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.     

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.     

Periphyton and phytoplankton associated with the tropical carnivorous plant Utricularia foliosa

The abundance and taxonomic composition of periphyton attached to the bladders and phytoplankton associated with the aquatic carnivorous plant Utricularia foliosa were quantified, to determine whether periphyton associated with U. foliosa would enhances predation success. Bladder size, periphyton abundance and periphyton richness together explained 76% of the variation observed in the number of prey captured by the bladders. The abundance and richness of periphyton followed the same pattern as phytoplankton, i.e., both increased as dissolved inorganic phosphate concentration rose. This nutrient concentration explained 84 and 74% of the variation observed in richness and abundance of periphyton, respectively. This suggests that abundance and richness of the periphyton associated with U. foliosa depend mostly on environmental conditions rather than on facilitation mechanisms displayed by the plant. In conclusion, if periphyton affects U. folisosa negatively due to the competition for light or nutrients, the plant is “fated to get along with the enemy” but apparently without the capacity to manipulate this “enemy” to its own advantage.     

The utilization of paramecia by the carnivorous plant Utricularia gibba

Summary A method has been devised to ensure capture of large numbers of live paramecia within a short period of time under controlled conditions by the bladders of Utricularia gibba. The method permits a direct evaluation of the role of entrapped animals in the nutrition of this carnivorous plant. Paramecia captured by the bladders of plants growing in a near optimal inorganic medium do not cause an increase in number or length of internodes. In contrast, feeding paramecia to plants grown in a poorly balanced or incomplete medium does result in an increase in both number and length of internodes produced. Feeding paramecia to Utricularia also results in an increase in number of bladders.This study was supported in part by an Undergraduate Research Participant stipend from Public Health Service, grant number 2-TIHE 5 303-09, to the first author and in part by Agricultural Research Service, U.S. Department of Agriculture, Grant No. 12-14-100-7981 (34) to the second author, administered by Crops Research Division, Beltsville, Maryland.     

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.     

The biomechanics of fast prey capture in aquatic bladderworts

Carnivorous plants match their animal prey for speed of movements and hence offer fascinating insights into the evolution of fast movements in plants. Here, we describe the mechanics of prey capture in aquatic bladderworts Utricularia stellaris, which prey on swimming insect larvae or nematodes to supplement their nitrogen intake. The closed Utricularia bladder develops lower-than-ambient internal pressures by pumping out water from the bladder and thus setting up an elastic instability in bladder walls. When the external sensory trigger hairs on their trapdoor are mechanically stimulated by moving prey, the trapdoor opens within 300-700 μs, causing strong inward flows that trap their prey. The opening time of the bladder trapdoor is faster than any recorded motion in carnivorous plants. Thus, Utricularia have evolved a unique biomechanical system to gain an advantage over their animal prey.     

Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important?

Utricularia purpurea is a rootless, free-floating, aquatic, carnivorous plant. I quantified biomass investment in U. purpurea traps and determined when traps begin to function and what they trap in natural habitats. In the Everglades of south Florida, plants invest an average of 26% of their biomass in bladders, although bladder number varies among sites and over time. Leaves begin trapping as they mature, and on leaves one whorl older than the most recently matured leaves, almost 100% of bladders have allochthonous material. Despite the substantial investment in their biomass, bladders capture few aquatic microinvertebrates. Almost all mature bladders, however, have living communities of algae, zooplankton, and associated debris. These results support the hypotheses that the important association in U. purpurea bladders is a mutualism rather than a predator-prey interaction and that the major benefit to the plants from bladders is derived from this community.     

