Pollution-induced community tolerance (PICT)
is an approach to measuring the response of
pollution
Pollution is the introduction of contaminants into the natural environment that cause adverse change. Pollution can take the form of any substance (solid, liquid, or gas) or energy (such as radioactivity, heat, sound, or light). Pollutants, the ...
-induced selective pressures on a community. It is an
eco-toxicological tool that approaches community
tolerance to pollution from a holistic standpoint. Community Tolerance can increase in one of three ways: physical
adaptations
In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process of natural selection that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the p ...
or
phenotypic plasticity
Phenotypic plasticity refers to some of the changes in an organism's behavior, morphology and physiology in response to a unique environment. Fundamental to the way in which organisms cope with environmental variation, phenotypic plasticity encompa ...
, selection of favorable
genotype
The genotype of an organism is its complete set of genetic material. Genotype can also be used to refer to the alleles or variants an individual carries in a particular gene or genetic location. The number of alleles an individual can have in a ...
s, and the replacement of sensitive
species
In biology, a species is the basic unit of classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of the appropriate s ...
by tolerant species in a
community
A community is a social unit (a group of living things) with commonality such as place, norms, religion, values, customs, or identity. Communities may share a sense of place situated in a given geographical area (e.g. a country, village, tow ...
.
PICT differs from the population tolerance approach to community tolerance in that it can be easily applied to any ecosystem and it is not critical to use a representative test organism, as with the population tolerance approach.
Community tolerance
Community tolerance can be used as indicator for determining if a
toxicant
A toxicant is any toxic substance, whether man-made or naturally occurring. By contrast, a toxin is a poison produced naturally by an organism (e.g. plant, animal, insect). The different types of toxicants can be found in the air, soil, water, or ...
has a
disturbance
Disturbance and its variants may refer to:
Math and science
* Disturbance (ecology), a temporary change in average environmental conditions that causes a pronounced change in an ecosystem
* Disturbance (geology), linear zone of faults and folds ...
on an exposed community for multiple types of
organism
In biology, an organism () is any living system that functions as an individual entity. All organisms are composed of cells (cell theory). Organisms are classified by taxonomy into groups such as multicellular animals, plants, and ...
s.
Tolerance of a toxicant can increase by three ways: physiological adaptation, also known as the phenotypic plasticity of an individual; tolerant genotypes selected within a population over time; and the replacement of species with more tolerant ones within a community.
Physiological adaptation, or phenotypic plasticity, is the ability of an individual organism to change its
phenotype
In genetics, the phenotype () is the set of observable characteristics or traits of an organism. The term covers the organism's morphology or physical form and structure, its developmental processes, its biochemical and physiological proper ...
in response to changes in the environment.
[Miner, Benjamin G., Sonia E. Sultan, Steven G. Morgan, Dianna K. Padilla, and Rick A. Relyea. 12 December 2005. "Ecological Consequences of Phenotypic Plasticity." Elsevier. Trends in Ecology and Evolution. 20 (12): 685–692). http://bama.ua.edu/~rlearley/Miner_2005.pdf.] This can occur with huge variance between the type of organism and the type of the disturbance they experience.
Natural selection
Natural selection is the differential survival and reproduction of individuals due to differences in phenotype. It is a key mechanism of evolution, the change in the heritable traits characteristic of a population over generations. Charle ...
that occurs over several generations causes an entire population to exhibit specific selection of genotypes.
[Darwin, Charles. 1859. "Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life." London: John Murray. 1st Edition. http://graphics8.nytimes.com/packages/images/nytint/docs/charles-darwin-on-the-origin-of-species/original.pdf] Over time, tolerant genotypes can be selected over non-tolerant ones and can cause a shift in a population’s
genome
In the fields of molecular biology and genetics, a genome is all the genetic information of an organism. It consists of nucleotide sequences of DNA (or RNA in RNA viruses). The nuclear genome includes protein-coding genes and non-coding ge ...
.
