Assimilation of Cd and Cu by the Carnivorous Plant Sarracenia

Feb 8, 2010 - The School of Conservation Sciences, Bournemouth University, Talbot ... fax: +44 (0)1202 965046; e-mail: [email protected]...
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Environ. Sci. Technol. 2010, 44, 1610–1616

Assimilation of Cd and Cu by the Carnivorous Plant Sarracenia leucophylla Raf. fed Contaminated Prey CHRISTOPHER MOODY AND IAIN D. GREEN* The School of Conservation Sciences, Bournemouth University, Talbot Campus, Poole, Dorset, BH12 5BB, United Kingdom

Received July 1, 2009. Revised manuscript received January 18, 2010. Accepted January 21, 2010.

Many species of carnivorous plants have become endangered through exposure to multiple risks such as habitat loss, illegal poaching, and pollution. A potential threat to these plants posed by pollution stems from the contamination of their invertebrate prey with trace metals. This study examined the potential for prey to act as sources of the trace metals Cd and Cu for the pitcher plant Sarracenia leucophylla. Cd- and Cucontaminated Diptera larvae were fed to S. leucophylla plants in separate experiments. The results demonstrated that Cd and Cu were readily transferred to the shoots of S. leucophylla in a dose-dependent manner. While the assimilation of Cu decreased with treatment level, the assimilation of Cd did not. Some assimilated Cu appeared to be translocated to the roots, but Cd was strongly retained in the shoots, where it was related to a reduction in shoot biomass. This suggested that on exposure to Cd-contaminated prey, the plants either experienced phytotoxicity or there was disruption of nutrient acquisition from the prey. Accumulation of Cu was not related to any sign of phytotoxicity.

Introduction Because of nutrient deficient soils typical of the ecosystems they inhabit, carnivorous plants have evolved mechanisms to obtain at least part of their mineral nutrition from invertebrate prey (1, 2). The American pitcher plants (Sarracenia spp.) are a genus of carnivorous plant that utilize a pitfall trap mechanism to capture and break down invertebrate prey into a solution. Some nutrients from this solution are readily taken up by the cells lining the pitcher (3). Experiments utilizing radiotracers added to the pitcher fluid have shown that Mn2+ is among the nutrients taken up from this fluid, but Fe2+ and Zn2+ are not (3, 4). Consequently, not all divalent trace metals present in the prey will be assimilated by the plant. Some trace metals are essential nutrients for plants, while others are nonessential. All trace metals are capable of causing toxicity to plants if the concentration of the metal within tissues exceeds a certain threshold concentration. For example, at low concentrations Cu is an essential cofactor required for the correct function of several important enzymes, but at high concentrations it causes toxicity (5). By contrast, Cd is a xenobiotic element with no known beneficial * Corresponding author phone: +44 (0)1202 961598; fax: +44 (0)1202 965046; e-mail: [email protected]. 1610

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function in animals or terrestrial plants and is considered to be highly toxic (5). Symptoms of trace metal toxicity include reduced photosynthetic and metabolic activity (6, 7) as well as interference with the uptake of water and essential elements by the roots (8). Studies on the transfer of trace metals between plants and invertebrates have focused exclusively on the transfer of metal from the plant to the invertebrate. These studies have demonstrated that trace metals can be biomagnified in herbivorous invertebrates feeding on plants (9-12). This can be compounded by further biomagnification in carnivorous invertebrates (12, 13). The mobility of invertebrates, especially those that can fly, may make them vectors for the transport of trace metals from contaminated to uncontaminated sites. Although it is not currently clear how widespread a phenomena biomagnification is in invertebrates, the process may expose carnivorous plants to much higher levels of trace metals than would be apparent from a measurement of the concentrations in the surrounding soils. Consequently, this may be a critical pathway through which carnivorous plants are exposed to trace metals, but it is not clear how such exposure will affect carnivorous plants. Many species of carnivorous plants, including, Sarracenia spp., are in decline due to habitat loss, pollution, changes in habitat, and poaching (14-16). Plants of the genus Sarracenia are important contributors to the biodiversity of ecosystems inhospitable to other plant life, and therefore, it is important to ensure their conservation (17, 18). For fully informed efforts to conserve Sarracenia spp., it is imperative that all of the potential threats to these plants, including the presence of elevated trace metals in their invertebrate prey, are understood. It is possible that Cd and Cu in invertebrate prey are transported along with other minerals into the systems of carnivorous plants. In the case of Cu, this may benefit the plant by increasing the supply of this essential element, but it may also result in the exposure of plants to phytotoxic levels of Cd or Cu, which in turn may affect conservation measures. Consequently, this study aims to (1) improve the general understanding of the uptake of trace metals in carnivorous plants by determining whether a carnivorous plant, Sarracenia leucophylla Raf., can assimilate Cd and Cu from it is prey, and (2) determine whether Cd or Cu assimilation from prey has any effect on plant fitness as measured by dry biomass production.

