The significance of carnivory for the fitness of Drosera in its natural habitat

Summary The effects on Drosera intermedia and D. rotundifolia of supplementary feeding with Drosophila melanogaster were studied in plants growing in their natural habitat. The artificial food supply was within the natural range of prey quantity. In both species supplementary feeding led to significantly higher dry weights of summer and winter plant, more leaves, more flowers, more seeds, and a larger trapping area. The dry weight of plants increased much more than the dry weight of prey added, indicating a fertilizing effect. Thus, animal food supply is an important limiting factor in the field. The essential component of the prey is probably its mineral content. There were significant differences between the two species of sundew. In D. rotundifolia the effect of feeding on dry weight was smaller and plants nerver showed axillary budding. However the effect on the percentage of blooming plants was more than twice as strong as in D. intermedia. Considering only the prey actually absorbed per unit of plant biomass, both species show about the same fertilizing effect. The number of fruits per unit of biomass was about twice as large in D. rotundifolia as in D. intermedia. The reasons for these differences are discussed in the light of niche segregation with respect to habitat and range of prey.     

The significance of carnivory for the fitness of Drosera in its natural habitat

Summary A field study of two carnivorous plant species, Drosera intermedia and D. rotundifolia, was carried out in a small silting-up bog in Southern Bavaria (FR Germany). Various parameters of undisturbed individuals of both species were measured for a period of two years and subjected to a partial correlation analysis. The importance of prey as a limiting factor for various fitness parameters was confirmed for both species. Other factors may occasionally also be limiting, e.g. assimilation area and water supply. Benefits obtained from the prey are partly transferred to the next year via the winter bud. The importance of the relative demonstrated: Plants of D. rotundifolia showed higher fitness values in higher positions, those of D. intermedia in lower positions. Growth characteristics of both species tended to influence the height of their own position in a corresponding direction: D. intermedia downwards and D. rotundifolia upwards. In both species negative effects of intraspecific neighbourhood were evident, whereas interspecific effects were not detectable. Plants of D. intermedia tend to influence their neighbourhood situation by changing their position by rhizome-like stem growth. In D. intermedia the decision to reproduce by seeds or axillary buds seems to be made at least partially already in the year before. D. rotundifolia was only observed reproducing by seeds. In spite of different catching characteristics (plant shape, plant size, microhabitats, prey spectra), the general catching success, measured as prey biomass per plant biomass, was equal in both species of sundew. This agrees with earlier findings that in this bog both species have the same biomass per ground area.     

Three carnivorous plant species (Drosera spp.) in European Russia: peaceful coexistence?

In spite of the recent improvements in the understanding of carnivorous plants’ biology, some questions have remained unanswered. In this study, the segregation of food niches (i.e. specialization on different categories of prey) for three sympatric carnivorous temperate Drosera species with different shapes of trapping leaves is tested. Potentially available prey was also taken into account, by using artificial traps. Almost all the prey trapped by the three Drosera species and by passive traps belonged to four insect orders: Diptera, Hymenoptera, Coleoptera, Homoptera, as well as Araneae. Diptera specimens were the main prey for all the species. This study demonstrates that arthropods caught by the three temperate sympatric sundew species (D. rotundifolia, D. obovata and D. anglica), belong to the same orders. The proportions of prey from different orders, caught by different sundew species did not differ significantly. The result does not necessarily imply the absence of interspecific competition for prey: arthropods were identified only to order, and competition may have resulted in specialization on prey taxa of lower rank.     

Prey-induced changes in the accumulation of amino acids and phenolic metabolites in the leaves of <Emphasis Type="Italic">Drosera capensis</Emphasis> L

Effect of prey feeding (ants Formica fusca) on the quantitative changes in the accumulation of free amino acids, soluble proteins, phenolic metabolites and mineral nutrients in the leaves of carnivorous plant Drosera capensis was studied. Arginine was the most abundant compound in Drosera leaves, while proline was abundant in ants. The amount of the majority of amino acids and their sum were elevated in the fed leaves after 3 and 21 days, and the same, but with further enhancement after 21 days, was observed in ants. Accumulation of amino acids also increased in young non-fed leaves of fed plants. Soluble proteins decreased in ants, but were not enhanced in fed leaves. This confirms the effectiveness of sundew’s enzymatic machinery in digestion of prey and suggests that amino acids are not in situ deposited, but rather are allocated within the plant. The content of total soluble phenols, flavonoids and two selected flavonols (quercetin and kaempferol) was not affected by feeding in Drosera leaves, indicating that their high basal level was sufficient for the plant’s metabolism and prey-induced changes were mainly N based. The prey also showed to be an important source of other nutrients besides N, and a stimulation of root uptake of some mineral nutrients is assumed (Mg, Cu, Zn). Accumulation of Ca and Na was not affected by feeding.     

