Impacts of Agricultural Pesticides on Terrestrial Ecosystems | Bentham Science
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This last initiative permits to identify susceptible species to environmental stressors such as HM. In terrestrial environments, small mammals are commonly used because of their similar physiological systems to humans. Ecosystems are open thermodynamic systems of matter and energy effluxes, which maintain stable from the balance of their biotic and abiotic components [ 53 ]. Ecosystem stability may be altered because of the incorporation of HM, derived from mining activities [ 54 ].
Under this situation, ecosystems may be or may not be affected by HM, depending on the magnitude and exposure time, or if one of the functions that maintain the ecosystem integrity is compromised e. Many ecotoxicological studies that assess HM effects on terrestrial ecosystems have focused on the analysis of HM concentrations in soils, their bioavailability and bioaccumulation, but few have analyzed their biomagnification trough the trophic chain and their effects on ecosystem integrity [ 54 ].
The first step of HM incorporation into the ecosystems is because their bioavailability potential and soil mobility, where metallic cations adhere to negative charged particles like clay and organic matter, when metals separate from these soil particles, they enter the soluble soil fraction, being bioavailable and having the potential to bioaccumulate in different organisms [ 56 ].
Microorganisms, plants and invertebrate species have mechanisms to incorporate trace metals for their development and survival e. Also, these same mechanisms facilitate the entrance of non-trace metals As, Cd, Hg and Pb in the organisms, which are highly toxic at low concentrations [ 58 ].
Microorganism are vital elements of soils, they participate in nutrient and inorganic element recycling, like minerals and trace metals, for plants that constitute the first trophic level in terrestrial ecosystems [ 59 ].
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However, HM pollution may affect microorganism communities, generating changes in their structure and biodiversity, which in turn, has consequences on the soil processes in which they participate [ 60 , 61 ]. For example, development alterations and in biochemical processes of microorganism have been reported [ 61 , 62 , 63 ]. Such alterations affect organic matter decomposition process, reducing nutrient accumulation and availability for plants and compromising matter and energy fluxes at the base of the trophic chains [ 61 ].
On the other hand, soil invertebrates can bioaccumulate HM because of their feeding preferences, like crustaceans, snails, and earthworms that inhabit leaf litter and feed on organic matter with high HM concentrations [ 64 , 65 ]. In fact, it has been proven that these invertebrate groups had the highest HM concentrations in comparison to beetles or butterflies, or even higher concentrations than some vertebrate groups [ 18 , 64 ].
In particular, it has been suggested that HM hyperaccumulation by plants as a defense mechanism against herbivores, may transcend to higher trophic levels. For example, the plant Streptanthus polygaloides Brassicaceae is a Ni hyperaccumulator species, that is consumed by the herbivore Melanotrichus boydi Hemiptera who bioaccumulates Ni in its body as a defense mechanism against the predator species Misumena vatia Araneae [ 66 ]. HM transfer along the trophic chains varies depending on the type of metal, the trophic level in question and the number and type of species that integrate it.
Another interesting example is that Cd is more mobile towards herbivores and their predators, while Zn is less efficient in its transfer to higher trophic levels [ 67 , 68 ]. HM transfer along the trophic chain has been reported, for example for the Ni hyperaccumulator plant Alyssum pintodalsilvae Brassicaceae , that transfers Ni to grasshoppers herbivore and spiders carnivorous insect , having the spiders higher Ni concentrations [ 69 ]. Similar results were reported by Boyd and Wall [ 66 ].
These studies demonstrate that HM can be transferred among invertebrate species, mobilizing metals from one trophic level to another, reaching animals such as small mammals [ 70 , 71 , 72 ]. These last studies evaluated HM concentration in small mammals, reporting higher HM levels in carnivorous or omnivorous mammals in comparison to those that feed only by plants. So, HM transfer along the trophic chain not only depends on the magnitude of exposure, but on the species type, season, gender, age and metal type [ 73 ].
