Trap closure and prey retention in Venus flytrap (Dionaea muscipula) temporarily reduces photosynthesis and stimulates respiration

Background and Aims

The carnivorous plant Venus flytrap (Dionaea muscipula) produces a rosette of leaves: each leaf is divided into a lower part called the lamina and an upper part, the trap, with sensory trigger hairs on the adaxial surface. The trap catches prey by very rapid closure, within a fraction of a second of the trigger hairs being touched twice. Generation of action potentials plays an important role in closure. Because electrical signals are involved in reduction of the photosynthetic rate in different plant species, we hypothesized that trap closure and subsequent movement of prey in the trap will result in transient downregulation of photosynthesis, thus representing the energetic costs of carnivory associated with an active trapping mechanism, which has not been previously described.

Methods

Traps were enclosed in a gas exchange cuvette and the trigger hairs irritated with thin wire, thus simulating insect capture and retention. Respiration rate was measured in darkness (R_D). In the light, net photosynthetic rate (A_N), stomatal conductance (g_s) and intercellular CO₂ concentration (c_i) were measured, combined with chlorophyll fluorescence imaging. Responses were monitored in the lamina and trap separately.

Key Results

Irritation of trigger hairs resulted in decreased A_N and increased R_D, not only immediately after trap closure but also during the subsequent period when prey retention was simulated in the closed trap. Stomatal conductance remained stable, indicating no stomatal limitation of A_N, so c_i increased. At the same time, the effective quantum yield of photosystem II (Φ_PSII) decreased transiently. The response was confined mainly to the digestive zone of the trap and was not observed in the lamina. Stopping mechanical irritation resulted in recovery of A_N, R_D and Φ_PSII.

Conclusions

We put forward the first experimental evidence for energetic demands and carbon costs during insect trapping and retention in carnivorous plants, providing a new insight into the cost/benefit model of carnivory.     

Feeding on prey increases photosynthetic efficiency in the carnivorous sundew Drosera capensis

Backround and Aims

It has been suggested that the rate of net photosynthesis (A_N) of carnivorous plants increases in response to prey capture and nutrient uptake; however, data confirming the benefit from carnivory in terms of increased A_N are scarce and unclear. The principal aim of our study was to investigate the photosynthetic benefit from prey capture in the carnivorous sundew Drosera capensis.

Methods

Prey attraction experiments were performed, with measurements and visualization of enzyme activities, elemental analysis and pigment quantification together with simultaneous measurements of gas exchange and chlorophyll a fluorescence in D. capensis in response to feeding with fruit flies (Drosophila melanogaster).

Key Results

Red coloration of tentacles did not act as a signal to attract fruit flies onto the traps. Phosphatase, phophodiesterase and protease activities were induced 24 h after prey capture. These activities are consistent with the depletion of phosphorus and nitrogen from digested prey and a significant increase in their content in leaf tissue after 10 weeks. Mechanical stimulation of tentacle glands alone was not sufficient to induce proteolytic activity. Activities of β-D-glucosidases and N-acetyl-β-D-glucosaminidases in the tentacle mucilage were not detected. The uptake of phosphorus from prey was more efficient than that of nitrogen and caused the foliar N:P ratio to decrease; the contents of other elements (K, Ca, Mg) decreased slightly in fed plants. Increased foliar N and P contents resulted in a significant increase in the aboveground plant biomass, the number of leaves and chlorophyll content as well as A_N, maximum quantum yield (F_v/F_m) and effective photochemical quantum yield of photosystem II (Φ_PSII).

Conclusions

According to the stoichiometric relationships among different nutrients, the growth of unfed D. capensis plants was P-limited. This P-limitation was markedly alleviated by feeding on fruit flies and resulted in improved plant nutrient status and photosynthetic performance. This study supports the original cost/benefit model proposed by T. Givnish almost 30 years ago and underlines the importance of plant carnivory for increasing phosphorus, and thereby photosynthesis.     

Rearrangement of leaf traits with changing source-sink relationship in blueberry (Vaccinium corymbosum L.) leaves

The source-sink relationship is one of major determinants of plant performance. The influence of reproductive sink demand on light-saturated photosynthesis (P_max), dark respiration (R_D), stomatal conductance (g_s), intrinsic water-use efficiency (WUE_i), contents of soluble sugar (SSC), nitrogen, carbon, and photosynthetic pigments was examined in blueberry (Vaccinium corymbosum L. cv. ‘Brigitta’) during the final stage of rapid fruit growth. Measurements were performed three times per day on developed, sun-exposed leaves of girdled shoots with 0.1, 1, and 10 fruit per leaf (0.1F:L, 1F:L, and 10F:L, respectively) and nongirdled shoots bearing one fruit per leaf (NG). Girdling and lower fruit amount induced lower P_max, g_s, N, and total chlorophyll (Chl) and higher WUE_i, SSC, R_D, Chl a/b ratio and carotenoids-to-chlorophylls ratio (Car/Chl) for the 1F:L and 0.1F:L treatments. The impact of girdling was counterbalanced by 10F:L, with NG and 10F:L having similar values. Variables other than P_max, R_D, g_s, WUE_i, and SSC were unaffected throughout the course of the day. P_max and g_s decreased during the course of the day, but g_s decreased more than P_max in the afternoon, while WUE_i was increasing in almost all treatments. SSC increased from the morning until afternoon, whereas R_D peaked at noon regardless of the treatment. Generally, P_max was closely and negatively correlated to SSC, indicating that sugar-sensing mechanisms played an important role in regulation of blueberry leaf photosynthesis. With respect to treatments, P_max and N content were positively related, while R_D was not associated to substrate availability. The enhanced Car/Chl ratio showed a higher photoprotection under the lower sink demand. Changes in the source-sink relationship in ‘Brigitta’ blueberry led to a rearrangement of physiological and structural leaf traits which allowed adjusting the daily balance between carbon assimilation and absorbed light energy.     

