{{Short description|Species that reveals the status of an environment}} [[File:Trichoptera caddisfly 1.jpg|thumb|Caddisfly (order Trichoptera), a macroinvertebrate used as an indicator of water quality.<ref name="EPA=RBP">{{cite report |url=https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=20004OQK.txt |title=Rapid Bioassessment Protocols for Use in Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and Fish, Second Edition |last1=Barbour |first1=M.T. |last2=Gerritsen |first2=J. |date=1999 |publisher=U.S. Environmental Protection Agency (EPA) |location=Washington, D.C. |id=EPA 841-B-99-002 |last3=Stribling |first3=J.B.}}</ref>]] 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.<ref>{{Cite journal |title=How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators |url=https://www.researchgate.net/publication/282633318 |journal= Ecological Indicators|year=2016 |language=en |doi=10.1016/j.ecolind.2015.06.036|last1=Siddig |first1=Ahmed A.H. |last2=Ellison |first2=Aaron M. |last3=Ochs |first3=Alison |last4=Villar-Leeman |first4=Claudia |last5=Lau |first5=Matthew K. |volume=60 |pages=223–230 |s2cid=54948928 |doi-access=free |bibcode=2016EcInd..60..223S }}</ref> 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.<ref name="Karr">{{cite journal |last1=Karr |first1=James R. |year=1981 |title=Assessment of biotic integrity using fish communities |journal=Fisheries |volume=6 |issue= 6 |pages=21–27 |doi=10.1577/1548-8446(1981)006<0021:AOBIUF>2.0.CO;2 |bibcode=1981Fish....6f..21K |issn=1548-8446}}</ref>
A '''biological monitor''' or '''biomonitor''' is an organism that provides quantitative information on the quality of the environment around it.<ref>{{cite web |url=http://www.water.ncsu.edu/watershedss/info/biomon.html |title=Biomonitoring |author=NCSU Water Quality Group |website=WATERSHEDSS: A Decision Support System for Nonpoint Source Pollution Control |publisher=North Carolina State University |location=Raleigh, NC |access-date=2016-07-31 |archive-url=https://web.archive.org/web/20160723012523/http://www.water.ncsu.edu/watershedss/info/biomon.html |archive-date=2016-07-23 }}</ref> 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'').<ref>{{cite web |url=https://www.protakscientific.com/biological-indicators |title=Biological ind |author=Protak Scientific |website=Protak Scientific |location=United Kingdom |access-date=2017-08-05 |date=2017-02-03 |archive-date=2019-02-07 |archive-url=https://web.archive.org/web/20190207015759/https://www.protakscientific.com/biological-indicators }}</ref> 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:
# their content of certain elements or compounds # their morphological or cellular structure # metabolic biochemical processes # behaviour # 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.<ref>{{cite book |last1=Tingey |first1=David T. |year=1989 |title=Bio indicators in Air Pollution Research – Applications and Constraints |journal=Biologic Markers of Air-Pollution Stress and Damage in Forests. |pages=73–80 |url=http://www.nap.edu/openbook.php?record_id=1414&page=73 |publisher=National Academies Press |location=Washington, DC |isbn=978-0-309-07833-7}}</ref> 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.<ref>{{cite web |url=https://www.sciencelearn.org.nz/resources/1538-bioindicators |title=Bioindicators |author=<!