Bioindicator

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Caddisfly (order Trichoptera), a macroinvertebrate used as an indicator of water quality. Trichoptera caddisfly 1.jpg
Caddisfly (order Trichoptera), a macroinvertebrate used as an indicator of water quality.

A bioindicator is any species (an indicator species) or group of species whose function, population, or status can reveal the qualitative status of the environment. The most common indicator species are animals. [2] For example, copepods and other small water crustaceans that are present in many water bodies can be monitored for changes (biochemical, physiological, or behavioural) that may indicate a problem within their ecosystem. Bioindicators can tell us about the cumulative effects of different pollutants in the ecosystem and about how long a problem may have been present, which physical and chemical testing cannot. [3]

Contents

A biological monitor or biomonitor is an organism that provides quantitative information on the quality of the environment around it. [4] Therefore, a good biomonitor will indicate the presence of the pollutant and can also be used in an attempt to provide additional information about the amount and intensity of the exposure.

A biological indicator is also the name given to a process for assessing the sterility of an environment through the use of resistant microorganism strains (e.g. Bacillus or Geobacillus ). [5] Biological indicators can be described as the introduction of a highly resistant microorganisms to a given environment before sterilization, tests are conducted to measure the effectiveness of the sterilization processes. As biological indicators use highly resistant microorganisms, any sterilization process that renders them inactive will have also killed off more common, weaker pathogens.

Overview

A bioindicator is an organism or biological response that reveals the presence of pollutants by the occurrence of typical symptoms or measurable responses and is, therefore, more qualitative. These organisms (or communities of organisms) can be used to deliver information on alterations in the environment or the quantity of environmental pollutants by changing in one of the following ways: physiologically, chemically or behaviourally. The information can be deduced through the study of:

  1. their content of certain elements or compounds
  2. their morphological or cellular structure
  3. metabolic biochemical processes
  4. behaviour
  5. population structure(s).

The importance and relevance of biomonitors, rather than man-made equipment, are justified by the observation that the best indicator of the status of a species or system is itself. [6] Bioindicators can reveal indirect biotic effects of pollutants when many physical or chemical measurements cannot. Through bioindicators, scientists need to observe only the single indicating species to check on the environment rather than monitor the whole community. [7] Small sets of indicator species can also be used to predict species richness for multiple taxonomic groups. [8]

The use of a biomonitor is described as biological monitoring and is the use of the properties of an organism to obtain information on certain aspects of the biosphere. Biomonitoring of air pollutants can be passive or active. Experts use passive methods to observe plants growing naturally within the area of interest. Active methods are used to detect the presence of air pollutants by placing test plants of known response and genotype into the study area.[ citation needed ]

The use of a biomonitor is described as biological monitoring. This refers to the measurement of specific properties of an organism to obtain information on the surrounding physical and chemical environment. [9]

Bioaccumulative indicators are frequently regarded as biomonitors. Depending on the organism selected and their use, there are several types of bioindicators. [10] [11]

Use

In most instances, baseline data for biotic conditions within a pre-determined reference site are collected. Reference sites must be characterized by little to no outside disturbance (e.g. anthropogenic disturbances, land use change, invasive species). The biotic conditions of a specific indicator species are measured within both the reference site and the study region over time. Data collected from the study region are compared against similar data collected from the reference site in order to infer the relative environmental health or integrity of the study region. [12]

An important limitation of bioindicators in general is that they have been reported as inaccurate when applied to geographically and environmentally diverse regions. [13] As a result, researchers who use bioindicators need to consistently ensure that each set of indices is relevant within the environmental conditions they plan to monitor. [14]

Plant and fungal indicators

The lichen Lobaria pulmonaria is sensitive to air pollution. Lobaria pulmonaria 010108c.jpg
The lichen Lobaria pulmonaria is sensitive to air pollution.

The presence or absence of certain plant or other vegetative life in an ecosystem can provide important clues about the health of the environment: environmental preservation. There are several types of plant biomonitors, including mosses, lichens, tree bark, bark pockets, tree rings, and leaves. As an example, environmental pollutants can be absorbed and incorporated into tree bark, which can then be analyzed to pollutant presence and concentration in the surrounding environment. [15] The leaves of certain vascular plants experience harmful effects in the presence of ozone, particularly tissue damage, making them useful in detecting the pollutant. [16] [17] These plants are observed abundantly in Atlantic islands in the Northern Hemisphere, the Mediterranean Basin, equatorial Africa, Ethiopia, the Indian coastline, the Himalayan region, southern Asia, and Japan. [18] These regions with high endemic richness are particularly vulnerable to ozone pollution, emphasizing the importance of certain vascular plant species as valuable indicators of environmental health in terrestrial ecosystems. Conservationists use such plant bioindicators as tools, allowing them to ascertain potential changes and damages to the environment.