Altitudinal Change in the Photosynthetic Capacity of Tropical Trees: A Case Study from Ecuador and a Pantropical Literature Analysis

In tropical mountains, trees are the dominant life form from sea level to above 4,000-m altitude under highly variable thermal conditions (range of mean annual temperatures: <8 to >28°C). How light-saturated net photosynthesis of tropical trees adapts to variation in temperature, atmospheric CO₂ concentration, and further environmental factors, that change along elevation gradients, is not precisely known. With gas exchange measurements in mature trees, we determined light-saturated net photosynthesis at ambient temperature (T) and [CO₂] (A _sat) of 40 tree species from 21 families in tropical mountain forests at 1000-, 2000-, and 3000-m elevation in southern Ecuador. We tested the hypothesis that stand-level averages of A _sat and leaf dark respiration (R _D) per leaf area remain constant with elevation. Stand-level means of A _sat were 8.8, 11.3, and 7.2?μmol?CO₂?m^?2?s^?1; those of R _D 0.8, 0.6, and 0.7?μmol?CO₂?m^?2?s^?1 at 1000-, 2000-, and 3000-m elevation, respectively, with no significant altitudinal trend. We obtained coefficients of among-species variation in A _sat and R _D of 20–53% (n?=?10–16 tree species per stand). Examining our data in the context of a pan-tropical A _sat data base for mature tropical trees (c. 170 species from 18 sites at variable elevation) revealed that area-based A _sat decreases in tropical mountains by, on average, 1.3?μmol?CO₂?m^?2?s^?1?per?km altitude increase (or by 0.2?μmol?CO₂?m^?2?s^?1 per K temperature decrease). The A _sat decrease occurred despite an increase in leaf mass per area with altitude. Local geological and soil fertility conditions and related foliar N and P concentrations considerably influenced the altitudinal A _sat patterns. We conclude that elevation is an important influencing factor of the photosynthetic activity of tropical trees. Lowered A _sat together with a reduced stand leaf area decrease canopy C gain with elevation in tropical mountains.     

A novel insight into the cost–benefit model for the evolution of botanical carnivory

Background The cost–benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (A_N) in the microsites inhabited by carnivorous plants.Scope This review summarizes results from the classical interpretation of the cost–benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost–benefit model.Conclusions Traps of carnivorous plants have lower A_N than leaves, and the leaves have higher A_N after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, R_D) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.     

Are species photosynthetic characteristics good predictors of seedling post-hurricane demographic patterns and species spatiotemporal distribution in a hurricane impacted wet montane forest?

In situ measurements of leaf level photosynthetic response to light were collected from seedlings of ten tree species from a tropical montane wet forest, the John Crow Mountains, Jamaica. A model-based recursive partitioning ('mob') algorithm was then used to identify species associations based on their fitted photosynthetic response curves. Leaf area dark respiration (R_D) and light saturated maximum photosynthetic (A_max) rates were also used as 'mob' partitioning variables, to identify species associations based on seedling demographic patterns (from June 2007 to May 2010) following a hurricane (Aug. 2007) and the spatiotemporal distribution patterns of stems in 2006 and 2012. R_D and A_max rates ranged from 1.14 to 2.02 μmol (CO₂) m⁻²s⁻¹ and 2.97–5.87 μmol (CO₂) m⁻²s⁻¹, respectively, placing the ten species in the range of intermediate shade tolerance. Several parsimonious species 'mob' groups were formed based on 1) interspecific differences among species response curves, 2) variations in post-hurricane seedling demographic trends and 3) R_D rates and species spatiotemporal distribution patterns at aspects that are more or less exposed to hurricanes. The composition of parsimonious groupings based on photosynthetic curves was not concordant with the groups based on demographic trends but was partially concordant with the R_D - species spatiotemporal distribution groups. Our results indicated that the influence of photosynthetic characteristics on demographic traits and species distributions was not straightforward. Rather, there was a complex pattern of interaction between ecophysiological and demographic traits, which determined species successional status, post-hurricane response and ultimately, species distribution at our study site.     

Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis

Background and Aims

Cost–benefit models predict that carnivory can increase the rate of photosynthesis (A_N) by leaves of carnivorous plants as a result of increased nitrogen absorption from prey. However, the cost of carnivory includes decreased A_N and increased respiration rates (R_D) of trapping organs. The principal aim of the present study was to assess the costs and benefits of carnivory in the pitcher plant Nepenthes talangensis, leaves of which are composed of a lamina and a pitcher trap, in response to feeding with beetle larvae.

