Open access peer-reviewed chapter

Ecotoxicology of Glyphosate-Based Herbicides on Aquatic Environment

Written By

Bruno Bastos Gonçalves, Percilia Cardoso Giaquinto, Douglas dos Santos Silva, Carlos de Melo e Silva Neto, Amanda Alves de Lima, Adriano Antonio Brito Darosci, Jorge Laço Portinho, Wanessa Fernandes Carvalho and Thiago Lopes Rocha

Submitted: 10 June 2018 Reviewed: 12 February 2019 Published: 16 July 2019

DOI: 10.5772/intechopen.85157

From the Edited Volume

Biochemical Toxicology - Heavy Metals and Nanomaterials

Edited by Muharrem Ince, Olcay Kaplan Ince and Gabrijel Ondrasek

Chapter metrics overview

1,746 Chapter Downloads

View Full Metrics

Abstract

Glyphosate-based herbicides (GBHs) are chemicals developed to control unwanted plants such as weeds or algae. These chemicals act on EPSPS enzyme that blocks the production of tyrosine, phenylalanine, and tryptophan amino acids causing plant death. This biochemical pathway exists only in plant organisms. Despite the target use, GBHs have been related to toxic effects on nonplant organisms, such as invertebrates, fishes, amphibians, reptiles, birds, and mammals, including humans. This chapter is focused on ecotoxicological effects of GBHs on aquatic environment, showing a perspective of studies since this kind of product was developed until nowadays, an analysis of how many studies for each taxonomic group. Furthermore, we analyzed specifically the toxic effect of GBHs on each taxon, and finally, we discuss future perspectives and suggestions for a better regulation and application for this chemical.

Keywords

  • ecotoxicology
  • water quality
  • weed control
  • Roundup®
  • Monsanto

1. Introduction

Herbicides are chemical compounds used mostly to control weed (i.e., uncultivated) plants in agriculture and forestry and also for algae control [1, 2]. Herbicide formulations are designed to affect mainly plants, affecting specific plant biochemical pathways. However, it is common that this kind of pesticides affects nontarget organisms such animals, including aquatic organisms [3, 4].

The most used herbicide worldwide is glyphosate-based herbicide (GBH), such as Roundup® from Monsanto, and its usage has been increased [5] mainly due to the development of transgenic glyphosate-resistant crops [6]. Glyphosate (N-(phosphonomethyl) glycine (CAS no. 1071-83-6)) is a weak organic acid with a molecular weight of 169.09 M and has a half-life of 7–142 days in water and 76–240 in soil [6, 7]. Glyphosate has high solubility in water (10,000–15,700 mg L−1 at 25°C), and it readily dissolves and disperses in an aquatic environment.

Glyphosate affects a specific plant biochemical pathway, inhibiting the action of the enzyme 3-enolpyruvylshikimic acid 5-phosphate synthase (EPSPS) that is necessary for biosynthesis of amino acids such as phenylalanine, tyrosine, and tryptophan [8] (Figure 1). Animals do not have this biochemical pathway, and hypothetically, they would be safe from glyphosate. However, the use of glyphosate requires that some other compounds as surfactants are added to the commercial formulation to increase adhesion to the leaf surface and absorbance by plants, trespassing the waxy cuticle [6]. There are a variety of surfactants, but the most common used on glyphosate-based formulations has been polyethoxylated amine (POEA). This surfactant is known to be more toxic to animals then glyphosate itself [6, 9].

Figure 1.

Glyphosate action on the biochemical pathway of plants inhibiting 3-enolpyruvylshikimic acid 5-phosphate synthase (EPSPS) enzyme and production of essential amino acids as phenylalanine, tyrosine, and tryptophan, causing plant death.

As mentioned above, glyphosate per se has low toxicity when compared to its commercial formulation containing surfactants. However, those formulations are toxic to a large number of organisms due mainly to products added to the formulae. Many studies have reported tissue damages, DNA damages, enzyme inhibition such as acetylcholinesterase (AChE) and aromatase, endocrine disruption, development disruption causing malformations, and carcinogenesis caused by GBH in animals as fish, amphibians, and mammals, including humans [6, 10, 11, 12, 13, 14, 15, 16, 17].

In terrestrial animals, glyphosate reaches these organisms through direct application and contaminated food consumption. However, application of GBH in an aquatic environment is not so common when compared to terrestrial environments. Despite this, GBH can reach the aquatic environment through many ways. It can be applied directly on water bodies for algae control, although the opposite effect can be found, with proliferation of some species of algae due to the increase of phosphorus levels [18]. GBH can also reach the aquatic environment through leaching, run-off, and contaminated food source [6].

As mentioned, glyphosate has high solubility in an aquatic environment. Some studies say that 50% of glyphosate in natural waters dissipates by water flow and decomposition in a few days to 2 weeks [19, 20, 21]. Despite that, glyphosate binds to soil particles and solid surfaces [22], which makes its dissipation difficult. The by-products of glyphosate decomposition are sarcosine and aminomethylphosphonic acid (AMPA). The first one is known to be nontoxic [23] and the second one less or equally toxic for aquatic organisms than glyphosate [24, 25]. This substance has also a great solubility and dissipates in water in 7–14 days. POEA in natural environments degrades by microbial decomposition in 14 weeks and its half-life is estimated in 21–42 days [24].

Considering that glyphosate per se and the commercial formulations are widely used around the world, being the most popular herbicide, this chapter summarizes the available data from the literature on the ecotoxicity of glyphosate and its formulation compounds, as well as its degraded products, to aquatic organisms (aquatic plants, invertebrates, fish, reptiles, amphibians, and birds) and analyzes the worldwide politics about glyphosate use and environment safety.

Advertisement

2. Studies about glyphosate-based herbicides on the aquatic environment

One of the first studies that evaluated the effects of glyphosate and GBH in aquatic environments was performed by Folmar et al. [26]. According to Thomson’s ISI WoS (Institute for Scientific Information, Web of Science) database, using keywords as “glyphosate,” and “aquatic environment,” since 1979 to the present day, 233 papers have been published that evaluated the toxicological effects of glyphosate in aquatic environments (Figure 2). These papers addressed the toxic effects of glyphosate on various types of organisms. The invertebrate group was the most studied, with 52 published articles (21.3%), followed by fish with 51 (20.9%), amphibians 40 (16.4%), plant 31 (12.7%), and aquatic environment 30 (12.3%). The other groups were present in 40 published articles (16.4%) (Figure 3). For the investigated period and database, there were no papers which have evaluated the toxicological effects of glyphosate in aquatic mammals and birds. This scarcity of studies demonstrates the lack of knowledge on the risk of exposure of these groups in aquatic environments contaminated by glyphosate.

Figure 2.

Number of papers published per year. Black bars represent the number of papers published in each year. Grey bars represent the number of papers accumulated per year. (*) Papers published until August 2018.

Figure 3.

Number of papers per organism group. Black bars represent the number of papers on toxicological effects of glyphosate published for each aquatic organism groups. Asterisk indicates lack of studies evaluating the toxicological effects of glyphosate in aquatic mammals and birds.

2.1 Aquatic plants

Glyphosate in the aquatic environment causes the death of the macrophyte community, which serves as a microhabitat for zooplanktonic, phytoplanktonic, and periphytic communities, and this leads to top-down control of planktonic organisms, affecting refuge and feeding to fish [27], triggering a chain effect. Studies have evaluated the effects of glyphosate on aquatic lentils (Lemna gibba) [28] (Table 1), showing that larval mortality of tadpoles was caused by predation without their micro-habitats in the absence of macrophytes, due to contamination of water body by glyphosate.