Materials and Methods Contamination of Prey. Arthropod prey, in the form of larval Calliphora vicina R.-D. (Diptera, Calliphoridae), were contaminated using a slightly modified version of the method described by Kramarz (19). Briefly, larvae were fed on a diet consisting of 200 g of extruded dog food, 8 g of powdered skimmed milk, 4 g of sucrose, 0.008 g of baker’s yeast, and 100 mL of distilled water (for control) or 100 mL of CdCl2/ CuCl2 solution (for metal treatments). The concentrations of Cd and Cu solutions were calculated to contaminate the larval food with nominal Cd concentrations of 10, 25, or 50 mg kg -1 or nominal Cu concentrations of 100, 250, or 500 mg kg -1 Cu. Higher Cu concentrations reflect the generally higher concentration of this metal in the environment. Fresh batches of larvae were prepared each time the plants were fed. Plant Growth and Feeding Regimes. Forty-eight Sarracenia leucophylla (white-topped pitcher plants), grown from seed harvested from the same seedpod and approximately 5 yrs old, were obtained from a commercial supplier (Southwest Carnivorous Plants, Devon, U.K.). The 10.1021/es9019386

 2010 American Chemical Society

Published on Web 02/08/2010

growth medium consisted of 6 parts of medium grade moss peat, 2 parts of medium grade perlite, and 1 part of elutriated grit. Plants were separated into two groups, one of which was exposed to Cd contaminated prey and the other exposed to Cu contaminated prey. Individual plants within each group were randomly assigned to one treatment (control or one of the three metal treatments). Each metal treatment was replicated six times and Cd and Cu treatments had separate control treatments. All forty-eight plants were grown in a controlled environment chamber maintained at 60% relative humidity, atmospheric CO2 concentration, and a 14 h 25 °C day and a 10 h 18 °C night. Photon flux density during the day period was measured as 200 µmol s-1 m-2 at shoot height. The plants were fed every seven days, with approximately half the number of healthy open pitchers receiving prey at each feed. This ensured that the pitchers were not overloaded with prey, while ensuring the plants received a steady amount of prey intake. The prey material was weighed to four decimal places and recorded prior to feeding, providing a record of fresh mass fed to each plant. Subsamples of prey were freezedried and analyzed to produce a figure for the metal concentration of each sample group for each week. Feeding was continued for 35 d. After the final feed, a further 35 d were allocated to allow for digestion of prey material and uptake of nutrients from solution. Chemical Analysis. At the end of the experiment, the whole plants, including the roots, were harvested. Pitchers were emptied of undigested contents before the plants were washed and then dried at 60 °C for 48 h. Plants were then weighed to determine dry biomass and separated into root (including the rhizome) and shoot material, which were then passed through a rotary mill to homogenize the samples prior to digestion. Subsamples of plant material (about 0.25 g) were digested in 10 mL of 69% nitric acid. Digests were then evaporated to dryness before resuspension in 25 mL of 5% nitric acid (12). Samples of about 0.1 g of washed and oven-dried (60 °C) prey material was digested in 10 mL of 69% nitric acid at 90 °C for 1 h. Samples were then cooled, 7.5 mL of 15% hydrogen peroxide added, and the samples heated for a further 2 h at 90 °C. Samples were then cooled to check that all lipids had been digested. Treatment with hydrogen peroxide was repeated if lipids remained, otherwise samples were heated to dryness. Dried samples were resuspended in 10 mL of 5% nitric acid. The concentration of Cd in sample digests was determined by graphite furnace atomic absorption spectrometry (ThermoUnicam Solaar 939, Cambridge, U.K.), using a deuterium background correction. Concentrations of Cu were determined by inductively coupled plasma-optical emission spectrometry (Varian Vista Pro, Yarnton, U.K.). Data Analysis. The dose of metal fed to each plant was calculated from the eq 1

