Ultra-fast underwater suction traps

Carnivorous aquatic Utricularia species catch small prey animals using millimetre-sized underwater suction traps, which have fascinated scientists since Darwin's early work on carnivorous plants. Suction takes place after mechanical triggering and is owing to a release of stored elastic energy in the trap body accompanied by a very fast opening and closing of a trapdoor, which otherwise closes the trap entrance watertight. The exceptional trapping speed--far above human visual perception--impeded profound investigations until now. Using high-speed video imaging and special microscopy techniques, we obtained fully time-resolved recordings of the door movement. We found that this unique trapping mechanism conducts suction in less than a millisecond and therefore ranks among the fastest plant movements known. Fluid acceleration reaches very high values, leaving little chance for prey animals to escape. We discovered that the door deformation is morphologically predetermined, and actually performs a buckling/unbuckling process, including a complete trapdoor curvature inversion. This process, which we predict using dynamical simulations and simple theoretical models, is highly reproducible: the traps are autonomously repetitive as they fire spontaneously after 5-20 h and reset actively to their ready-to-catch condition.     

Predation by the tropical plant Utricularia foliosa

1. We examined the prey captured by individual plants of the tropical carnivorous plant Utricularia foliosa, located in different areas along a creek in the Colombian Amazon and the zooplankton and macroinvertebrate communities associated with the plants. The aims were: (i) to determine whether bladders of different sizes within each plant catch different numbers of prey or exploit different size ranges and types of prey, (ii) if the quantity and composition of prey captured varies temporally and/or spatially and (iii) if the plant has evolved effective mechanisms of attracting prey. 2. Utricularia foliosa captured the most abundant species of macroinvertebrates associated with the plant. Larger bladders captured more, larger and more diverse prey. However, benefits of the extra prey caught by large bladders were not offset by the greater cost of producing bladders larger than approximately 1650 μm. 3. The number of prey captured was higher in those plants with more carbohydrates per bladder and with a higher ratio of antenna size/bladder length. The antennae enhance capture success by offering the prey a favourable substratum that exploits their natural locomotor and feeding behaviour. However, although carbohydrates may lure prey, carbohydrate production was not a strategy of the plant to enhance the capture of prey, because the amount of carbohydrates in the bladder was related to the abundance of periphyton.     

The effect of bladderwort (Utricularia) predation on microcrustacean prey

SUMMARY 1. The effects of the carnivorous plant Utricularia ( bladderwort) on its microcrustacean and macroinvertebrate prey were studied under seminatural and natural conditions. The results suggest that Utricularia is a strong interactor in littoral communities that influences its prey populations by direct predation and indirect facilitation.
2. In an 8-week enclosure experiment, effects on prey density were compared in three treatments with (1) U. vulgaris with intact trapbladders, (2) U. vulgaris without bladders and (3) no Utricularia present.
3. Utricularia predation caused a decrease in prey density over time, whereas presence of Utricularia without bladders increased prey density. In the controls without Utricularia , prey density was relatively constant over time.
4. Field samples were collected to quantify predation rates of three Utricularia species on two natural prey populations. Daily consumption rates on prey peaked from mid-July to mid-August for all Utricularia species, but were low in June and September. This pattern was explained mainly by a high number of trapbladders at this time, but also by a slight increase in the number of prey caught per bladder. Per capita prey mortality rates caused by Utricularia were substantial and ranged between 0.14 and 0.43 day⁻¹ for copepods, 0.1–0.27 day⁻¹ for ostracods and 0.04–0.2 day⁻¹ for chydorid cladocerans.
5. Predation and facilitation effects were observed for total prey and separately for epiphytic and benthic prey. Planktonic microcrustaceans showed no response to Utricularia presence.     