SpeciesGroupChemicalGlyphosate concentration (μg L−1)EffectReference
Amphora venetaCatenulaceaeRoundup®8456Increases mortality[36]
Anabaena sp.NostocaceaeGly. (acid)0.1–8.8 mMIncreases growth[28]
Arthrospira fusiformisPhormidiaceaeGly. (acid)0.005–0.048 mMIncreases growth[2]
Chlorella vulgarisChlorellaceaeGly. (acid)293,000Chlorophyll fluorescence/decreases PP[35]
Gomphonema parvulumNaviculaceaeRoundup®1000–10,000Increases mortality[30]
Halophila ovalisHydrocharitaceaeDCMU Gly. (acid)11,600Decreases chlorophyll fluorescence[31]
Roundup®[30]
Lemna gibbaLemnaceaeRoundup®2800Increases growth[2]
Gly. (acid) Roundup®46,900Increases growth[29]
Leptolyngbya boryanaLeptolyngbyaceaeGly. (acid)0.003–0.02 mMIncreases growth[2]
Ludwigia peploidesOnagraceaeGly. (acid)4000 and 108,000Bioaccumulation[2]
Microcystis aeruginosaMicrocystaceaeGly. (acid)3–37Increases growth and toxin production[28]
[18]
Gly. (acid)15,000Increases growth and toxin production[2]
Myriophyllum aquaticumHaloragaceaeGly. (acid) Roundup®840Decreases root[30]
Gly. (n.c.)220Chlorophyll fluorescence[33]
Myriophyllum spicatumHaloragaceaeRodeo®1000Increases growth[34]
Nostoc punctiformeNostocaceaeGly. (acid)>50 mMIncreases growth[2]
Scenedesmus quadricaudaChlorophyceaeGly. (acid)200,000Chlorophyll fluorescence/decreases primary productivity (PP)[2]
Spirulina platensisNostocaceaeGly. (acid)0.005–0.02 mMIncreases growth[2]

Table 1.

Ecotoxicity of glyphosate-based herbicide (GBH) to aquatic plants worldwide.

Dörr [18] studied the effect of glyphosate on the growth and production of secondary metabolites by toxigenic strains of the cyanobacteria Microcystis aeruginosa and Cylindrospermopsis raciborskii. The author assessed the influence of different concentrations of glyphosate on the growth and production of these cyanobacteria and observed that toxin production and growth increased at 15 mg L−1. When exposed to 20 mg L−1, their growths and toxin production increased as well, while concentration above 20 mg L−1 prevented their growth. The species C. raciborskii was more resistant to GBH, and this species uses the metabolite AMPA as a source of nitrogen for its growth. Considering that microalgae and cyanobacteria are the principal primary producers in aquatic ecosystems, use of the herbicide can stimulate the growth and production of toxins of certain groups. This affects water quality and modifies the functionality of the ecosystem of interest.

The effects of herbicides on nontarget aquatic plants are emerging as a major conservation issue in aquatic biodiversity [29]. Ludwigia peploides, an aquatic macrophyte, showed that glyphosate bioaccumulates in water surface and can, therefore, be used as a biomonitoring organism to evaluate glyphosate levels in freshwater. This is because it increases the concentration of the herbicide in the leaf, facilitating its detection in the biological matrix instead of the water. In the study, surface water and sediment samples were collected at the same time to measure glyphosate and calculate both the bioconcentration factors (BCFs) and biota-sediment accumulation factors (BSAFs). Glyphosate was detected in 94.11% in the leaves, presenting concentrations between 4 and 108 mg kg−1. In surface waters and sediments, it was detected in 75 and 100% of the samples at concentrations ranging from 0 to 1.7 mg L−1 and 5 and 10.50 mg kg−1 of dry weight, respectively. The mean BCF and BSAFs were 88.10 and 7.61 L kg−1, respectively. These results indicate that L. peploides bioaccumulates glyphosate that is mainly bioavailable in surface waters. Thus, since the plant accumulates the herbicide, the high concentrations in the organisms are evidence of the trophic levels that will feed or interact with the plant [28]. The researchers also observed that only 0.5 mg L−1 glyphosate was sufficient to inhibit the growth of Lemna gibba, change its shape, and lower chlorophyll content, decreasing its photosynthetic rate and consequently its metabolism.

Another important community in aquatic ecosystems that is also affected by the use of glyphosate is the periphyton. In terms of primary production, the periphyton has a photosynthetic contribution 77% higher than that of phytoplankton [30]. Among the most common and potentially toxic outcrossing cyanobacteria, M. aeruginosa uses glyphosate as a source of phosphorus, growing uncontrollably and causing eutrophication of the aquatic ecosystem that modifies ecological conditions. As shown by Forlani and collaborators [31], there is a tolerance to glyphosate by cyanobacteria Spirulina platensis, Nostoc punctiforme, Arthrospira fusiformis, Anabaena sp., and Leptolyngbya boryana, and four of them were able to use phosphorus as the only source. Anabaena sp. presented the highest toxicity (C = 50 mg L−1). Vera and collaborators [32] observed that the interaction of the periphyton with other communities and also with the abiotic environment was low when the mesocosms were treated with glyphosate, presenting an imbalance in the trophic webs of the ecosystem.

The exposure to GBH reduced 78% of the primary productivity of phytoplankton when used at low concentrations (0.125 mg L−1) [33] and at high concentrations (3.8 mg L−1) [34], causing a disturbance in the trophic levels. In freshwater systems, glyphosate at high levels stimulated eutrophication by increasing total phosphorus and favoring the growth of cyanobacteria on the periphyton, which altered the typology of the study ecosystem that was a mesocosm [32].

Species-based differences in sensitivity to GBH exposure may lead to decreased richness and abundance of ecosystem species [34]. Even though herbicides are thought to kill terrestrial plants, it can have an even more devastating effect in water, due to the imbalance that causes mortality of algae and aquatic plants. This causes an increase in decomposing organic matter in the water, which will reduce the concentrations of dissolved oxygen in the system and increase the stress of aquatic communities [35]. Thus, algae and aquatic plants are considered as nontarget organisms that are sensitive to the effects of glyphosate, and the damage to the balance of the aquatic environment is of concern. The damage of glyphosate on the aquatic plant community ranges from the death of the plant itself to the reduction of environmental heterogeneity promoted by the local plants. Consequently, this leads to the death of other aquatic species, causing an imbalance in the ecosystem.

2.2 Aquatic invertebrates

One of the pioneer studies of the effects of GBH on invertebrate organisms was carried out by Tsui and Chu [9] that studied the effects of this chemical on Ceriodaphnia dubia and Acartia tonsa, both crustaceans, in addition to other organisms such as algae, bacteria, and protozoans. They found the toxicity of this pesticide to these organisms and the most sensible was A. tonsa with a LC50 of 1.77 mg L−1. There is a high variability of sensibility of invertebrate organisms to GBHs (Table 2).

SpeciesChemicalExposure time (h)LC50 (μg L−1)Reference
Acartia tonsaRoundup®481770 (1330–2340)[38]
Burnupia stenochoriasRoundup®964304 (2121–7902)[44]
Caridina niloticaRoundup®962842 (2524–3190)[44]
Ceriodaphnia dubiaRoundup®485390 (4810–6050)[38]
Eskoba®, Panzer Gold®, Roundup Ultramax®, Sulfosato Touchdown®48250–16,770[45]
Chironomus plumosusRoundup®, POEAE, Glyphosate acid9618,000 (9400–32,000)[46]
Chironomus ripariusRodeo®, X-77 Spreader®, ChemTrol®481,216,000 (996,000–1,566,000)[47]
Daphnia magnaEskoba®, Panzer Gold®, Roundup Ultramax®, Sulfosato Touchdown®482670–15,430[45]
Roundup®, POEAE, Glyphosate acid483000 (2600–3400)[46]
Eskoba®, Sulfosato Touchdown®481620–31,410[48]
Rodeo®, X-77 Spreader®, ChemTrol®48218,000 (150,000–287,000)[47]
Daphnia pulexRoundup®96657 (472–914)[44]
Gammarus pseudolimnaeusRoundup®, POEAE, Glyphosate acid4862,000 (40,000–98,000)[46]
Roundup®, POEAE, Glyphosate acid9643,000 (28,000–66,000)[46]
Roundup®96340,000[49]
Hyalella aztecaRodeo®, X-77 Spreader®, ChemTrol®96720,000 (399,000–1,076,000)[47]
Laeonereis acutaRoundup®968199 (6690–9580)[50]
Nephelopsis obscuraRodeo®, X-77 Spreader®, ChemTrol®961,177,000 (941,000–1,415,000)[47]
Notodiaptomus coniferEskoba®, Sulfosato Touchdown®481220–1,282,000[48]
Ruditapes decussatusRoundup®14402200[51]
Tanytarsus flumineusRoundup®9612,240 (9454–22,360[44]
Utterbackia imbecillisRoundup®2418.3 ± 12.9[52]

Table 2.

Ecotoxicity of glyphosate-based herbicide (GBH) to aquatic invertebrates, exposure time, LC50 value (lower-upper values), and reference.