Methods

Pitchers of Nepenthes grown at 200 µmol m⁻² s⁻¹ photosynthetically active radiation (PAR) were fed with insect larvae for 2 months, and the effects on the photosynthetic processes were then assessed by simultaneous measurements of gas exchange and chlorophyll fluorescence of laminae and pitchers, which were correlated with nitrogen, carbon and total chlorophyll concentrations.

Key Results

A_N and maximum (F_v/F_m) and effective quantum yield of photosystem II (Φ_PSII) were greater in the fed than unfed laminae but not in the fed compared with unfed pitchers. Respiration rate was not significantly affected in fed compared with unfed plants. The unfed plants had greater non-photochemical quenching (NPQ) of chlorophyll fluorescence. Higher NPQ in unfed lamina did not compensate for their lower Φ_PSII, resulting in lower photochemical quenching (QP) and thus higher excitation pressure on PSII. Biomass and nitrogen and chlorophyll concentration also increased as a result of feeding. The cost of carnivory was shown by lower A_N and Φ_PSII in pitchers than in laminae, but R_D depended on whether it was expressed on a dry weight or a surface area basis. Correlation between nitrogen and A_N in the pitchers was not found. Cost–benefit analysis showed a large beneficial effect on photosynthesis from feeding as light intensity increased from 200 to 1000 µmol m⁻² s⁻¹ PAR after which it did not increase further. All fed plants began to flower.

Conclusion

Feeding pitchers with insect larvae increases A_N of leaf laminae, due to higher nutrient acquisition, with strong correlation with nitrogen concentration, but A_N of pitchers does not increase, despite increased nitrogen concentration in their tissue. Increased A_N improves growth and reproduction and is likely to increase the competitive advantage of carnivorous over non-carnivorous plants in nutrient-poor habitats.Key words: carnivorous plants, chlorophyll fluorescence, Nepenthes talangensis, nitrogen, pitcher plant, photosynthetic rate, photosystem II, respiration rate     

Irradiance acclimation,capture ability,and efficiency in invasive and non-invasive alien plant species

We tested the hypothesis that invasive (IN) species could capture resources more rapidly and efficiently than noninvasive (NIN) species. Two IN alien species, Ageratina adenophora and Chromolaena odorata, and one NIN alien species, Gynura sp. were compared at five irradiances. Photon-saturated photosynthetic rate (P _max), leaf mass (LMA) and nitrogen content (N_A) per unit area, and photosynthetic nitrogen utilization efficiency (PNUE) increased significantly with irradiance. LMA, N_A, and PNUE all contributed to the increased P _max, indicating that both morphological and physiological acclimation were important for the three alien species. Under stronger irradiance, PNUE was improved through changes in N allocation. With the increase of irradiance, the amount of N converted into carboxylation and bioenergetics increased, whereas that allocated to light-harvesting components decreased. The three alien species could adequately acclimate to high irradiance by increasing the ability to utilize and dissipate photon energy and decreasing the efficiency of photon capture. The two IN species survived at 4.5 % irradiance while the NIN species Gynura died, representing their different invasiveness. Ageratina generally exhibited higher respiration rate (R _D) and N_A. However, distinctly higher P _max, PNUE, P _max/R _D, or P _max/LMA were not detected in the two invasive species, nor was lower LMA. Hence the abilities to capture and utilize resources were not always associated with invasiveness of the alien species.     

Dynamics of amino acid redistribution in the carnivorous Venus flytrap (Dionaea muscipula) after digestion of 13C/15N‐labelled prey

• Amino acids represent an important component in the diet of the Venus flytrap (Dionaea muscipula), and supply plants with much needed nitrogen resources upon capture of insect prey. Little is known about the significance of prey‐derived carbon backbones of amino acids for the success of Dionaea's carnivorous life‐style.
• The present study aimed at characterizing the metabolic fate of ¹⁵N and ¹³C in amino acids acquired from double‐labeled insect powder. We tracked changes in plant amino acid pools and their δ¹³C‐ and δ¹⁵N‐signatures over a period of five weeks after feeding, as affected by contrasting feeding intensity and tissue type (i.e., fed and non‐fed traps and attached petioles of Dionaea).
• Isotope signatures (i.e., δ¹³C and δ¹⁵N) of plant amino acid pools were strongly correlated, explaining 60% of observed variation. Residual variation was related to contrasting effects of tissue type, feeding intensity and elapsed time since feeding. Synthesis of nitrogen‐rich transport compounds (i.e., amides) during peak time of prey digestion increased ¹⁵N‐ relative to ¹³C‐ abundances in amino acid pools. After completion of prey digestion, ¹³C in amino acid pools was progressively exchanged for newly fixed ¹²C. The latter process was most evident for non‐fed traps and attached petioles of plants that had received ample insect powder.
• We argue that prey‐derived amino acids contribute to respiratory energy gain and loss of ¹³CO₂ during conversion into transport compounds (i.e., 2 days after feeding), and that amino‐nitrogen helps boost photosynthetic carbon gain later on (i.e., 5 weeks after feeding).

