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0 Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA
Received for publication September 21, 1999. Accepted for publication March 28, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: bladderworts • Lentibulariaceae • periphyton • plant carnivory • plant nutrients • trapping rates • Utricularia • Utricularia purpurea
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The complexity of these adaptations encourages hypotheses about function on the basis of structures. A critical evaluation of function, however, requires quantification of the numbers and types of prey captured in natural environments, as well analysis of the prey's contribution to the plant's nutrient budget. The number of prey captured by Drosera and Pinguicula species under natural conditions has been reported (Karlsson et al., 1987
; Thum, 1988
; Zamora, 1995
), but comparable data are lacking for Utricularia, the most species-rich genus of carnivorous plants.
Carnivorous plants are defined as plants that (1) absorb nutrients from dead animals next to their surfaces and thus obtain increased fitness and (2) have some morphological, physiological, or behavioral feature to attract, capture, and/or digest prey (Givnish, 1989
; Juniper, Robins, and Joel, 1989
). The carnivorous habit has arisen independently at least six times (Albert, Williams, and Chase, 1992
). Forty-two percentage of the species classified as carnivorous occur in Utricularia (Juniper, Robins, and Joel, 1989
), and Utricularia has the widest geographical distribution of any carnivorous genus, with species found worldwide from the tropics to arctic regions (Taylor, 1989
). Habit varies in the genus, including free-floating and affixed aquatics (
27%), lithophytes and epiphytes (13%), and terrestrial species that grow in seasonally wet or moist environments (60%) (Taylor, 1989
). Members of the genus are rootless and have small bladders that can trap allochthonous material. Each bladder has a door that flexes inward. Internal glands in the bladders pump water out, so that "set" traps are under tension with the door lodged against a lip of cells. Mechanical stimulation causes the bladder door to flex open, allowing water and material to be sucked into the bladder.
A cost-benefit model for the evolution of carnivory in plants predicts that carnivory will evolve in sunny, moist, nutrient-poor environments (Givnish, 1989
). This description typifies Utricularia habitats in the Everglades of south Florida. Several recent studies of Utricularia have examined the costs of carnivory, measuring investment in carnivory as investment in bladders, quantified as bladder number, size, and/or biomass (Friday, 1991, 1992
; Knight and Frost, 1991
; Knight, 1992
). Bladders are known to trap small aquatic animal prey, such as rotifers, copepods, ostracods, cladocerans, and chironomids (Friday, 1989
; Knight and Frost, 1991
), and they absorb N and P from these prey (Friday and Quarmby, 1994
). Thus, in Utricularia species the benefit for investing in bladders is assumed to be nutrients derived from trapping and digesting aquatic organisms. Studies of Utricularia that quantify trapping rates and prey in natural environments, however, are limited. This study quantifies investment in bladders and natural trapping rates in Utricularia purpurea growing in the Everglades of south Florida. In order to understand plasticity in investment in carnivory, it also examines morphological variation in this species.
Terminology
Although the morphological homology of the trap-bearing structures in U. purpurea has been debated (Rutishauser and Sattler, 1989
; Taylor, 1989
), here they are referred to as leaves. These leaves occur in whorls along the stem, are subdivided into photosynthetic filaments (the "capillary filaments" of Taylor, 1989
) and bear bladders at their tips (Fig. 1). The time between the initiation of successive leaf whorls is referred to as a plastochron, a developmentally defined unit of time (Erickson and Michelini, 1957; Larson and Isebrands, 1971).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). This study was conducted in south Florida, where U. purpurea occurs as isolated individuals or as an integral part of a floating periphyton mat. All of the data reported in this study were collected on plants that were free-floating, rather than those in the periphyton mat. These plants grow throughout the water column from the surface to the benthic muck. Plants were collected from Shark River Slough in Everglades National Park at three sites (sites A, B, and C) that are part of a long-term experimental study on the effects of phosphorus additions on the Everglades ecosystem (Childers et al., in press). The three sites are located in long-hydroperiod marshes dominated by Eleocharis cellulosa, Panicum hemitomon, Nymphaea odorata, Nymphoides aquatica, Sagittaria lancifolia, and the U. purpurea–periphyton mat. Two other species of Utricularia, U. foliosa L. and U. gibba L., are also found at these sites. Water column depth in the study area ranges from 0.25 to 1 m. Growth rates were measured on plants in flume channels prior to P dosing. Plants for morphological studies and bladder-content analyses were collected adjacent to the experimental flumes.