Specifically about microinvertebrates (<35 μm), these organisms persist within resting eggs (or egg banks) in lake sediments [36]. They represent a major source of regenerative potential in lake ecosystems near agricultural areas, and play a key role in influencing the active population and community dynamics, seasonal succession, biogeographic patterns, and the evolution of populations [36, 37]. Despite the widely accepted importance of resting egg banks in the ecology of aquatic micro-invertebrates’ communities, recently, experimental studies have demonstrated that the extensive and inappropriate use of commercial GBH, associated with agricultural activities, may impair the hatching of resting eggs in the sediment of lakes [38, 39]. Gutierrez and collaborators [38] indicated that the GBHs (Sulfosato Touchdown®) affect the hatching dynamics of micro-invertebrates, and selectively alter the species richness and abundance of community hatched from lake sediment. Portinho and associates [39] extended these findings and indicated that commercial herbicides as Roundup® (a.i. glyphosate) separate or in combination with 2,4-dichlorophenoxyacetic acid (2,4-D) have the potential to suppress emergences of micro-invertebrates from resting egg banks from lake sediments.

The environmental implication of this scenario suggests that changes in micro-invertebrates’ structure and composition induced by herbicides will occur, causing not only negative impacts on the process of recolonization from resting egg banks but also shifts in community composition. Recent attempts to develop guidelines for protecting aquatic organisms have focused on emergence from resting egg banks within the context of an ecological community [40], with potential implications for studies related to environmental risk to, and integrity assessment of, aquatic ecosystems.

2.3 Fish

Fish species are particularly vulnerable to GBH and their susceptibility depends on the commercial formulation, fish species, fish developmental stages, and exposure conditions, such as concentrations, exposure time, and route of exposure. Furthermore, gender-specific response of fish to GBH has been indicated in guppy P. reticulata exposed to glyphosate (50–73.2 mg L−1) and their metabolite AMPA (86.8–180 mg L−1) for 96 h [25], indicating the need for further studies about the molecular mechanisms of gender-specific effects.

In general, the surfactant and the commercial formulation showed higher toxicity to fish when compared to active ingredient (glyphosate pure) and their metabolite (AMPA). The 50% lethal concentration (i.e., LC50) of GBHs for fish has high variability, ranging from 1000 to 9750 μg L−1 [6, 41]. Chandrasekera and Weeratunga [42] found a LC50 of 976 μg L−1 for 48 h of exposure in fries of P. reticulata, while Sadeghi and Hedayati [43] found a LC50 = 12,640 μg L−1 in adults for a 41% commercial formulation and Souza-Filho and collaborators [44] found 4212 μg L−1 for 48 h.

Glyphosate and formulation compounds can be taken by fish via gills and digestive tract through ingestion of contaminated food or water [6, 45]. Once inside the organisms, glyphosate is absorbed and distributed to the whole body through blood circuit, reaching several tissues. GBHs can affect fishes in different ways, affecting many organs and as well molecular levels. In liver, vacuolization process was reported in hepatocytes and nuclear pyknoses; in kidney, studies report Bowman capsule dilatation and accumulation of hyaline drops in tubular cells; and in gills, glyphosate causes hyperplasia, lamellar fusion and aneurism [46, 47, 48, 49, 50]. Besides that, Langiano and Martinez [49] showed activation of the stress axis, with increased blood glucose levels. Souza-Filho and collaborators [44] also showed genotoxic effects in fish cells. Concerning to enzymes, Sandrini and collaborators [17] showed that glyphosate impairs acetylcholinesterase activity in synapses, preventing detaching of acetylcholine from receptors, impairing electric transmission by neurons. This can impair muscle contraction and information transmittance. GBH in sub-lethal levels can also impair fish feeding behavior as shown by Giaquinto and collaborators [51]. Also, a recent in vitro study [52] showed that low concentrations of GBH, even those allowed by the USA, Canadian, and Brazilian laws (50 μg L−1) kill yellowtail tetra fish (Astyanax lacustris) sperm cells, compromising fish reproduction and natural population persistence.

OMIC technologies, such as proteomics, transcriptomics, and metabolomics, have been applied to investigate the molecular mechanisms and toxicity of GBHs on fish. For example, proteomics-based methods (two-dimensional gel electrophoresis associated with mass spectrometry and bioinformatics) were used to complement the knowledge about the ecotoxicity of GBH on P. reticulata [53, 54]. The female guppy exposed to GBH (1.82 mg L−1) for 24 h changed different cell processes in the gills (energy metabolism, regulation and maintenance of cytoskeleton, nucleic acid metabolism, and stress response) [53] and liver (cellular structure, motility and transport, energy metabolism, and apoptosis) [54], confirming tissue-specific responses at molecular levels.

2.4 Herpetofauna

The herpetofauna is composed of reptiles and amphibians, and due to the low mobility, physiological requirements, and habitat specificity, this group has become ideal models for environmental conservation studies [55]. Amphibians are sensitive to exposure to contaminants and are considered good bioindicators in monitoring water quality [56]. Characteristics such as permeable skin, reproduction, and larval stages dependent on the aquatic environment make anuran amphibians highly vulnerable to pesticide contamination [57]. Evidence suggests that anuran species decline is related to the intensive use of pesticides [58, 59, 60].

The decline of amphibian populations is related to the increase of environmental pollutants, the influence of climate change, habitat fragmentation, exposure to ultraviolet radiation, and human-induced environmental changes [61, 62]. Contamination of water bodies next to agricultural areas generally increases during the rainy season, that is, widely used to breed by most species of amphibians, and many species use temporary ponds and small streams adjacent to agricultural areas as part of their life cycle, harming the reproductive period and larval development [57, 58, 63]. During the rainy season, the agrochemical present in the soil are susceptible to be transported down the soil profiles and/or surfaces/underground water bodies and consequently affect the amphibian population [58] and other environmental (a) biotic elements [6, 64].

Herbicides may delay or inhibit the metamorphosis of amphibians directly impacting their reproduction [57]. According to Walker and collaborators [65], the main routes of herbicide absorption in anuran amphibians are through contaminated food ingestion and skin absorption of pollutants dissolved or suspended in water. After absorption, the substance is transported to different compartments of the body through blood. The effect of herbicides on tadpoles is less known when compared to adult amphibians, since the larvae of the anurans are less visible, and unlike adults, they do not have vocalization. Tadpoles of various species have not yet been described, which makes it even more difficult to study these organisms in depth [66].

The reduction in larval survival due to exposure to glyphosate was observed by Simioni and collaborators [67], Figueiredo and Rodrigues [68], and Costa and collaborators [69] in larvae of Physalaemus albonotatus, Physalaemus centralis, and Physalaemus cuvieri [70]. Rissoli and collaborators [71] also observed that the exposure of bullfrog tadpoles to Roundup Original® causes damage to the epithelium causing hypoxia in these animals. In the last 30 years, populations of amphibians have been suffering a great decline or even being extinct; almost half of the species are experiencing some population decline. On the basis of toxicity studies, sensitivity to glyphosate differs among species; however, there are several variations in experimental conditions and pesticide formula (different commercial formulations of glyphosate, different exposure times, different surfactant substances, number of replicates, abiotic conditions in the experiment, and stage of development) which make it difficult to compare and define which groups or species are more tolerant to contamination [67, 72, 73]. The LC50 values for the herpetofauna species are shown in Table 3.

SpeciesChemicalExposure time (h)LC50 mg a.i./LReference
Anaxyrus americanusRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[80]
Anaxyrus boreasRoundup®960.8–2.0[31]
Crinia insigniferaRoundup®482.9–11.6[31]
Dendropsophus minutusRoundup®960.28[85]
Heleioporus eyreiRoundup®482.9–11.6[31]
Hyla versicolorRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[31]
Litoria mooreiRoundup®482.9–11.6[31]
Lithobates sylvaticusRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[31]
Lithobates pipiensRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[31]
Lithobates clamitansRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[31]
Lithobates catesbeianusRoundup®3840.55–2.52[31]
Roundup®960.8–2.0[31]
Limnodynastes dorsalisRoundup®482.9–11.6[31]
Pseudacris cruciferRoundup®960.8–2.0[31]
Rana cascadaeRoundup®960.8–2.0[31]
Rhinella arenarumRoundup®482.42[83]
Scinax nasicusRoundup®481.74[82]

Table 3.

Ecotoxicity of glyphosate-based herbicide (GBH) to herpetofauna, exposure time, and LC50 value.

