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Agriculture, Ecosystems and Environment 78 (2000) 85–91 Short communication Accumulation of heavy metals in food plants and grasshoppers from the Taigetos Mountains, Greece B. Devkota a , G.H. Schmidt b,∗ a b Department of Ecology, Faculty-5, University of Osnabrueck, Barbarastr. 11, D-49076 Osnabrueck, Germany Department of Zoology–Entomology, University of Hanover, Herrenhaeuserstr. 2, D-30419 Hanover, Germany Received 11 November 1998; received in revised form 18 June 1999; accepted 9 September 1999 Abstract Geogenic, as well as anthropogenic heavy metals from distant sources, gradually increase the level of toxic metals in natural environments and these will be increasingly taken up by the plants and transferred further up the food chain. The level of different heavy metals (Hg, Cd, Pb) was studied in the producers (food plants) and consumers [four species of acridid grasshoppers: Calliptamus italicus (L.), Oedipoda caerulesens (L.), O. germanica (Latr.) and Chorthippus(Glyptobothrus) crassiceps(Ramme, 1926)] of a grassland located 1200 m above the sea level in the Taigetos Mountains, Peloponnesus, Greece. The concentrations of heavy metals in the food plants and grasshoppers were in the order Pb > Cd > Hg and the mean concentration of Pb was about 55 and 20 times the concentrations of Hg and Cd, respectively. The solely herbivorous C.(G.) crassiceps had a significantly higher Hg-concentration than in the food plants, but it did not exceed that of Cd and Pb. Cd-concentration in the grasshoppers was significantly higher than in food plants, and female grasshoppers had higher Cd accumulation than males. Lead accumulation in grasshoppers was always lower than in their food plants. The accumulation factors of these elements in the grasshoppers were found in the order Cd > Hg > Pb, thus showing greater affinity to Cd accumulation. Significantly higher concentration of Hg in both sexes of C.(G.) crassiceps than in other three grasshoppers proved this species to be a comparatively better bioindicator of Hg pollution. Elevated concentrations of Cd in both, females and males of all four grasshopper species suggested that any grasshopper, irrespective of the sex, could equally play the role of bioindicator. Studies on the bioaccumulation and biotransfer of different heavy metals showed that the organisms of such distantly located ecosystems were also exposed to measurable amounts of toxic heavy metals. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Heavy metals; Hg; Cd; Pb; Accumulation; Bioaccumulation factors; Grasshoppers 1. Introduction The occurrence of toxic heavy metals in the soil is of geogenic or anthropogenic origins. The natural content ∗ Corresponding author. Tel.: +49-511-7625548; fax: +49-511-7625381. of heavy metals in the soil is dependent on geochemical and geophysical processes. Heavy metals from the point and other sources of emission can be transported to distant environments (Steinnes, 1980). Transport of heavy metals from the atmosphere to the soil and vegetation takes place by dust fall, bulk precipitation and gas or aerosol adsorption processes (Andersen et al., 0167-8809/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 8 8 0 9 ( 9 9 ) 0 0 1 1 0 - 3 86 B. Devkota, G.H. Schmidt / Agriculture, Ecosystems and Environment 78 (2000) 85–91 1978). The bulk of the elements is naturally bound as insoluble compounds in rock and sediments, and a multitude of ions can be released from sediments by redox changes (Lieth and Markert, 1990). The input of anthropogenic toxic metals in distantly located mountain ecosystems is generally lower than in valleys and settlement areas, but due to different natural (geophysical and geochemical) processes, the amount of pedogenic and lithogenic metals is also gradually increasing and is capable of interacting with biota. Some elements, such as mercury (Hg), zinc (Zn), cadmium (Cd), lead (Pb), and arsenic (As), may be increasingly taken up by the crop and transferred further to the food chain (Beijer and Jernelöv, 1986). About 20–30% of the total arthropod biomass during summer in a grassland ecosystem is due to acridid grasshoppers (Schmidt, 1986). Being herbivorous (primary consumer) and being preyed upon by other insectivorous vertebrates and arthropods, they play a significant role in accumulating and further transferring toxic metals to higher trophic levels. The studies on the transfer of heavy metals in an aquatic ecosystem by Jamil and Hussain (1992), and in a copper (Cu) and Cd contaminated grassland by Hunter et al. (1987) showed that the accumulation and biotransfer of anthropogenic heavy metals can be very high. Organisms, like grasshoppers, occurring in such environments are also exposed to gradually increasing toxic metals and contribute to the accumulation and biotransfer of heavy metals. Hunter et al. (1987) studied the influence of toxic heavy metals on the acridids Chorthippus(Glyptobothrus) brunneus (Thunbg.) from a Cd and Cu contaminated grassland. Higher accumulation of Hg in males than in females of Eyprepocnemis plorans (Charp.), but more Hg in females than in males of Aiolopus thalassinus (Fabr.), and no clear difference in Cd and Pb concentrations between the two sexes of A. thalassinus exposed to contaminated food under laboratory conditions showed that different grasshoppers accumulate different heavy metals in various concentrations and the accumulation of toxic metals might be sex dependent (Devkota, 1992). This study was undertaken to evaluate the dynamics of toxic heavy metals in a relatively less polluted grassland ecosystem and to determine whether some species are more suitable bioindicators and whether there is any sex-specific metal accumulation in the grasshoppers of such grasslands. 