A sensitive flower: mechanical stimulation induces rapid flower closure in Drosera spp. (Droseraceae)

Some plants rapidly close their leaves in response to mechanical stimulation, but no case is known in which mechanical stimulation causes rapid petal closure. In this study, we found that Drosera tokaiensis closes petals within 2–10 min after experimental stimulation of the calyx, closed flowers or scapes with a pair of tweezers. Although petal closure was induced more rapidly by touching a position closer to a flower, it was not induced by stimulating stamens and pistils. The habit of petal closure varies among species of Drosera: after experimental stimulations of the calyx or scapes, D. tokaiensis and D. spatulata often closed petals but D. rotundifolia and D. toyoakensis did not close them. The petal closure may function as defense against a specialist florivore.     

Insect capture and growth of the insectivorous Drosera rotundifolia L.

Summary Rates of insect capture increased with leaf area in the insectivorous plant Drosera rotundifolia, and growth of new leaves was related to insect capture. However, increased leaf growth was counterbalanced by leaf abscission which was in turn related to insect capture and leaf growth. Leaf loss equaled leaf growth in plants having natural rate of insect capture. A large proportion of the nitrogen gain from prey was stored in the hypocotyl; it was estimated from feeding experiments that about 24% to 30% of the nitrogen stored in the hypocotyl after winter originated from insect capture in the previous season. The effect of insect capture is discussed in relation to the life cycle of Drosera.     

The utilization of nitrogen from insect capture by different growth forms of Drosera from Southwest Australia

Summary Plants of Drosera species, neighbouring noncarnivorous plants, and arthropods on or near each Drosera sp. were collected at 11 contrasting habitat locations in SW Australia. At three of the sites clones of the rare glandless mutant form of D. erythrorhiza were collected alongside fully glandular counterparts. The ¹⁵N value (¹⁵N/¹⁴N natural isotope composition) of insect-free leaf and stem fractions was measured, and the data then used to estimate proportional dependence on insect N (%N_dI) for the respective species and growth forms of Drosera. The data indicated lower %N_dI values for rosette than for self-supporting erect or for climbing vine species. The latter two groups showed an average %N_dI value close to 50%. The %N_dI increased with length and biomass of climbing but not erect forms of Drosera. ¹⁵N values of stems were positively correlated with corresponding values for leaves of Drosera. Leaf material was on average significantly more ¹⁵N enriched than stems, possibly due to delayed transport of recent insect-derived N, or to discrimination against ¹⁵N in transfer from leaf to the rest of the plant. The comparison of ¹⁵N values of insects and arthropod prey, glandless and glandular plants of D. erythrorhiza indicated %N_dI values of 14.3, 12.2 and 32.2 at the respective sites, while matching comparisons based on ¹⁵N of insect, reference plants and glandular plants proved less definitive, with only one site recording a positive %N_dI (value of 10.4%) despite evidence at all sites of feeding on insects by the glandular plants. The use of the ¹⁵N technique for studying nutrition of carnivorous species and the ecological significance of insect feeding of different growth forms of Drosera growing in a large range of habitats is discussed.     

Studies on the isolation of plumbagin from in vitro and in vivo grown Drosera species

The rapid clonal multiplication of two species of South African Drosera is described. Levels of plumbagin, (5-hydroxy-2-methyl-1,4-naphthoquinone) from in vivo and in vitro grown plants are compared to those present in Plumbago roots. P. auriculata Lam. roots contained more than twice as much plumbagin as in vivo grown D. capensis L. plants which in turn contained more than twice as much as comparable plants of D. natalensis Diels. It is concluded that the extraction of plumbagin from Drosera plants is not commercially feasible.     