Methods
Morphological measurements and biomass allocation
Plants for morphological measurements, bladder content data, and biomass allocation studies were collected during the wet season, which occurs from May to October in south Florida. Plants from site A were collected on 23 October and 28 October 1998, from site B on 13 July and 22 July 1998, and from site C on 22 July 1998. Plants from sites B and C were also processed for biomass allocation data; the material for biomass allocation from site A was lost, so an additional collection from site A was made during the dry season on 21 March 1999. Plastic collecting bags were submerged and filled with water, and plants were then moved gently from the water column into the bags, so they were not exposed to air during collection. Plants were brought back to the laboratory, refrigerated, and processed within 4 d of collection.
Similar morphological data were taken on all plants. Traits measured were internode length and diameter, leaf number per whorl, leaf length, number of primary photosynthetic whorls per leaf, and bladder number. For morphological data a single leaf was measured per node from the two most recently matured nodes per plant. For biomass allocation studies, three leaves from the most recently matured node were measured.
Since each whorl of leaves is a developmental unit and the plant then consists of units that are produced at the apex and sloughed off at the base, I analyzed biomass investment in trapping on the basis of investment in a nodal unit, equal to the whorl of leaves and the subtending internode. The first mature nodal unit of plants was removed. Internode length and leaf length were measured with a ruler to the nearest millimetre (Fig. 1). Internode diameter was measured with electronic digital calipers (MAX-CAL, Fowler Co., Inc., Newton, Massachusetts, USA). Leaf number per node and number of whorls of primary photosynthetic filaments per leaf were counted on three leaves at the node. On each of these three leaves, bladders were counted, removed, and dried in an 80°C oven to constant mass. Each leaf minus its bladders was dried separately, as was the subtending internode. These parts were weighed on a microbalance (Mettler Toledo AB54, Mettler Toledo Inc., Westerville, Ohio, USA). Percentage investment in bladders and support structures was calculated from these data. Biomasses of leaves and bladders per leaf for a whorl were averaged and multiplied by the number of leaves per whorl to obtain biomass per leaf whorl. This was added to the dry mass of the subtending internode to determine biomass per nodal unit, and relative biomass allocations to bladders, leaves, and stem (internode) were calculated.
Growth-rate determinations
Growth rates were determined for free-floating plants; initial measurements indicated that plants in mats had much slower growth rates than those reported here. I marked 12–15 plants at four permanent quadrats at each flume site. The free end of a string tied to a styrofoam packing peanut was tied above the most recently matured node of an individual U. purpurea plant. This node was defined based on internode length, leaf length, amount of leaf reflexion, and bladder expansion. The floating styrofoam peanut enabled me to relocate marked plants after several weeks of growth in situ. Plants grew for 4–6 wk, and then the number of mature nodes above the marked node was counted. New plants were marked and followed for every sampling date. Growth was measured every 2–4 mo from October 1997 to November 1998.