D ) (WLM)C

(1)

Where D is the dose (µg or ng), WL is the fresh mass of larvae (kg), M is the percentage dry mass of larvae (%) and C is the concentration of metal in the larvae (mg kg-1) Comparisons of metal concentrations in larvae and dose received by plants among the treatments were determined nonparametrically using the Kruskal-Wallis test. The feeding strategy employed resulted in plants within the same treatment receiving widely varying doses of metal and dose levels overlapping among the treatments. This wide variation in dose received by each individual plant was utilized to establish the dose relationship between metal dose fed to the plant and subsequent metal concentration in and biomass of the plants. These relationships were determined by regression analysis. Data sets were tested for normality, linearity, homoscedasticity, and independence of residuals by examination of residuals scatter plots and normal probability plots. Inverse (1/variable), log10, or the log of the variable + 1 [log10 (1+ variable)] transformations of the data was performed or outliers removed when necessary in order for these assumptions to be met. Two plants in the 50 mg kg-1 Cd treatment failed to put out pitchers that were large enough to be fed, and these plants were removed from the statistical analysis. The assimilation efficiency for metal uptake was calculated for the plants subjected to the metal treatments by dividing the mass of metal in a plant by the estimated mass of metal that the plant would have contained if it had taken up 100% of the metal dose it received. This theoretical mass of metal at 100% assimilation (MT) was estimated by adding the dose received over and above the mean dose received by control plants to the mean mass of metal in the control plants using eq 2. MT ) CM + (DT - DC)

(2)

Where CM is the mean mass of metal in the control plants, DT is the dose received by a plant, and DC is the mean dose received by control plants. The actual mass of metal in the plant was calculated by multiplying the concentration of metal in the plant (mg kg-1) by the dry mass of the plant expressed in killigrams.

Results Metal Uptake by Larvae and Plants. Larval C. vicina readily accumulated Cd and Cu from the contaminated food, resulting in significantly elevated concentrations of both metals in C. vicina tissue (Table 1). Accumulation was most pronounced in the case of Cd, where concentrations in the larvae fed the most contaminated diet were almost 10 times higher than those in the control larvae. Accumulation was less pronounced in the case of Cu, but concentrations were

TABLE 1. Nominal Concentration of Cadmium and Copper in Food of Larval C. vicina, in Larvae that Fed on the Food, and Total Dose Received by S. leucophylla Plants Subsequently Fed on Larvae over the Course of the Experimenta Cd treatment Cd conc. in larval food (mg kg-1)

a

Cu treatment

Cd conc. in larvae (mg kg-1)

plant Cd dose (ng)

Cu conc. in larval food (mg kg-1)

Cu conc. in larvae (mg kg-1)

plant Cu dose (µg)

0 10 25 50

0.13 ( 0.06 0.37 ( 0.06 1.18 ( 0.45 1.26 ( 0.12

12.2 ( 1.2 47.6 ( 4.5 150.9 ( 40.5 196.0 ( 67.5

0 100 250 500

9.6 ( 0.9 18.7 ( 4.4 27.7 ( 4.4 37.7 ( 9.6

12.1 ( 0.9 21.7 ( 7.0 33.3 ( 5.5 48.0 ( 28.8

significance

H ) 14.83 P ) 0.002

H ) 12.99 P ) 0.005

H ) 11.37 P ) 0.01

H ) 14.87 P ) 0.002

Mean values ( 1 SE.

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FIGURE 1. Relationship between the concentration of cadmium in S. leucophylla shoots or roots and the dose of cadmium received from feeding on cadmium-contaminated prey (line fitted through observations by a linear OLS models).