Relationship between types of prey captured and growth form in Drosera in southwestern Australia

Abstract Sympatrically growing species of Drosera were examined, including rosette forms, climbers and upright, self-supporting species, in southwestern Australia, to see whether the height above ground of the capturing leaves influenced the kinds of prey caught. The leaves examined for invertebrate prey remains were all collected at the same time and the results thus represent a snapshot of the prey situation. Although the number of fully opened, active leaves and leaf size among species varied 40-fold and 22-fold, respectively, total catch per unit leaf area was relatively constant, regardless of growth form. Growth form was strongly correlated with the kinds of prey caught. Prostrate species caught mainly walking, non-aerial prey, while self-supporting and climbing species caught predominantly aerial prey.     

Variation in resource abundance affects diet and feeding morphology in the pumpkinseed sunfish (Lepomis gibbosus)

Summary Growth responses and accumulation of N and P were studied in two pygmy south-west Australian species of Drosera following supplementary feeding of arthropods (collembolans, Hypogastrura vernalis and fruit flies, Drosophila melanogaster) and/or a balanced mineral nutrient supplement (N as nitrate) via the roots. One feeding experiment used glasshouse-raised germlings from vegetative propagules (gemmae) of the perennial Drosera closterostigma, the other three (two on D. closterostigma and one on the annual D. glanduligera) involved natural populations engaging in natural captures of indigenous prey. All experiments recorded highly significant increases in plant dry matter, N and P (all plant age groups) and in reproductive performance (adult plants only) from artificial feeding of arthropods, but no apparent benefits from minerals alone or additive effects of minerals above that due to insects. Unresponsiveness to mineral nutrients was suggested to relate to inability of the species to use nitrate, while up to three-fold growth and nutrient uptake response to insects indicated that growth of natural populations might be severely limited by inadequate catches of prey. It is concluded that the highly nutrient-poor conditions typical of the habitat of pygmy species of Drosera may have promoted marked specialization towards carnivory and an attendant decline in ability to utilize soil-derived sources of nutrients.     

Red trap colour of the carnivorous plant Drosera rotundifolia does not serve a prey attraction or camouflage function

The traps of many carnivorous plants are red in colour. This has been widely hypothesized to serve a prey attraction function; colour has also been hypothesized to function as camouflage, preventing prey avoidance. We tested these two hypotheses in situ for the carnivorous plant Drosera rotundifolia. We conducted three separate studies: (i) prey attraction to artificial traps to isolate the influence of colour; (ii) prey attraction to artificial traps on artificial backgrounds to control the degree of contrast and (iii) observation of prey capture by D. rotundifolia to determine the effects of colour on prey capture. Prey were not attracted to green traps and were deterred from red traps. There was no evidence that camouflaged traps caught more prey. For D. rotundifolia, there was a relationship between trap colour and prey capture. However, trap colour may be confounded with other leaf traits. Thus, we conclude that for D. rotundifolia, red trap colour does not serve a prey attraction or camouflage function.     

Breeding systems of the Japanese-endemic carnivorous sundew species Drosera makinoi and Drosera toyoakensis (Droseraceae)

In response to unfavorable environmental conditions, some Drosera species in the northern hemisphere do not open their flowers but form bud-like flowers. The bud-like flowers exhibit pseudo-cleistogamous behavior and produce similar numbers of seeds as open flowers. However, it is not clear how common this type of reproduction is in the genus Drosera. In this study, we examined the effects of flowering (opening flowers/forming bud-like flowers) and pollinator visitation on seed production in Drosera makinoi and D. toyoakensis, two endemic species in Japan. D. makinoi and D. toyoakensis plants did not open 20%–40% chasmogamous flowers to form bud-like flowers. The numbers of mature seeds produced by bud-like flowers were significantly lower than those produced by open flowers (0%–2% of open flowers). In D. makinoi, the percentage of bud-like flowers correlated negatively with the seed production per plant, suggesting that the production of bud-like flowers decreased the lifetime reproductive success. In both D. makinoi and D. toyoakensis, pollinator-excluded flowers produced similar numbers of seeds as control flowers. Our results suggest that pseudo-cleistogamy does not occur in D. makinoi and D. toyoakensis, and they produce seeds without pollinator visits once flowers open.     

