Time-delayed effect of petroleum-derived products in soil and their bioremediation on plant – herbivore interaction

Abstract

The aim of the study was to determine the time-delayed (after three years from the moment of soil pollution) effect of petroleum-derived products (PDPs) (petrol, diesel fuel and used engine oil) on the interaction between selected host plant (broad bean) and a herbivorous insect closely related to it (Sitona spp.). We assessed the condition of the plant exposed to pollutants (i.e. its growth and chemical composition), then we evaluated the attractiveness of the plant for both larvae and adults of the insect. The evaluation covered also the effect of bioremediation by using ZB-01 biopreparation. The results showed that after 3 years from soil contamination, engine oil and diesel fuel limited the feeding of adult sitona weevils while petrol caused increase in the attractiveness of plants for these insects. The PDPs negatively affected the growth of plants. The changes in element content depended on the type of pollutant. The biopreparation ZB-01 eliminated or reduced the differences caused by the presence of PDPs in the soil regarding the chemical composition of the host plant, and limited feeding by both the larvae and adult individuals of sitona weevils. The negative relationships between the contents of both some macroelements (Mg, S) and heavy metals (Zn, Ni), and feeding of imago of Sitona were observed. The obtained results indicate that PDPs remain for a long time in the environment and adversely affect not only the organisms directly exposed to the pollution – plants growing on polluted soil but also further links of the trophic chain, i.e. herbivores. List of abbreviations used at work: PDPs – petroleum-derived products EO – soil contaminated with engine oil, DF – soil contaminated with diesel fuel, P – soil contaminated with petrol, C – control soil, 0R – without bioremediation, R – with bioremediation ZB-01 – the name of the biopreparation used TPH – total petroleum hydrocarbons 72 M. Rusin, J. Gospodarek, A. Nagórska-Socha The effects of PDPs on the growth and development of plants and soil organisms exposed directly to the contact with pollutants are relatively well known (Pennings et al. 2014, Grifoni et al. 2020), but there is very scarce information about indirect effects of these compounds from polluted soil through plants to the subsequent links of trophic chain i.e. phytophagous insects. The results of studies on the impact of different oil concentrations on herbivory invertebrates (grass shrimp Palaemonete spugio and amphipods Gammarus mucronatus) of water plant (Ruppia maritima) suggest a significant and indirect influence of pollutants (Martin and Swenson 2018). Changes in the composition of the host plant due to oil-exposure affected the food preferences of herbivores as well as the amount of food they eat. However, no similar data are available on the effects of PDPs on terrestrial herbivores, which is the purpose of this experiment. Because of their diversity, easy collection and breeding, great fertility, and the short period of development, invertebrates are useful element for the determination of the effects of contamination on the environment. Our earlier research confirmed that PDPs have adverse effect on the developmental parameters in black bean aphid (Aphis fabae Scop.), resulting in the decrease of its fecundity, shortening of its average life span, and lowering of the population intrinsic growth rate (Rusin et al. 2017). Still, we do not know how PDPs could influence food preferences of herbivores and the amount of eaten food. Moreover, most of the available literature provide information on the effect of petroleum products on the natural environment immediately after the emergence of contamination or after a short time (Grifoni et al. 2020, Martin and Swenson 2018). The data on the subsequent (time-delayed) effects of the PDPs are still scarce. Especially rare are experiments involving realistic environmental conditions i.e., in the field (Sylvain et al. 2019). Finally, the effect of bioremediation on proposed soil-plant-herbivore system is still unrecognized. Sitona weevils (Sitona spp., Coleoptera, Curculionidae) are common herbivorous insects that feed on the Fabaceae family plants. They damage cotyledons still in the soil before they emerge on the ground surface. They gnaw out semicircular-shape feeds fragments on leaf edges, markedly reducing the assimilation surface of leaves, which is particularly harmful at the early stage of plant development. The larvae of the insect feed on root nodules, thus reducing the quantity of nitrogen fixed by plants, as well as disturbing their water management, which leads to deteriorated growth and development (Hanavan and Bosque-Pérez 2012). The broad bean (Vicia faba L.) has been already used as a model plant in studies on the effect of soil contaminants (including PDPs) on the growth and development of plants (Malallah et al. 1996). The aim of the study was to determine