Non-carnivorous Plants Research Articles

Murderous plants

The year 2009 was the 150th anniversary of Charles Darwin’s publication of On the Origin of Species (Darwin 1859). It was marked by many celebratory articles including a paper by Mark Chase, Maarten Christenhusz, Dawn Sanders, and Michael Fay published in Botanical Journal of the Linnean Society called “Murderous plants: Victorian Gothic, Darwin and modern insights into vegetable carnivory” (Chase et al. 2009). In line with the catchy title, the article was a very broad review of carnivorous plants, real and imaginary, along with many plants that the authors considered incomplete carnivores. The article was not a proposal that we call all these plants murderous plants. What the article did though was argue that there is a clear continuum between carnivorous and non-carnivorous plants. That is, one can make up definitions of what is and what is not a carnivorous plant, but in the end any definition is totally arbitrary. I disagree. Carnivorous plants are unique. I think there is an obvious place to draw the line between carnivores and non-carnivores. Any waffling is due to our lack of understanding the plants. However, the Chase et al. (2009) article ends with “We may be surrounded by many more murderous plants than we think.” This is true; there are more murderous plants than we think.

Carnivory in plants as a beneficial trait in wetlands

A new hypothesis for the benefit of carnivory in plants (i.e., an alternative to aerenchyma for avoiding hypoxia) is evaluated. Root porosity and root depth were quantified in eight carnivorous plant species and 48 non-carnivorous species within a nutrient-poor wet pine savanna in south Mississippi, USA. Carnivorous and non-carnivorous plant species were contrasted with respect to their indication of wetlands, open habitats, and habitats with nutrient-poor soils. We used path analysis, multiplicative regression, and a field experiment to test hypotheses of the effects of soil moisture/hypoxia on the abundance of carnivorous and non-carnivorous plants. All carnivorous plant species produced non-porous roots (or no roots), which were shallower than the average for non-carnivorous plants (6.9 ± 0.95 cm vs. 11.9 ± 0.96 cm), even after correcting for plant size. Root porosity in non-carnivorous species (mean = 22%) was positively correlated with root depth ( r = 0.6). Despite lacking porous roots, carnivorous plants were four times more indicative of wetland habitats than were the non-carnivorous species encountered in the wetland studied here. Carnivorous plants, along with non-carnivorous plants with well-developed aerenchyma, were positively associated with the wettest microsites and were more negatively affected by elevating the substrate than were non-carnivorous plants with low-porosity roots. Non-carnivorous plants with shallow roots, while less indicative of wetlands and less abundant in wet microsites of the wet pine savanna than were carnivorous plants, were no less indicative of nutrient-poor soils than were carnivorous plants. Results supported the hypothesis that carnivory is advantageous in wet soils and disadvantageous in drier (including mesic) soils and are more indicative of wetland conditions than of low soil fertility.

Tissue mineral nutrient content in turions of aquatic plants: does it represent a storage function?

Turions are frost resistant, vegetative dormant organs produced by aquatic plants. Tissue N, P, K, Ca, and Mg content was estimated in turions of 5 rooting, non-carnivorous plant species of the genera Caldesia, Hy- drocharis, and Potamogeton and in 7 rootless carnivorous plant species of the genera Aldrovanda and Utricularia, and compared with concentrations of these nutrients in ambient waters either in the fi eld or in culture. Mean turion content of N in all species was 1.87 % DW, P 0.26 %, K 0.65 %, Ca 0.15 %, and of Mg 0.19 % DW. Of all nutri- ents, only turion K content differed signifi cantly between carnivorous and non-carnivorous species (0.48 ± 0.03 vs. 1.04 ± 0.10 % DW). For all plant species and sites (n = 18), turion nutrient content did not depend on nutrient concentrations in the ambient water at the time of turion initiation. Results of a literature survey conducted for the 12 plant species revealed that mean turion nutrient content was moderately (N, P) or markedly (K, Ca, Mg) lower than shoot or leaf nutrient content for the same 12 species. In conclusion, turions of aquatic plants also represent storage organs for mineral nutrients (N, P) though their storage function is presumably less distinct than in the case of carbohydrates.