     

Spatio-temporal changes of photosynthesis in carnivorous plants in response to prey capture,retention and digestion

Carnivorous plants have evolved modified leaves into the traps that assist in nutrient uptake from captured prey. It is known that the traps of carnivorous plants usually have lower photosynthetic rates than assimilation leaves as a result of adaptation to carnivory. However, a few recent studies have indicated that photosynthesis and respiration undergo spatio-temporal changes during prey capture and retention, especially in the genera with active trapping mechanisms. This study describes the spatio-temporal changes of effective quantum yield of photochemical energy conversion in photosystem II (Φ_PSII) in response to ant-derived formic acid during its capture and digestion.Key words: action potential, carnivorous plants, formic acid, photosynthesis, respiration, animal-plant interactionCarnivorous plants have evolved their leaves into the modified structures called traps, which assist in nutrient uptake from prey bodies.¹ The traps attract, catch and digest the animal prey; however, some species obtain substantial amount of nutrients from leaf litter (Nepenthes ampullaria), algae (Utricularia) or from faeces of tree shrew Tupaia montana (Nepenthes lowii, N. rajah, N. macrophylla) as a result of adaptive radiation with regard to nitrogen sequestration.^2–5 Carnivorous plants are mainly restricted to sunny, moist and nutrient-poor environment, because only in this environment would the cost of producing traps be lower than the benefits gained from prey.⁶ From carbon metabolism point of view, the benefit is in term of increased rate of photosynthesis per unit leaf mass as a result of increased nitrogen concentration in the leaf or an increase in the total leaf mass that can be supported.^6–8 The costs of carnivory include reduced rate of net photosynthesis (A_N) in traps as a result of leaf adaptation to carnivory or increased rate of respiration (R_D) as a result of extra energy requirements for attracting, capturing and digesting the prey.⁹ Whereas the reduced A_N in the traps has been confirmed several times, the higher R_D in traps is still ambiguous.^9–12Until now studies assessing the cost of carnivory have usually been confined to measurements of A_N and R_D in carnivorous traps vs. non-carnivorous leaves, to the construction costs and payback times for carnivorous organs or to the carbon costs of sticky mucilage secretion by glands.^9–16 There is a growing body of evidences that prey-catching is active process involving spatio-temporal changes in A_N and R_D in traps, at least in carnivorous plants with active trapping mechanisms.¹⁷ First evidence, however not convincing, came from the work of Knight.⁹ She found that bladders of aquatic bladderwort Utricularia macrorhiza had a slightly greater R_D (10%) than assimilation leaves, but these differences were not significant. Later Adamec found that R_D of bladders in six Utricularia species was 75–200% greater than that in the leaves.¹⁸ The action of Utricularia bladder is one of the fastest movement in plant kingdom. When the trap of Utricularia is set, ready for trapping, it looks shrunken due to negative hydrostatic pressure. When the trapdoor is stimulated by prey it opens, sucks the water with prey and the door rapidly shuts. This firing process takes about 30 ms. Then the bladder restores its negative hydrostatic pressure by the removal of water from trap lumen through the glands. The resetting of bladders is a respiration-dependent process accompanied by the consumption of ATP.^1,19,20 Adamec suggests that the bladders of Utricularia were in post-firing state and were therefore pumping water and is possible that their R_D in this state was much higher than in their resting state.¹⁸ Adaptative changes in cytochrome c oxidase in the genus Utricularia may provide respiratory power for bladder function.²¹ The most famous carnivorous plant the Venus flytrap (Dionaea muscipula) also uses active trapping mechanism for prey capture. Recently, Hájek and Adamec published that the traps of D. muscipula had lower A_N, whereas the R_D in lamina and trap was comparable.¹² This is in accordance with the classical interpretation of cost/benefit model of carnivory. However, in our previous study we have shown that trigger hair irritation in the open as well as in closed trap of Dionaea muscipula resulted in the rapid increase of R_D and decrease of effective quantum yield of photochemical energy conversion in photosystem II (Φ_PSII).¹⁷ We have suggested that this is a result of generation of action potentials upon trigger hair irritation.^22–25The link between electrical signals and inhibition of photosynthesis and stimulation of respiration has been described in several plant species, however it has not been known in carnivorous plants.^26–30 Another genus of carnivorous plants that generates action potentials in response to mechanical irritation is sundew (Drosera). In the Dionaea traps, the action potential originates in any one of the six trigger hair and the potential propagates over the entire trap blade more rapidly across the lower (abaxial) surface. In the Drosera tentacle, action potentials are initiated by a receptor potential just below the swollen head of the tentacle and propagate only to its base and do not reach the leaf lamina.^31–33 This is in accordance with the results that separated D. prolifera tentacles have many times greater R_D in comparison with that of leaf lamina. This proves a very high metabolic and physiological activity of tentacles probably as a results of electrical irritability.¹¹ It has been suggested that at least some of the energy connected with the rise of R_D after action potential is utilized for the restoration of the state of ionic balance (i.e., restore the resting state).