Leaf development and bladder contents
Plants used for morphological measurements from sites A, B, and C were analyzed for bladder contents. Leaf whorls were numbered based on relative developmental stage. The most recently matured leaf whorl, as determined by morphological criteria (see description above), was designated as 0. Older leaf whorls were numbered positively, and younger whorls numbered negatively from the 0 whorl. For developmental and bladder content analysis, a single leaf was sampled from each node beginning with node 1 and sampling toward the apex to the -3 to -4 whorl. Leaf length and length of the subtending internode were measured for each whorl, while leaf number and the number of whorls of leaf subdivisions were counted. Bladder number was also counted for all but the youngest leaves. Twenty bladders from each leaf were examined under a Leitz Dialux 20 compound light microscope. Bladders were analyzed by focusing down through the bladder and recording presence or absence of allochthonous material. The bladder walls are a single cell thick and relatively transparent, as illustrated in Figs. 7 and 9, which were taken through bladder walls, and as can be seen in Figs. 5, 6, and 8, which show dark contents through transparent bladder walls. Internal and external walls of bladders were identified by the different types of glands present on the inside and outside of bladders (Juniper, Robins, and Joel, 1989
; Taylor, 1989
). The types of multicellular invertebrates present per bladder were quantified for samples from sites A and C.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.5 m in total length in Shark River Slough. The plants produce whorls of leaves as they grow at the tip and rot at the base (Fig. 1). Every second node can produce a branch bud and an inflorescence bud. Inflorescences grow above the water and produce one or two flowers (Fig. 1; for additional details of development, see Rutishauser and Sattler, 1989
). Internodes of plants used for the bladder content study averaged 29 mm in length and 1.1 mm in diameter (Table 1). A typical plant in Shark River Slough tends to produce five leaves per whorl (Table 1; 63% of nodes had five leaves, 34% had six leaves, and 3% had four leaves). Each leaf produced whorls of four or fewer photosynthetic filaments, which could themselves be subdivided (Figs. 1B, 3). Most Shark River Slough plants had five of these whorls per leaf (Table 1; 65% had five whorls, 27% had four whorls, and 8% had six whorls). Individual leaf length averaged 39 mm (Table 1). Bladders of U. purpurea are borne at the tips of all orders of leaf filaments.
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Neither internode diameter nor leaf length varied significantly among sites, and plants had similar numbers of leaves per nodal whorl and similar numbers of whorls of photosynthetic filaments per leaf (Table 1). Plants did differ significantly among sites with respect to internode length and the number of bladders. In general, plants at sites A and B tended to resemble each other and to differ from plants at site C. Plants at site C produced more bladders per leaf and node than plants at the other two sites (Table 1).
Plants at site A that were collected in the wet season and the dry season were not significantly different in leaf length (40 ± 9 mm in October 1998, vs. 44 ± 8 mm in March 1999) but did differ significantly in bladder number (55 ± 31 bladders per leaf in October 1999 vs. 87 ± 34 bladders per leaf in March 1999).
Investment in bladders
Individual leaves in a whorl produced an average of 74 bladders per leaf (Table 2). Given an average of five leaves per whorl, each whorl was estimated to have 370 bladders.
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Leaf and internode dry masses did not vary significantly among sites, but bladder dry mass per leaf and individual bladder biomass did (Table 2). Plants at site C produced significantly more bladders per leaf than those at site B during the wet season. The dry-season plants from site A were similar to wet-season site C plants in their investment in bladders and differed significantly from wet-season site B plants (Table 2). Bladder number was negatively correlated with individual bladder biomass, so that plants with more bladders tended to have lighter bladders, although the correlation was not strong (R2 = 0.09, P = 0.0052, N = 86).