Reptiles are extremely sensitive to herbicide formulations and may exhibit changes in their behavior after exposure of these xenobiotics [74]. This group is fairly uniform and exposure to GBHs may affect its energy storage process [75, 76]. Schaumburg and collaborators [77] found that exposure to sublethal concentrations of glyphosate during the embryonic phase of Salvator merianae may cause an increase in genetic damage. Therefore, it is assumed that glyphosate is capable of causing DNA damage, promoting chromatin fragmentation of epidermal cells, impairing cell division. Exposure to glyphosate does not alter the thermoregulatory behavior of lizards of the species Oligosoma polychroma [78]. Sub-lethal concentrations of the commercial glyphosate formulation (Roundup®) cause genotoxic damage and chromosome breaks in Anguilla anguilla. The increase in the damage index in this species can cause reproductive damage and adverse effects in the long term [79].

Currently in the Neotropical region, about 40 studies relate the indiscriminate use of herbicides based on glyphosate with the risk to biodiversity of herpetofauna. Schiesari and collaborators [80] reported that some species of amphibians, including tadpoles and adults and some reptiles are sensitive to exposure to formulations based on glyphosate. Exposure to sublethal concentrations of glyphosate is sufficient to cause irreversible damage to the DNA of amphibians and reptiles, so the use of GBH should be controlled in arable areas avoiding the decline of species that make up the herpetofauna group.

2.5 Aquatic birds

Glyphosate when used in recommended rates is considered not bioaccumulative and of low toxicity in birds [81]. However, the present acquaintance is not enough to make affirmation about low toxicity risk and low exposure of birds to herbicide considering the possible complex process behind the movement and accumulation of glyphosate, additives, and waste in the environment. Moreover, even the few available studies [82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 94, 95, 96] have found direct and indirect effects of glyphosate on bird species (Figure 4). Among those, only five studies along years 1994 and 2017 on Google Scholar database have analyzed effects on aquatic bird species. Direct effects have been analyzed on male ducks (Anas platyrhynchos) that receive two different concentrations of Roundup dissolved in distilled water according to the body weight (5 and 100 mg kg−1). There was a decrease in testosterone level in blood plasma of about 90%. Moreover, anatomical and histological changes in seminiferous tubes and anatomical changes in the epididymis region have also been found [82].

Figure 4.

Ecotoxicity of glyphosate-based herbicide (GBH) to aquatic birds. Direct (continuous arrows) and indirect (dashed arrows) effects of GBH on birds.

Indirect effects have been found in wetlands where the glyphosate is used to control the increase of Typha spp. population [83, 84, 85]. Species of blackbirds and wren can be affected by habitat changes in target and nontarget plant communities that decrease available places to sheltering, nesting, and feeding. The lacks of those places lead birds to starvation, strong competition for resources, or leave the environment [84]. Part of control in coastal dunes of invasive species Chrysanthemoides monilifera ssp. rotundata is due to glyphosate. An 8-year study has found that a typical bird from coastal region, Myzomela sanguinolenta, was the rarest in places that receive the handling herbicide [86]. Environmental heterogeneity (e.g., microclimate and flora) and specific vegetation that is dead by glyphosate can be very important for conservation of some bird populations in the environment [85]. Sometimes, there is the increase of some bird populations after the glyphosate application. However, it can be related with an immediate advantage due the removal of abundant plant species and other changes in the environment and in available food. Under those circumstances, other population traits, like reproductive success, could have been affected but not detected [83].

The direct effect of glyphosate on aquatic plants and macroalgae [87] can also affect aquatic birds once they make up the varied and plentiful diet of many of those birds. Changes in physiological, histological, and behavioral levels and lethal cases have been documented in fishes due to use of glyphosate [87, 88]. In this way, piscivorous birds can also be suffering indirect effects. In fact, all aquatic birds’ food chain can be affected by glyphosate once effects on invertebrates [81, 87, 88], amphibians [89], and reptiles [90] have already been confirmed.

Birds are very similar in their physiology and anatomy. Then, studies that have tested direct and indirect effects of glyphosate on nonaquatic birds can be also considered here. In Japanese quails (Coturnix japonica), the low food consumption due to reduced palatability and the low absorption of nutrients in the digestive tract are responsible for body weight loss. Moreover, those birds have been fed with high glyphosate doses (250 and 500 mg kg−1 of food) and have exposed clinical symptoms of behavioral changes, malformed feathers, and slow development [91]. A total of 57.5% of dead embryos from chicken eggs have received glyphosate solution (0.1 ml with 2% Glialka Star) inside shell [92]. Herbicides can also act in synergy with other agrochemicals turning these toxic effects more complex. In this way, the combined effect between glyphosate and other chemicals on birds has been analyzed and all studies have demonstrated the increase of potential toxicological: 97.5% of dead embryos (0.1% of lead acetate plus 2% of glyphosate) [92] and decrease of hemoglobin and leucocytes (indoxacarb, an insecticide, plus glyphosate) [91]. Indirect effects on nonaquatic birds due the low vegetation complexity have also been reported: habitat loss replacing shrub by trees, for example, [93]; imbalance in the population structure (i.e., sex ratio) eliminating only habitats of one bird group [94, 95]; and changes in richness of the communities benefiting only birds related to sparse vegetation [96].

Therefore, the controlled and scaled use of glyphosate in large areas is necessary to contribute to conservation of environmental heterogeneity and biological diversity avoiding the plausible effects on bird communities [83, 84, 85, 94]. To know what plants are important to bird diet and to promote techniques that do not eliminate all of those plants from the place are important activities before glyphosate application [91]. More studies that aim to analyze the bird contamination by herbicides are also necessary [97]. Long-term studies that encourage collaborative work between ecologist, toxicologist, and chemist are more pertinent [98].

2.6 Aquatic mammals

For the best of our knowledge, GBH or glyphosate only was not tested in aquatic mammals. Searching on Web of Science website for the terms “Glyphosate AND mammal AND aquatic,” there is no study reported to date. Despite that, mammals in general are considered less sensible to GBH damages than other groups due to reduced contact with the environment of mammals when compared to other groups as fishes, amphibians, or aquatic invertebrates [99]. The main way that GBH or the active ingredient glyphosate reaches mammals’ bodies is through the digestive tract. However, it seems to be poorly absorbed and is excreted essentially nonmetabolized [100]. Essentially, mammals that were tested were rats, mice, and dogs [101], tested through injection or ingestion. Some studies report glyphosate in humans in medical case studies. Reported direct effects of GBH on mammals are described as a “wide range of clinical manifestations” such as skin and throat irritation, hypotension, or death [102] and include heart arrhythmias and atrioventricular block, cardiac electrophysiological changes and conduction blocks [103], pregnancy problems [104], disrupt transcriptional expression of the steroidogenic acute regulatory protein in testicle [105] and aromatase activity, alter mRNA levels, and interact with enzymes [106]. Indirect effects on mammals can be due to reduction of vegetation and animals that are a source of food such as invertebrates [101] and fishes. Although these mentioned studies were conducted in nonaquatic mammals, it is expected that aquatic mammals have similar or even more accentuated effect, since they have intense contact with water, and if it is contaminated, the exposure will be higher.

Advertisement

3. Regulations and perspectives

Despite the fact that GBHs were developed to control weeds, acting specifically in a restrict plan biochemical pathway, several studies demonstrated that there are many side effects on nontarget organisms in all great groups as reported extensively here. Looking to control these side effects, governments for many countries around the world established limits for usage and concentrations in water bodies. The USA, for example, allows 700 μg L−1 in water bodies, while Canada allows 280 μg L−1 in drink water. The Brazilian law is a little more restrictive, allowing 65 μg L−1 in water bodies class 2 that is used for crop and recreation of first degree (direct contact) [107]. However, we could check here that these maximum concentrations allowed are not safe for biodiversity conservation. Considering the Brazilian law, the more restrictive in American countries, populations of yellowtail tetra fish (A. lacustris) are not safe since sperm cells of this species are dead in lower concentrations than 65 μg L−1 [52]. In this way, European regulations are more plausible, because it is more restrictive (0.1 μg L−1) [108] and can be more precise on conservation of aquatic biodiversity.

However, even with all those regulations, it is not being obeyed, since there is a large range of glyphosate and its metabolite (e.g., AMPA) concentrations in hydroresources [6, 64]. Therefore, another way of action for environment safety is preserving marginal forests of rivers, surveillance, and environment education. Another sustainable way to achieve this goal is changing the crop production matrix from large scale, that is, conventional-based production model to a smaller integrative-/organic-based production system, with controlled or restrictive usage of pesticides and other agrochemicals.