2. Materials and methods Using insect nets, males and females, ten each, of four species of acridid grasshoppers Calliptamus italicus (L.), Oedipoda caerulcesens (L.), O. germanica (Latr.) and Chorthippus (Glyptobothrus) crassiceps (Ramme, 1926) were collected from a grassland (1200 m above the sea level) in the Taigetos Mountains, Peloponnesus, Greece, during the summer of 1991. A mixture of food plants (grass) from the same grassland was also collected. During transportation to the Department of Zoology–Entomology, University of Hanover (Germany), the grasshoppers were fed the same grass. The grass samples were washed with deionised water to remove the heavy metals attached on the surface and were freeze-dried. Five samples each of both, males and females, and two grasshoppers in each sample, of all four grasshopper species were ground in a vibrating mill (Retsch, Germany) to a homogenous powder. For the food plants, only one sample was ground. 2.1. Determination of elements Cadmium (Cd) and lead (Pb) were determined with a Zeemann AAS SM30 (Gruen Optiker, Wetzlar, Germany) equipped with graphite furnace and suitable for element determinations in solid samples (Steubing et al., 1980; Grobecker and Kurfürst, 1990; Devkota and Schmidt, 1992). About 40–60 g of a homogenous sample weighed in a graphite boat was introduced into graphite tube furnace using special tweezers. After stepwise heating and ashing, the samples were atomised at 2000◦ C (for Cd) and 2300◦ C (for Pb) in an argon atmosphere. Atomic absorption was measured at wavelengths of 228.3 nm during Cd and 283.3 nm during Pb determination using respective hollow cathode lamps. BCR reference materials CRM 060 (Aquatic plant) and CRM 061(Aquatic plant) for plant samples and CRM 185 (Bovine liver) and CRM 186 (Pig kidney) for insect samples were used for calibration. Along with the samples, the solid reference materials were also determined for Cd and Pb concentrations. The obtained data were within the range of certified values. Mercury (Hg) in the samples was determined according to the flameless cold-vapour technique (Welz, B. Devkota, G.H. Schmidt / Agriculture, Ecosystems and Environment 78 (2000) 85–91 1985) using a Perkin–Elmer AAS 1100 equipped with a mercury hydride system (MHS 10). About 200 mg of finely ground sample was wet digested in 3 ml aqua regia (conc. H2 SO4 and conc. HNO3 in 2 : 1 V/V of spectroscopic grade (Riedel-de Haen) at 140–150◦ C for 4 h; one digestion per sample of grasshoppers and three digestions of the grass sample were carried in parallel. Sample aliquots were diluted to 20 ml with deionised water. From diluted sample solution, 10 ml was pipetted for each determination and reduced by 3% NaHBO4 and 1% NaOH in the presence of KMnO4 . The atomic absorption of the elemental mercury was measured at 253.6 nm using a hollow cathode mercury lamp. Nitrogen (extra pure) was used as carrier gas and Fixanal mercury standard solution (manufacturer: Riedel-de Haen, Germany) was used for calibration. The Hg concentration in the blank sample was also determined and this value was subtracted from sample values to avoid any unwanted contamination during sample preparation. 2.2. Analysis and presentation of data Mean and standard deviation of five determinations (one measurement per sample of five separate samples 87 in case of grasshoppers, but five measurements of one grass sample) of each heavy metal was calculated and the data are given in g g−1 dry weight of the sample. Differences between the mean concentrations in food plants and in grasshoppers were calculated using Student’s t-test (Wardlaw, 1985). The data were subjected to analysis of variance to calculate the F-ratio of intergroups variance (variations in metal concentrations between species means) to intragroups variance (variations of individual concentrations within each species) of heavy metal concentrations in grasshoppers. 3. Results As shown in Fig. 1, heavy metals (Hg, Cd, Pb) were found in remarkably high concentrations in the grass samples from the Taigetos Mountains, where the concentrations of these heavy metals were in the order Pb > Cd > Hg. The mean concentration of Pb was about 55 and 20 times the concentrations of Hg and Cd, respectively. Concentrations in grass vs. grasshoppers showed that these toxic metals have been differently accumulated in different trophic levels in this ecosystem. The Fig. 1. Concentrations (mean ± SD in g/g dry weight) of heavy metals (Hg, Cd, Pb) in food plants and in females (F) and males (M) of four species of grasshoppers from the Taigetos Mountains. Each bar represents the mean of five measurements and the differences in the mean concentrations between food plants and grasshoppers are indicated by ***p < 0.001, **p < 0.01, *p < 0.05 and ns — not significant differences. 