Trapping efficiency
Bladders on very young leaves of U. purpurea did not have allochthonous material inside them (Fig. 2). These bladders, which were small, anthocyanic, and had bladder doors that were not fully developed (Figs. 4, 5), were on leaf whorls 2–4 plastochrons younger than the first whorl of mature leaves. The youngest leaf with bladder contents was two plastochrons younger than the first mature leaves (Fig. 2). From this leaf whorl the number of occupied bladders increased exponentially with leaf age until bladders in the leaf one plastochron older than the first mature leaf were almost 100% occupied (Figs. 2, 4–9). The amount of material in each bladder also increased with increasing leaf age (Figs. 5, 6, 8). Occupied bladders contained a mixture of living and detrital material. All bladders with contents had some type of photosynthetic tenants, primarily blue–green algae, diatoms, green algae, and/or photosynthetic protists (Figs. 7, 9). Many bladders also had living rotifers. A variety of larger organisms, such as copepods, ostracods, and cladocerans, were found more rarely. At sites A and C, 880 of 1400 bladders examined from different-aged leaves had contents. Of these, 20.2% had living rotifers, 5.1% had cladocerans, 1.3% had chironomids, 0.6% had ostracods, 0.5% had copepods, and 0.9% had other multicellular invertebrates. The rotifers in these samples were swimming around in the bladders, whereas the larger invertebrates were usually dead.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Are the trapping rates and trap contents reported here unique to Utricularia species in the Everglades? Whether the trapping rates and bladder communities found in the Everglades are representative of Utricularia species in other environments or of terrestrial species of Utricularia needs further study. Previous researchers, however, have reported the presence of living algae and ciliates in bladders of Utricularia species (Botta, 1976
; Mosto, 1979
; Juniper, Robins, and Joel, 1989
).
Investment in bladders
Species of Utricularia invest a large proportion of their biomass in bladders. While U. purpurea invested approximately one-quarter of its biomass in bladders, U. macrorhiza growing in lakes in northern Wisconsin invested 38–48% (Knight and Frost, 1991
), and U. vulgaris growing in disused clay pits in Cambridgeshire, UK, invested 50% biomass in bladders (Friday, 1992
). I have also found an average of 29% investment in bladders from plants collected from a pond on the Florida International University campus (J. H. Richards, Florida International University, unpublished data). This percentage investment is similar to what terrestrial plants in moderately low-nutrient environments invest in root biomass (Tilman, 1988
)
The percentage of biomass invested in bladders is plastic and can vary with environmental conditions. In all studies that have considered the question, the largest variation in bladder number is between sites. In U. purpurea, as in other species of Utricularia (Knight and Frost, 1991
; Friday, 1992
), variation among leaves on a plant sampled at a single time is usually minor. Variation among plants at a single site is more complex and probably represents the degree of habitat heterogeneity displayed at a particular site. Whereas Knight and Frost (1991)
found minor variation in bladder number among plants in a lake, Friday (1992)
found large variation among plants at a single site. In the data reported here U. purpurea bladder number varied among plants both within and between sites.
Benefits from bladders
The conventional view of bladderwort carnivory is that these plants benefit from nutrients derived by digestion of trapped microinvertebrates (Friday, 1989
; Juniper, Robins, and Joel, 1989
; Knight and Frost, 1991
; Ulanowicz, 1995
). In south Florida bladders of U. purpurea on plants in natural habitats trap very low percentages of these microinvertebrates, except for rotifers, and the rotifers observed inside bladders were alive. Similarly low invertebrate trapping rates were found for U. foliosa in the Everglades (Bern, 1997
; A. Bern, J. H. Richards, and B. Fry, Florida International University, unpublished data). Calculations of how much nitrogen and phosphorus plants could derive from these trapping rates, if the only benefit is from digestion of microinvertebrates, suggest that the return on a 25–50% investment in bladders is <1% of the plant N and P (Bern, 1997
; A. Bern, J. H. Richards, and B. Fry, Florida International University, unpublished data).
Although plants had few bladders with dead microinvertebrates, almost 100% of mature U. purpurea bladders supported living communities of microorganisms and associated detritus. These communities were derived from the external environment, as very young bladders lacked them, and the number of inhabited bladders, as well as inhabitant density and diversity, increased over time. The ubiquitous presence of these communities supports the hypothesis that Utricularia plants derive more benefit from by-products of this community than from carnivory, i.e., that the important association in Utricularia bladders is a mutualism rather than a predator–prey interaction. The bladders in Utricularia, therefore, may provide benefit through a detrital food web rather than a carnivorous interaction.