Advertisement

Acknowledgments

We are thankful to FAPEG (#201710267001261) for financial support.

Advertisement

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. 1. Brooker MP, Edwards RW. Aquatic herbicides and the control of water weeds. Water Research. 1975;9(1):1-15. Available from: https://www.sciencedirect.com/science/article/pii/0043135475901463 [Accessed: 04 February 2019]
  2. 2. Cedergreen N, Streibig JC. The toxicity of herbicides to non-target aquatic plants and algae: Assessment of predictive factors and hazard. Pest Management Science. 2005;61(12):1152-1160. DOI: 10.1002/ps.1117 [Accessed: 30 September 2018]
  3. 3. Brown AA, Thompson AR. In: Brown AA, Thompson AR, editors. Ecology of Pesticides. 1st ed. Vol. 65. New York: John Wiley & Sons Inc; 1978. 536 p. DOI: 10.1002/iroh.19800650121 [Accessed: 29 August 2018]
  4. 4. Edwards CA. In: Edwards CA, editor. Environmental Pollution by Pesticides. London: Springer US; 1973. 542 p
  5. 5. Gilbert N. Case studies: A hard look at GM crops. Nature. 2013;497(7447):24-26. DOI: 10.1038/497024a [Accessed: 29 August 2018]
  6. 6. Annett R, Habibi HR, Hontela A. Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. Journal of Applied Toxicology. 2014;34(5):458-479. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24615870 [Accessed: 18 September 2017]
  7. 7. Glyphosate|C3H8NO5P—PubChem [Internet]. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/glyphosate#section=3D-Conformer [Accessed: 29 August 2018]
  8. 8. Steinrücken HC, Amrhein N. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochemical and Biophysical Research Communications. 1980;94(4):1207-1212. Available from: http://www.sciencedirect.com/science/article/pii/0006291X80905471
  9. 9. Tsui MTK, Chu LM. Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factors. Chemosphere. 2003;52(7):1189-1197. Available from: https://www.sciencedirect.com/science/article/pii/S0045653503003060?via%3Dihub [Accessed: 30 September 2018]
  10. 10. Lajmanovich RC, Sandoval MT, Peltzer PM. Induction of mortality and malformation in Scinax nasicus tadpoles exposed to glyphosate formulations. Bulletin of Environmental Contamination and Toxicology. 2003;70(3):612-618. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12592539 [Accessed: 18 September 2018]
  11. 11. Costa R, Nomura F. Measuring the impacts of Roundup original® on fluctuating asymmetry and mortality in a neotropical tadpole. Hydrobiologia. 2015:1-12. DOI: 10.1007/s10750-015-2404-0
  12. 12. Cattaneo R, Clasen B, Loro VL, de Menezes CC, Pretto A, Baldisserotto B, et al. Toxicological responses of Cyprinus carpio exposed to a commercial formulation containing glyphosate. Bulletin of Environmental Contamination and Toxicology. 2011;87(6):597-602. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21931962 [Accessed: 18 September 2018]
  13. 13. Glusczak L, dos Santos Miron D, Crestani M, Braga da Fonseca M, de Araújo Pedron F, Duarte MF, et al. Effect of glyphosate herbicide on acetylcholinesterase activity and metabolic and hematological parameters in piava (Leporinus obtusidens). Ecotoxicology and Environmental Safety. 2006;65(2):237-241. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16174533
  14. 14. Menéndez-Helman RJ, Ferreyroa GV, Dos Santos Afonso M, Salibián A. Glyphosate as an acetylcholinesterase inhibitor in Cnesterodon decemmaculatus. Bulletin of Environmental Contamination and Toxicology. 2012;88(1):6-9. Available from: www.proquest.com [Accessed: 18 September 2018]
  15. 15. Modesto KA, Martinez CB. Effects of roundup Transorb on fish: Hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere. 2010;81(6):781-787. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20684975 [Accessed: 23 July 2012]
  16. 16. Salbego J, Pretto A, Gioda CR, de Menezes CC, Lazzari R, Radünz Neto J, et al. Herbicide formulation with glyphosate affects growth, acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Archives of Environmental Contamination and Toxicology. 2010;58(3):740-745. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20112104
  17. 17. Sandrini JZ, Rola RC, Lopes FM, Buffon HF, Freitas MM, Martins CDMG, et al. Effects of glyphosate on cholinesterase activity of the mussel Perna perna and the fish Danio rerio and Jenynsia multidentata: In vitro studies. Aquatic Toxicology. 2013;130-131:171-173. DOI: 10.1016/j.aquatox.2013.01.006
  18. 18. Dörr F. Efeito Do Herbicida Glifosato Sobre o Crescimento e produção de metabólitos secundários Em Microcystis Aeruginosa e Cylindrospermopsis Raciborskii. São Paulo: Biblioteca Digital de Teses e Dissertações da Universidade de São Paulo; 2015. Available from: http://www.teses.usp.br/teses/disponiveis/9/9141/tde-10062015-171941/ [Accessed: 30 September 2018]
  19. 19. Newton M, Howard KM, Kelpsas BR, Danhaus R, Lottman CM, Dubelman S. Fate of glyphosate in an Oregon forest ecosystem. Journal of Agricultural and Food Chemistry. 1984;32(5):1144-1151. DOI: 10.1021/jf00125a054 [Accessed: 30 September 2018]
  20. 20. Newton M, Horner LM, Cowell JE, White DE, Cole EC. Dissipation of glyphosate and aminomethylphosphonic acid in North American forests. Journal of Agricultural and Food Chemistry. 1994;42(8):1795-1802. DOI: 10.1021/jf00044a043 [Accessed: 30 September 2018]
  21. 21. Goldsborough LG, Brown DJ. Dissipation of glyphosate and aminomethylphosphonic acid in water and sediments of boreal forest ponds. Environmental Toxicology and Chemistry. 1993;12(7):1139-1147. DOI: 10.1002/etc.5620120702 [Accessed: 30 September 2018]
  22. 22. Mackay D, Shiu WY, Ma KC. Illustrated Handbook of Physical-Chemical Properties and Environmental Fate for Organic Chemicals. Florida, USA: Lewis Publishers; 1992
  23. 23. National Center for Biotechnology Information. Sarcosine [Internet]. Pubchem compound Database. 2018. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/sarcosine#section=Top [Accessed: 17 October 2018]
  24. 24. Giesy JP, Dobson S, Solomon KR. Ecotoxicological risk assessment for roundup® herbicide. Reviews of Environmental Contamination and Toxicology. 2000;167:35-120. DOI: 10.1007/978-1-4612-1156-3_2 [Accessed: 30 September 2018]
  25. 25. Antunes AM, Rocha TL, Pires FS, de Freitas MA, Leite VRMC, Arana S, et al. Gender-specific histopathological response in guppies Poecilia reticulata exposed to glyphosate or its metabolite aminomethylphosphonic acid. Journal of Applied Toxicology. 2017;37(9):1098-1107. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28425566 [Accessed: 12 November 2018]
  26. 26. Folmar LC, Sanders HO, Julin AM. Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Archives of Environmental Contamination and Toxicology. 1979;8(3):269-278. DOI: 10.1007/BF01056243 [Accessed: 08 October 2018]
  27. 27. Jeppesen E, Jensen JP, Søndergaard M, Lauridsen T, Pedersen LJ, Jensen L. Top-down control in freshwater lakes: The role of nutrient state, submerged macrophytes and water depth. Hydrobiologia. 1997;342/343(0):151-164. DOI: 10.1023/A:1017046130329 [Accessed: 30 September 2018]
  28. 28. Sobrero C, Martin ML, Ronco A. Fitotoxicidad del herbicida roundup® max sobre la especie no blanco Lemna gibba en estudios de campo y laboratorio. Hidrobiológica. 2007;17(1):31-39. Available from: http://www.scielo.org.mx/scielo.php?pid=S0188-88972007000400004&script=sci_abstract [Accessed: 30 September 2018]
  29. 29. Pérez DJ, Okada E, Menone ML, Costa JL. Can an aquatic macrophyte bioaccumulate glyphosate? Development of a new method of glyphosate extraction in Ludwigia peploides and watershed scale validation. Chemosphere. 2017;185:975-982. Available from: https://www.sciencedirect.com/science/article/pii/S0045653517311451?via%3Dihub [Accessed: 30 September 2018]
