Synergistic effects of glyphosate formulation herbicide and tank-mixing adjuvants on Pardosa spiders

Higtlights

• Pardosa foraging behavior studied after agronomical supermixtures treatments.

• Short- and long-term predatory activity after treatments recorded.

• Supermixtures and surfactants significantly affected short-term predatory activity.

• Glyphosate herbicide alone did not have the effect on predatory activity.

• Agrochemicals in tank mixes have unexpected properties.

Abstract

Glyphosate-based herbicides are the world’s most consumed agrochemicals, and they are commonly used in various agroecosystems, including forests, as well as in urban zones and gardens. These herbicides are sold as formulations containing adjuvants. Other tank-mixing adjuvants (most often surfactants) are commonly added to these formulations prior to application. According to the manufacturers of agrochemicals, such tank mixes (as these are known in agronomic and horticultural practice) have modified properties and perform better than do the herbicides as used alone. The effects of these tank mixes on the environment and on beneficial arthropods are almost unknown. Therefore, we studied whether a herbicide formulation mixed with adjuvant has modified effects on one of the most common genera of ground-dwelling wolf spiders vis-à-vis the herbicide formulation and adjuvants themselves. Specifically, we studied the synergistic effect in the laboratory on the predatory activity (represented by the number of killed flies) of wolf spiders in the genus Pardosa after direct treatment using the glyphosate-based herbicide formulation Roundup klasik Pro^®, Roundup klasik Pro^® in a mixture with the surfactant Wetcit^®, Roundup klasik Pro^® in a mixture with the surfactant Agrovital^®, and the surfactants alone. We found that pure surfactants as well as herbicide-and-surfactants tank mixes significantly decrease the predatory activity of Pardosa spiders in the short term even as Roundup klasik Pro^® did not itself have any such effect. Our results support the hypothesis that plant protection tank mixes may have modified effect on beneficial arthropods as compared to herbicide formulations alone. Therefore, testing of pesticide tank mixes is highly important, because it is these tank mixes that are actually applied to the environment.

Introduction

Agroecosystems, but also ecosystems of gardens, parks, and urban greenery, are inhabited by numerous beneficial arthropods that are useful in terms of the valuable ecosystem services and biodiversity they provide (Miller, 2008, Pekár and Kocourek, 2004). Agrochemicals in the environment have many direct negative effects and can seriously affect beneficial invertebrate organisms such as predators (Biondi et al., 2012, Desneux et al., 2007, Galvan et al., 2006, Niedobová et al., 2016). Increasing evidence suggests that pest suppression can be weakened by plant protection products having lethal but also sublethal effects on spiders (Benamú et al., 2010, Benamú et al., 2013, Brown et al., 2015, Evans et al., 2010, Korenko et al., 2016, Niedobová et al., 2016, Niedobová et al., 2018). Reduced foraging behavior, changes in fecundity, and changes in mobility are examples of sublethal effects that have been found in spiders after agrochemical exposure (Brown et al., 2015, Benamú et al., 2013, Everts et al., 1991, Niedobová et al., 2016, Niedobová et al., 2018). Predatory activity, which is connected with foraging behavior in spiders, may be a very important feature of the food web and consequently a driver of population and community dynamics, and so contact with agrochemicals could shift these very important food web linkages within the environment.

The world’s best-selling agrochemicals are glyphosate-based herbicides. Since the late 1970s, glyphosate consumption has increased approximately 100-fold (Myers et al., 2016). Glyphosate is the active ingredient contained in more than 750 different products used in numerous agroecosystems as well as for urban and home application (Guyton et al., 2015). These products are also commonly used as desiccants due to their ability to accelerate harvest of soybeans and other oil seed crops, dry edible beans, wheat, barley, and many other crops (Bennet and Shaw, 2000, Blackburn and Boutin, 2003, Gottrup et al., 1975, McNaughton et al., 2015, Mitsis et al., 2011, Whigham and Stoller, 1979). Over the past decade, 6.1 billion kilograms of glyphosate have been applied to agroecosystems, and their global consumption continues to grow (Benbrook, 2016). Changes in foraging behavior after exposure to glyphosate-based herbicide formulation in spiders have been reported by Behrend and Rypstra, 2018, Benamú et al., 2010, Korenko et al., 2016, and Rittman et al. (2013).