²⁶ Except the electrical signals, chemical substances seem to be also effective in effecting photosynthesis in carnivorous plants. This study describes negative impact of ant-derived formic acid on effective quantum yield of photochemical energy conversion in PSII (Φ_PSII), which is a sensitive indicator of plant photosynthetic performance.We measured the chlorophyll fluorescence in response to prey capture (ant Lasius niger L.) by the leaf of Drosera capensis L. Ten one-year-old Drosera capensis L plants were grown in growth chamber at a irradiance 200 µmol m⁻² s⁻¹ photosynthetic active radiation (PAR), 14/10 h day/night cycle and daily temperature ∼25°C. Before the measurement, the plant was adapted to light intensity 100 µmol m⁻² s⁻¹ PAR for 10 minutes (time required for steady state values of chlorophyll fluorescence in light-adapted state, F_t). The actinic light was provided by fluorcam FC-1000 LC (Photon System Instruments, Czech Republic) using red emitting LED diodes (λ = 620 nm). The experiment started by application of first saturation pulse (4,000 µmol m⁻² s⁻¹ PAR, 800 ms duration, λ = 620 nm). Then (after 10 seconds) one ant (Lasius niger) was gently put on the D. capensis leaf. During the first two hours, saturation pulses were applied every three minute, thereafter every hour and later every 24 hour. After each saturation flash the visible pictures were taken by camera Nikon D60 (Nikon, Thailand). The Φ_PSII, which indicates the proportion of the light absorbed by chlorophyll associated with photosystem II that is used in photochemistry, was calculated as (F_m′ - F_t)/F_m′.^34,35 The experiment was repeated without ant''s abdomen (the abdomen was cut by scalpel but ants survive and their moving was not affected). In the last experiment 1 µL 15 M formic acid (Fluka) was dropped on the leaf. All experiments were repeated four times independently and data presented are representative.The inhibition of Φ_PSII occurred within a few minutes after the ant was trapped by Drosera tentacles and then again after 96 hours (Fig. 1). Repeating the experiment without ant''s abdomen had no negative impact on Φ_PSII in spite of ant-induced leaf folding (Fig. 2). The most common substance in ant''s abdomen is formic acid.³⁶ This indicates that the inhibition of Φ_PSII was caused first by the spraying of the formic acid on the leaf by the struggling ant and then by releasing the formic acid after 96 hours from ant''s abdomen as a result of digestion. Therefore, the preliminary observation in Drosera mentioned at the end of discussion of our previous study was not associated with electrical signals.¹⁷ The inhibition was caused by the ant Lasius niger, which inhibits the Φ_PSII in D. capensis by releasing the formic acid from its abdomen. This is consistent with the findings that propagation of action potentials in Drosera is restricted only to the tentacles and therefore had no effect on photosynthesis in leaf blade (Fig. 2). Further, application of 1 µL 15 M formic acid resulted in very similar effect like the living ant with intact abdomen (Fig. 3). The concentration of formic acid was chosen according to data that the venom of Formica rufa contains 5–17 M formic acid.³⁶Open in a separate windowFigure 1The visible response (A) and the response of effective quantum yield of photochemical energy conversion in photosystem II (Φ_PSII, B) of Drosera capensis leaf to prey capture (intact ant Lasius niger). The ant was put on the leaf in time 10 seconds.Open in a separate windowFigure 2The response of effective quantum yield of photochemical energy conversion in photosystem II (Φ_PSII) of Drosera capensis leaf to prey capture (ant Lasius niger without abdomen). The ant without abdomen was put on the leaf in time 10 seconds. Note that no changes in Φ_PSII occurred in spite of leaf folding.Open in a separate windowFigure 3The response of effective quantum yield of photochemical energy conversion in photosystem II (Φ_PSII) of Drosera capensis leaf to 1 µL of 15 M formic acid. The drop of formic acid was put on the leaf in time 10 seconds.The production of formic acid by ants is thought to have evolved to improve capture of invertebrate prey and aid colony defence.³⁷ Some examples document that negative effect of ant-derived formic acid on plant growth is not novel, but it has not been described in carnivorous plants previously. It is known that ants Myrmelachista schumanni use formic acid as a herbicide. The ants live inside the hollow stems of Duroia hirsuta, kill all plants other than their host plant by injecting formic acid into the leaves. By killing these others plants, the ants gain more nest sites and they create a single species stand of plants.³⁸ Also, weaver ants (Oecophylla smaragdina) damage mango fruit by deposition of formic acid as a result of fighting between weaver colonies.³⁹The mechanism of action is very similar to the well known herbicide 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU). Formic acid causes significant inhibition of the electron transfer on the acceptor side of photosystem II, particularly from plastoquinone A to plastoquinone B.^40,41 From the data analysis of carnivorous plants published recently the genera with the highest proportions of ants in their diets are Brocchinia (90%), Nepenthes (73%) and Sarracenia (55%).⁴² All the mentioned genera have pitcher traps, with the permanent level of digestive fluid, in which the formic acid is diluted during digestion and thus the pitchers are probably prevented against its toxic effect. Captures of ants is much less frequent for sticky traps of Drosera (3.4%) and Pinguicula (0.5%); however it may have deteriorate effect.Carnivorous plants are not just killers but are a fascinating group of plant. They do not just eat the animals but may form a complicated social network with them. Complicated animal-plant interaction, as has been described e.g. between carnivorous pitcher plant Nepenthes bicalcarata and ants may have direct impact on physiological processes similar as a well known relationship between acacia and ants.⁴³ The possible impact of formic acid of ant species co-occurring with carnivorous plants in their natural habitat on photosynthesis remains to be elucidated.     