88 B. Devkota, G.H. Schmidt / Agriculture, Ecosystems and Environment 78 (2000) 85–91 Table 1 Accumulation factors (concentration in grasshoppers/concentration in food plants) of three heavy metals (Hg, Cd, Pb) in females (F) and males (M) of four grasshopper species, where the factor >1 means higher concentration in grasshoppers than in food plants Metal Hg Cd Pb C. italicus O. caerulescens O. germanica C.(G.) crassiceps Remarks F F F M F M concentration in acridids 0.70 4.35 0.57 ∼ =0.71 >2.15 <0.62 2.00 3.27 0.47 ∼ =2.04 >2.72 >0.39 either ∼ = or > or > in food plants always > in food plants always < in food plants 0.84 4.19 0.53 M <0.99 >3.09 >0.32 1.30 2.97 0.42 M >0.62 >2.16 <0.47 concentration of Hg in these grasshoppers showed no sex-specific difference in bioaccumulation. The solely herbivorous C.(G.) crassiceps had Hg-concentration significantly higher than in food plants and both sexes of this grasshopper had the same level of accumulation (accumulation factor 2.00 in female and 2.04 in male) (Table 1). All four species of grasshoppers had significantly higher Cd concentration than the food plants. Cadmium accumulation in female grasshoppers was always higher (accumulation factors 2.97–4.35) than in males (accumulation factors 2.15–3.09) and it was remarkably high in O. germanica and C. italicus. In the case of Pb, the accumulation in grasshoppers (herbivores) never exceeded that of food plants (producers). In all grasshoppers, the concentration of Pb was higher than Hg and Cd. Though O. germanica was found to accumulate the highest amount of Pb, the accumulation factor was still <1. Like Hg, accumulation behaviour towards Pb in these grasshoppers was also quite different, and neither the females nor the males were found to have higher concentrations of Pb than food plants. In C.(G.) crassiceps, the accumulation behaviour of Hg and Cd was different (significantly higher) than of Pb (significantly low), but in other grasshoppers such differences between different heavy metals could not be observed within the same species. The accumulation factors of these elements in the grasshoppers were in the order Cd > Hg > Pb, with Cd bioaccumulation being significantly higher in all grasshoppers. Mercury in females of O. caerulescens was found in significantly higher concentrations than in males, but in other grasshoppers there was no intraspecific difference between the females and the males (Table 2). Though both sexes of all grasshoppers accumulated significantly high amounts of Cd, the difference in Cd concentration between females and males was significantly high only in O. germanica, where females had higher concentration than males. Significantly lower concentrations of Pb in O. caerulescens and C.(G.) crassiceps than in food plants could not deliver any intraspecific difference in Pb accumulation between the females and the males of these species. The variations in Hg concentration between different species (inter-group variations) was greater than the variations within each species (intra-group variations), which could be verified with the very large F value (F = 25.453, significant at p = 1% level). In case Table 2 Differences in the mean concentrations of Hg, Cd and Pb in grasshoppers (Ci: C. italicus; Oc: O. caerulescens; Og: O. germanica; Ch: C.(G.) crassiceps) between females and males of the same species and F-ratio of intergroup (four different species) and intragroup (males and females of all four species of grasshoppers) variances in metal concentrations Difference in metal concentrations between females and males of the same species of grasshoppers Hg Cd Pb ∗ a Ci Oc nsa ∗ ns ns ns ns ANOVA table for metal concentrations of four species of grasshoppers (n = 40, k = 4) Og Ch intergroup intragroup F-ratio ns * ns ns ns ns 0.2815 1.2148 16.266 0.011 0.731 10.992 25.453 (**) 1.728 (ns) 1.479 (ns) Levels of significance are indicated as: **p < 0.01, *p < 0.05. Not significant differences. B. Devkota, G.H. Schmidt / Agriculture, Ecosystems and Environment 78 (2000) 85–91 of Cd and Pb, such inter- and intragroup variations did not vary significantly and the variations between different species and within the species were same. 4. Discussion The concentration of heavy metals in the food plants and grasshoppers from the Taigetos mountains was proportional in the order Pb > Cd > Hg, with the same pattern of occurrence, both in producers and in herbivores. The concentrations of Cd, Cu, Pb and Zn in the larvae of four ephemeroptera species from a polluted stream were also proportional to the concentrations in water and sediment in the order Cd < Pb < Cu < Zn (Jop, 1991). Plants have a key function in the biotransformation of chemical elements from soil, water and air (Ernst, 1990), but green plants are unable to take up much mercury from contaminated soil (Lodenius, 1990). Rauter (1976) found only 4.6 g Hg kg−1 in grasses of an industrially contaminated area and its concentration in grasses of distantly located grassland of the Taigetos Mountains