  30. 30. Saxton MA, Morrow EA, Bourbonniere RA, Wilhelm SW. Glyphosate influence on phytoplankton community structure in Lake Erie. Journal of Great Lakes Research. 2011;37(4):683-690. Available from: https://www.sciencedirect.com/science/article/pii/S0380133011001675 [Accessed: 30 September 2018]
  31. 31. Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J. Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant & Cell Physiology. 2008;49(3):443-456. Available from: https://academic.oup.com/pcp/article-lookup/doi/10.1093/pcp/pcn021 [Accessed: 30 September 2018]
  32. 32. Vera MS, Lagomarsino L, Sylvester M, Pérez GL, Rodríguez P, Mugni H, et al. New evidences of roundup® (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems. Ecotoxicology. 2010;19(4):710-721. DOI: 10.1007/s10646-009-0446-7 [Accessed: 30 September 2018]
  33. 33. Schaffer JD, Sebetich MJ. Effects of aquatic herbicides on primary productivity of phytoplankton in the laboratory. Bulletin of Environmental Contamination and Toxicology. 2004;72(5):1032-1037. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15266702 [Accessed: 30 September 2018]
  34. 34. Relyea RA. The impact of inseticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications. 2005;15(2):618-627. DOI: 10.1890/03-5342 [Accessed: 30 September 2018]
  35. 35. Mueller TC, Main CL, Thompson MA, Steckel LE. Comparison of glyphosate salts (isopropylamine, diammonium, and potassium) and calcium and magnesium concentrations on the control of various weeds. Weed Technology. 2006;20(01):164-171. Available from: https://www.cambridge.org/core/product/identifier/S0890037X00018108/type/journal_article
  36. 36. Gyllstrom M, Hansson L-A. Dormancy in freshwater zooplankton: Induction, termination and the importance of benthic-pelagic coupling. Aquatic Sciences. 2004;66(3):274-295. Available from: http://link.springer.com/10.1007/s00027-004-0712-y [Accessed: 06 October 2018]
  37. 37. Ricci C. Dormancy patterns in rotifers. Hydrobiologia. 2001;446/447(1):1-11. DOI: 10.1023/A:1017548418201 [Accessed: 06 October 2018]
  38. 38. Gutierrez MF, Battauz Y, Caisso B. Disruption of the hatching dynamics of zooplankton egg banks due to glyphosate application. Chemosphere. 2017;171:644-653. Available from: https://www.sciencedirect.com/science/article/pii/S0045653516318422 [Accessed: 06 October 2018]
  39. 39. Portinho JL, Nielsen DL, Daré L, Henry R, Oliveira RC, Branco CCZ. Mixture of commercial herbicides based on 2,4-D and glyphosate mixture can suppress the emergence of zooplankton from sediments. Chemosphere. 2018;203:151-159. Available from: https://www.sciencedirect.com/science/article/pii/S0045653518305794 [Accessed: 06 October 2018]
  40. 40. European food Safety Authority. Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-of-field surface waters. EFSA Journal. 2013;11(7):3290. DOI: 10.2903/j.efsa.2013.3290 [Accessed: 06 October 2018]
  41. 41. Nwani CD, Ibiam UA, Ibiam OU, Nworie O, Onyishi G, Atama C. Investigation on acute toxicity and behavioral changes in Tilapia zillii due to glyphosate-based herbicide, Forceup. Journal of Animal and Plant Sciences. 2013;23(3):888-892
  42. 42. Chandrasekera WU, Weeratunga NP. The lethal impacts of roundup ® (glyphosate) on the fingerlings of guppy, Poecilia reticulata Peters, 1859. Asian Fisheries Science. 2011;24:367-378
  43. 43. Sadeghi A, Hedayati A. Investigation of LC50, NOEC and LOEC of glyphosate, deltamethrin and pretilachlor in guppies (Poecilia reticulata). Iranian Journal of Toxicology. 2014;8(26):1124-1129
  44. 44. De Souza Filho J, Sousa CCN, Da Silva CC, De Sabóia-Morais SMT, Grisolia CK. Mutagenicity and genotoxicity in gill erythrocyte cells of Poecilia reticulata exposed to a glyphosate formulation. Bulletin of Environmental Contamination and Toxicology. 2013;91:583-587. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24042842 [Accessed: 09 October 2013]
  45. 45. Hued AC, Oberhofer S, de los Ángeles Bistoni M. Exposure to a commercial glyphosate formulation (roundup®) alters normal gill and liver histology and affects male sexual activity of Jenynsia multidentata (Anablepidae, Cyprinodontiformes). Archives of Environmental Contamination and Toxicology. 2012;62(1):107-117. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21643816 [Accessed: 15 August 2013]
  46. 46. Ayoola SO. Histopathological effects of glyphosate on juvenile African catfish (Clarias gariepinus). American Journal of Environmental Science. 2008;4(3):362-367. Available from: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.328.8044&rep=rep1&type=pdf [Accessed: 18 September 2017]
  47. 47. Harayashiki CAY, Junior ASV, Machado AADS, Cabrera LDC, Primel EG, Bianchini A, et al. Toxic effects of the herbicide roundup in the guppy Poecilia vivipara acclimated to fresh water. Aquatic Toxicology. 2013;142-143:176-184. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0166445X13002130 [Accessed: 05 September 2013]
  48. 48. Jiraungkoorskul W, Upatham ES, Kruatrachue M, Sahaphong S, Vichasri-Grams S, Pokethitiyook P. Biochemical and histopathological effects of glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Environmental Toxicology. 2003;18(4):260-267. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12900945 [Accessed: 18 September 2017]
  49. 49. Langiano VDC, Martinez CBR. Toxicity and effects of a glyphosate-based herbicide on the neotropical fish Prochilodus lineatus. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology. 2008;147(2):222-231. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17933590 [Accessed: 23 July 2012]
  50. 50. Nesković NK, Poleksić V, Elezovíc I, Karan V, Budimir M. Biochemical and histopathological effects of glyphosate on carp, Cyprinus carpio L. Bulletin of Environmental Contamination and Toxicology. 1996;56(2):295-302. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8720103 [Accessed: 18 September 2017]
  51. 51. Giaquinto PC, de Sá MB, Sugihara VS, Gonçalves BB, Delício HC, Barki A. Effects of glyphosate-based herbicide sub-lethal concentrations on fish feeding behavior. Bulletin of Environmental Contamination and Toxicology. 2017;98(4):460-464
  52. 52. Gonçalves BB, Nascimento NF, Santos MP, Bertolini RM, Yasui GS, Giaquinto PC. Low concentrations of glyphosate-based herbicide cause complete loss of sperm motility of yellowtail tetra fish Astyanax lacustris. Journal of Fish Biology. 2018;92(4):1218-1224
  53. 53. Rocha TL, Santos AP, Yamada ÁT, Soares CM, Borges CL, Bailão AM, et al. Proteomic and histopathological response in the gills of Poecilia reticulata exposed to glyphosate-based herbicide. Environmental Toxicology and Pharmacology. 2015;40(1):175-186. DOI: 10.1016/j.etap.2015.04.016
  54. 54. Santos AP, Rocha TL, Borges CL, Bailão AM, de Almeida Soares CM, de Sabóia-Morais SMT. A glyphosate-based herbicide induces histomorphological and protein expression changes in the liver of the female guppy Poecilia reticulata. Chemosphere. 2017;168:933-943
  55. 55. Silvano DL, Segalla MV. Conservação de anfíbios no Brasil. In: Megadiversidade [Internet]. 1st ed. Belo Horizonte: Conservação internacional; 2005. pp. 79-86. Available from: https://books.google.com.br/books?id=nGCySCIb3eIC&pg=PA84&lpg=PA84&dq=.+Conservação+de+anfíbios+no+Brasil+Megadiversidade&source=bl&ots=fgsM9Mn_Ap&sig=GTTGyuhtXffw4CbzCDuFtFevuek&hl=pt-BR&sa=X&ved=2ahUKEwj8y6PZ3oPeAhUChZAKHWztB1w4ChDoATAEeg