Consumption of introduced prey by native predators: Argentine ants and pit-building ant lions

When populations of native predators are subsidized by numerically dominant introduced species, the structure of food webs can be greatly altered. Surprisingly little is known, however, about the general factors that influence whether or not native predators consume introduced species. To learn more about this issue, we examined how native pit-building ant lions (Myrmeleon) are affected by Argentine ant (Linepithema humile) invasions in coastal southern California. Compared to areas without L. humile, invaded areas contained few native ant species and were deficient in medium-sized and large bodied native ants. Based on these differences, we predicted that Argentine ants would negatively affect ant lion larvae. Contrary to this expectation, observational surveys and laboratory growth rate experiments revealed that Myrmeleon were heavier, had longer mandibles, and grew more quickly when their main ant prey were Argentine ants rather than native ants. Moreover, a field transplant experiment indicated that growth rates and pupal weights were not statistically different for larval ant lions reared in invaded areas compared to those reared in uninvaded areas. Argentine ants were also highly susceptible to capture by larval Myrmeleon. The species-level traits that presumably make Argentine ant workers susceptible to capture by larval ant lions—small size and high activity levels—appear to be the same characteristics that make them unsuitable prey for vertebrate predators, such as horned lizards. These results underscore the difficulties in predicting whether or not numerically dominant introduced species serve as prey for native predators.     

Application of rapd in the determination of genetic fidelity in micropropagated Drosera plantlets

Summary Random amplified polymorphic DNA (RAPD) markers were used to verify the clonal fidelity of two micropropagated Drosera species, D. anglica and D. binata, which were regenerated by adventitious budding from leaf explants and shoot tips, respectively. Twenty arbitrary decamers were used to screen 15 randomly selected plantlets of each species. No genetic variation was detected among D. binata regenerants, whereas a 0.08% polymorphism frequency was estimated for D. anglica plantlets. These results indicate that the regeneration of plants through shoot-tip culture is a low-risk method for generating genetic variability, whereas material regenerated through leaf explants requires further verification.     

Phytochemistry of the Carnivorous Sundew Genus Drosera (Droseraceae) – Future Perspectives and Ethnopharmacological Relevance

Species of the carnivorous genus Drosera L. have long been a source of valuable natural products. The various phytochemicals characteristic of these species, particularly 1,4‐naphthoquinones and flavonoids, have contributed to the diverse utilization of sundews in traditional medicine systems worldwide. A growing number of studies have sought to investigate the comparative phytochemistry of Drosera species for improved sources of pharmaceutically important compounds. The outcomes of these studies are here collated, with emergent trends discussed in detail. Important factors which affect production of secondary metabolites in plants are critically examined, such as environmental influences and in vitro culture, and recommendations subsequently presented based on this. Explicitly, the current review aims to i) present an updated, comprehensive listing of the phytochemical constituents of the genus (including quantitative data where available), ii) summarize important factors which may influence the production of phytopharmaceuticals in plants, and iii) recommend guidelines for future research based on the above, including improved standardization and quality control. We have also included a section discussing future perspectives of research on Drosera spp. based on three different research lines i) the potential to produce much needed lead compounds for treatment of tuberculosis, ii) the potential role of anthocyanins in nitrogen transport, and iii) research into ‘Natural Deep Eutectic’ solvents produced by Drosera spp. in the droplets or ‘dew’ employed to capture insect prey.     

Wound and insect‐induced jasmonate accumulation in carnivorous Drosera capensis: two sides of the same coin

Carnivorous sundew plants catch and digest insect prey for their own nutrition. The sundew species Drosera capensis shows a pronounced leaf bending reaction upon prey capture in order to form an ‘outer stomach’. This formation is triggered by jasmonates, phytohormones typically involved in defence reactions against herbivory and wounding. Whether jasmonates still have this function in D. capensis in addition to mediating the leaf bending reaction was investigated here. Wounded, insect prey‐fed and insect‐derived oral secretion‐treated leaves of D. capensis were analysed for jasmonates (jasmonic acid, JA; jasmonic acid‐isoleucine conjugate, JA‐Ile) using LC‐MS/MS. Prey‐induced jasmonate accumulation in D. capensis leaves was persistent, and showed high levels of JA and JA‐Ile (575 and 55.7 pmol·g·FW^?1, respectively), whereas wounding induced a transient increase of JA (maximum 500 pmol·g·FW^?1) and only low (3.1 pmol·g·FW^?1) accumulation of JA‐Ile. Herbivory, mimicked with a combined treatment of wounding plus oral secretion (W+OS) obtained from Spodoptera littoralis larvae induced both JA (4000 pmol·g·FW^?1) and JA‐Ile (25 pmol·g·FW^?1) accumulation, with kinetics similar to prey treatment. Only prey and W+OS, but not wounding alone or OS, induced leaf bending. The results indicate that both mechanical and chemical stimuli trigger JA and JA‐Ile synthesis. Differences in kinetics and induced jasmonate levels suggest different sensing and signalling events upon injury and insect‐dependent challenge. Thus, in Drosera, jasmonates are still part of the response to wounding. Jasmonates are also employed in insect‐induced reactions, including responses to herbivory and carnivory.     