was still lower (0.284 g g−1 ). In grasshoppers, the accumulation factor was in the order Cd > Hg > Pb, where Cd was in significantly higher concentrations than Hg and Pb. This might indicate that different metals have different affinities leading to bioaccumulation in different organisms. Among these three elements, the concentration of Pb in grass was high (about 55 and 20 times higher than Hg and Cd, respectively), but it was comparatively low (10–49 times of Hg and only 2–6 times of Cd) in the grasshoppers. The higher bioaccumulation of Cd could be responsible for its higher toxicity, whereas the poor accumulation of Pb in the organisms could be one cause to its less toxicity. The difference in the accumulation behaviour towards Cd and Pb may be due to the opposite solubility properties and to the chemical similarities between Cd and the essential Zn (Roth-Holzapfel, 1990). Cadmium can replace the Zn in the enzyme carbonic anhydrase (Hopkin, 1989), changing the properties and activity of this enzyme. Jamil and Hussain (1992) studied the transfer of heavy metals through water — aquatic plants — aquatic insect system using the plant Eichhornia crassipes Solms. and its specific feeder Neochetina eichhorniae. The study showed the biotransfer of 89 metals by a simple food chain model representing the transfer of metals from polluted waters to insects via aquatic plants. Clark (1992) measured the concentrations of organochlorine compounds and heavy metals in the 17-year cicada to determine the possible food chain hazards to birds. This homopteran contained metal concentrations similar to or less than other local invertebrates. Roth-Holzapfel (1990) could not find an enrichment of elements, except Cd and Ni, with increasing trophic level. Also during the present study, Cd was found to be enriched in the grasshoppers, but the concentration of Hg in all four species of grasshoppers was lower than Cd. Mukherjee and Nuorteva (1994) likewise reported lower concentrations of Hg than Cd in bark beetles and ants from a forest surrounding the steel works in northern Finland. In the beetles and ants, the concentrations of these metals were near background levels. Copper and Zn, being essential for insect metabolism, are accumulated and Cd, due its chemical property related to Zn, is also accumulated (Roth-Holzapfel, 1990). Devkota and Schmidt (1992) after feeding Hg-, Cdand Pb-contaminated food to adult Aiolopus thalassinus (Fabr.) found very high concentrations of Cd in midgut, malpighian tubules, muscles, fat bodies and gonads of these grasshoppers, but concentration of Hg was high only in midgut and malpighian tubules (sites of absorption and excretion, respectively), and Pb was very low in these organs. With the growth of muscle tissues and fat bodies during post-embryonic development (nymph — adult) the concentration of Cd was found to be steadily increasing (Devkota, 1992). Herbivorous animals, like most short-horned grasshoppers, can magnify heavy metals in their bodies and may transfer them to higher trophic levels (Roberts et al., 1979). During the present study, it was found to be true only in the case of Cd. Being herbivorous (primary consumers), acridid grasshoppers accumulate heavy metals from food plants (producers) and also directly from the soil through the eggs laid there. Due to feeding and oviposition behaviour, the acridid grasshoppers are thus simultaneously exposed to toxic substances through different paths. The transport of Cd through the trophic level via acridid grasshoppers seemed to be more efficient than that of the other two heavy metals, Hg and Pb. According to Hunter et al. (1987), Cd and Cu are highly mobile in the invertebrate food web. Heliovaara (1990) also 90 B. Devkota, G.H. Schmidt / Agriculture, Ecosystems and Environment 78 (2000) 85–91 found a higher accumulation of Cd in the European pine sawfly Neodiprion sertifer (Hymenoptera; Diprionidae) than in pine needles, whereas the levels of Cu, Ni and Fe were higher in pine needles than in the insects. Because N. sertifer might be one of the most abundant forest insects, this might be an important pathway for these metals to higher trophic levels. Likewise, grasshoppers constitute significantly large amounts of the arthropod biomass of the grassland (Schmidt, 1986) and. thus, the biotransfer of geogenic heavy metals, especially Cd, via the grasshoppers to higher trophic levels may be very important. Insignificant differences in the metal concentrations between the females and the males of the same species of grasshoppers showed that both sexes could equally accumulate the heavy metals in their bodies and, for the purpose of biomonitoring, the preference to one sex of grasshopper might not be necessary. Significantly higher concentrations of Hg in both sexes of C.(G.) crassiceps than in those of other three grasshoppers showed that this species might serve better as test animal for the evaluation of Hg pollution. Significantly higher concentrations of Cd in both females and males of all four grasshopper species would suggest that any grasshopper irrespective of the sex could equally play the role of a bioindicator. 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