FIGURE 2. Relationship between the concentration of copper in S. leucophylla roots or shoots and the dose of copper received from feeding on copper-contaminated prey (lines fitted through observations by linear OLS model).

still almost four times higher than those in the control in the larvae fed the most contaminated food. Despite the relatively wide variation in the amount of prey material fed to the S. leucophylla plants, there was a clear and significant increase in the dose of Cd and Cu received by the plants as the metal treatment level increased (Table 1). An analysis of the response of shoot concentration to increasing Cd dose showed that there was a significant positive relationship with the received Cd dose (Figure 1, r ) 0.48, F ) 6.12, P ) 0.02). No significant relationship was found between root concentration and dose (r ) 0.14, F ) 0.39, P ) 0.54, data inversely transformed). For Cu, the concentrations in the shoots showed a positive relationship with dose received (Figure 2, r ) 0.51, F ) 7.62, P ) 0.01). In contrast to Cd, root Cu concentrations also showed a significant relationship with dose, although this was weaker than that found for the shoots (r ) 0.42, F ) 4.66, P ) 0.04). Metal Assimilation Efficiency. The mean ((1 SE) efficiency with which Cd was assimilated by the plants was 46% ((6), 31% ((4), and 38% ((9) in the 10, 25, and 50 mg kg-1 treatments, respectively. One-way analysis of variance showed no significant difference in assimilation efficiency among the treatments (F ) 1.8, P ) 0.21). The respective efficiencies for Cu were 109% ((10), 65% ((15), and 41% ((10) in the 100, 250, and 500 mg kg-1 treatments, respectively. This decrease in assimilation efficiency with increasing treatment level was statistically significant (F ) 8.24, P ) 0.004). 1612

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Effects on Plant Growth. Shoot and root dry biomass of the Cd fed plants showed no significant correlation with the total mass of invertebrate material fed to them (r ) -0.14, P ) 0.55, and r ) -0.31; P ) 0.16 for shoots and roots, respectively). By contrast, Cu fed plants showed a significant positive correlation between the total mass of invertebrate material fed and both shoot (r ) 0.45, P ) 0.03) and root (r ) 0.49, P ) 0.02) dry biomass. The potential sublethal consequences of increased concentrations of the two metals in S. leucophylla tissues were determined via effects on the dry biomass of the harvested plants. There was no significant relationship between the Cd dose and biomass of the shoots (Figure 3A; r ) 0.09, F ) 0.09, P ) 0.70, log10 transformed data) or roots (Figure 3B; r ) 0.07, F ) 0.08, P ) 0.78, log10 transformed data) harvested from the plants treated with Cd. However, the biomass of harvested shoots showed a significant negative relationship with the concentration of Cd in the shoot (Figure 3C; r ) 0.46, F ) 5.3, P ) 0.03). No significant relationship was found between root biomass and root Cd concentration (Figure 3D; r ) 0.02, F ) 0.01, P ) 0.94). The Cu-treated plants showed a positive relationship between shoot biomass and Cu dose (Figure 4A; r ) 0.51, F ) 7.6, P ) 0.01), but no relationship was found for root biomass (Figure 4B; r ) 0.07, F ) 1.0, P ) 0.75). The biomass of shoots showed no significant relationship with the concentration of Cu in the shoot (Figure 4C; r ) 0.17, F ) 0.6, P ) 0.45), but root mass showed a significant positive

FIGURE 3. Relationship between the dry mass of harvested S. leucophylla roots or shoots and the dose of cadmium received from feeding on cadmium-contaminated prey (line fitted through observations by a linear OLS model).

relationship with Cu concentration in the root (Figure 4D; r ) 0.44, F ) 5.3, P ) 0.03). As the dose of metal received by the plants was a factor of prey mass and Cu concentration in the prey, plants receiving higher doses may have received more prey. To determine if the positive relationship between Cu dose and increased shoot biomass was due to greater quantities of food being fed to the plants, we performed a partial correlation to control for the mass of arthropod material fed. This showed that there was no significant relationship between Cu dose and dry mass for shoots (r ) 0.29, P ) 0.17), which indicates that the observed positive effect on the plants was due to increased food supply rather than Cu assimilation.