Fluorescent prey traps in carnivorous plants

Carnivorous plants acquire most of their nutrients by capturing ants, insects and other arthropods through their leaf‐evolved biological traps. So far, the best‐known attractants in carnivorous prey traps are nectar, colour and olfactory cues. Here, fresh prey traps of 14 Nepenthes, five Sarracenia, five Drosera, two Pinguicula species/hybrids, Dionaea muscipula and Utricularia stellaris were scanned at UV 366 nm. Fluorescence emissions of major isolates of fresh Nepenthes khasiana pitcher peristomes were recorded at an excitation wavelength of 366 nm. N. khasiana field pitcher peristomes were masked by its slippery zone extract, and prey capture rates were compared with control pitchers. We found the existence of distinct blue fluorescence emissions at the capture spots of Nepenthes, Sarracenia and Dionaea prey traps at UV 366 nm. These alluring blue emissions gradually developed with the growth of the prey traps and diminished towards their death. On excitation at 366 nm, N. khasiana peristome 3:1 CHCl₃–MeOH extract and its two major blue bands showed strong fluorescence emissions at 430–480 nm. Masking of blue emissions on peristomes drastically reduced prey capture in N. khasiana pitchers. We propose these molecular emissions as a critical factor attracting arthropods and other visitors to these carnivorous traps. Drosera, Pinguicula and Utricularia prey traps showed only red chlorophyll emissions at 366 nm.     

Quantification of insect nitrogen utilization by the venus fly trap Dionaea muscipula catching prey with highly variable isotope signatures.

Dionaea is a highly specialized carnivorous plant species with a unique mechanism for insect capture. The leaf is converted into an osmotically driven trap that closes when an insect triggers sensory trichomes. This study investigates the significance of insect capture for growth of Dionaea at different successional stages after a fire, under conditions where the prey is highly variable in its isotope signature. The contribution of insect-derived nitrogen (N) was estimated using the natural abundance of 15N. In contrast to previous 15N studies on carnivorous plants, the problem emerges that delta15N values of prey insects ranged between -4.47 per thousand (grasshoppers) and +7.21 per thousand (ants), a range that exceeds the delta15N values of non carnivorous reference plants (-4.2 per thousand) and soils (+3 per thousand). Thus, the isotope-mixing model used by Shearer and Kohl to estimate the amount of insect-derived N is not applicable. In a novel approach, the relationships of delta15N values of different organs with delta15N of trapping leaves were used to estimate N partitioning within the plant. It is estimated that soon after fire approximately 75% of the nitrogen is obtained from insects, regardless of plant size or developmental stage. The estimates are verified by calculating the average isotope signatures of insects from an isotope mass balance and comparing this with the average measured delta15N values of insects. It appears that for Dionaea to survive and reach the flowering stage, seedlings must first reach the 6th-leaf rosette stage, in which trap surface area nearly doubles and facilitates the capture of large insects. Large amounts of nitrogen thus made available to plants may facilitate an enhanced growth rate and the progressive production of additional large traps. Dionaea reaches a maximum abundance after fire when growth of the competing vegetation is suppressed. About 10 years after fire, when grasses and shrubs recover, Dionaea becomes overtopped by other species. This would not only reduce carbon assimilation but also the probability of catching larger prey. The amount of insect-derived nitrogen decreases to 46%, and Dionaea becomes increasingly dependent on N-supply from the soil. Competition for both light and N may cause the near disappearance of Dionaea in older stages of the fire succession.     

Temperature Responses of Photosynthesis and Respiration of Maize (<Emphasis Type="Italic">Zea mays</Emphasis>) Plants to Experimental Warming

Understanding the key processes and mechanisms of photosynthetic and respiratory acclimation of maize (Zea mays L.) plants in response to experimental warming may further shed lights on the changes in the carbon exchange and Net Primary Production (NPP) of agricultural ecosystem in a warmer climate regime. In the current study, we examined the temperature responses and sensitivity of foliar photosynthesis and respiration for exploring the mechanisms of thermal acclimation associated with physiological and biochemical processes in the North China Plain (NCP) with a field manipulative warming experiment. We found that thermal acclimation of A_n as evidenced by the upward shift of A_n-T was determined by the maximum velocity of Rubisco carboxylation (V_cmax), the maximum rate of electron transport (J_max), and the stomatal- regulated CO₂ diffusion process (g_s), while the balance between respiration and photosynthesis (R_d/A_g), and/or regeneration of RuBP and the Rubisco carboxylation (J_max/V_cmax) barely affected the thermal acclimation of A_n. We also found that the temperature response and sensitivity of R_d was closely associated with the changes in foliar N concentration induced by warming. These results suggest that the leaf-level thermal acclimation of photosynthesis and respiration may mitigate or even offset the negative impacts on maize from future climate warming, which should be considered to improve the accuracy of process-based ecosystem models under future climate warming.     