This view is a simplification of Ulanowicz's (1995)
positive feedback model for Utricularia carnivory, in which the benefit funneled to Utricularia from periphyton comes through ingestion of animal grazers. In the model this benefit allows Utricularia carnivory to be advantageous in oligotrophic environments (Ulanowicz, 1995
). I suggest that the carnivory part of the periphyton-Utricularia association may be incidental to the direct interaction.
In the summer plants expand a leaf whorl about every 5 d, and they begin trapping in -2 leaves, so they become 100% occupied after 15 d. Free-floating plants generally have at least three whorls of mature leaves before they become completely covered with algae and appear to be senescent. Thus, after bladders are fully occupied, they may support these communities for another 15 d. After a bladder has been tripped, it can reset itself (Lloyd, 1933; Sydenham and Findlay, 1975
; Juniper, Robins, and Joel, 1989
). Whether communities are constantly augmented by material from new trapping events or whether bladder contents increase through reproduction inside the bladders is unknown.
Although the importance of the Utricularia-periphyton interaction has been recognized (Friday, 1989
; Ulanowicz, 1995
), the possible importance of the direct interaction has been overshadowed by concepts derived from models of carnivory. The interpretation of the benefit of carnivory presented here provides an explanation for Knight and Frost's (1989) otherwise anomalous result that U. macrorhiza plants in more nutrient-rich environments invested more in bladders. If the benefit of the bladders depends on the productivity of the microcommunity and that productivity increases with increased nutrients, plants would be predicted to produce more bladders under increased nutrient levels.
Currency of the "carnivorous" interaction in aquatic plants
Utricularia is the most diverse genus of carnivorous plants, accounting for a little less than half of all carnivorous species (Juniper, Robins, and Joel, 1989
), but the genus is unusual in having submerged aquatic species. The interaction in an aquatic species, such as Utricularia purpurea, may differ substantially from carnivory in terrestrial species of Utricularia or in species of other carnivorous plants. If the community interaction inside bladders provides the benefit for investment of biomass in bladders in U. purpurea, the currency in the interaction may not be solely mineral nutrients. For example, carbon dioxide concentrations potentially limit photosynthesis in freshwater aquatic plants (Falkowski and Raven, 1997
). Carbon dioxide derived from respiratory processes in the bladders could be a significant benefit in the slow-moving aquatic environments typical for some Utricularia species, similar to the benefit obtained from CO2 uptake through the roots in isoetids (Raven et al., 1988
). This benefit could help to explain Utricularia's success in the aquatic environment. The endangered Aldrovanda vesiculosa (Droseraceae), a miniature aquatic version of Dionea, is the only other free-floating aquatic carnivorous species. A recent study found that the most important condition for rapid growth in A. vesiculosa was a high-CO2 concentration in the water (Adamec, 1997
).
In addition to the possible benefit of CO2 supplements, bladders in aquatic species could also be advantageous because they provide a contained microenvironment to enhance breakdown of organic matter, prevent diffusion of the breakdown products, and provide Utricularia plants with a monopoly on released nutrients.