Glyphosate herbicides are sold as formulations. Pesticide formulations generally contain active ingredients, which are toxicologically tested (Desneux et al., 2007), as well as specific additives, which are classified as inert and their specification is a trade secret (Mesnage et al., 2014, Surgan et al., 2010). Adjuvants are among the very important such additives, and large proportions of them are commonly included into plant protection products (Cox and Surgan, 2006). These materials enhance the activity or other properties of a pesticide mixture (Holland, 1996). The consumption of agronomic adjuvants is increasing. It has been projected that the agricultural adjuvants market has been expanding at a compound annual growth rate of 5.6% in recent years and that it will reach the value of $3.18 billion by 2019 (MarketsAndMarketscom, 2015). Neither toxicological evaluation nor authorization is required for adjuvants (Commission Regulation (EC) No 1107/2009), although it has been found that they can have lethal effect on various organisms, including beneficial arthropods (Cowles et al., 2000, Druart et al., 2010, Goodwin and McBrydie, 2000, Sims and Appel, 2007). Only very rarely have surfactants and their sublethal effects on beneficial arthropods been studied. Niedobová et al. (2016) did, however, find that agronomic surfactants significantly affected short-term predatory activity of Pardosa agrestis (Westring, 1861) spiders.

Although in the past glyphosate herbicides have been described as minimally harmful to the environment (Baylis, 2000, Lundgren et al., 2009, Howe et al., 2004), in 2015 the World Health Organization’s International Agency for Research on Cancer classified glyphosate as “probably carcinogenic to humans” (Guyton et al., 2015). Numerous studies have shown glyphosate-based herbicide formulations to be harmful to human cells and to rat liver cells, and adjuvants have been found to be the cause of toxicity (Mesnage et al., 2013, Mesnage et al., 2015, Peixoto, 2005). These findings are very serious, because agronomic adjuvants are also offered separately for tank mixing. Most commonly these adjuvants are surfactants and are mixed with the formulated product and water in the sprayer tank before field application (Hochberg, 1996, Leaper and Holloway, 2000). This procedure produces chemical tank mixes with completely unknown effects on beneficial arthropods, the terrestrial environment, and human health. Although Cedergreen (2014) reviewed the cocktail effect and synergistic interactions within the environment of chemicals in mixtures, studies dealing with mixtures of formulated pesticides and adjuvants are still lacking, despite the frequent use of such mixtures. It is very important, therefore, to determine the real effect of the pesticide tank mixes actually applied and to identify which compounds of tank mixes or their combinations could negatively affect the ecosystem services provided by beneficial arthropods. These ecosystem services have been valued at several billion dollars annually in the United States alone (Wyckhuys et al., 2013). Because such natural enemies as predators and parasitoids are able significantly to suppress pest populations, they are today valued components of pest management programs that are directed to agricultural sustainability (Barzman et al., 2015, Furlong and Zalucki, 2010).

Spiders are ideal model organisms for testing the effects of agrochemicals on beneficial arthropods. Ground-dwelling spiders, and in particular wolf spiders (Lycosidae), are the most ubiquitous generalist predators in the temperate zone (Wise, 1993). Their prey spectrum consists of species at different trophic levels, including herbivore pest species, and therefore they are able to reduce pest populations significantly (Birkhofer et al., 2008, Kuusk et al., 2008, Oelbermann et al., 2008, Oelbermann and Scheu, 2009, Wise, 1993). To our knowledge, agrochemical mixtures of herbicide and surfactant have been studied only once, the result being that such mixture was shown to be lethal to theridiid spiders (Evans et al., 2010). The lack of evidence about tank mixtures of herbicide and surfactant is surprising, because agrochemical mixtures are commonly applied to field and forest agroecosystems, as well as to urban parks and gardens.

Because predatory activity in spiders is directly connected with pest suppression, our research was directed to studying prey capture efficiency and its changes over time in lycosid spiders of the genus Pardosa after direct exposure to the glyphosate formulation Roundup klasik Pro^®, to Roundup klasik Pro^® in a mixture with the surfactant Wetcit^®, to Roundup klasik Pro^® in a mixture with the surfactant Agrovital^®, and to the surfactants alone. The impact of mere disturbance caused by agrochemicals can be sometimes comparable with lethal effect, because spiders cease attacking prey (e.g., Michalko and Košulič, 2015).