Effects of zooplankton and conductivity on tropical Utricularia foliosa investment in carnivory

Investment by bladderwort (Utricularia foliosa) in carnivory was estimated in lakes from the Colombian and Brazilian Amazon with different dissolved mineral nutrients and prey availability. As zooplankton abundance in the lake decreased, an increase in the number of bladders per leaf and in the mean bladder size was observed. However, this investment increment in carnivory diminished as the overall availability of dissolved ions in the lake increased. Our results show that carnivorous plants U. foliosa optimise their investment in carnivory, changing bladder number and bladder size according to zooplankton abundance and conductivity.     

Effects of light and microcrustacean prey on growth and investment in carnivory in Utricularia vulgaris

SUMMARY 1. In a 5-week enclosure experiment, we studied the effects of light (ambient light, low light) and prey availability (no prey, prey added) on growth and investment in carnivory in Utricularia vulgaris .
2. Investment in carnivory, measured as the proportion of biomass allocated to bladders, was strongly affected by our manipulations of light intensity and prey density. In the treatment with high prey density the light reduction decreased the investment in bladders from 25% to zero. The effect of prey density on investment in bladders was negative. Because prey addition increased the concentration of nutrients, especially phosphorus, we propose that the effect of the prey treatment on investment reflected altered nutrient concentrations.
3. Availability of prey increased growth and apical biomass of Utricularia . As Utricularia had very few bladders in some treatments we suggest that the effect was due to a combination of live prey trapped and increased nutrient availability from dead prey.
4. Abundance of periphyton on Utricularia and on the enclosure walls was highest in the treatments with high prey density where nutrient concentrations were highest. Thus we interpret the response of periphyton as primarily reflecting nutrient availability.     

Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants

It has been widely accepted that the growth-related phytohormone auxin is the endogenous signal that initiates bending movements of plant organs. In 1875, Charles Darwin described how the bending movement of leaves in carnivorous sundew species formed an ‘outer stomach’ that allowed the plants to enclose and digest captured insect prey. About 100 years later, auxin was suggested to be the factor responsible for this movement. We report that prey capture induces both leaf bending and the accumulation of defence-related jasmonate phytohormones. In Drosera capensis fed with fruitflies, within 3 h after prey capture and simultaneous with leaf movement, we detected an increase in jasmonic acid and its isoleucine conjugate. This accumulation was spatially restricted to the bending segment of the leaves. The application of jasmonates alone was sufficient to trigger leaf bending. Only living fruitflies or the body fluids of crushed fruitflies induced leaf curvature; neither dead flies nor mechanical treatment had any effect. Our findings strongly suggest that the formation of the ‘outer stomach’ in Drosera is a chemonastic movement that is triggered by accumulation of endogenous jasmonates. These results suggest that in carnivorous sundew plants the jasmonate cascade might have been adapted to facilitate carnivory rather than to defend against herbivores.     

The smallest but fastest: Ecophysiological characteristics of traps of aquatic carnivorous Utricularia

Aquatic Utricularia species usually grow in standing, nutrient-poor humic waters. They take up all necessary nutrients either directly from the water by rootless shoots or from animal prey by traps. The traps are hollow bladders, 1–6 mm long with elastic walls and have a mobile trap door. The inner part of the trap is densely lined with quadrifid and bifid glands and these are involved in the secretion of digestive enzymes, resorption of nutrients and pumping out the water. The traps capture small aquatic animals but they also host a community of microorganisms considered as commensals. How do these perfect traps function, kill and digest their prey? How do they provide ATP energy for their demanding physiological functions? What are the nature of the interactions between the traps and the mutualistic microorganisms living inside as commensals? In this mini review, all of these questions are considered from an ecophysiologist''s point of view, based on the most recent literature data and unpublished results. A new concept on the role of the commensal community for the plants is presented.Key words: aquatic carnivorous plants, bladderwort, bladders, firing, resetting, enzyme secretion, water pumping, microbial commensals     

Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences

Many animals sequester dietary defensive compounds and incorporate them into the offspring, which protects the young against predation. One possible but poorly investigated question is whether females of such species actively prey upon toxic diets. The snake Rhabdophis tigrinus sequesters defensive steroids from toads consumed as prey; it also feeds on other amphibians. Females produce chemically armed offspring in direct proportion to their own level of toad-derived toxins by provisioning the toxins to their eggs. Our field observations of movements and stomach contents of radio-tracked R. tigrinus showed that gravid snakes preyed upon toads by actively foraging in the habitat of toads, even though toads were a scarce resource and toad-searching may incur potential costs. Our Y-maze experiments demonstrated that gravid females were more likely to trail the chemical cues of toads than were males or non-gravid females. These results showed behavioural switching in females and active foraging for scarce, toxic prey during gestation. Because exploitation of toads by gravid females results in their offspring being more richly endowed with prey-derived toxins, active foraging for toxic prey is expected to be an adaptive antipredator trait, which may enhance chemical defence in offspring.     

The role of phytoplankton in the diet of the bladderwort Utricularia australis R.Br. (Lentibulariaceae)

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Top carnivores increase their kill rates on prey as a response to human-induced fear

The fear induced by predators on their prey is well known to cause behavioural adjustments by prey that can ripple through food webs. Little is known, however, about the analogous impacts of humans as perceived top predators on the foraging behaviour of carnivores. Here, we investigate the influence of human-induced fear on puma foraging behaviour using location and prey consumption data from 30 tagged individuals living along a gradient of human development. We observed strong behavioural responses by female pumas to human development, whereby their fidelity to kill sites and overall consumption time of prey declined with increasing housing density by 36 and 42%, respectively. Females responded to this decline in prey consumption time by increasing the number of deer they killed in high housing density areas by 36% over what they killed in areas with little residential development. The loss of food from declines in prey consumption time paired with increases in energetic costs associated with killing more prey may have consequences for puma populations, particularly with regard to reproductive success. In addition, greater carcass availability is likely to alter community dynamics by augmenting food resources for scavengers. In light of the extensive and growing impact of habitat modification, our study emphasizes that knowledge of the indirect effects of human activity on animal behaviour is a necessary component in understanding anthropogenic impacts on community dynamics and food web function.     

Assassin bug uses aggressive mimicry to lure spider prey

Assassin bugs (Stenolemus bituberus) hunt web-building spiders by invading the web and plucking the silk to generate vibrations that lure the resident spider into striking range. To test whether vibrations generated by bugs aggressively mimic the vibrations generated by insect prey, we compared the responses of spiders to bugs with how they responded to prey, courting male spiders and leaves falling into the web. We also analysed the associated vibrations. Similar spider orientation and approach behaviours were observed in response to vibrations from bugs and prey, whereas different behaviours were observed in response to vibrations from male spiders and leaves. Peak frequency and duration of vibrations generated by bugs were similar to those generated by prey and courting males. Further, vibrations from bugs had a temporal structure and amplitude that were similar to vibrations generated by leg and body movements of prey and distinctly different to vibrations from courting males or leaves, or prey beating their wings. To be an effective predator, bugs do not need to mimic the full range of prey vibrations. Instead bugs are general mimics of a subset of prey vibrations that fall within the range of vibrations classified by spiders as 'prey'.     

Temporal and spatial change of the investment in carnivory of the tropical Utricularia foliosa

Investment by bladderwort (Utricularia foliosa L.) in carnivory, in terms of biochemical composition (carbohydrates per bladder), elemental composition (carbon and nitrogen per bladder), and morphology of the bladders (length, depth, size of the trap door, and size of antennae), was estimated in seven plants located in Yahuarcaca creek (Colombian Amazon) five times from March to May 2005. The aims were to determine whether investment in carnivory varies temporally (over the growing season of the plant) and/or spatially, and if this potential change in carnivory investment varies according to nutrient conditions. The main differences in the investment in carnivory (changes in bladder number and bladder size, and changes in the size of the antennae) were among locations and there were not important differences over the growing season of the plant. Nitrogen and not phosphorus, was the element that stimulated the investment in carnivory. In addition to changes in bladder number and bladder size, we observed a new strategy to enhance prey capture under nitrogen limitation: changes in the size of the antennae. The size of the antennae was approximately 1.3 higher in those plants located in sites with low NO₃⁻. However, we did not observed changes in the carbon/nitrogen ratio of the bladders or in the relationship between bladder length with bladder depth or size of the trap door. The amount of carbohydrates per bladder was also 1.8 higher in those plants located in sites with low NO₃⁻ (0.13 μM) than those with higher NO₃⁻ concentration (0.39 μM). However, the amount of carbohydrates in the bladder was related with the abundance of periphyton and, hence, it is not possible to conclude that carbohydrate production was a strategy of the plant to enhance the capture of prey. Therefore, our findings do not support the carbohydrate mucilage lure speculations.     