  56. 56. den Besten PJ, Munawar M, Suter G. Ecotoxicological testing of marine and freshwater ecosystems: Emerging techniques, trends and strategies. Integrated Environmental Assessment and Management. 2007;(2):3, 305-306. DOI: 10.1002/ieam.5630030221 [Accessed: 13 October 2018]
  57. 57. Hayes TB, Falso P, Gallipeau S, Stice M. The cause of global amphibian declines: A developmental endocrinologist’s perspective. The Journal of Experimental Biology. 2010;213(6):921-933. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20190117
  58. 58. David M, Marigoudar SR, Patil VK, Halappa R. Behavioral, morphological deformities and biomarkers of oxidative damage as indicators of sublethal cypermethrin intoxication on the tadpoles of D. melanostictus (Schneider, 1799). Pesticide Biochemistry and Physiology. 2012;103(2):127-134. Available from: https://www.sciencedirect.com/science/article/pii/S0048357512000582 [Accessed: 13 October 2018]
  59. 59. Freire C, Koifman RJ, Sarcinelli PN, Simões Rosa AC, Clapauch R, Koifman S. Long-term exposure to organochlorine pesticides and thyroid status in adults in a heavily contaminated area in Brazil. Environmental Research. 2013;127:7-15. Available from: https://www.sciencedirect.com/science/article/pii/S0013935113001552 [Accessed: 13 October 2018]
  60. 60. Relyea RA. Amphibians are not ready for roundup®. In: Elliott JE, Bishop CA, Morrissey C, editors. Wildlife Ecotoxicology: Forensic Approaches. 3rd ed. New York: Springer; 2011. pp. 267-300. Available from: http://link.springer.com/10.1007/978-0-387-89432-4_9 [Accessed: 13 October 2018]
  61. 61. Davidson C, Shaffer HB, Jennings MR. Declines of the California red-legged frog: Climate, UV-B, habitat, and pesticides hypotheses. Ecological Applications. 2001;11(2):464-479. Available from: https://esajournals.onlinelibrary.wiley.com/doi/full/10.1890/1051-0761%282001%29011%5B0464%3ADOTCRL%5D2.0.CO%3B2 [Accessed: 13 October 2018]
  62. 62. Woehl G Jr, Woehl EN. In: Woehl G Jr, Woehl EN, editors. Anfíbios da Mata Atlântica. 1st ed. Jaraguá do Sul: Instituto Rã-Bugio para conservação da biodiversidade; 2008. 32 p. Available from: www.ra-bugio.org.br [Accessed: 13 October 2018]
  63. 63. Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N. Toxicity of glyphosate-based pesticides to four North American frog species. Environmental Toxicology and Chemistry. 2004;23(8):1928. DOI: 10.1897/03-71
  64. 64. Ondrasek G. Introductory chapter: Irrigation after millennia—Still one of the most effective strategies for sustainable management of water footprint in agricultural crops. In: Ondrasek G, editor. Irrigation in Agroecosystems. Zagreb, Croatia: Intech Open; 2019. pp. 1-3. Available from: https://www.intechopen.com/books/irrigation-in-agroecosystems/introductory-chapter-irrigation-after-millennia-still-one-of-the-most-effective-strategies-for-susta [Accessed: 05 February 2019]
  65. 65. Walker CH, Colin H, Sibly RM, Hopkin SP, Peakall DB. In: Walker CH, Colin H, Sibly RM, Hopkin SP, Peakall DB, editors. Principles of Ecotoxicology. 3rd ed. Florida, USA: CRC Press; 2012. 381 p
  66. 66. McDiarmid RW, Altig R. In: McDiarmid RW, Altig R, editors. Tadpoles: The Biology of Anuran Larvae. Chicago and London: University of Chicago Press; 1999. 444 p
  67. 67. Simioni F, da Silva DFN, Mott T. Toxicity of glyphosate on Physalaemus albonotatus (Steindachner, 1864) from Western Brazil. Ecotoxicology and Environmental Contamination. 2013;8(1):55-58. Available from: https://siaiap32.univali.br/seer/index.php/eec/article/view/3356 [Accessed: 13 October 2018]
  68. 68. Figueiredo J, de Jesus Rodrigues D. Effects of four types of pesticides on survival, time and size to metamorphosis of two species of tadpoles (Rhinella marina and Physalaemus centralis) from the southern Amazon, Brazil. Herpetological Journal. 2014;24:65-68. Available from: https://ppbio.inpa.gov.br/sites/default/files/10.0000%40ingentaconnect.com%40content%40bhs%40thj%402014%4000000024%4000000001%40art00003.pdf [Accessed: 13 October 2018]
  69. 69. Costa RN, Nomura F. Measuring the impacts of roundup original® on fluctuating asymmetry and mortality in a neotropical tadpole. Hydrobiologia. 2016;765(1):85-96. DOI: 10.1007/s10750-015-2404-0 [Accessed: 13 October 2018]
  70. 70. Blaustein AR, Kiesecker JM. Complexity in conservation: Lessons from the global decline of amphibian populations. Ecology Letters. 2002;5(4):597-608. DOI: 10.1046/j.1461-0248.2002.00352.x [Accessed: 13 October 2018]
  71. 71. Rissoli RZ, Abdalla FC, Costa MJ, Rantin FT, McKenzie DJ, Kalinin AL. Effects of glyphosate and the glyphosate based herbicides roundup original® and roundup Transorb® on respiratory morphophysiology of bullfrog tadpoles. Chemosphere. 2016;156:37-44. Available from: https://www.sciencedirect.com/science/article/pii/S0045653516305690 [Accessed: 13 October 2018]
  72. 72. Relyea RA, Jones DK. The toxicity of roundup original max® to 13 species of larval amphibians. Environmental Toxicology and Chemistry. 2009;28(9):2004. DOI: 10.1897/09-021.1 [Accessed: 13 October 2018]
  73. 73. Mann RM, Bidwell JR. The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Archives of Environmental Contamination and Toxicology. 1999;36(2):193-199. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9888965 [Accessed: 13 October 2018]
  74. 74. Angilletta MJ, Niewiarowski PH, Navas CA. The evolution of thermal physiology in ectotherms. Journal of Thermal Biology. 2002;27(4):249-268. Available from: https://www.sciencedirect.com/science/article/pii/S0306456501000948 [Accessed: 13 October 2018]
  75. 75. Peixoto F. Comparative effects of the roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere. 2005;61(8):1115-1122. Available from: https://www.sciencedirect.com/science/article/pii/S0045653505004558?via%3Dihub [Accessed: 13 October 2018]
  76. 76. Pianka ER, Vitt LJ, Greene HW. In: Pianka ER, Vitt LJ, Greene HW, editors. Lizards: Windows to the Evolution of Diversity. Berkeley: University of California Press; 2003. 333 p. Available from: https://www.jstor.org/stable/10.1525/j.ctt1pp0q8 [Accessed: 13 October 2018]
  77. 77. Schaumburg LG, Siroski PA, Poletta GL, Mudry MD. Genotoxicity induced by roundup® (glyphosate) in tegu lizard (Salvator merianae) embryos. Pesticide Biochemistry and Physiology. 2016;130:71-78. Available from: https://www.sciencedirect.com/science/article/pii/S0048357515300699 [Accessed: 13 October 2018]
  78. 78. Carpenter JK, Monks JM, Nelson N. The effect of two glyphosate formulations on a small, diurnal lizard (Oligosoma polychroma). Ecotoxicology. 2016;25(3):548-554. DOI: 10.1007/s10646-016-1613-2 [Accessed: 13 October 2018]
  79. 79. Guilherme S, Gaivao I, Santos MA, Pacheco M. European eel (Anguilla anguilla) genotoxic and pro-oxidant responses following short-term exposure to roundup(R)—A glyphosate-based herbicide. Mutagenesis. 2010;25(5):523-530. Available from: https://academic.oup.com/mutage/article-lookup/doi/10.1093/mutage/geq038 [Accessed: 13 October 2018]
  80. 80. Schiesari L, Waichman A, Brock T, Adams C, Grillitsch B. Pesticide use and biodiversity conservation in the Amazonian agricultural frontier. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 2013;368(1619):20120378. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23610177 [Accessed: 13 October 2018]
  81. 81. Sullivan TP, Sullivan DS. Vegetation management and ecosystem disturbance: Impact of glyphosate herbicide on plant and animal diversity in terrestrial systems. Environmental Reviews. 2003;11(1):37-59. Available from: http://www.nrcresearchpress.com/doi/10.1139/a03-005 [Accessed: 01 October 2018]