Dark respiration of leaves and traps of terrestrial carnivorous plants: are there greater energetic costs in traps?

In this study, O₂-based dark respiration rate (R_D) in leaf and trap cuttings was compared in 9 terrestrial carnivorous plant species of 5 genera to decide whether traps represent a greater energetic (maintanence) cost than leaves or photosynthetic parts of traps. R_D values of cut strips of traps or leaves of terrestrial carnivorous plants submerged in water ranged between 2.2 and 8.4 nmol g⁻¹ s⁻¹ (per unit dry weight) in pitcher traps of the genera Sarracenia, Nepenthes, and Cephalotus, while between 7.2 and 25 nmol g⁻¹ _DW s⁻¹ in fly-paper or snapping traps or leaves of Dionaea and Drosera. No clear relationship between R_D values of traps (or pitcher walls) and leaves (or pitcher wings or petioles) was found. However, RD values of separated Drosera prolifera tentacles exceeded those of leaf lamina 7.3 times.     

基于树干液流技术的北京市刺槐冠层吸收臭氧特征研究

全球范围内加速的城市化导致空气质量严重退化。随着北京市建设范围不断扩大和机动汽车数量迅猛增长,空气污染日益严重。浓度不断增加的近地层臭氧作为影响全球气候变化的重要因素和危害人类健康、动植物生长的二次污染物,受到广泛关注。城市树木能够有效地去除大气污染物,进而提高空气质量。目前已有很多研究关于区域尺度上城市树木吸收臭氧,然而,冠层尺度上城市树木吸收臭氧特征少有研究。因此,本文基于树干液流技术,结合天气变化和大气臭氧浓度分析,研究夏秋季节北京市典型绿化树种刺槐（Robinia pseudoacacia）整树冠层吸收臭氧特征及环境影响因素。结果表明,在日尺度上,刺槐吸收臭氧速率变化呈单峰曲线,于下午15:00左右达到峰值;夏季峰值范围较宽,秋季峰值范围较窄;中午前后累积吸收臭氧量增加最明显。在季节尺度上,夏季刺槐吸收臭氧速率高于秋季;夏季累积吸收臭氧量显著增加,秋季略有增加。刺槐吸收臭氧的时间变化规律取决于大气臭氧浓度和冠层对臭氧的导度。臭氧浓度日变化和季节变化明显,导致刺槐吸收臭氧速率时间变化格局与之接近。在一定的臭氧浓度下,刺槐吸收臭氧速率的变化主要由冠层对臭氧的导度调控,进而受水汽压亏缺和总辐射的影响。随着水汽压亏缺降低,刺槐冠层对臭氧的导度明显下降;总辐射大于600 W/m2,冠层对臭氧的导度迅速下降。研究树种刺槐单位冠层投影面积上年吸收臭氧量约为0.16 g/m2,明显低于基于模型得到的结果,表明评估森林受臭氧危害的风险应考虑树种冠层臭氧通量。     

Capture of algae promotes growth and propagation in aquatic Utricularia

Background and Aims Some carnivorous plants trap not only small animals but also algae and pollen grains. However, it remains unclear if these trapped particles are useless bycatch or whether they provide nutrients for the plant. The present study examines this question in Utricularia, which forms the largest and most widely spread genus of carnivorous plants, and which captures prey by means of sophisticated suction traps.Methods Utricularia plants of three different species (U. australis, U. vulgaris and U. minor) were collected in eight different water bodies including peat bogs, lakes and artificial ponds in three regions of Austria. The prey spectrum of each population was analysed qualitatively and quantitatively, and correlated with data on growth and propagation, C/N ratio and δ¹⁵N.Key Results More than 50 % of the prey of the Utricularia populations investigated consisted of algae and pollen, and U. vulgaris in particular was found to capture large amounts of gymnosperm pollen. The capture of algae and pollen grains was strongly correlated with most growth parameters, including weight, length, budding and elongation of internodes. The C/N ratio, however, was less well correlated. Other prey, such as moss leaflets, fungal hyphae and mineral particles, were negatively correlated with most growth parameters. δ¹⁵N was positively correlated with prey capture, but in situations where algae were the main prey objects it was found that the standard formula for calculation of prey-derived N was no longer applicable.Conclusions The mass capture of immotile particles confirms the ecological importance of autonomous firing of the traps. Although the C/N ratio was little influenced by algae, they clearly provide other nutrients, possibly including phosphorus and trace elements. By contrast, mosses, fungi and mineral particles appear to be useless bycatch. Correlations with chemical parameters indicate that Utricularia benefits from nutrient-rich waters by uptake of inorganic nutrients from the water, by the production of more traps per unit of shoot length, and by the capture of more prey particles per trap, as nutrient-rich waters harbour more prey organisms.     

