Study of the effect of cypermethrin on the spider Polybetes phytagoricus in different energy states
Graphical abstract
Introduction
At present the use of pyrethroids is worldwide justified, since these xenobiotics have many desirable properties that include high toxicity for target insects, low toxicity for mammals, high biodegradability, photostability and effect on minimum doses (Baatrup and Bayley, 1993; Stenersen, 2007).
Pyrethroid insecticides are neurotoxic compounds that affect not only the peripheral nervous system but also the central one of insects. They act on the voltage-gate sodium channels placed in nervous cell membranes. When the opening of these channels is prolonged, pyrethroids stimulate nervous cells to produce repetitive discharges thus provoking paralysis and death of insects (Ray and Fry, 2006; García et al., 2011; Clark and Symington, 2012; Kaisarevic et al., 2019).
Cypermethrin (IUPAC name: [cyano-(3-phenoxyphenyl)methyl] 3-(2,2-dichloroethenyl)-2,2-dimethylcyclopropane-1-carboxylate) is an insecticide of the pyrethroid class type II, synthetic, fast action (Santos et al., 2007), used extensively to control both a wide range of agricultural and horticultural insects. It has a broad action range against external parasites of animals and humans. Also, pyrethroids are commonly used in urban environments to control undesirable pests such as spiders and termites (Fernandez et al., 2012; Weston and Lydy, 2012; Weston et al., 2015; Maruya et al., 2016).
Most of the studied related to this topic analyses the undesirable ecotoxicological effects of the use of pesticides on vertebrates, but there is a great proportion of non-target invertebrate organisms that are affected, for instance, arthropods and particularly arachnids. The ecotoxicology of spiders has received rather limited attention (Babczyńska et al., 2006; Pekár, 2012).
Spiders are important regulators of insect populations, due to their quantity (they constitute the most numerous and important order of the Class Arachnida) and their biodiversity (they are distributed virtually in all the terrestrial habitats), inhabiting even in strongly changed ecosystems (Nentwig, 1986; Majkus, 1988.; Nyffeler, 1999). They are capable of consuming until 50% of the insect biomass present in crops, with a prevailing role in the biological control of the species damaging crops of economic importance (Riechert and Lockley, 1984; Oraze and Grigarick, 1989; Tarabaev and Sheykin, 1990; Riechert, 1999; Birkhofer et al., 2008). And also, they are widely distributed in all kinds of crops (Riechert and Lockley, 1984).
Spiders as generalist predators which are exposed to elevated level of environmental insecticide (Pekár, 2012). Spiders were the most abundant beneficial arthropod (Loch, 2005). It has been recently estimated of 400 specimens of arthropods, the spiders have the most biomass consumption from bod length by dry weight (Straus and Aviles, 2018).
Undernourishment or malnutrition of spiders in croplands seems to be frequent, since insecticide application significantly reduces prey availability and places for web locations (Vickerman and Sunderland, 1977; Pedersen et al., 2002; Pekár, 2012). Studies on diverse insects have demonstrated a dependence between insecticide tolerance and food levels and diet composition (Kramer et al., 1990; Singh and Sarup, 1991; Kalushkov, 1999). In the spider Pardosa prativaga it has been observed that the effect of insecticides can vary in relation to the nutritional history of the animal (Pedersen et al., 2002).
The entry pathways of cypermethrin spiders in the field can be performed by contact or by food (insects mainly). The concern about the impact of pesticides on spiders surpasses the effect of insecticides, since it is extended to not only acaricides but also fungicides and herbicides. Also, it has been demonstrated that glyphosate herbicide affects spiders (Haughton et al., 1999; Haughton et al., 2001a; Haughton et al., 2001b; Benamú et al., 2010). In general, the scientific community is in accordance with the fact that biological control is a pathway to minimize the contamination generated by the indiscriminate use of pesticides. Among others it possesses the advantages of: having scarce or non-existent resistance of the plagues to the biological control, avoiding secondary pests, the lack of intoxication problems, the favourable condition of the cost-benefit relationship. Many efforts are being carried out to preserve the different natural enemies of pest insects, spiders being among them (Liao et al., 2016; Rathod et al., 2016; Rauch et al., 2017).