Response of Sphagnum papillosum and Drosera rotundifolia to Reduced and Oxidized Wet Nitrogen Deposition

We transplanted Sphagnum ??turfs?? containing abundant Drosera rotundifolia into an existing nitrogen deposition experiment at Whim Moss near Edinburgh. These mesocosms received simulated N deposition as either NH ₄ ⁺ or NO ₃ ^- , to give total N deposition rates of approximately 8, 16 or 32, or 64?kg?N?ha^-1?year^-1. Simulated N deposition was added in a realistic way (i.e., with rainfall throughout the year). The ??¹⁵N of this added N was elevated relative to background N. We measured the tissue chemistry and ??¹⁵N of Sphagnum papillosum and D. rotundifolia over two years after transplant. Our aim was to determine uptake of the deposited N and the impact on S. papillosum tissue chemistry and D. rotundifolia tissue chemistry and ecology. We found clear, significant impacts of N deposition on S. papillosum, with increased capitula N content and reduced C:N ratio. Increased ??¹⁵N indicated uptake of deposited N. The response of D. rotundifolia was less clear with impacts only at the highest rate of N deposition. There was no evidence of differential uptake of reduced or oxidized wet N deposition by either S. papillosum or D. rotundifolia. Using the natural abundance stable isotope method we estimated the minimum contribution of prey N to the total N in D. rotundifolia to be 35%. The results suggest that differences in the uptake of reduced or oxidized wet N deposition might not be ecologically significant when wet N deposition is added realistically. They also support the suggestion that a model of N dynamics in Sphagnum-dominated ecosystems that includes the role of Sphagnum as a small-scale ecosystem engineer, is required to predict vascular plant responses to N deposition accurately.     

The distribution of weaver ant pheromones on host trees

The visible anal spots deposited by Oecophylla smaragdina ants have been suggested to deter ant prey, affect interspecific competition and facilitate mutualists and parasites in tracking down Oecophylla ants. I measured the density of anal spots on host trees with and without ants and tested for correlations between spot density, ant activity and the likelihood of being detected by an ant. Spots were only found on trees with ants. On ant-trees, spots were distributed throughout the trees but with higher densities in areas with high ant activity and pheromone densities were higher on twigs compared to leaves. Also there was a positive correlation between spot density and the likelihood of being detected by ants. Anal spots may thus function as reliable cues to interacting species and be an important factor in shaping the community around Oecophylla colonies. Received 31 August 2006; revised 27 April 2007; accepted 2 May 2007.     

Out of the Frying Pan and into the Fire: a Novel Trade-Off for Batesian Mimics

A mimicry system was investigated in which the models were ants (Formicidae) and both the mimics and the predators were jumping spiders (Salticidae). By using motionless lures in simultaneous‐presentation prey‐choice tests, how the predators respond specifically to the static appearance of ants and ant mimics was determined. These findings suggest a rarely considered adaptive trade‐off for Batesian mimics of ants. Mimicry may be advantageous when it deceives ant‐averse potential predators, but disadvantageous in encounters with ant‐eating specialists. Nine myrmecophagic (ant‐eating) species (from Africa, Asia, Australia and North America) and one araneophagic (spider‐eating) species (Portia fimbriata from Queensland) were tested with ants (five species), with myrmecomorphic (ant‐like) salticids (six species of Myrmarachne) and with non‐ant‐like prey (dipterans and ordinary salticids). The araneophagic salticid chose an ordinary salticid and chose flies significantly more often than ants. Portia fimbriata also chose the ordinary salticid and chose flies significantly more often than myrmecomorphic salticids. However, there was no significant difference in how P. fimbriata responded to ants and to myrmecomorphic salticids. The myrmecophagic salticids chose ants and chose myrmecomorphic salticids significantly more often than ordinary salticids and significantly more often than flies, but myrmecophagic salticids did not respond significantly differently to myrmecomorphic salticids and ants.