Photosynthesis and dark respiration of leaves of terrestrial carnivorous plants

Using CO2 gasometry, net photosynthetic (P N) and dark respiration rates (R D) were measured in leaves or traps of 12 terrestrial carnivorous plant species usually grown in the shade. Generally, mean maximum P N (60 nmol CO2 g−1(DM) s−1 or 2.7 μmol m−2 s−1) was low in comparison with that of vascular non-carnivorous plants but was slightly higher than that reported elsewhere for carnivorous plants. After light saturation, the facultatively heliophytic plants behaved as shade-adapted plants. Mean R D in leaves and traps of all species reached about 50% of maximum P N and represents the high photosynthetic (metabolic) cost of carnivory.

Construction costs, payback times, and the leaf economics of carnivorous plants

Understanding how different plant species and functional types "invest" carbon and nutrients is a major goal of plant ecologists. Two measures of such investments are "construction costs" (carbon needed to produce each gram of tissue) and associated "payback times" for photosynthesis to recover construction costs. These measurements integrate among traits used to assess leaf-trait scaling relationships. Carnivorous plants are model systems for examining mechanisms of leaf-trait coordination, but no studies have measured simultaneously construction costs of carnivorous traps and their photosynthetic rates to determine payback times of traps. We measured mass-based construction costs (CC(mass)) and photosynthesis (A(mass)) for traps, leaves, roots, and rhizomes of 15 carnivorous plant species grown under greenhouse conditions. There were highly significant differences among species in CC(mass) for each structure. Mean CC(mass) of carnivorous traps (1.14 ± 0.24 g glucose/g dry mass) was significantly lower than CC(mass) of leaves of 267 noncarnivorous plant species (1.47 ± 0.17), but all carnivorous plants examined had very low A(mass) and thus, long payback times (495-1551 h). Our results provide the first clear estimates of the marginal benefits of botanical carnivory and place carnivorous plants at the "slow and tough" end of the universal spectrum of leaf traits.

Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis

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. Pitchers of Nepenthes grown at 200 micromol 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. A(N) and maximum (F(v)/F(m)) and effective quantum yield of photosystem II (Phi(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 Phi(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 Phi(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 micromol m(-2) s(-1) PAR after which it did not increase further. All fed plants began to flower. 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.

Energetics and the evolution of carnivorous plants—Darwin's ‘most wonderful plants in the world’

Carnivory has evolved independently at least six times in five angiosperm orders. In spite of these independent origins, there is a remarkable morphological convergence of carnivorous plant traps and physiological convergence of mechanisms for digesting and assimilating prey. These convergent traits have made carnivorous plants model systems for addressing questions in plant molecular genetics, physiology, and evolutionary ecology. New data show that carnivorous plant genera with morphologically complex traps have higher relative rates of gene substitutions than do those with simple sticky traps. This observation suggests two alternative mechanisms for the evolution and diversification of carnivorous plant lineages. The 'energetics hypothesis' posits rapid morphological evolution resulting from a few changes in regulatory genes responsible for meeting the high energetic demands of active traps. The 'predictable prey capture hypothesis' further posits that complex traps yield more predictable and frequent prey captures. To evaluate these hypotheses, available data on the tempo and mode of carnivorous plant evolution were reviewed; patterns of prey capture by carnivorous plants were analysed; and the energetic costs and benefits of botanical carnivory were re-evaluated. Collectively, the data are more supportive of the energetics hypothesis than the predictable prey capture hypothesis. The energetics hypothesis is consistent with a phenomenological cost-benefit model for the evolution of botanical carnivory, and also accounts for data suggesting that carnivorous plants have leaf construction costs and scaling relationships among leaf traits that are substantially different from those of non-carnivorous plants.

Longevity, lignin content and construction cost of the assimilatory organs of Nepenthes species.