As an example, Lobaria pulmonaria has been identified as an indicator species for assessing stand age and macrolichen diversity in Interior Cedar–Hemlock forests of east-central British Columbia, highlighting its ecological significance as a bioindicator. [19] The abundance of Lobaria pulmonaria was strongly correlated with this increase in diversity, suggesting its potential as an indicator of stand age in the ICH. [20] Another Lichen species, Xanthoria parietina, serves as a reliable indicator of air quality, effectively accumulating pollutants like heavy metals and organic compounds. Studies have shown that X. parietina samples collected from industrial areas exhibit significantly higher concentrations of these pollutants compared to those from greener, less urbanized environments. [21] This highlights the lichen's valuable role in assessing environmental health and identifying areas with elevated pollution levels, aiding in targeted mitigation efforts and environmental management strategies.

Fungi is also useful as bioindicators, as they are found throughout the globe and undergo noticeable changes in different environments. [22]

Lichens are organisms comprising both fungi and algae. They are found on rocks and tree trunks, and they respond to environmental changes in forests, including changes in forest structure – conservation biology, air quality, and climate. The disappearance of lichens in a forest may indicate environmental stresses, such as high levels of sulfur dioxide, sulfur-based pollutants, and nitrogen oxides. The composition and total biomass of algal species in aquatic systems serve as an important metric for organic water pollution and nutrient loading such as nitrogen and phosphorus. There are genetically engineered organisms that can respond to toxicity levels in the environment; e.g., a type of genetically engineered grass that grows a different colour if there are toxins in the soil. [23]

Animal indicators and toxins

Populations of American crows (Corvus brachyrhynchos) are especially susceptible to the West Nile Virus, and can be used as a bioindicator species for the disease's presence in an area. Corvus-brachyrhynchos-001.jpg
Populations of American crows (Corvus brachyrhynchos) are especially susceptible to the West Nile Virus, and can be used as a bioindicator species for the disease's presence in an area.

Changes in animal populations, whether increases or decreases, can indicate pollution. [24] For example, if pollution causes depletion of a plant, animal species that depend on that plant will experience population decline. Conversely, overpopulation may be opportunistic growth of a species in response to loss of other species in an ecosystem. On the other hand, stress-induced sub-lethal effects can be manifested in animal physiology, morphology, and behaviour of individuals long before responses are expressed and observed at the population level. [25] Such sub-lethal responses can be very useful as "early warning signals" to predict how populations will further respond.

Pollution and other stress agents can be monitored by measuring any of several variables in animals: the concentration of toxins in animal tissues; the rate at which deformities arise in animal populations; behaviour in the field or in the laboratory; [26] and by assessing changes in individual physiology. [27]

Frogs and toads

Amphibians, particularly anurans (frogs and toads), are increasingly used as bioindicators of contaminant accumulation in pollution studies. [28] Anurans absorb toxic chemicals through their skin and their larval gill membranes and are sensitive to alterations in their environment. [29] They have a poor ability to detoxify pesticides that are absorbed, inhaled, or ingested by eating contaminated food. [29] This allows residues, especially of organochlorine pesticides, to accumulate in their systems. [29] They also have permeable skin that can easily absorb toxic chemicals, making them a model organism for assessing the effects of environmental factors that may cause the declines of the amphibian population. [29] These factors allow them to be used as bioindicator organisms to follow changes in their habitats and in ecotoxicological studies due to humans increasing demands on the environment. [30]

Knowledge and control of environmental agents is essential for sustaining the health of ecosystems. Anurans are increasingly utilized as bioindicator organisms in pollution studies, such as studying the effects of agricultural pesticides on the environment.[ citation needed ] Environmental assessment to study the environment in which they live is performed by analyzing their abundance in the area as well as assessing their locomotive ability and any abnormal morphological changes, which are deformities and abnormalities in development.[ citation needed ] Decline of anurans and malformations could also suggest increased exposure to ultra-violet light and parasites. [30] Expansive application of agrochemicals such as glyphosate have been shown to have harmful effects on frog populations throughout their lifecycle due to run off of these agrochemicals into the water systems these species live and their proximity to human development. [31]