--Not stated--> |date=2015-02-10 |website=Science Learning Hub |publisher=The University of Waikato, New Zealand}}</ref> Small sets of indicator species can also be used to predict species richness for multiple taxonomic groups.<ref>{{Cite journal |last1=Fleishman |first1=Erica |last2=Thomson |first2=James R. |last3=Mac Nally |first3=Ralph |last4=Murphy |first4=Dennis D. |last5=Fay |first5=John P. |date=August 2005 |title=Using Indicator Species to Predict Species Richness of Multiple Taxonomic Groups |url=https://onlinelibrary.wiley.com/doi/10.1111/j.1523-1739.2005.00168.x |journal=Conservation Biology |language=en |volume=19 |issue=4 |pages=1125–1137 |doi=10.1111/j.1523-1739.2005.00168.x |bibcode=2005ConBi..19.1125F |s2cid=53659601 |issn=0888-8892|url-access=subscription }}</ref>
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|date=October 2023}}
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.<ref name=":2">{{Cite web|url=https://www.epa.gov/sites/default/files/2016-03/documents/nrsa_0809_march_2_final.pdf|title=National Rivers and Streams Assessment 2008-2009: A Collaborative Study|last=U.S. Environmental Protection Agency. Office of Water and Office of Research and Development.|date=March 2016|location=Washington D.C.}}</ref>
Bioaccumulative indicators are frequently regarded as biomonitors. Depending on the organism selected and their use, there are several types of bioindicators.<ref name="bioportal">{{cite web |url=http://www.biobasics.gc.ca/english/View.asp?x=740 |author=Government of Canada |title=Biobasics: bio-indicatorrs |archive-url=https://web.archive.org/web/20111003162258/http://www.biobasics.gc.ca/english/View.asp?x=740 |archive-date=October 3, 2011 }}</ref><ref name=chessman>{{cite book |title=SIGNAL 2 – A Scoring System for Macro-invertebrate ('Water Bugs') in Australian Rivers |last=Chessman |first=Bruce |year=2003 |series=Monitoring River Heath Initiative Technical Report no. 31 |publisher=Commonwealth of Australia, Department of the Environment and Heritage |location=Canberra |isbn=978-0-642-54897-9 |url=http://www.environment.gov.au/water/publications/environmental/rivers/nrhp/pubs/signal.pdf |archive-url=https://web.archive.org/web/20070913163911/http://www.environment.gov.au/water/publications/environmental/rivers/nrhp/pubs/signal.pdf |archive-date=2007-09-13 }}</ref>
=== 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.<ref>{{Cite journal|last1=Lewin|first1=Iga|last2=Czerniawska-Kusza|first2=Izabela|last3=Szoszkiewicz|first3=Krzysztof|last4=Ławniczak|first4=Agnieszka Ewa|last5=Jusik|first5=Szymon|date=2013-06-01|title=Biological indices applied to benthic macroinvertebrates at reference conditions of mountain streams in two ecoregions (Poland, the Slovak Republic)|journal=Hydrobiologia|language=en|volume=709|issue=1|pages=183–200|doi=10.1007/s10750-013-1448-2|issn=1573-5117|doi-access=free|bibcode=2013HyBio.709..183L }}</ref>
