Triazine Herbicide and NPK Fertilizer Exposure: Accumulation of Heavy Metals and Rare Earth Elements, Effects on Cuticle Melanization, and Immunocompetence in the Model Species Tenebrio molitor

Abstract

The increasing use of agrochemicals, including fertilizers and herbicides, has led to worrying metal contamination of soils and waters and raises serious questions about the effects of their transfer to different levels of the trophic web. Accumulation and biomagnification of essential (K, Na, Mg, Zn, Ca), nonessential (Sr, Hg, Rb, Ba, Se, Cd, Cr, Pb, As), and rare earth elements (REEs) were investigated in newly emerged adults of Tenebrio molitor exposed to field-admitted concentrations of a metribuzin-based herbicide and an NPK blend fertilizer. Chemical analyses were performed using inductively coupled plasma tandem mass spectrometry (ICP-MS/MS) supported by unsupervised pattern recognition techniques. Physiological parameters such as cuticle melanization, cellular (circulating hemocytes), and humoral (phenoloxidase enzyme activity) immune responses and mass loss were tested as exposure markers in both sexes. The results showed that NPK fertilizer application is the main cause of REE accumulation in beetles over time, besides toxic elements (Sr, Hg, Cr, Rb, Ba, Ni, Al, V, U) also present in the herbicide-treated beetles. The biomagnification of Cu and Zn suggested a high potential for food web transfer in agroecosystems. Gender differences in element concentrations suggested that males and females differ in element uptake and excretion. Differences in phenotypic traits show that exposure affects metabolic pathways involving sequestration and detoxification during the transition phase from immature-to-mature beetles, triggering a redistribution of resources between sexual maturation and immune responses. Our findings highlight the importance of setting limits for metals and REEs in herbicides and fertilizers to avoid adverse effects on species that provide ecosystem services and contribute to soil health in agroecosystems.

Anatomical changes of Tenebrio molitor and Tribolium castaneum during complete metamorphosis

“…For these reasons, they are useful model species (Brai et al 2023 ; Brown et al 2009 ; Campbell et al 2022 ) for genetic (Suzuki et al 2008 ), physiological, immunological (Abdel-Latief and Hoffmann 2014 ; Park et al 2014 ; Vigneron et al 2019 ; Vommaro et al 2021 , b ), developmental, behavioural (Pai and Bernasconi 2008 ) and evolutionary (Pointer et al 2021 ) studies. In addition, both species are used to address the effects of pesticides (Kostaropoulos et al 2001 ; Pedersen et al 2020 ), applied to control populations infesting food commodities (Arthur et al 2019 ; Ntalli et al 2021 ; Tungjitwitayakul et al 2022 ), including insect resistance (Campbell et al 2022 ; Rösner et al 2020 ) and in terms of ecotoxicological effects (Naccarato et al 2023 ). Despite the great interest towards these species, the morphology of T. castaneum has been scarcely studied (Dönitz et al 2013 ; Vommaro et al 2023a ; Zohry and El-Sayed 2019 ) and the pupal stage has been completely neglected.…”

First Optimization of Tomato Pomace in Diets for Tenebrio molitor (L.) (Coleoptera: Tenebrionidae)

“…Therefore, dueto the quality and quantity of its macronutrients and the presence of carotenoids in TP, the use of an optimal diet based on this by-product can support the production of mealworms and its products (flour and oil), to be used both as foods [121][122][123] and as feed [124][125][126] with high nutritional value and positive effects on human and animal health [59,127]. Great attention must be paid to the origin and traceability of by-products used in diets to avoid accumulating and biomagnifying heavy metals in larvae [128].…”

Granulated Animal Feed and Fuel Based on Sea Buckthorn Agro-Waste Biomass for Sustainable Berry Production

“…The contents of the macroelements and heavy metals were determined by ICP-MS analysis using a Thermo Fisher Scientific iCAP TQe (Bremen, Germany) fitted with a nebulizer, a quartz spray chamber, with a sampling cone made of nickel, and a skimmer cone with platinum tip, as described in Naccarato et al [45]. A peristaltic pump and an autosampler ASX-560 (both from Thermo Fisher Scientific, GmbH, Bremen, Germany) were used to pump the solutions from the tubes.…”