Pond-breeding anurans are especially sensitive to pollution because of their complex life cycles, which could consist of terrestrial and aquatic living. [28] During their embryonic development, morphological and behavioral alterations are the effects most frequently cited in connection with chemical exposures. [32] Effects of exposure may result in shorter body length, lower body mass and malformations of limbs or other organs. [28] The slow development, late morphological change, and small metamorph size result in increased risk of mortality and exposure to predation. [28]

Crustaceans

Crayfish have also been hypothesized as being suitable bioindicators, under the appropriate conditions. [33] One example of use is an examination of accumulation of microplastics in the digestive tract of red swamp crayfish (Procambarus clarkii) being used as a bioindicator of wider microplastics pollution. [34]

Microbial indicators

Chemical pollutants

Microorganisms can be used as indicators of aquatic or terrestrial ecosystem health. Found in large quantities, microorganisms are easier to sample than other organisms. Some microorganisms will produce new proteins, called stress proteins, when exposed to contaminants such as cadmium and benzene. These stress proteins can be used as an early warning system to detect changes in levels of pollution.[ citation needed ]

In oil and gas exploration

Microbial Prospecting for oil and gas (MPOG) can be used to identify prospective areas for oil and gas occurrences.[ citation needed ] In many cases, oil and gas is known to seep toward the surface as a hydrocarbon reservoir will usually leak or have leaked towards the surface through buoyancy forces overcoming sealing pressures. These hydrocarbons can alter the chemical and microbial occurrences found in the near-surface soils or can be picked up directly. Techniques used for MPOG include DNA analysis, simple bug counts after culturing a soil sample in a hydrocarbon-based medium or by looking at the consumption of hydrocarbon gases in a culture cell. [35]

Microalgae in water quality

Microalgae have gained attention in recent years due to several reasons including their greater sensitivity to pollutants than many other organisms. In addition, they occur abundantly in nature, they are an essential component in very many food webs, they are easy to culture and to use in assays and there are few if any ethical issues involved in their use.

Gravitactic mechanism of the microalgae Euglena gracilis (A) in the absence and (B) in the presence of pollutants. Gravitactism Euglena.png
Gravitactic mechanism of the microalgae Euglena gracilis (A) in the absence and (B) in the presence of pollutants.

Euglena gracilis is a motile, freshwater, photosynthetic flagellate. Although Euglena is rather tolerant to acidity, it responds rapidly and sensitively to environmental stresses such as heavy metals or inorganic and organic compounds. Typical responses are the inhibition of movement and a change of orientation parameters. Moreover, this organism is very easy to handle and grow, making it a very useful tool for eco-toxicological assessments. One very useful particularity of this organism is gravitactic orientation, which is very sensitive to pollutants. The gravireceptors are impaired by pollutants such as heavy metals and organic or inorganic compounds. Therefore, the presence of such substances is associated with random movement of the cells in the water column. For short-term tests, gravitactic orientation of E. gracilis is very sensitive. [36] [37] Other species such as Paramecium biaurelia (see Paramecium aurelia ) also use gravitactic orientation. [38]

Automatic bioassay is possible, using the flagellate Euglena gracilis in a device which measures their motility at different dilutions of the possibly polluted water sample, to determine the EC50 (the concentration of sample which affects 50 percent of organisms) and the G-value (lowest dilution factor at which no-significant toxic effect can be measured). [39] [40]

Macroinvertebrates

Macroinvertebrates are useful and convenient indicators of the ecological health of water bodies [41] and terrestrial ecosystems. [42] [43] They are almost always present, and are easy to sample and identify. This is largely due to the fact that most macro-invertebrates are visible to the naked eye, they typically have a short life-cycle (often the length of a single season) and are generally sedentary. [44] Pre-existing river conditions such as river type and flow will affect macro invertebrate assemblages and so various methods and indices will be appropriate for specific stream types and within specific eco-regions. [44] While some benthic macroinvertebrates are highly tolerant to various types of water pollution, others are not. Changes in population size and species type in specific study regions indicate the physical and chemical state of streams and rivers. [9] Tolerance values are commonly used to assess water pollution [45] and environmental degradation, such as human activities (e.g. selective logging and wildfires) in tropical forests. [46] [47]