An important limitation of bioindicators in general is that they have been reported as inaccurate when applied to geographically and environmentally diverse regions.<ref name=":4">{{Cite journal|last1=Monteagudo|first1=Laura|last2=Moreno|first2=José Luis|date=2016-08-01|title=Benthic freshwater cyanobacteria as indicators of anthropogenic pressures|url=http://www.sciencedirect.com/science/article/pii/S1470160X1630139X|journal=Ecological Indicators|language=en|volume=67|pages=693–702|doi=10.1016/j.ecolind.2016.03.035|bibcode=2016EcInd..67..693M |issn=1470-160X|url-access=subscription}}</ref> 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.<ref>{{Cite journal|last1=Mazor|first1=Raphael D.|last2=Rehn|first2=Andrew C.|last3=Ode|first3=Peter R.|last4=Engeln|first4=Mark|last5=Schiff|first5=Kenneth C.|last6=Stein|first6=Eric D.|last7=Gillett|first7=David J.|last8=Herbst|first8=David B.|last9=Hawkins|first9=Charles P.|date=2016-03-01|title=Bioassessment in complex environments: designing an index for consistent meaning in different settings|journal=Freshwater Science|volume=35|issue=1|pages=249–271|doi=10.1086/684130|bibcode=2016FWSci..35..249M |s2cid=54717345|issn=2161-9549}}</ref>
==Plant and fungal indicators== [[File:Lobaria pulmonaria 010108c.jpg|thumb|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.<ref>{{Cite journal |last1=Caldana |first1=Cristiane R. G. |last2=Hanai-Yoshida |first2=Valquiria M. |last3=Paulino |first3=Thais H. |last4=Baldo |first4=Denicezar A. |last5=Freitas |first5=Nobel P. |last6=Aranha |first6=Norberto |last7=Vila |first7=Marta M. D. C. |last8=Balcão |first8=Victor M. |last9=Oliveira Junior |first9=José M. |date=2023-01-01 |title=Evaluation of urban tree barks as bioindicators of environmental pollution using the X-ray fluorescence technique |url=https://www.sciencedirect.com/science/article/pii/S004565352203750X |journal=Chemosphere |volume=312 |issue=Pt 2 |article-number=137257 |doi=10.1016/j.chemosphere.2022.137257 |pmid=36423726 |bibcode=2023Chmsp.31237257C |issn=0045-6535|url-access=subscription }}</ref> The leaves of certain vascular plants experience harmful effects in the presence of ozone, particularly tissue damage, making them useful in detecting the pollutant.<ref>{{Cite web |title=Bioindicators - Air (U.S. National Park Service) |url=https://www.nps.gov/subjects/air/bioindicators.htm |access-date=2024-03-31 |website=www.nps.gov |language=en}}</ref><ref>{{Cite journal |last=Manning |first=William J. |date=1998 |title=The use of plants as bioindicators of ozone |url=https://research.fs.usda.gov/treesearch/26947 |journal=In: Bytnerowicz, Andrzej; Arbaugh, Michael J.; Schilling, Susan L., Tech. Coords. Proceedings of the International Symposium on Air Pollution and Climate Change Effects on Forest Ecosystems. Gen. Tech. Rep. PSW-GTR-166. Albany, CA: U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station: 19-26 |language=en |volume=166}}</ref> 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.<ref>{{Cite journal |last1=Agathokleous |first1=Evgenios |last2=Feng |first2=Zhaozhong |last3=Oksanen |first3=Elina |last4=Sicard |first4=Pierre |last5=Wang |first5=Qi |last6=Saitanis |first6=Costas J. |last7=Araminiene |first7=Valda |last8=Blande |first8=James D. |last9=Hayes |first9=Felicity |last10=Calatayud |first10=Vicent |last11=Domingos |first11=Marisa |last12=Veresoglou |first12=Stavros D. |last13=Peñuelas |first13=Josep |last14=Wardle |first14=David A. |last15=De Marco |first15=Alessandra |date=2020-08-14 |title=Ozone affects plant, insect, and soil microbial communities: A threat to terrestrial ecosystems and biodiversity |journal=Science Advances |language=en |volume=6 |issue=33 |article-number=eabc1176 |doi=10.1126/sciadv.abc1176 |issn=2375-2548 |pmc=7423369 |pmid=32851188|bibcode=2020SciA....6.1176A }}</ref> 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.