[Blanck, Hans. 22 September 2010. “A Critical Review of Procedures and Approaches Used for Assessing Pollution-Induced Community Tolerance (PICT) in Biotic Communities, Human and Ecological Risk Assessment.” Human and Ecological Risk Assessment. 8 (5): 1003–1034. http://www.tandfonline.com/doi/pdf/10.1080/1080-700291905792.] Natural selection can also cause a replacement of less tolerant species with more tolerant species.
All of these aspects can alter a community's structure drastically, and if a toxicant can be identified as the culprit, action can take place to prevent the accumulation and environmental impacts of that toxicant.
PICT can be used for linkage between cause (exposure) and effect of the toxicants due to the structure of a community that has survived the event, also known as toxicant-induced succession (TIS).
Toxicant-induced succession would be the development of more tolerant generations once a chemical was introduced into the environment. This is why the PICT method is most often applied to communities with short generation times such as microbial and algal communities,
whereas there are rare works that use the PICT tool on organisms other than microorganisms.
There are two types of tolerances that can occur: multiple and co-tolerance.
Multiple tolerances can elevate an individual' ability to tolerate several toxicants present at once.
This means that the type of chemicals present in the environment, the
concentration
In chemistry, concentration is the abundance of a constituent divided by the total volume of a mixture. Several types of mathematical description can be distinguished: '' mass concentration'', ''molar concentration'', ''number concentration'', an ...
, and the organisms that are affected could alter the environment in multiple different ways. Co-tolerance is the ability of an organism to develop a tolerance to a certain toxicant in short-term tests, and obtain that tolerance for other toxicants similar to the first.
Furthermore, co-tolerance depends on the interaction of different factors, such as the toxicant to which communities have been chronically exposed, the mode(s) of action of the different toxicants, but also the detoxification mechanisms implemented by the organisms, and the targeted biological community (e.g., heterotrophs, heterotrophs)
It can be difficult to determine which type of tolerance is occurring if there are multiple types of toxicants in a community because they could be acting simultaneously. Basically it is difficult to understand what exactly may be going on in a community without testing it with multiple ecotoxicological tools with long- and short-term toxicity tests. However, in the context of biomonitoring with the PICT method, co-tolerance could be an advantage, as it would allow working step by step. A first step would then be to use a model toxicant from a class of pollutants (selected on the basis of their co-tolerance properties) in order to limit the number of suspect pollutants in the ecotoxicological assessment of an environment
For example, a PICT study on soil in microcosms amended with organic manure observed co-tolerance only between antibiotics of the same group (oxytetracycline and tetracycline), as expected from their identical mode of action. This type of approach is still preliminary, there is a need for further in situ studies combining PICT with chemical monitoring of environments, experimental work under controlled laboratory conditions, and integration of PICT into modeling approaches to precise theses parterns of co-tolerance.
A complementary approach derived from Pesce et al. (2011) and Foulquier et al. (2015) was recently applied by Tlili et al (2020), combining passive sampling systems with PICT bioassays on river biofilms collected upstream and downstream of wastewater treatment plants at two-year intervals (before and after a change in effluent treatment). Their results demonstrate the value of combining the PICT approach with the use of passive sampler extracts to establish causality between in situ exposure to complex mixtures of micropollutants and ecotoxic effects on autotrophic and heterotrophic microbial communities.
Field studies
Assessing pollution-induced community tolerance can be done utilizing
in situ
''In situ'' (; often not italicized in English) is a Latin phrase that translates literally to "on site" or "in position." It can mean "locally", "on site", "on the premises", or "in place" to describe where an event takes place and is used in ...
techniques, many of which involve the use of known or created chemical exposure gradients. One example is the use of a known concentration gradient of
Tri-n-butylin to assess PICT in
periphyton
Periphyton is a complex mixture of algae, cyanobacteria, heterotrophic microbes, and detritus that is attached to submerged surfaces in most aquatic ecosystems. The related term Aufwuchs (German "surface growth" or "overgrowth") refers to the col ...
.