the time-delayed (i.e. after three years from contamination) effect of PDPs, such as petrol, diesel fuel, and spent engine oil on the interaction between host plant (broad bean) and a herbivore insect closely related to it (Sitona spp.). The effect of PDPs on the growth of broad bean and on the content of selected nutrients in plant organs was also investigated. Furthermore, the effects of the bioremediation process (by adding biopreparation ZB-01) on the abovementioned features were also determined. ZB-01 biopreparation is a microbial preparation which has been widely used to initiate and stimulate biodegradation of petroleum-derived substances in contaminated waters and soils. We chose it because its usefulness in decomposition of petroleum-derived contaminants has been already confirmed by many studies (Petryszak et al. 2008, Kaszycki et al. 2010, Kaszycki et al. 2011, Kaszycki et al. 2015). Finally, we analyzed the relationships between Sitona spp. feeding, soil contamination with PDPs, and broad bean chemical composition (macroelements and heavy metals). By this new multi-trophic approach we sought to determine whether soil contamination by PDPs may affect organisms indirectly exposed to pollution and the same way further links of the food chain, as well as evaluate the usefulness of bioremediation initiated by especially prepared microbial biopreparation in restoring balance in the soil-plant-herbivore system. Materials and methods Experimental setup The field experiment was conducted in 2013 at the Experimental Station of the University of Agriculture in Krakow, situated in Mydlniki near Krakow (Poland; 50.0815°N, 19.84730°E). In November 2009, indigenous soil (loamy sand; pH(KCl) = 6.45; pH(H2O) = 7.12; Carbon total = 10.4 g kg -1; nitrogen = 0.90 g kg-1; C:N = 11.6; CaCO3 = 1.7 g kg -1; available phosphorus = 7.14 mg 100 g-1; available magnesium = 5.64 mg 100 g-1; available potassium = 14.25 mg 100 g-1) was placed in 32 special containers of 1 m3 volume (1 m × 1 m × 1 m), retaining the natural arrangement of layers. We used plastic containers certified for the storage of such substances as oils, petroleum products and solvents. The containers were double-bottomed. The upper bottom, propped on supports, was perforated to enable the possible effluence of water (with possible contaminants). Before filling them with soil, the containers were additionally lined with a nonwoven geotextile to prevent soil leakage through the bottom perforation. A tank was installed on the side of each container below its bottom (connected with the container bottom) to collect possible effluent from the soil inside the container. The tank was provided with a plastic duct running towards the surface, which enabled excess water to be pumped out. This procedure was adopted to avoid environmental pollution with effluents from the contaminated soil. All containers were also supplied with perforated plastic tubes (placed at approx. 30 cm distances, 4 per container) to provide adequate soil aeration in a gravity system, which is a prerequisite for bioremediation to proceed correctly. The containers were sunk in the ground so that their upper edge was at the same level as the surface of the soil. The soil in the containers was left for eight months without any intervention in order to regain its natural biological functions. In June 2010, the soil surface was artificially contaminated with petrol (BP Unleaded 95) (P), spent engine oil (PLATINUM Classic Semisynthetic 10W-40, used for one year in a petrol engine) (EO), and diesel fuel (BP Diesel Fuel) (DF) in a quantity of 6000 mg of each PDP per 1 kg of dry mass, by pouring it on the soil. The PDPs were used separately. After one week, and then after one year starting from the moment of contamination by PDPs, half of the number of containers were subjected to the bioremediation process by adding biopreparation ZB-01. ZB-01 was specially produced for this experiment in Biochemistry Department of the University of Agriculture Time-delayed effect of petroleum-derived products in soil and their bioremediation on plant – herbivore interaction 73 in Kraków and contained selected prokaryotic organisms (Stenotrophomonas, Pseudomonas, Moraxella, Acinetobacter, Alcaligenes, Ochrobactrum, Comamonas, Burkholderia, Corynebacterium, and Oligella), which were isolated over years from sites heavily polluted with organic compounds (Kaszycki et al. 2001). The activity of this biopreparation in degradation of petroleum contaminants was confirmed also by our earlier investigations (Gospodarek et al. 2016). The treatment was performed by sprinkling, while maintaining 60% sorption moisture of the soil. Before the ZB-01 application, the soil surface in the containers intended for this treatment was treated with a compound fertilizer (Azofoska; 13.6% N, 2.8% P and 15.8% K) at a dose of 100 g per container. The noncontaminated soil, placed in identical containers, constituted the control treatment. ZB-01 contains strains of bacteria naturally occurring in the environm