Nitrogen uptake from prey and substrate as affected by prey capture level and plant reproductive status in four carnivorous plant species

Uptake of nitrogen from prey and substrate and partitioning of prey-derived nitrogen were studied in the carnivorous plant species Pinguicula alpina, P. villosa, P. vulgaris and Drosera rotundifolia in a subarctic environment. Efficiency in nitrogen uptake from prey was evaluated by tracing ¹⁵N from ¹⁵N-enriched Drosophila flies fed to the plants. The in situ uptake efficiency differed somewhat between species and ranged from 29 to 41% of prey N. This efficiency was not affected by different feeding levels or plant reproductive status (flowering or non-flowering). A test of the amount of N absorbed from prey caught on flower stalks of Pinguicula villosa and P. vulgaris showed that both species took up little of what was available in prey (2.5% or less). The uptake efficiency found in greenhouse grown plants was higher than in plants in situ (40–50% vs. 30–40% respectively). This could probably best be explained by the absence of rain and a higher temperature in the greenhouse. The prey-derived ¹⁵N was traced to reproductive organs and winter buds. Non-flowering individuals allocated 58–97% of the N derived from prey to their winter buds. Flowering individuals allocated 17–43% of the N income from prey to reproduction, while 34–71% were allocated to buds. Root uptake of nitrogen was stimulated by increased prey capture. This increase in uptake of nitrogen from the substrate was larger than the potential direct uptake of nitrogen from captured prey.     

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.     

Enzyme production in the traps of aquatic <Emphasis Type="Italic">Utricularia</Emphasis> species

We studied the influence of habitat and increased mineral phosphorus and nitrogen loading on the extracellular activity of five selected hydrolases and pH in the trap fluid of the aquatic carnivorous plants, Utricularia vulgaris, U. australis, and U. foliosa (Lentibulariaceae). Enzyme activities in the trap fluid were determined using fluorometry. Phosphatase exhibited the highest activities in the traps of the European species as well as field-grown tropical U. foliosa. Trap enzyme production appeared to be uninfluenced by elevated dissolved mineral N or P concentrations both in the trap and ambient environment and thus, it seems to be constitutive. Enzyme activity in the trap fluid was determined by species and environmental conditions and varied significantly among sites within a single species. Trap fluid pH was between 4.2–5.1 in U. vulgaris and U. australis but between 5.7–7.3 in U. foliosa and seems to be regulated by the traps.     

The roles of visual and proprioceptive information during motor program choice in frogs

Previous studies have shown that leopard frogs, Rana pipiens, use tongue prehension to capture small prey and jaw prehension to capture large prey. After hypoglossal nerve transection, the frogs fail to open their mouths when attempting to feed on small prey, but open their mouths and capture large prey. Here, we investigate how visual information about the prey and proprioceptive information from the tongue interact to influence the motor program choice. Using pieces of earthworm of various sizes, we found that Rana exhibits two different behavior patterns based on prey size. The frogs captured the 1.5-cm prey using tongue prehension, whereas 2.0-cm and larger prey were captured using jaw prehension. After hypoglossal transection, the frogs never opened their mouths when they tried to feed on 1.5-cm prey. When feeding on 3.0-cm and larger prey after transection, they always opened their mouths and captured the prey using jaw prehension. When offered 2.0-cm prey, they alternated randomly between opening and not opening the mouth. Therefore, deafferentation changed the pattern of motor program choice at the behavioral border. This implies that afferents from the tongue interact with visual input to influence motor program choice.     

Capture efficiency and trophic adaptations of a specialist and generalist predator: A comparison

Specialist true predators are expected to exhibit higher capture efficiencies for the capture of larger and dangerous prey than generalist predators due to their possession of specialized morphological and behavioral adaptations. We used an araneophagous spider (Lampona murina) and a generalist spider (Drassodes lapidosus) as phylogenetically related model species and investigated their realized and fundamental trophic niches and their efficacy with respect to prey capture and prey handling. The trophic niche of both species confirmed that Lampona had a narrow trophic niche with a predominance of spider prey (including conspecifics), while the niche of Drassodes was wide, without any preference. DNA analysis of the gut contents of Lampona spiders collected in the field revealed that spiders form a significant part of its natural diet. Lampona captured significantly larger prey than itself and the prey captured by Drassodes. As concerns hunting strategy, Lampona grasped the prey with two pairs of legs possessing scopulae, whereas Drassodes immobilized prey with silk. Lampona possess forelegs equipped with scopulae and a thicker cuticle similar to other nonrelated araneophagous spiders. Lampona fed for a longer time and extracted more nutrients than Drassodes. We show that specialized behavioral and morphological adaptations altogether increase the hunting efficiency of specialists when compared to generalists.     