Lichen are well known bio-indicators used to monitor and measure pollution levels. Recognised scales exist allowing the level of pollution to be assessed depending on the species composition present.<ref>{{cite book |last=Walker |first=Mark |date=2024 |title=British Lichens |url=https://www.researchgate.net/publication/396916115 |location=Sheffield, UK |publisher=Sicklebrook publishing |isbn=9781326780197}}</ref> Most well known is the Hawskworth Rose scale. The utility of lichen in this respects comes from the different tolerance different species have to various pollutants, meaning presence and absence of certain key species can be used to gauge overall pollution levels. 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.<ref name="Campbell2004">{{Cite journal |last1=Campbell |first1=Jocelyn |last2=Fredeen |first2=Arthur L |date=2004-07-01 |title=Lobaria pulmonaria abundance as an indicator of macrolichen diversity in Interior CedarHemlock forests of east-central British Columbia |url=http://www.nrcresearchpress.com/doi/10.1139/b04-074 |journal=Canadian Journal of Botany |language=en |volume=82 |issue=7 |pages=970–982 |doi=10.1139/b04-074 |bibcode=2004CaJB...82..970C |issn=0008-4026|url-access=subscription }}</ref> 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.<ref name="Campbell2004" /> 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.<ref>{{Cite journal |last1=Vitali |first1=Matteo |last2=Antonucci |first2=Arianna |last3=Owczarek |first3=Malgorzata |last4=Guidotti |first4=Maurizio |last5=Astolfi |first5=Maria Luisa |last6=Manigrasso |first6=Maurizio |last7=Avino |first7=Pasquale |last8=Bhattacharya |first8=Badal |last9=Protano |first9=Carmela |date=2019-11-01 |title=Air quality assessment in different environmental scenarios by the determination of typical heavy metals and Persistent Organic Pollutants in native lichen Xanthoria parietina |journal=Environmental Pollution |volume=254 |issue=Pt A |article-number=113013 |doi=10.1016/j.envpol.2019.113013 |pmid=31415978 |bibcode=2019EPoll.25413013V |issn=0269-7491}}</ref> 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.<ref>{{Cite journal |last1=Warnasuriya |first1=Sashika D. |last2=Udayanga |first2=Dhanushka |last3=Manamgoda |first3=Dimuthu S. |last4=Biles |first4=Charles |date=September 2023 |title=Fungi as environmental bioindicators |journal=Science of the Total Environment |volume=892 |article-number=164583 |doi=10.1016/j.scitotenv.2023.164583 |pmid=37277042 |bibcode= 2023ScTEn.89264583W|issn=0048-9697}}</ref>
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.<ref>{{Cite news |url=http://content.time.com/time/magazine/article/0,9171,1565508,00.html#ixzz0geEjnTG1 |title=Saving Lives And Limbs With a Weed |last=Halper |first=Mark |date=2006-12-03 |newspaper=Time |access-date=2016-06-22 |archive-date=2016-08-07 |archive-url=https://web.archive.org/web/20160807091036/http://content.time.com/time/magazine/article/0,9171,1565508,00.html#ixzz0geEjnTG1 |url-status=dead }}</ref>
=== Indicator fungi === ''Penicillium'' species, ''Aspergillus niger'' and ''Candida albicans'' are used in the pharmaceutical industry for microbial limit testing, bioburden assessment, method validation, antimicrobial challenge tests, and quality control testing.<ref name="Clontz">{{cite book |last1=Clontz |first1=Lucia |year=2009 |chapter=Microorganisms of interest |title=Microbial Limit and Bioburden Tests: Validation Approaches and Global Requirements, Second Edition |url=https://archive.org/details/microbiallimitbi00clon |url-access=limited |edition=2nd |location=Boca Raton, Florida |publisher=CRC Press |pages=[https://archive.org/details/microbiallimitbi00clon/page/n47 31]–33 |isbn=978-1-4200-5349-4}}</ref> When used in this capacity, ''Penicillium'' and ''A. niger'' are compendial mold indicator organisms.<ref name="Clontz"/>