Bladder mechanics and community dynamics
The absence of microinvertebrates from many bladders coupled with the presence of some type of material in all of the bladders means either that trapping is very inefficient or that bladders do not require animals to trip them under natural conditions. Alternative possibilities that need to be investigated are (1) debris carried by currents or the current itself is sufficient to cause opening or (2) endogenous factors, such as internal tension, can cause bladder opening. Lloyd (1933) reports that movement of U. purpurea plants in water often releases the traps.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Albert, V. A., S. E. Williams, and M. W. Chase. 1992 Carnivorous plants: phylogeny and structural evolution. Science 257: 1491–1495
Bern, A. L. 1997 Studies on nitrogen and phosphorus uptake by the carnivorous bladderwort, Utricularia foliosa, in south Florida wetlands. Master's thesis, Florida International University, Miami, Florida, USA
Botta, S. M. 1976 Sobre las trampas y las victimas o presas de algunas especies argentinas del genero Utricularia. Darwiniana 20: 127–154
Childers, D. L., R. D. Jones, J. Trexler, C. Buzzelli, S. Dailey, A. Edwards, E. Gaiser, K. Jayachandaran, A. Kenne, D. Lee, J. Meeder, M. K. Nair, J. H. K. Pechmann, A. Renshaw, J. Richards, M. Rugge, L. J. Scinto, P. Sterling, and W. Van Gelder. In press. Quantifying the effects of low-level phosphorus enrichment on unenriched Everglades wetlands with in situ flumes and phosphorus dosing. In K. Porter and J. Porter [eds.], The Everglades hydroscape. St. Lucie Press, Delray Beach, Florida, USA
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———. 1991 The size and shape of traps of Utricularia vulgaris L. Functional Ecology 5: 602–607[CrossRef][ISI]
———. 1992 Measuring investment in carnivory: seasonal and individual variation in trap number and biomass in Utricularia vulgaris L. New Phytologist 121: 439–445[CrossRef][ISI]
———, and C. Quarmby. 1994 Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L. New Phytologist 126: 273–281[CrossRef][ISI]
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Juniper, B. E., R. J. Robins, and D. M. Joel. 1989 The carnivorous plants. Academic Press, London, UK
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———, and T. M. Frost. 1991 Bladder control in Utricularia macrorhiza: lake-specific variation in plant investment in carnivory. Ecology 72: 728–734[CrossRef][ISI]
Larson, P. R., and J. G. Isebrands. The plastochron index as applied to developmental studies of cottonwood. Canadian Journal of Forest Research 1: 1–11
Lloyd, F. E. 1933 The structure and behavior of Utricularia purpurea. Canadian Journal of Research 8: 234–252
Mosto, P. 1979 Algas en trampas de Utricularia oligosperma St. Hill. Boletin. Sociedad Argentina de Botanica 18: 89–100
Raven, J. A., L. L. Handley, J. J. MacFarlane, S. McInroy, L. McKenzie, J. H. Richards, and G. Samuelsson. 1988 The role of CO2 uptake by roots and CAM in acquisition of inorganic C by plants of the isoetid lifeform: a review, with new data on Eriocaulon decangulare L. New Phytologist 108: 125–148[CrossRef][ISI]
Rutishauser, R., and R. Sattler. 1989 Complementarity and heuristic value of contrasting models in structural botany. III. Case study on shoot-like "leaves" and leaf-like "shoots" in Utricularia macrorhiza and U. purpurea (Lentibulariaceae). Botanische Jahrbücher Systematic für Pflanzengeschichte und Pflanzengeographie 111: 121–137
Sydenham, P. H., and G. P. Findlay. 1975 Transport of solutes and water by resetting bladders of Utricularia. Australian Journal of Plant Physiology 2: 225–351
Taylor, P. 1989 The genus Utricularia. Kew Bulletin Additional Series XIV. HMSO, London, UK
Thum, M. 1988 The significance of carnivory for the fitness of Drosera in its natural habitat. 2. The amount of captured prey and its effect on Drosera intermedia and Drosera rotundifolia. Oecologia 81: 401–411[ISI]
Tilman, D. 1988 Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, New Jersey, USA
Turner, A. M., J. C. Trexler, C. F. Jordan, S. J. Slack, P. Geddes, J. H. Chick, and W. F. Loftus. 1999 Targeting ecosystem features for conservation: standing crops in the Florida Everglades. Conservation Biology 13: 898–911[CrossRef][ISI]
Ulanowicz, R. E. 1995 Utricularia's secret: the advantage of positive feedback in oligotrophic environments. Ecological Modelling 79: 49–57[CrossRef]
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80 for each point. Error bars = ±1 SD