Effect of hunger on the allocation of time among pea plants by the larvae of an aphidophagous hover fly,Eupeodes corollae [Dipt: Syrphidae]

We observed the movement of predatory larvae of the syrphid flyEupeodes corollae (F.) (formerlyMetasyrphus corollae) among small pea plants with and without aphids. Starved larvae spent longer time than well-fed larvae on similar plants and both groups of larvae stayed longer on plants with aphids than on plants without aphids. On plants with aphids, larvae which failed to capture prey left the plant sooner than those which captured aphids. The capture of at least one aphid on a plant increased the persistence of syrphid larvae. The average rate of energy gain was higher for well-fed larvae than for starved larvae because starved larvac stayed on plants even when their rate of return was lower. When larvae that had captured aphids left plants, their rate of energy gain, tended to be lower than at any time following capture of the 2^nd, aphid. The 1^st aphid was captured in less time than similar larvae spent on plants without aphids. Time between captures of aphids by well-fed larvae was less than the time such larvae spent on plants without aphids. Among starved larvae, the intercatch intervals were similar to the time on plants without aphids. We discuss the significance of these results relative to current predator foraging theory and the efficiency ofE. corollae as a biological control agent.      

Rapid turnover of traps in Utricularia vulgaris L.

Summary Utricularia vulgaris growing at Wicken Fen, England, showed rapid turnover of the trapping apparatus. New groups of leaves, each bearing many traps, were produced at a rate of 1.4–2.8 groups per day from April to September, 1987. Old leaves decayed at a comparable rate, so that individual leaves survived for less than 50 days. In July, trapping efficiency of individual bladders was greatest between 1 and 6 days of age and then declined rapidly. Very few traps more than 19 days old could capture prey and most were lost from the leaves within 32 days. The lifespan of traps was closely related to their size and position on the leaves. Because of the rapidity of changes in trap condition with age, trap age is a vital consideration in any studies of the functional ecology of U. vulgaris     

Ants provide nutritional and defensive benefits to the carnivorous plant Sarracenia minor

Ants can have important, but sometimes unexpected, effects on the plants they associate with. For carnivorous plants, associating with ants may provide defensive benefits in addition to nutritional ones. We examined the effects of increased ant visitation and exclusion of insect prey from pitchers of the hooded pitcher plant Sarracenia minor, which has been hypothesized to be an ant specialist. Visitation by ants was increased by placing PVC pipes in the ground immediately adjacent to 16 of 32 pitcher plants, which created nesting/refuge sites. Insects were excluded from all pitchers of 16 of the plants by occluding the pitchers with cotton. Treatments were applied in a 2 × 2 factorial design in order to isolate the hypothesized defensive benefits from nutritional ones. We recorded visitation by ants, the mean number of ants captured, foliar nitrogen content, plant growth and size, and levels of herbivory by the pitcher plant mining moth Exyra semicrocea. Changes in ant visitation and prey capture significantly affected nitrogen content, plant height, and the number of pitchers per plant. Increased ant visitation independent of prey capture reduced herbivory and pitcher mortality, and increased the number of pitchers per plant. Results from this study show that the hooded pitcher plant derives a double benefit from attracting potential prey that are also capable of providing defense against herbivory.     