This study examined level of causal relationships amongst functional traits in leaves and conjoint pitcher cups of the carnivorous Nepenthes species. Physico-chemical properties, especially lignin content, construction costs, and longevity of the assimilatory organs (leaf and pitcher) of a guild of lowland Nepenthes species inhabiting heath and/or peat swamp forests of Brunei, northern Borneo were determined. Longevity of these assimilatory organs was linked significantly to construction cost, lignin content and structural trait of tissue density, but these effects are non-additive. Nitrogen and phosphorus contents (indicators of Rubisco and other photosynthetic proteins), were poor predictors of organ longevity and construction cost, suggesting that a substantial allocation of biomass of the assimilatory organs in Nepenthes is to structural material optimized for prey capture, rigidity and escape from biotic and abiotic stresses rather than to light interception. Leaf payback time - a measure of net carbon revenue - was estimated to be 48-60 d. This is in line with the onset of substantial mortality by 2-3 months of tagged leaves in many of the Nepenthes species examined. However, this is a high ratio (i.e. a longer minimum payback time) compared with what is known for terrestrial, non-carnivorous plants in general (5-30 d). It is concluded that the leaf trait bivariate relationships within the Nepenthes genus, as in other carnivorous species (e.g. Sarraceniaceae), is substantially different from the global relationship documented in the Global Plant Trait Network.

Nutrient Limitation and Stoichiometry of Carnivorous Plants

The cost-benefit model for the evolution of carnivorous plants posits a trade-off between photosynthetic costs associated with carnivorous structures and photosynthetic benefits accrued through additional nutrient acquisition. The model predicts that carnivory is expected to evolve if its marginal benefits exceed its marginal costs. Further, the model predicts that when nutrients are scarce but neither light nor water is limiting, carnivorous plants should have an energetic advantage in competition with non-carnivorous plants. Since the publication of the cost-benefit model over 20 years ago, marginal photosynthetic costs of carnivory have been demonstrated but marginal photosynthetic benefits have not. A review of published data and results of ongoing research show that nitrogen, phosphorus, and potassium often (co-)limit growth of carnivorous plants and that photosynthetic nutrient use efficiency is 20 - 50 % of that of non-carnivorous plants. Assessments of stoichiometric relationships among limiting nutrients, scaling of leaf mass with photosynthesis and nutrient content, and photosynthetic nutrient use efficiency all suggest that carnivorous plants are at an energetic disadvantage relative to non-carnivorous plants in similar habitats. Overall, current data support some of the predictions of the cost-benefit model, fail to support others, and still others remain untested and merit future research. Rather than being an optimal solution to an adaptive problem, botanical carnivory may represent a set of limited responses constrained by both phylogenetic history and environmental stress.

Adaptations to Foliar Absorption of Faeces: a Pathway in Plant Carnivory

Roridula plants capture insects but have no digestive enzymes. It has been hypothesized that Roridula leaves absorb nitrogen from the faeces of obligately associated, carnivorous hemipterans. But rapid movement across the leaf surfaces of most plant leaves is prevented by the presence of an impermeable cuticle. However, in carnivorous plants, cuticular gaps or pores in digestive/absorptive cells allow rapid movement across the leaf surface. Recently, it was suggested that the hemipteran-plant interaction constituted a new pathway for plant carnivory. Here, a further adaptation to this pathway is described by demonstrating how Roridula plants probably absorb hemipteran faeces rapidly through their leaf cuticles. The dye neutral red was used to document the rapidity of foliar absorption and TEM to determine the nature of cuticular discontinuities in the leaf of Roridula. Aqueous compounds diffuse rapidly across the cuticle of Roridula's leaves but not across the cuticles of co-occurring, non-carnivorous plant leaves. Furthermore, immature Roridula leaves were unable to absorb neutral red whereas mature leaves could. Using TEM, cuticular gaps and pores similar to those in other carnivorous plants were found in the epidermal cells of mature Roridula leaves. The leaf cuticle of Roridula is very thin (0-120 nm) and cell wall elements project close to the leaf surface, possibly enhancing foliar absorption. In addition to these, cuticular gaps were frequently seen and probably perform a function similar to those found in other carnivorous plants: namely the absorption of aqueous compounds. The cuticular gaps of Roridula are probably an adaptation to plant carnivory, supporting the newly described pathway.