Interference coloration as an anti-predator defence

Interference coloration, in which the perceived colour varies predictably with the angle of illumination or observation, is extremely widespread across animal groups. However, despite considerable advances in our understanding of the mechanistic basis of interference coloration in animals, we still have a poor understanding of its function. Here, I show, using avian predators hunting dynamic virtual prey, that the presence of interference coloration can significantly reduce a predator''s attack success. Predators required more pecks to successfully catch interference-coloured prey compared with otherwise identical prey items that lacked interference coloration, and attacks against prey with interference colours were less accurate, suggesting that changes in colour or brightness caused by prey movement hindered a predator''s ability to pinpoint their exact location. The pronounced anti-predator benefits of interference coloration may explain why it has evolved independently so many times.     

Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae)

BACKGROUND AND AIMS: Species of Utricularia and Genlisea (Lentibulariaceae) are carnivorous, capturing small prey in traps which are physiologically very active, with abundant quadrifid and bifid glands. Traps of Utricularia have walls composed of two cell layers, and are filled with water. Diverse communities of commensal microorganisms often live inside the traps. Genlisea forms long, hollow subterranean traps of foliar origin, growing in anoxic wet substrate. Knowledge of the O(2) concentrations inside Utricularia and Genlisea traps is vital for understanding their physiological functioning and conditions for the life of commensals. To test the hypothesis that prey are killed by anoxia inside the traps, and to measure respiration of traps, [O(2)] was measured in the fluid in mature traps of these species. METHODS: Oxygen concentration and electrical redox potential were measured using a small Clark-type oxygen sensor and a miniature platinum electrode, respectively, in the fluid of excised and intact traps of six aquatic Utricularia species and in Genlisea hispidula traps. KEY RESULTS: Steady-state [O(2)] in the traps of both genera always approached zero (median 0.0-4.7 microm). The [O(2)] decreased after electrodes were inserted into Utricularia traps at a rate which ranged from 0.09 to 1.23 mm h(-1) and was lower in traps of irradiated and intact shoots with higher [O(2)] in shoot tissues. Redox potential ranged from -24 to -105 mV in the traps, confirming the very small or zero [O(2)]. CONCLUSIONS: Very small or zero [O(2)], effectively anoxia, is demonstrated in Utricularia and Genlisea traps. This is probably below the critical [O(2)] for prey survival, and causes captured prey to die of suffocation. Internal trap glands and trap commensals are considered to be adapted to facultative anoxia interrupted by limited periods of higher [O(2)] after firings.     

Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities

BACKGROUND: Carnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs. PITCHER: Fluid as a Habitat The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O(2) and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water. INQUILINE: Diversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. MUTUALISTIC: Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N(2). CONCLUSIONS: There is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.     

Nectar,not colour,may lure insects to their death

We experimentally demonstrate in the field that prey of the carnivorous plant Sarracenia purpurea are attracted to sugar, not to colour. Prey capture (either all taxa summed or individual common taxa considered separately) was not associated with total red area or patterning on pitchers of living pitcher plants. We separated effects of nectar availability and coloration using painted ‘pseudopitchers’, half of which were coated with sugar solution. Unsugared pseudopitchers captured virtually no prey, whereas pseudopitchers with sugar solution captured the same amount of prey as living pitchers. In contrast to a recent study that associated red coloration with prey capture but that lacked controls for nectar availability, we infer that nectar, not colour, is the primary means by which pitcher plants attract prey.     

Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant

Nepenthes pitcher plants are typically carnivorous, producing pitchers with varying combinations of epicuticular wax crystals, viscoelastic fluids and slippery peristomes to trap arthropod prey, especially ants. However, ant densities are low in tropical montane habitats, thereby limiting the potential benefits of the carnivorous syndrome. Nepenthes lowii, a montane species from Borneo, produces two types of pitchers that differ greatly in form and function. Pitchers produced by immature plants conform to the ‘typical’ Nepenthes pattern, catching arthropod prey. However, pitchers produced by mature N. lowii plants lack the features associated with carnivory and are instead visited by tree shrews, which defaecate into them after feeding on exudates that accumulate on the pitcher lid. We tested the hypothesis that tree shrew faeces represent a significant nitrogen (N) source for N. lowii, finding that it accounts for between 57 and 100 per cent of foliar N in mature N. lowii plants. Thus, N. lowii employs a diversified N sequestration strategy, gaining access to a N source that is not available to sympatric congeners. The interaction between N. lowii and tree shrews appears to be a mutualism based on the exchange of food sources that are scarce in their montane habitat.     

Recent ecophysiological,biochemical and evolutional insights into plant carnivory

BackgroundCarnivorous plants are an ecological group of approx. 810 vascular species which capture and digest animal prey, absorb prey-derived nutrients and utilize them to enhance their growth and development. Extant carnivorous plants have evolved in at least ten independent lineages, and their adaptive traits represent an example of structural and functional convergence. Plant carnivory is a result of complex adaptations to mostly nutrient-poor, wet and sunny habitats when the benefits of carnivory exceed the costs. With a boost in interest and extensive research in recent years, many aspects of these adaptations have been clarified (at least partly), but many remain unknown.ScopeWe provide some of the most recent insights into substantial ecophysiological, biochemical and evolutional particulars of plant carnivory from the functional viewpoint. We focus on those processes and traits in carnivorous plants associated with their ecological characterization, mineral nutrition, cost–benefit relationships, functioning of digestive enzymes and regulation of the hunting cycle in traps. We elucidate mechanisms by which uptake of prey-derived nutrients leads to stimulation of photosynthesis and root nutrient uptake.ConclusionsUtilization of prey-derived mineral (mainly N and P) and organic nutrients is highly beneficial for plants and increases the photosynthetic rate in leaves as a prerequisite for faster plant growth. Whole-genome and tandem gene duplications brought gene material for diversification into carnivorous functions and enabled recruitment of defence-related genes. Possible mechanisms for the evolution of digestive enzymes are summarized, and a comprehensive picture on the biochemistry and regulation of prey decomposition and prey-derived nutrient uptake is provided.     

Context-dependent ‘safekeeping’ of foraging tools in New Caledonian crows

Several animal species use tools for foraging, such as sticks to extract embedded arthropods and honey, or stones to crack open nuts and eggs. While providing access to nutritious foods, these behaviours may incur significant costs, such as the time and energy spent searching for, manufacturing and transporting tools. These costs can be reduced by re-using tools, keeping them safe when not needed. We experimentally investigated what New Caledonian crows do with their tools between successive prey extractions, and whether they express tool ‘safekeeping’ behaviours more often when the costs (foraging at height), or likelihood (handling of demanding prey), of tool loss are high. Birds generally took care of their tools (84% of 176 prey extractions, nine subjects), either trapping them underfoot (74%) or storing them in holes (26%)—behaviours we also observed in the wild (19 cases, four subjects). Moreover, tool-handling behaviour was context-dependent, with subjects: keeping their tools safe significantly more often when foraging at height; and storing tools significantly more often in holes when extracting more demanding prey (under these conditions, foot-trapping proved challenging). In arboreal environments, safekeeping can prevent costly tool losses, removing a potentially important constraint on the evolution of habitual and complex tool behaviour.