The concern about this topic is increasing since some reports have comparatively analyzed the toxicity of insecticides on pest insects and natural enemies (Croft and Whalon, 1982). In 2015 Li and collaborators observed that cypermethrin among other insecticides affected the natural enemy (wolf spider) in a greater extent than target insects (Li et al., 2015).
Pesticides can cause various metabolic effects, including increased endogenous production of reactive oxygen species (ROS) (Masoud et al., 2003; Wilczek et al., 2013). Tolerance to this metabolic imbalance is possible due to the antioxidant defense system that includes, among other enzymes, superoxide dismutase (SOD, EC1.15.1.1), catalase (CAT, EC1.11.1.6) glutathione-s-transferase (GST, EC2.5.1.18) and glutathione reductase (GR, EC1.8.1.7) (Nielsen et al., 1999; Wilczek et al., 2013).
Because the response to insecticides depends on the metabolic and nutritional state of the organism (Nielsen and Toft, 2000; Pedersen et al., 2002), and that this nutritional state may vary in relation to age, sex, or reproductive status (Romero et al., 2018, Romero et al., 2019), the aim of this study was to analyse the effect of the insecticide cypermethrin on the different physiological/metabolic stages on the spider.
We analyzed comparatively the enzymes related to the antioxidant defense system of the spider Polybetes pythagoricus (Sparassidae): superoxide dismutase, catalase, glutathione-s-transferase and glutathione reductase as well as MDA levels, and AChE inhibition. The choice of P. pythagoricus was based on the fact that there is a great deal of information with relation to its biochemistry (Cunningham et al., 2007; Laino et al., 2009, Laino et al., 2011) and that it is a large species and could be analyzed more easily. The purpose of the present study was to obtain essential data to support an overall understanding of the effects of cypermethrin on non-target organisms such as spiders and to provide useful information on the potential ecological risks of cypermethrin for agricultural ecosystems.
Section snippets
Specimen collection and maintenance
The species P. pythagoricus used for the experiments is not protected or endangered.
In order to observe the changes occurred in spider maturation, young and adults were comparatively analyzed. To observe sex-associated changes males and pre-vitellogenic females were examined, and to compare changes in the vitellogenesis, pre-vitellogenic and post-vitellogenic females were used.
Adults and young of the spider P. pythagoricus were collected from Eucalyptus sp. trees in an area free of contaminants
Lipid and glycogen
In Table 1 it can be observed that glycogen calories/g wet weight was 0.16 +/− 0.06 in young, 0.36 +/− 0.013 for post-vitellogenic females, 1.4 +/− 0.032 for males, and 3.1 +/− 0.17 in pre-vitellogenic females. Energetic lipid calories/g wet weight was 22 +/− 3 for post-vitellogenic females, approximately 33 +/− 3 for pre-vitellogenetic females and males, and 56 ±5 for young. Lipid mobilization measured as the triacylglycerides/free fatty acids relationship was 0.7, 1.3, 2.6 and 3.5 for young,
Discussion
The caloric content is a parameter used to be able to estimate the energetic/metabolic state of invertebrates, among them, different arthropods (Heras et al., 2000; García-Guerrero et al., 2003). In spiders it was mainly employed in relation to reproduction and development (Laino et al., 2013; Ruhland et al., 2016; Trabalon et al., 2017). For the case of spiders just like in most of arthropods (Kanazawa and Koshio, 1994; Arrese et al., 2001; Canavoso et al., 2004; Laino et al., 2009), the major
Acknowledgments
This work was supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (PICT-2017- 0684) and UNLP Argentina. L. A. and G. F. are members of CONICET, Argentina. The authors are grateful to Rosana del Cid for the revision of the English, Mario Ramos the figure design. Capture permits were No 117/16 Protected Areas, Province of Buenos Aires.
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