Discussion Calliphora larvae readily accumulated Cd and Cu from their food. This was particularly evident in the case of Cd, where the highest treatment increased concentrations in the larvae by a factor of 10. S. leucophylla plants readily assimilated both metals in a dose-dependent manner when fed the larvae as prey. Assimilation of Cd by the plants was relatively high (30-45%) and was unaffected by treatment level, which may indicate a poor ability to regulate this element. By contrast, the assimilation of the essential element Cu was very high at low treatment levels (∼100%), but this decreased significantly as treatment level increased. This may indicate that the plants had homeostatic mechanisms to reduce the uptake of Cu. This implies that essential elements may be more tightly regulated than xenobiotic elements.

Increasing concentrations of Cd in S. leucophylla shoots as Cd dose rose were not reflected in increased concentrations in the roots, showing that Cd was strongly retained in the shoots. This very low level of translocation may have arisen from poor loading of this xenobiotic element into the phloem sap, adsorption of Cd to exchange sites associated with the cell wall (5), or from detoxification of Cd through sequestration by phytochelatins and subsequent transport into the vacuole (20). However, these mechanisms did not appear to effectively detoxify Cd because retention was associated with negative effects on shoot growth as measured by biomass. Retarded shoot growth is symptomatic of Cd toxicity (21) and is considered a good indicator that toxicity has occurred in plants (22). It is generally accepted that the growth of carnivorous plants is positively affected when the quantity of prey is increased (1) and Farnsworth and Ellison (23) have demonstrated that the relative growth rate of Sarracenia spp. is related to the dose of food in a linear fashion. The results found in the Cu-treated plants in the present study confirm this finding for S. leucophylla. Consequently, the lack of a significant relationship between food dose and shoot biomass found in the Cd-treated plants in the present study presents further evidence to suggest that Cd treatment had a negative impact on plant growth. However, Kabata-Pendias and Pendias (5) suggested that Cd becomes phytotoxic at concentrations above 5 mg kg-1. The highest shoot concentration seen in the present study was considerably below this level at 0.23 mg kg-1. VOL. 44, NO. 5, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Relationship between the dry mass of harvested S. leucophylla roots or shoots and the dose of copper received from feeding on copper-contaminated prey (lines fitted through observations by linear OLS models).

Carnivorous plants may be particularly sensitive to factors affecting photosynthesis. Givnish et al. (24) suggested, on the basis of a cost-benefit model, that carnivorous plants benefit from an increased rate of photosynthesis because of the increased nutrient uptake provided by the captured prey. Balanced against this is the cost of producing trapping mechanisms, which are less photosynthetically active than leaves. Givnish et al. (24) developed their argument further by suggesting that the gains from carnivory would be reduced if photosynthesis is limited by factors other than nutrient levels, such as low light or water levels, and this in turn would limit plant growth (24). Empirical evidence that carnivory benefits carnivorous plants through increasing photosynthesis is provided by a study conducted by Farnsworth and Ellison (23). They demonstrated that fed Sarracenia plants showed increased chlorophyll levels, increased photosynthetic rate, and lowered photosystem stress compared to unfed plants. This translated into a higher relative growth rate in fed plants (23). Thus, the plant obtains benefit from carnivory through being able to increase photosynthesis, and this translates into increased growth. Perhaps unfortunately for carnivorous plants, the metabolic pathways of photosynthesis may be among the most easily disrupted by trace metals (25). Cadmium has several mechanisms through which it can cause toxicity to plants, including the disruption of photosynthesis (25). Consequently, the accumulation of Cd from prey may disrupt photosynthesis, negating the nutrient benefit from the prey and reducing growth as a consequence. If this hypothesis is true, then it may mean that carnivorous plants as a group may be particularly susceptible to Cd toxicity. 1614