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     

The “ricochet effect” and prey capture in colonial spiders

Summary Increased prey capture efficiency in colonial spiders is a consequence of the ricochet effect, as prey are captured after they bounce off several webs in succession. In this study, the prey capture of three species of colonial spiders in the genus Metepeira from Mexico are compared. These species, from different habitats, show varying levels of social organization (group size and withingroup spacing) that affect prey capture from ricochets. Metepeira sp. a (a presumed new species tentatively named atascadero) from desert grassland habitats, occur solitarily or in small groups, and gain little from prey ricochets: prey capture rates are low and variance in prey captured/spider is high. M. spinipes, from mesic agricultural sites, occur in groups of 10–150, and show a ricochet effect resulting in more and larger prey, and reduced variance in capture rate. M. incrassata, from tropical rainforest/agricultural sites, occur in large colonies of hundreds to thousands of individuals, and show a similar ricochet effect. The ricochet effect does not influence taxonomic composition of prey in either M. atascadero or M. spinipes, but does in tropical M. incrassata. This result, however, is primarily due to the capacity of certain taxa (eg., Lepidoptera), more common in the tropics, to escape more easily from spider webs. A comparison of prey capture efficiency of colonial M. incrassata with that of solitary M. atascadero shows that the ricochet effect provides an increase in efficiency across all size classes of prey.     

Foraging behavior of the communal spider,Philoponella republicana (Araneae: Uloboridae)

The communal orb-weaving spider, Philoponella republicana,was observed in the subtropical moist forest of Southeast Peru. These spiders live in colonies of conspecifics whose individual orbs are connected by silk. The wrapping of a prey prior to feeding is a large component of the prey capture process because P. republicanahas no venom with which to kill an insect. Wrapping time was the only aspect of prey capture that was strongly correlated with the size of the insect captured. Occasionally we observed several individuals working together to wrap a prey item. These joint efforts were more frequent on prey larger than the capturing spider. Although group captures accounted for only 5.5% of captures, they represented 14.7% of the biomass obtained. A comparison of the relationship between wrapping time and prey size for solitary and group efforts suggested that, by working together, the spiders reduced their total handling time. In most cases only one spider fed on the captured prey.     

Sticky plant captures prey for symbiotic bug: is this digestive mutualism?

Many plants capture and kill insects but, until relatively recently, only carnivorous plants with digestive enzymes were known to gain directly from the nutrients of those insects. Recent studies show that some carnivorous plants lack digestive enzymes and have evolved digestive mutualisms with symbiotic insects that digest their prey for them. Rhododendron macrosepalum, a plant with sticky leaves that captures insects, has an association with symbiotic Mirid bugs that consume the insects captured. Here, we determine what the nature of the relationship is between Mirid and plant. We find that R. macrosepalum has no digestive enzymes of its own but that it does not seem to have the ability to absorb hemipteran faeces through its leaf cuticle. Naturally occurring levels of ¹⁵N and ¹⁴N were used to determine that R. macrosepalum gains no nitrogen through its association with the Mirid bugs and that it obtains all of its nitrogen from the soil. The Mirids, on the other hand, seem to obtain nitrogen from insects captured by the plant, as well as from plant tissues. The relationship between plant and Mirid is not a digestive mutualism but more likely an antagonistic relationship. This study adds to our understanding of how digestive mutualisms evolve and shows that insect capture alone, or in combination with a symbiotic insect relationship does not necessarily make a plant ‘carnivorous’.     

Crustaceans and rotifers in the predatory feeding of Utricularia

The contents of bladders in the predatory plant Utricularia from three waterbodies were studied. The composition and number of prey depended on the development of zooplankton and phytophilous fauna in the environment. The probability of getting the prey into the bladder was determined by the specificity of the prey’s behavior and size. The most numerous prey were predatory Copepoda and nonpredatory Cladocera, which use the bladderwort as a substrate. The shares of other cladocerans in the bladders were inconsiderable when there were high densities of these species in the waterbody. No negative impact of the bladderwort on the rotifer abundance was revealed.