Benthic indicators for water quality testing

Benthic macroinvertebrates are found within the benthic zone of a stream or river. They consist of aquatic insects, crustaceans, worms and mollusks that live in the vegetation and stream beds of rivers. [9] Macroinvertebrate species can be found in nearly every stream and river, except in some of the world's harshest environments. They also can be found in mostly any size of stream or river, prohibiting only those that dry up within a short timeframe. [48] This makes the beneficial for many studies because they can be found in regions where stream beds are too shallow to support larger species such as fish. [9] Benthic indicators are often used to measure the biological components of fresh water streams and rivers. In general, if the biological functioning of a stream is considered to be in good standing, then it is assumed that the chemical and physical components of the stream are also in good condition. [9] Benthic indicators are the most frequently used water quality test within the United States. [9] While benthic indicators should not be used to track the origins of stressors in rivers and streams, they can provide background on the types of sources that are often associated with the observed stressors. [49]

Global context

In Europe, the Water Framework Directive (WFD) went into effect on October 23, 2000. [50] It requires all EU member states to show that all surface and groundwater bodies are in good status. The WFD requires member states to implement monitoring systems to estimate the integrity of biological stream components for specific sub-surface water categories. This requirement increased the incidence of biometrics applied to ascertain stream health in Europe [13] A remote online biomonitoring system was designed in 2006. It is based on bivalve molluscs and the exchange of real-time data between a remote intelligent device in the field (able to work for more than 1 year without in-situ human intervention) and a data centre designed to capture, process and distribute the web information derived from the data. The technique relates bivalve behaviour, specifically shell gaping activity, to water quality changes. This technology has been successfully used for the assessment of coastal water quality in various countries (France, Spain, Norway, Russia, Svalbard (Ny-Ålesund) and New Caledonia). [26]

In the United States, the Environmental Protection Agency (EPA) published Rapid Bioassessment Protocols, in 1999, based on measuring macroinvertebrates, as well as periphyton and fish for assessment of water quality. [1] [51] [52]

In South Africa, the Southern African Scoring System (SASS) method is based on benthic macroinvertebrates, and is used for the assessment of water quality in South African rivers. The SASS aquatic biomonitoring tool has been refined over the past 30 years and is now on the fifth version (SASS5) in accordance with the ISO/IEC 17025 protocol. [44] The SASS5 method is used by the South African Department of Water Affairs as a standard method for River Health Assessment, which feeds the national River Health Programme and the national Rivers Database.[ citation needed ]

The imposex phenomenon in the dog conch species of sea snail leads to the abnormal development of a penis in females, but does not cause sterility. Because of this, the species has been suggested as a good indicator of pollution with organic man-made tin compounds in Malaysian ports. [53]

See also

Related Research Articles

<span class="mw-page-title-main">Benthos</span> Community of organisms that live in the benthic zone

Benthos, also known as benthon, is the community of organisms that live on, in, or near the bottom of a sea, river, lake, or stream, also known as the benthic zone. This community lives in or near marine or freshwater sedimentary environments, from tidal pools along the foreshore, out to the continental shelf, and then down to the abyssal depths.

<span class="mw-page-title-main">Water quality</span> Assessment against standards for use

Water quality refers to the chemical, physical, and biological characteristics of water based on the standards of its usage. It is most frequently used by reference to a set of standards against which compliance, generally achieved through treatment of the water, can be assessed. The most common standards used to monitor and assess water quality convey the health of ecosystems, safety of human contact, extent of water pollution and condition of drinking water. Water quality has a significant impact on water supply and often determines supply options.

Freshwater ecosystems are a subset of Earth's aquatic ecosystems. They include lakes, ponds, rivers, streams, springs, bogs, and wetlands. They can be contrasted with marine ecosystems, which have a larger salt content. Freshwater habitats can be classified by different factors, including temperature, light penetration, nutrients, and vegetation. There are three basic types of freshwater ecosystems: Lentic, lotic and wetlands. Freshwater ecosystems contain 41% of the world's known fish species.