Additionally, HM bioaccumulation in plants may also affect interactions with their pollinators, since HM can transfer to nectar, a fact that alters pollinators feeding patterns, suggesting that metals and metalloids such as Se found in pollen and nectar affect negatively the pollinators, which results in changes in plant communities due to the nonappearance of pollinators on such plants [ 74 , 75 , 76 , 77 ].
Most of the studies about metal transfer along trophic chains in terrestrial ecosystems focus on at least three trophic chains levels. In contrast, a study by Hsu and collaborators in more than three trophic levels, they report high levels of Cd, Hg, Pb and Sn and their biomagnification in all analyzed levels, being the snails and the earthworms the groups who registered the highest metal concentrations [ 64 ].
All the aforementioned studies have evaluated HM transfer in small trophic chains in terrestrial ecosystems, the majority of them analyze three trophic levels. These studies are of great importance because the information generated helps to understand the general patterns of HM transfer along trophic chains, especially for the most common metals like Cd, Cu, Pb and Zn. Also, these studies highlight that HM transfer, assimilation and excretion in organisms along the trophic chain, can have extended effects, at the individual level altering their health and physiology at the population level modifying population dynamics, abundance, distribution and their genetic pool at the community level altering species richness and diversity , affecting then, the ecosystem dynamics.
Therefore, is very important to conduct studies where more than three trophic chain levels are analyzed and to integrate new biomarkers e. Chronic environmental metal exposures exert their negative effects on individuals health, having consequences at the population and community levels, putting ecosystem integrity at risk. However, the recognition and use of biomarkers in ecotoxicology has been a difficult task, due to the unspecific responses and multiple variables that affect physiological responses to toxic stress.
Ecological Impacts of Toxic Chemicals
Therefore, it becomes necessary that ecotoxicological studies include: HM concentrations in soils, bioaccumulation parameters in vertebrate and invertebrate species, the relationship between these biomarkers with morphological, anatomic and physiological alterations that may alter population parameters.
In particular, the use of bioindicator or sentinel species is necessary in order to evidence the consequences of HM exposure in wild populations. Terrestrial invertebrates have been used as an ideal system to evaluate community responses to environmental chemical stress, due their easy capture, wide distribution, great abundance, low mobility and close contact to HM from soils. Especially, earthworms and arthropods are the most studied organisms. On the contrary, the studies that evaluate HM effects on vertebrate community structure are scarce, probably due to their body size, mobility and sampling difficulties.
However, when working with vertebrates, an excellent alternative has been the study of small mammal species that serve as good bioindicators and the results may be easily compared to humans. Also, a methodological strategy in many studies has been the use of pollution gradients in order to visualize slight changes in HM concentrations along the soil gradient and to relate these changes to some community structure parameters.
At the moment, we can conclude that HM affect differently the community structure and the community functioning of the different animal groups studied so far. At the community level, the search for new biomarkers continues.
In this context, abundance changes in different guilds that conform the community may also be used as a biomarker since changes in abundance or guild disappearance in exposed communities may serve as an ecological response to chemical stress. At the ecosystem level, ecotoxicological studies are very limited. Trophic chain alterations, biomagnification and modifications in nutrient and energy cycles have been reported.
Studies generally asses HM transfer along three trophic levels, such studies have concluded that metal flux depends on the biology of the species, on the trophic position in the chain and on the metal type or metal mixture in question. Mainly, HM transfer from plants to invertebrate herbivores insects and from insects to other invertebrates spiders or predator vertebrates small mammals has been the point of interest.
The information from these studies has gained attention, especially because human beings represent the last level of the trophic chain, such as in the case of agroecosystems. It is desirable to use as biomarkers in ecosystem studies, measures of stable carbon and nitrogen isotopes for evaluation of HM transfer along terrestrial trophic chains. Finally, it necessary that future efforts integrate different biological and ecological responses across all levels of biological organization as a result of biomarker approaches. Moreover, study designs should be more rigorous, including multispecies and multibiomarkers that permit the evaluation of HM exposure in a more realistic way, which in turn will allow to predict, understand and resolve in a better way HM pollution problems worldwide.
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