Effect of leaf age and position on light-saturated CO<Subscript>2</Subscript> assimilation rate,photosynthetic capacity,and stomatal conductance in rubber trees

Shoots of the tropical latex-producing tree Hevea brasiliensis (rubber tree) grow according to a periodic pattern, producing four to five whorls of leaves per year. All leaves in the same whorl were considered to be in the same leaf-age class, in order to assess the evolution of photosynthesis with leaf age in three clones of rubber trees, in a plantation in eastern Thailand. Light-saturated CO₂ assimilation rate (A _max) decreased more with leaf age than did photosynthetic capacity (maximal rate of carboxylation, V _cmax , and maximum rate of electron transport, J _max), which was estimated by fitting a biochemical photosynthesis model to the CO₂-response curves. Nitrogen-use efficiency (A _max/N_a, N_a is nitrogen content per leaf area) decreased also with leaf age, whereas J _max and V _cmax did not correlate with N _a. Although measurements were performed during the rainy season, the leaf gas exchange parameter that showed the best correlation with A _max was stomatal conductance (g _s). An asymptotic function was fitted to the A _max-g _s relationship, with R ² = 0.85. A _max, V _cmax, J _max and g _s varied more among different whorls in the same clone than among different clones in the same whorl. We concluded that leaf whorl was an appropriate parameter to characterize leaves for the purpose of modelling canopy photosynthesis in field-grown rubber trees, and that stomatal conductance was the most important variable explaining changes in A _max with leaf age in rubber trees.     

Parameters of photosynthesis light curve in <Emphasis Type="Italic">Salix dasyclados</Emphasis> and their changes during the growth season

A dependence of the photosynthesis rate on light is characterized by a number of parameters that are often used for comparison between plant species or for finding photosynthesis interconnections with other physiological processes. In order to properly assessed these parameters, we measured the maximum apparent photosynthesis rate (P _max), dark respiration rate (R _d), light compensation point (LCP), quantum yield corresponding to photosynthetic efficiency (QY), and the light saturation constant (K _s), taking into consideration the leaf plastochron index during vegetation of one of the willow species (Salix dasyclados Wimn.). The P _max value was the highest in the beginning of the growth season when the leaf reached 65% of its full area; after that P _max slowly declined. The most important cardinal value for R _d is its plateau reached by the end of leaf growth, i.e., later than the photosynthesis rate maximum. This plateau value also decreased during vegetation. The LCP value changed in the same way as R _d but reached its plateau simultaneously with the photosynthesis rate maximum. QY also reached its maximum at the same time with the photosynthesis rate; during vegetation it changed more than twofold. The K _s value also changed almost twofold during the season, reaching its maximum together or slightly later than the photosynthesis maximum and then remained constant. Thus, we have found significant changes in the parameters of the photosynthesis light curve during growth season. This shows that they can be used only after a thorough study of leaf development in each particular plant species. Usually performed measuring gas exchange parameters in fully developed leaves does not yield their maximum values and thus does not have any physiological sense.     

Growth and nitrate uptake properties of plants grown at different relative rates of nitrogen supply. II. Activity and affinity of the nitrate uptake system in Pisum and Lemna in relation to nitrogen availability and nitrogen demand

Abstract Net nitrate uptake rates were measured and the kinetics calculated in non-nodulated Pisum sativum L. cv. Marma and Lemna gibba L. adapted to constant relative rates of nitrate-N additions (R_A), ranging from 0.03 to 0.27 d^?1 for Pisum and from 0.05 to 0.40 d^?1 for Lemna, V_max of net nitrate uptake (measured in the range 10 to 100 mmol m^?3 nitrate, i.e. ‘system I’) increased with R_A in the growth limiting range but decreased when R_A exceeded the relative growth rate (RGR), K_m was not significantly related to changes in R_A. On the basis of previous ¹³N-flux experiments, it is concluded that the differences in V_max at growth limiting R_A are attributable to differences in influx rates. Linear relationships between V_max and tissue nitrogen concentrations were obtained in the growth limiting range for both species, and extrapolated intercepts relate well with the previously defined minimal nitrogen concentrations for plant growth (Oscarson, Ingemarsson & Larsson, 1989). Analysis of V_max for net nitrate uptake on intact plant basis in relation to nitrogen demand during stable, nitrogen limited, growth shows an increased overcapacity at lower R_A values in both species, which is largely explained by the increased relative root size at low R_A. A balancing nitrate concentration, defined as the steady state concentration needed to sustain the relative rate of increase in plant nitrogen (R_N), predicted by R_A, was calculated for both species. In the growth limiting range, this value ranges from 3.5 mmol m^?3 (R_A 0.03 d^?1) to 44 mmol m^?3 (R_A 0.21 d^?1) for Pisum and from 0.2 mmol m^?3 (R_A 0.05 d^?1) to 5.4 mmol m^?3 (R_A 0.03 d^?1) for Lemna. It is suggested that this value can be used as a unifying measure of the affinity for nitrate, integrating the performance of the nitrate uptake system with nitrate flux and long term growth and demand for nitrogen.