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The toxic effects of Cd may be compounded by the lack of shoot to root translocation observed in S. leucophylla. For most plant species, the major site of heavy metal uptake is the roots. The majority of plants have evolved mechanisms to retain Cd within the root system (26), protecting the more sensitive shoot from toxicity (21, 22). The lack of Cd translocation means that S. leucophylla is directly accumulating Cd into the most vulnerable tissues to toxicity, those that are actively involved in photosynthesis. The negative effect of Cd on shoot mass was only correlated with shoot Cd concentration and not to Cd dose. This is surprising given the relationship between Cd dose and Cd shoot concentration. However, higher doses of Cd were associated with higher feeding levels. Changes in growth can alter the concentration of Cd in plants by concentrating or diluting a given mass of metal in the plant (27). Furthermore, according to Das et al. (7) the toxic affects of Cd on plants can be altered by proteins and vitamins. Consequently, the relationship between dose and symptoms of toxicity may not be a simple one because of growth and nutrient affects derived from differing doses of food. Copper was also readily taken up by S. leucophylla shoots in a dose-dependent manner. Unlike Cd, this essential trace element also accumulated in the roots of S. leucophylla. Thus, Cu may have been far more phloem mobile than Cd, which suggests that invertebrate food can act as a Cu source for the whole plant. However, it is highly probable that some Cu entered the plant by root uptake, which would explain the assimilation efficiency of over 100% observed in the plants grown at low treatment level. The uptake of mineral nutrients by the roots can be stimulated by increased

nutrient supply to the leaves (1). As dose is a factor of prey mass and Cu concentration in the prey, increased nutrient availability may partially explain the increase in Cu concentration in the root. At excessive concentrations, Cu can become phytotoxic by disrupting enzyme systems and by partaking in Fenton reactions that produce hydroxyl radicals that in turn cause oxidative stress to the plant (28, 29). However, the present study found no evidence to suggest that Cu caused phytotoxicity to S. leucophylla at the doses to which the plants were exposed. As for Cd, the Cu concentrations found in the plant tissues were below the typical phytotoxic range for Cu of 20-100 mg kg-1 stated by Kabata-Pendias and Pendias (5). Consequently, S. leucophylla did not exhibit a particular sensitivity to Cu. This lack of sensitivity to Cu may be explained by the regulation of Cu assimilation and by the translocation of Cu from the shoot, which may protect the critical photosynthetically active tissues. Slack (30) reported that Cu-based fungicides are particularly lethal to carnivorous plants of the genus Heliamphora. Thus, some carnivorous plants may be particularly sensitive to Cu. This potential disparity in sensitivity to Cu among species may be explained if sensitivity is related to the type of invertebrate prey encountered. Species that regularly capture invertebrate prey containing naturally high Cu concentrations, such as those that use hemocyanin as a respiratory pigment, may have adapted to be more tolerant of Cu. Conversely, those species that almost entirely capture prey low in Cu, such as insects, may have a small and easily overwhelmed capacity to detoxify Cu. Implications for Carnivorous Plant Conservation. The present study provides evidence that S. leucophylla is particularly sensitive to Cd exposure. The observed negative trends of Cd exposure on shoot biomass suggest that Cdexposed plants are less able to utilize the nutrient benefit received from captured prey. Givnish et al. (24) suggested that carnivory may benefit plant reproduction by increasing the level of nutrients and photosynthate available for seed production. Positive relationships have been observed between prey-derived nutrition and carnivorous plant reproductive parameters such as seeds produced by per plant in Pinguicula spp (31) and Drosera spp (32). Moreover, increased plant biomass appears to be directly linked to increased seed production (32). Thus, it is highly likely that the negative impacts of Cd assimilation will reduce the reproductive fitness of S. leucophylla, potentially compromising the long-term viability of affected populations. This species is listed as vulnerable in the IUCN red list (33), which means that the wild population faces a high risk of becoming extinct. Future conservation measures should, therefore, take into account the apparent sensitivity of S. leucophylla to Cd pollution and avoid development of activities emitting Cd in the vicinity of its populations. S. leucophylla does not appear to be unduly sensitive to Cu, but further study is required to determine the exposure levels required elicit negative effects in this species.

Acknowledgments The authors gratefully acknowledge the help and advice provided by Southwest Carnivorous Plants and the valuable comments of the reviewers. This study was supported by a small research grant from School of Conservation Sciences.

Note Added after ASAP Publication There were errors in the units of Table 1 in the version of this paper published ASAP February 8, 2010; the corrected version published ASAP February 25, 2010.

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