Tolerance patterns showed that tolerance was highest closest to the marina that was the source of contamination. The use of reference sites in addition to contaminated sites is also commonly used for translocation assessments of PICT. A study in Germany cultured periphyton on glass discs in two river systems north of Leipzig, Germany. One system was the contaminated area of study and the other was 10 km upstream and uncontaminated, intended to be used as a reference. After the colonization period, 6 of the 10 racks of glass discs were trans-located to the other river system. During the experiment the community structure present on the glass discs from the reference site, when translocated to the contaminated site changed to mirror that of the control discs that were left in the contaminated sites.
Note the interest of using long-term observation sites to address the consequences of contamination and restoration of environments with PICT. One example is th
Ardières-Morcille river hydrology observatoryin the Beaujolais (vineyard region, France) where numerous in situ PICT studies have been conducted,
and which has also been used for many PICT experiments in the laboratory (see for example ). Of particular note at this site is the study conducted by Pesce et al. (2016) during three consecutive years (2009-2011): The authors monitored the decrease in tolerance of periphyton to diuron (herbicide applied in vineyards and banned since 2008) downstream of the river crossing this wine-growing watershed. Their results showed a direct link between the evolution of an agricultural practice (here the banning of diuron) and ecological changes in the river (through the loss of tolerance measured by the PICT). Lake Geneva is one of the subalpine lakes studied for a long time by the International Commission for the Protection of Lake Geneva (
CIPEL). A PICT study carried out 12 years apart showed the restoration of the lake's phytoplankton with a concomitant decrease in the tolerance of the communities towards atrazine and copper and in the concentrations of these two contaminants (following legislation limiting the use of atrazine in agriculture and framing the management of industrial waste). In another study in Denmark, enclosure experiments were done allowing for an assessment of PICT utilizing the lake water from Lake Bure as a baseline. By using this water from the lake potentially confounding variables would be nullified by comparing results to the control. Concentrations of
atrazine
Atrazine is a chlorinated herbicide of the triazine class. It is used to prevent pre-emergence broadleaf weeds in crops such as maize (corn), soybean and sugarcane and on turf, such as golf courses and residential lawns. Atrazine's primary manufa ...
and
copper
Copper is a chemical element with the symbol Cu (from la, cuprum) and atomic number 29. It is a soft, malleable, and ductile metal with very high thermal and electrical conductivity. A freshly exposed surface of pure copper has a pinkis ...
were added to these enclosures in varying concentrations. As in other experiments previously discussed periphyton communities were used in this experiment and were cultured using glass discs.
Photosynthetic
Photosynthesis is a process used by plants and other organisms to convert light energy into chemical energy that, through cellular respiration, can later be released to fuel the organism's activities. Some of this chemical energy is stored in c ...
activity was measured and used as a measurement of PICT throughout the experiment. The experiment showed that elevated levels of Cu lead to community tolerance of the phytoplankton community as well as co-tolerance of zinc. Total
Biomass
Biomass is plant-based material used as a fuel for heat or electricity production. It can be in the form of wood, wood residues, energy crops, agricultural residues, and waste from industry, farms, and households. Some people use the terms bi ...
decreased at the outset of the trials involving high concentrations of Cu indicating that Community Tolerance was increased due to direct mortality of the sensitive species.
The in situ study of Bérard & Benninghoff, (2001) in enclosures repeated over several years in the lake of Geneva, showed that the tolerance of phytoplankton to the herbicide atrazine (photosynthesis inhibitor) varied according to the seasons during which the experiment was carried out. These changes in tolerance for the same toxicant and at the same concentration (10 µg L-1) were probably linked to the initial compositions of the algal and cyanobacterial communities and to environmental factors associated with seasonal parameters (temperature, light, nutrients, etc.). PICT studies on large spatial scales are rare and difficult to conduct, note this European study by Blanck et al (2003) on zinc tolerance in river periphyton.
The use of PICT in an in situ fashion is not limited to aquatic systems. Studies on soil microbial communities have been conducted in industrial and agricultural contexts (see the review of Boivin et al., 2002). Thus, for examples in the context of industrial contamination a study involving
2,4,6-Trinitrotoluene utilized
respirometric techniques to measure Pollution-Induced Community Tolerance in soil microbial communities in response to the presence of TNT. The results of this study further corroborate the PICT Theory, in that treatments with long-term exposure to TNT had a larger proportion of TNT-resistant bacteria than soils with low levels of TNT.