WHY DON'T CARNIVOROUS PITCHER PLANTS COMPETE WITH NON-CARNIVOROUS PLANTS FOR NUTRIENTS?

Most field studies suggest that competition for nutrients is important in nutrient-limited systems. Nevertheless, the mechanisms by which species avoid competition for nutrients in nutrient-poor but species-rich communities remain poorly understood. I used a model system, the carnivorous pitcher plant Sarracenia alata, to measure competition for nutrients. In a field competition experiment, I increased the potential for nutrient-niche overlap between established juvenile pitcher plants and their non-carnivorous neighbors by denying a unique source of nutrients (prey) to pitcher plants. Contrary to predictions based on nutrient-niche complementarity, prey exclusion did not reduce the performance of pitcher plants competing with non-carnivorous neighbors. Hence, differences in nutrient-source specialization did not explain the coexistence of Sarracenia alata and its non-carnivorous neighbors in the field. Instead, prey exclusion reduced the positive growth response to increased light following the removal of neighbors. By reducing allocation to pitchers in the presence of neighbors, pitcher plants appeared to reduce their demand for nutrients when shaded. I hypothesize that carnivorous plants avoid competition with non-carnivorous plants by using changes in the light environment to cue adjustments in their demand for nutrients. I suggest that such plasticity is adaptive in any long-lived perennial plant that periodically experiences simultaneous pulses of light and nutrients during its lifetime (e.g., as might occur in fire-prone habitats). Corresponding Editor: E. S. Menges

Costs and Benefits of Carnivory in Plants: Insights from the Photosynthetic Performance of Four Carnivorous Plants in a Subarctic Environment

We measured photosynthetic performance in four subarctic carnivorous plants, Pinguicula alpina, P. villosa, P. vulgaris and Drosera rotundifolia, in order to test if there is a cost of combining photosynthetic and trapping devices into the same organ (leaves). We compared these data with published results on photosynthetic rates in subarctic non-carnivorous plants. In P. vulgaris, an experiment of prey addition and removal further tested the existence of a short-term benefit of increased nutrient gain from prey in terms of photosynthetic efficiency. Leaf area-based photosynthetic rates (P a ) ranged 2.0-3.0 μmol CO 2 m -2 s -1 , dry mass-based photosynthetic rates (P w ) 42--69 nmol CO 2 g - 1s -1 , and photosynthetic nitrogen use efficiency (PNUE) 29-45 μmol CO 2 mol N - 1 s 1 . In general, P a and P w of carnivorous plants increased with leaf nitrogen content. When each species was analysed separately, those relationships were weak (P. alpina and P. villosa) or non-significant (P. vulgaris and D. rotundifolia). The photosynthetic rate of carnivorous plants was lower than that of other subarctic growth forms. In addition, P w for a given leaf nitrogen content was significantly lower in carnivorous plants than in non-carnivorous ones. No change in P a , P w or PNUE occurred as a result of prey capture manipulation, but treatments differed only slightly in nutrient content. P w and PNUE showed a trend to be higher in reproductive P. alpina plants as compared to vegetative ones. In P. vulgaris, however, an increased leaf respiration was found in reproductive plants.

Natural Abundance of δ15N Confirms Insectivorous Habit ofRoridula gorgonias, Despite it Having No Proteolytic Enzymes

Abstract Natural abundance values of plant δ15N give an indication as to the source of nitrogen. In particular, carnivorous plants are expected to be relatively enriched due to trophic enrichment of their prey. Values of δ15N for adultRoridula gorgonias(mean+3.02‰) are 4–9‰ greater than co-occurring non-carnivorous plant species and 5.24‰ greater than juvenileR. gorgoniasplants. They are also 3.5–4.26‰ greater than co-occurringDroseraspecies which, being sundews, are considered to be carnivorous. These high levels of δ15N in adult plants are best explained as being due to access to trophically enriched N from insects. As is the case for other carnivorous plants, leaves and stems ofR. gorgoniasare highly ultraviolet reflective and are therefore probably attractive to potential insect prey. This is further support for this plant species being insectivorous.

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

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