RIVPACS is an aquatic biomonitoring system for assessing water quality in freshwater rivers in the United Kingdom. It is based on the macroinvertebrate species found at the study site during sampling. Some of these species are tolerant to pollution, low dissolved oxygen, and other stressors, but others are sensitive; organisms vary in their tolerances. Therefore, different species will usually be found, in different proportions, at different river sites of varying quality. Some organisms are especially good indicator species. The species found at the reference sites collectively make up the species assemblage for that site and are the basis for a statistical comparison between reference sites and non-reference sites. The comparison between the expected species and the observed species can then be used to estimate this aspect of the ecological health of a river.

<span class="mw-page-title-main">Aquatic biomonitoring</span>

Aquatic biomonitoring is the science of inferring the ecological condition of rivers, lakes, streams, and wetlands by examining the organisms that live there. While aquatic biomonitoring is the most common form of biomonitoring, any ecosystem can be studied in this manner.

In biomedical contexts, a biomarker, or biological marker, is a measurable indicator of some biological state or condition. Biomarkers are often measured and evaluated using blood, urine, or soft tissues to examine normal biological processes, pathogenic processes, or pharmacologic responses to a therapeutic intervention. Biomarkers are used in many scientific fields.

<span class="mw-page-title-main">Biological integrity</span>

Biological integrity is associated with how "pristine" an environment is and its function relative to the potential or original state of an ecosystem before human alterations were imposed. Biological integrity is built on the assumption that a decline in the values of an ecosystem's functions are primarily caused by human activity or alterations. The more an environment and its original processes are altered, the less biological integrity it holds for the community as a whole. If these processes were to change over time naturally, without human influence, the integrity of the ecosystem would remain intact. The integrity of the ecosystem relies heavily on the processes that occur within it because those determine what organisms can inhabit an area and the complexities of their interactions. Most of the applications of the notion of biological integrity have addressed aquatic environments, but there have been efforts to apply the concept to terrestrial environments. Determining the pristine condition of the ecosystem is in theory scientifically derived, but deciding which of the many possible states or conditions of an ecosystem is the appropriate or desirable goal is a political or policy decision and is typically the focus of policy and political disagreements. Ecosystem health is a related concept but differs from biological integrity in that the "desired condition" of the ecosystem or environment is explicitly based on the values or priorities of society.

The biological monitoring working party (BMWP) is a procedure for measuring water quality using families of macroinvertebrates as biological indicators.

An index of biological integrity (IBI), also called an index of biotic integrity, is a scientific tool typically used to identify and classify water pollution problems, although there have been some efforts to apply the idea to terrestrial environments. An IBI associates anthropogenic influences on a water body with biological activity in the water body, and is formulated using data developed from biosurveys. Biological integrity is associated with how "pristine" an environment is and its function relative to the potential or original state of an ecosystem before human alterations were imposed. Biological integrity is built on the assumption that a decline in the values of an ecosystem's functions are primarily caused by human activity or alterations. The more an environment and its original processes are altered, then by definition, the less biological integrity it holds for the community as a whole. If these processes were to change over time naturally, without human influence, the integrity of the ecosystem would remain intact. Similar to the concept of ecosystem health, the integrity of the ecosystem relies heavily on the processes that occur within it because those determine which organisms can inhabit an area and the complexities of their interactions. Deciding which of the many possible states or conditions of an ecosystem is appropriate or desirable is a political or policy decision.

<span class="mw-page-title-main">Macrobenthos</span> Organisms that live at the bottom of a water column

Macrobenthos consists of the organisms that live at the bottom of a water column and are visible to the naked eye. In some classification schemes, these organisms are larger than 1 mm; in another, the smallest dimension must be at least 0.5 mm. They include polychaete worms, pelecypods, anthozoans, echinoderms, sponges, ascidians, crustaceans.

A biotic index is a scale for showing the quality of an environment by indicating the types and abundances of organisms present in a representative sample of the environment. It is often used to assess the quality of water in marine and freshwater ecosystems. Numerous biotic indices have been created to account for the indicator species found in each region of study. The concept of the biotic index was developed by Cherie Stephens in an effort to provide a simple measurement of stream pollution and its effects on the biology of the stream.

<span class="mw-page-title-main">Biosurvey</span> Scientific study of organisms to assess the condition of an ecological resource

A biosurvey, or biological survey, is a scientific study of organisms to assess the condition of an ecological resource, such as a water body.