This PICT caused by TNT was also present in another study.
Microrespirometry measurements carried out on soil samples taken along three transects have highlighted the tolerance to Pb in a site bordering a lead smelter with long-term polymetallic contamination dominated by Pb. The PICT established causal relationships between Pb and its effect on microbial communities by considering the history of environmental contamination at the community level. Furthermore, a positive correlation between community metabolic quotient and PICT suggested that the acquisition of Pb stress-induced tolerance would have resulted in a higher energetic cost for microbial communities to cope with metal toxicity. Other studies have highlighted in various contexts, this cost of contaminant-induced tolerance.
In the context of agricultural contamination, Bérard et al. (2004) validated the PICT tool (by measuring photosynthetic activity) for atrazine tolerance on edaphic microalgae, comparing soils of conventionally and organically farmed corn fields. Changes in taxonomic structure of diatom communities sampled from soils under both types of farming practices, as well as nanocosm experiments, confirmed the selective effect of atrazine. In terrestrial environment, the PICT method is widely applied to metal contamination and since 2010, to antibiotic tolerance in interaction with metal contamination.
Ideally, pollution-induced community tolerance can be assessed in the field by using a representative sample of the natural community in response to environmental contamination. However, this is not always the case, which is why laboratory studies are necessary supplements to properly assess PICT.
Experimental studies
Experimental investigation of PICT is perform to eliminate factors other than pollution that may affect community structure and ecophysiology,
or on the contrary to study them (by controlling them).
Much work has been done in controlled systems (see reviews by Blanck, 2002
and Tlili et al. 2016
). They can be conducted in conjunction with field work, as in the study by Blanck and Dahl (1996). In this study, the results from laboratory acute toxicity tests of TBT on periphyton corroborated the results from the field study, supporting the conclusion that toxicity to periphyton resulted from TBT pollution at the site under investigation.
The results from
acute toxicity
Acute toxicity describes the adverse effects of a substance that result either from a single exposure or from multiple exposures in a short period of time (usually less than 24 hours). To be described as ''acute'' toxicity, the adverse effect ...
tests can thus help determine whether the effect identified is due to a specific contaminant. Bérard et al. (2003) used experimental systems of increasing complexity associated with monitoring of sites in Lake Geneva more or less contaminated by Irgarol (antifouling inhibitor of photosynthesis), and crossed the results of ecotoxicity of strains isolated from these sites and from non-contaminated control sites with experiments in nanocosms and PICT measurements. This work highlighted the high toxicity of Irgarol (compared to atrazine having the same site of action, and presenting a co-tolerance) on periphyton and phytoplankton and its potential for selection pressure at existing concentrations in the lake.
The PICT methodology
There are a variety of methods for laboratory testing PICT, but a general format includes
sampling, a
bioassay
A bioassay is an analytical method to determine the concentration or potency of a substance by its effect on living animals or plants (''in vivo''), or on living cells or tissues(''in vitro''). A bioassay can be either quantal or quantitative, dir ...
, and an analysis of community structure.
Samples can be collected on artificial or natural substrata, either
in situ
''In situ'' (; often not italicized in English) is a Latin phrase that translates literally to "on site" or "in position." It can mean "locally", "on site", "on the premises", or "in place" to describe where an event takes place and is used in ...
or in the laboratory.
[Blanck, Hans. 1985. “A simple, community level, ecotoxicological test system using samples of periphyton”. Hydrobiologia. 124: 251–261.] There must be a series of samples exposed to different concentrations of contaminant and a
control
Control may refer to:
Basic meanings Economics and business
* Control (management), an element of management
* Control, an element of management accounting
* Comptroller (or controller), a senior financial officer in an organization
* Controllin ...
sample. In situ sampling involves setting up a sampling device in an aquatic ecosystem and allowing it to colonize for some time (e.g. a couple of weeks). One example is the diatometer, a device that is deployed in the water that becomes colonized by
diatoms
A diatom (New Latin, Neo-Latin ''diatoma''), "a cutting through, a severance", from el, διάτομος, diátomos, "cut in half, divided equally" from el, διατέμνω, diatémno, "to cut in twain". is any member of a large group com ...
