitcher plants. A detailed scanning electron and transmission electron microscopy study of the cell types within the pitchers of Cephalotus was carried out and the evolutionary and taxonomic significance of its adaptions to carnivory are discussed.

PROF. JOHN MTJIRHEAD MACFARLANE, emeritus professor of botany in the University of Pennsylvania, died at his home in Philadelphia a few weeks ago. He was born in Kirkcaldy in 1855, and his work was over more than twenty years ago. One or two old friends still remember him when he and they were boys in Edinburgh, where he learned his botany from “Woody Fibre” and from Alexander Dickson, and became one of Bayley Balfour's first assistants. It was under Balfour's influence that he wrote his once well-known paper on the minute structure of plant hybrids, which remained perhaps his chief work to the end. It was a careful comparison, within the histological limitations of its day, between the tissues of various hybrids and their parents, in such curious cases as the so-called Philageria (that is, Lapageria x Philesia) Veitchii, and the famous 'graft-hybrid', Cytisus Adami. This investigation led to his first appointment in the University of Pennsylvania in 1892, and gained him the Banksian Medal of the Royal Horticultural Society a little later on. His old master Dickson had been interested in pitcher-plants, and the Edinburgh Garden was rich in these, in cluding the rare little Cephalotus and many hybrid Sarracenias and other things. Macfarlane had a note in NATURE on honey-glands in pitcher-plants, nearly sixty years ago. Long afterwards he did the pitcher - plants for various Floras, including those of British North Borneo and of New Guinea, and he wrote the chapters on Nepenthes, Sarracenia and Cephalotus for Engler. He was a very faithful and a very industrious man.

I OBSERVE that the last sentence but one of my brief notice of Cephalotus, which appeared in NATURE last week, is calculated to convey an erroneous impression. The lid g of Fig. 1 is seen to be a conical structure with a relatively broad base and a narrower indented apex. In the matured pitcher the free portion of the lid is much broader than its more contracted base; and the developed and involuted margin referred to extends round the mouth of the pitcher until it reaches that base, but does not cross it, as by an oversight on my part my words imply.