<span class="mw-page-title-main">Environmental monitoring</span> Monitoring of the quality of the environment

Environmental monitoring is the processes and activities that are done to characterize and describe the state of the environment. It is used in the preparation of environmental impact assessments, and in many circumstances in which human activities may cause harmful effects on the natural environment. Monitoring strategies and programs are generally designed to establish the current status of an environment or to establish a baseline and trends in environmental parameters. The results of monitoring are usually reviewed, analyzed statistically, and published. A monitoring program is designed around the intended use of the data before monitoring starts.

<span class="mw-page-title-main">Environmental impact of mining</span> Environmental problems from uncontrolled mining

Environmental impact of mining can occur at local, regional, and global scales through direct and indirect mining practices. Mining can cause erosion, sinkholes, loss of biodiversity, or the contamination of soil, groundwater, and surface water by chemicals emitted from mining processes. These processes also affect the atmosphere through carbon emissions which contributes to climate change.

<span class="mw-page-title-main">Macroinvertebrate Community Index</span> An indicator of water quality and overall stream health

Macroinvertebrate Community Index (MCI) is an index used in New Zealand to measure the water quality of fresh water streams. The presence or lack of macroinvertebrates such as insects, worms and snails in a river or stream can give a biological indicator on the health of that waterway. The MCI assigns a number to each species of macroinvertebrate based on the sensitivity of that species to pollution. The index then calculates an average score. A higher score on the MCI generally indicates a more healthy stream.

<span class="mw-page-title-main">Aquatic macroinvertebrate DNA barcoding</span>

DNA barcoding is an alternative method to the traditional morphological taxonomic classification, and has frequently been used to identify species of aquatic macroinvertebrates. Many are crucial indicator organisms in the bioassessment of freshwater and marine ecosystems.

<span class="mw-page-title-main">Algae DNA barcoding</span> Technique used for species identification and phylogenetic studies

DNA barcoding of algae is commonly used for species identification and phylogenetic studies. Algae form a phylogenetically heterogeneous group, meaning that the application of a single universal barcode/marker for species delimitation is unfeasible, thus different markers/barcodes are applied for this aim in different algal groups.

<span class="mw-page-title-main">Fresh water</span> Naturally occurring water with low amounts of dissolved salts

Fresh water or freshwater is any naturally occurring liquid or frozen water containing low concentrations of dissolved salts and other total dissolved solids. The term excludes seawater and brackish water, but it does include non-salty mineral-rich waters, such as chalybeate springs. Fresh water may encompass frozen and meltwater in ice sheets, ice caps, glaciers, snowfields and icebergs, natural precipitations such as rainfall, snowfall, hail/sleet and graupel, and surface runoffs that form inland bodies of water such as wetlands, ponds, lakes, rivers, streams, as well as groundwater contained in aquifers, subterranean rivers and lakes.

<span class="mw-page-title-main">Freshwater salinization</span> Salty runoff contaminating freshwater ecosystems

Freshwater salinization is the process of salty runoff contaminating freshwater ecosystems, which can harm aquatic species in certain quantities and contaminate drinking water. It is often measured by the increased amount of dissolved minerals than what is considered usual for the area being observed. Naturally occurring salinization is referred to as primary salinization; this includes rainfall, rock weathering, seawater intrusion, and aerosol deposits. Human-induced salinization is termed as secondary salinization, with the use of de-icing road salts as the most common form of runoff. Approximately 37% of the drainage in the United States has been affected by salinization in the past century. The EPA has defined two thresholds for healthy salinity levels in freshwater ecosystems: 230 mg/L Cl− for average salinity levels and 860 mg/L Cl− for acute inputs.

<span class="mw-page-title-main">Aquatic macroinvertebrates</span> Animals with a stage that lives in water

Aquatic macroinvertebrates are insects in their nymph and larval stages, snails, worms, crayfish, and clams that spend at least part of their lives in water. These insects play a large role in freshwater ecosystems by recycling nutrients as well as providing food to higher trophic levels.

References

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Herek, J. S., Vargas, L., Trindade, S. A. R., Rutkoski, C. F., Macagnan, N., Hartmann, P. A., & Hartmann, M. T. (2020). Can environmental concentrations of glyphosate affect survival and cause malformation in amphibians? Effects from a glyphosate-based herbicide on Physalaemus cuvieri and P. gracilis (Anura: Leptodactylidae). Environmental Science and Pollution Research, 27(18), 22619–22630. https://doi.org/10.1007/s11356-020-08869-z

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