, and then is removed for analysis.
[“Tools of a Scientist”. Urban Rivers Awareness. 2004.] In situ sampling devices are set up at increasing distances from the pollution source in the case of
point source pollution
A point source of pollution is a single identifiable source of air, water, thermal, noise or light pollution. A point source has negligible extent, distinguishing it from other pollution source geometries (such as nonpoint source or area source) ...
. The samples thus represent a gradient in contaminant concentration, assuming that the contaminant becomes more dilute with increasing distance from the point source. An example of laboratory sampling was used in a study by Schmitt-Jansen and Altenburger (2005). For 14 days communities were allowed to establish on discs set up in laboratory aquariums which were continuously mixed and inoculated with
algae
Algae (; singular alga ) is an informal term for a large and diverse group of photosynthetic eukaryotic organisms. It is a polyphyletic grouping that includes species from multiple distinct clades. Included organisms range from unicellular mic ...
from a pond. The aquariums were dosed with different concentrations of
herbicide
Herbicides (, ), also commonly known as weedkillers, are substances used to control undesired plants, also known as weeds.EPA. February 201Pesticides Industry. Sales and Usage 2006 and 2007: Market Estimates. Summary in press releasMain page fo ...
to get a gradient of long-term (14-day) contaminant exposures. Once a week the aquarium water was completely replaced and re-dosed with herbicide.
Terrestrial studies pose other difficulties because it is difficult to use colonization systems by the communities investigated. Generally one samples the soil with its intrinsic heterogeneity and components other than microorganisms (minerals, organics ..), which increases measurement difficulties and biases related to contaminant bioavailability.
A
bioassay
A bioassay is an analytical method to determine the concentration or potency of a substance by its effect on living animals or plants (''in vivo''), or on living cells or tissues(''in vitro''). A bioassay can be either quantal or quantitative, dir ...
is conducted on the samples to test for correlation between tolerance and long-term contaminant exposure. First, samples are exposed to different concentrations of contaminant. Then an endpoint is measured to determine the toxic effect on the sample organisms. The results from these measurements are used to produce a dose-response curve and an
EC50
]
Half maximal effective concentration (EC50) is a measure of the concentration of a drug, antibody or toxicant which induces a Stimulus%E2%80%93response_model, response halfway between the baseline and maximum after a specified exposure time. Mo ...
.
Both Blanck (1996) and Schmitt-Jansen and Altenburger (2005)
photosynthesis
Photosynthesis is a process used by plants and other organisms to convert light energy into chemical energy that, through cellular respiration, can later be released to fuel the organism's activities. Some of this chemical energy is stored i ...
as their endpoint.
Since the work of Blanck et al. (1988), other endpoints have been tested such as: induced fluorescence, PAM fluorimetry,
leucine incorporation and eco-plates,
microbial respiration,
enzyme activities,
potential ammonium oxidation assay
... In order to use the PICT method in biomonitoring and environmental risk assessment, it is necessary to advance in the standardization of these bioassays, both for the sampling of the tested communities, but also for the bioassays themselves.
Community structure of the samples is analyzed to check for a correlation between species prevalence and long-term contaminant exposure. Samples are
taxonomically
In biology, taxonomy () is the scientific study of naming, defining ( circumscribing) and classifying groups of biological organisms based on shared characteristics. Organisms are grouped into taxa (singular: taxon) and these groups are given ...
classified to determine the composition and
species diversity
Species diversity is the number of different species that are represented in a given community (a dataset). The effective number of species refers to the number of equally abundant species needed to obtain the same mean proportional species abundan ...
of the communities that established over the long term exposures. The results are compared to the concentration of contaminant in the long-term exposure to conclude if a relationship was found in the study.
Recent developments in microbial ecology using molecular biology and "omics" methods, chemotaxonomy methods,
functional diversity measurements,
biological trait and biological interaction network approaches,
are varied, complementary and promising ecological tools to address PICT selection pressure.
References
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