  82. 82. Oliveira AG, Telles LF, Hess RA, Mahecha GAB, Oliveira CA. Effects of the herbicide roundup on the epididymal region of drakes Anas platyrhynchos. Reproductive Toxicology. 2007;23(2):182-191. Available from: https://www.sciencedirect.com/science/article/pii/S0890623806002711 [Accessed: 01 October 2018]
  83. 83. Linz GM, Bergman DL, Blixt DC, Bleier WJ. Response of black terns (Chlidonias niger) to glyphosate-induced habitat alterations on wetlands. Colonial Waterbirds. 1994;17(2):160. Available from: https://www.jstor.org/stable/1521294?origin=crossref [Accessed: 01 October 2018]
  84. 84. Linz GM, Blixt DC, Hall S, Bergman DL, Bleier WJ. Responses of red-winged blackbirds, yellow-headed blackbirds and marsh wrens to glyphosate induced alterations in cattail density. Journal of Field Ornithology. 1996;67(1):167-176. Available from: https://sora.unm.edu/sites/default/files/journals/jfo/v067n01/p0167-p0176.pdf [Accessed: 01 October 2018]
  85. 85. Linz GM, Homan HJ. Use of glyphosate for managing invasive cattail (Typha spp.) to disperse blackbird (Icteridae) roosts. Crop Protection. 2011;30(2):98-104. Available from: https://www.sciencedirect.com/science/article/pii/S0261219410003005 [Accessed: 01 October 2018]
  86. 86. Lindenmayer DB, Wood J, Macgregor C, Hobbs RJ, Catford JA, Lindenmayer C, et al. Non-target impacts of weed control on birds, mammals, and reptiles. Ecosphere. 2017;8(5):1-19. Available from: www.esajournals.org [Accessed: 01 October 2018]
  87. 87. Gill JPK, Sethi N, Mohan A, Datta S, Girdhar M. Glyphosate toxicity for animals. Environmental Chemistry Letters. 2018;16(2):401-426. Available from: http://link.springer.com/10.1007/s10311-017-0689-0 [Accessed: 01 October 2018]
  88. 88. Carlisle SM, Trevors JT. Glyphosate in the environment. Water, Air, and Soil Pollution. 1988;39(3-4):409-420. DOI: 10.1007/BF00279485 [Accessed: 01 October 2018]
  89. 89. Wagner N, Reichenbecher W, Teichmann H, Tappeser B, Lötters S. Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environmental Toxicology and Chemistry. 2013;32(8):1688-1700. DOI: 10.1002/etc.2268 [Accessed: 01 October 2018]
  90. 90. Siroski PA, Poletta GL, Latorre MA, Merchant ME, Ortega HH, Mudry MD. Immunotoxicity of commercial-mixed glyphosate in broad snouted caiman (Caiman latirostris). Chemico-Biological Interactions. 2016;244:64-70. Available from: https://www.sciencedirect.com/science/article/pii/S0009279715301332 [Accessed: 01 October 2018]
  91. 91. Bhojane N, Ingole R, Hajare S, Kuralkar S, Manwar S, Waghmare S. Individual and combined toxicity effect of indoxacarb and glyphosate on general performance and hematological parameters in Japanese quails. Journal of Entomology and Zoology Studies. 2018;6(2):1212-1216. Available from: http://www.entomoljournal.com/archives/?year=2018&vol=6&issue=2&ArticleId=3326 [Accessed: 01 October 2018]
  92. 92. Szemerédy G, Szabó R, Kormos É, Szalai C, Lehel J, Budai P. Model study to investigate the toxic interaction between tebuconazole fungicide and lead acetate on chicken embryos. Columella-Journal of Agricultural and Environmental Sciences. 2017;4(1):15-19. Available from: https://www.cabdirect.org/cabdirect/abstract/20183050312 [Accessed: 01 October 2018]
  93. 93. Morrison ML, Meslow EC. Effects of the herbicide glyphosate on avian community structure in the Oregon coast range. Forest Science. 1984;30(1):95-106. Available from: https://pubs.er.usgs.gov/publication/5221931 [Accessed: 01 October 2018]
  94. 94. Santillo DJ, Brown PW, Leslie DM. Response of songbirds to glyphosate-induced habitat changes on clearcuts. Journal of Wildlife Management. 1989;53(1):64. Available from: https://www.jstor.org/stable/3801307?origin=crossref [Accessed: 01 October 2018]
  95. 95. Eggestad M, Enge E, Hjeljord O, Sahlgaard V. Glyphosate application in forest—Ecological aspects. Scandinavian Journal of Forest Research. 1988;3(1-4):129-135. DOI: 10.1080/02827588809382503 [Accessed: 01 October 2018]
  96. 96. Schulz CA, Leslie DM, Lochmiller RL, Engle DM, Engle DM. Herbicide effects on cross timbers breeding birds. Journal of Range Management. 1992;45(4):407. Available from: https://www.jstor.org/stable/4003093?origin=crossref [Accessed: 01 October 2018]
  97. 97. EFSA. Conclusion on the peer review of the pesticide risk assessment of the active substance glyphosate. EFSA Journal. 2015;13(11):1-107. Available from: http://enfo.agt.bme.hu/drupal/sites/default/files/(EFSA)-2015-EFSA_Journal.pdf [Accessed: 01 October 2018]
  98. 98. Kissane Z, Shephard JM. The rise of glyphosate and new opportunities for biosentinel early-warning studies. Conservation Biology. 2017;31(6):1293-1300. DOI: 10.1111/cobi.12955 [Accessed: 01 October 2018]
  99. 99. Zaranyika MF, Nyandoro MG. Degradation of glyphosate in the aquatic environment: An enzymatic kinetic model that takes into account microbial degradation of both free and colloidal (or sediment) particle adsorbed glyphosate. Journal of Agricultural and Food Chemistry. 1993;41:838-842. Available from: https://pubs.acs.org/sharingguidelines [Accessed: 03 October 2018]
  100. 100. Williams GM, Kroes R, Munro IC. Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regulatory Toxicology and Pharmacology. 2000;31(2):117-165. Available from: https://www.sciencedirect.com/science/article/pii/S0273230099913715 [Accessed: 03 October 2018]
  101. 101. Freedman B. Controversy over the use of herbicides in forestry, with particular reference to glyphosate usage. Journal of Environmental Carcinogenesis Reviews. 1990;8(2):277-286. DOI: 10.1080/10590509009373384 [Accessed: 03 October 2018]
  102. 102. Mahendrakar K, Venkategowda PM, Rao SM, Mutkule DP. Glyphosate surfactant herbicide poisoning and management. Indian Journal of Critical Care Medicine. 2014;18(5):328-330. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24914265 [Accessed: 03 October 2018]
  103. 103. Gress S, Lemoine S, Séralini G-E, Puddu PE. Glyphosate-based herbicides potently affect cardiovascular system in mammals: Review of the literature. Cardiovascular Toxicology. 2015;15(2):117-126. DOI: 10.1007/s12012-014-9282-y [Accessed: 03 October 2018]
  104. 104. Savitz DA, Arbuckle T, Kaczor D, Curtis KM. Male pesticide exposure and pregnancy outcome. American Journal of Epidemiology. 1997;146(12):1025-1036. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9420527 [Accessed: 03 October 2018]
  105. 105. Walsh LP, McCormick C, Martin C, Stocco DM. Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression. Environmental Health Perspectives. 2000;108(8):769-776. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10964798 [Accessed: 03 October 2018]
  106. 106. Richard S, Moslemi S, Sipahutar H, Benachour N, Seralini G-E. Differential effects of glyphosate and roundup on human placental cells and aromatase. Environmental Health Perspectives. 2005;113(6):716-720. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15929894 [Accessed: 18 September 2018]
  107. 107. Brasil. Resolução no 357 de 17 de março de 2005 [Internet]. Diário Oficial da União, 357 CONAMA; 2005. pp. 58-63. Available from: http://www.mma.gov.br/port/conama/res/res05/res35705.pdf
  108. 108. EPA. European Communities (Drinking Water) (No. 2) Regulations. Wexford, Ireland: Environmental Protection Agency; 2010. p. 327. Available from: http://www.wsntg.ie [Accessed: 01 October 2018]

Written By

Bruno Bastos Gonçalves, Percilia Cardoso Giaquinto, Douglas dos Santos Silva, Carlos de Melo e Silva Neto, Amanda Alves de Lima, Adriano Antonio Brito Darosci, Jorge Laço Portinho, Wanessa Fernandes Carvalho and Thiago Lopes Rocha

Submitted: 10 June 2018 Reviewed: 12 February 2019 Published: 16 July 2019