Molds such as ''Trichoderma'', ''Exophiala'', ''Stachybotrys'', ''Aspergillus fumigatus'', ''Aspergillus versicolor'', ''Phialophora'', ''Fusarium'', ''Ulocladium'' and certain yeasts are used as indicators of indoor air quality.<ref>{{cite book|editor1-last=Jantunen|editor1-first=Matti|editor2-last=Jaakkola|editor2-first=Jouni J. K.|editor3-last=Krzyzanowski|editor3-first=M.|title=Assessment of Exposure to Indoor Air Pollutants, WHO Regional Publications European Series, No. 78|date=1997|publisher=WHO Regional Office Europe|location=Copenhagen|isbn=92-890-1342-7|pages=101–102|chapter=20: Bacteria and fungi}}</ref><ref>{{cite book|last1=Cole|first1=Eugene C.|last2=Dulaney|first2=Pamela D.|last3=Leese|first3=Keith E.|last4=Hall|first4=Richard M.|last5=Foarde|first5=Karin K.|last6=Franke|first6=Deborah L.|last7=Myers|first7=Frank M.|last8=Berry|first8=Michael A.|editor1-last=Tichenor|editor1-first=Bruce A.|title=Characterizing Sources of Indoor Air Pollution and Related Sink Effects, Volume 1287|date=1996|publisher=ASTM International|location=West Conshohocken, PA|isbn=978-0-8031-2030-3|pages=164|chapter=Biopollutant Sampling and Analysis of Indoor Surface Dusts: Characterization of Potential Sources and Sinks}}</ref><ref>{{cite book|last1=Heikkinen|first1=M.S.A.|last2=Hjelmroos-Koski|first2=M.K.|last3=Haggblom|first3=M.M.|last4=Macher|first4=J.M.|editor1-last=Ruzer|editor1-first=L.S.|editor2-last=Harley|editor2-first=N.H.|title=Aerosols Handbook: Measurement, Dosimetry, and Health Effects|date=2004|publisher=CRC Press|location=Boca Raton, Florida|isbn=978-0-203-49318-2|pages=377–378|chapter=Chapter 13: Bioaerosols}}</ref>
Metagenomic techniques allow for the sequencing of whole populations of microorganisms in a single operation. With metagenomic sequencing, it is possible to use the entire community of fungal organisms, or mycobiome in the soil or water of a given area as a biological indicator<ref>{{Cite journal|last1=Bai|first1=Yaohui|last2=Wang|first2=Qiaojuan|last3=Liao|first3=Kailingli|last4=Jian|first4=Zhiyu|last5=Zhao|first5=Chen|last6=Qu|first6=Jiuhui|date=2018-12-21|title=Fungal Community as a Bioindicator to Reflect Anthropogenic Activities in a River Ecosystem|journal=Frontiers in Microbiology|volume=9|page=3152|doi=10.3389/fmicb.2018.03152|issn=1664-302X|pmc=6308625|pmid=30622523|doi-access=free }}</ref> of anthropogenic activity, such as sewage overflow from an urban area or fertilizer and pesticide runoff from an agricultural one.
Composition of fungal communities has been found to be a good indicator of environmental properties like pH, altitude and water temperature. Chauvet<ref>Chauvet E, (1991). "Aquatic hyphomycete distribution in south-western France". ''Journal of Biogeography''. '''18''': 699–706.</ref> used this approach to take ecosystem-wide measurements of these variables using a network of monitoring stations at 27 streams in Southwestern France.
Cudowski ''et al''.<ref>{{Cite journal|date=2015-02-01|title=Aquatic fungi in relation to the physical and chemical parameters of water quality in the Augustów Canal|url=https://www.sciencedirect.com/science/article/abs/pii/S1754504814001330|journal=Fungal Ecology|language=en|volume=13|pages=193–204|doi=10.1016/j.funeco.2014.10.002|issn=1754-5048|last1=Cudowski|first1=A.|last2=Pietryczuk|first2=A.|last3=Hauschild|first3=T.|bibcode=2015FunE...13..193C |url-access=subscription}}</ref> sampled fungi in the water of the Augustow canal in eastern Poland. They took many standard measures of water quality -- temperature, oxygen saturation, pH, and dissolved nitrogen, organic carbon and sulfur levels. They identified species with microscopic methods and RFLP analysis. They found 38 fungal species, including 12 hyphomycetiae and 13 potential pathogens, belonging either to the dermatophytes or to relatives of ''C. albicans''. Cudowski ''et al.'' found that they could determine whether a sample of water had been taken from the natural (lake-like) or artificial part of the canal. They also found that the three major groups of fungi that they found, hyphomycetes, dermatophytes and Candida relatives, could predict many of their water quality measurements, which formed two clusters in a redundancy analysis.
Bouffand ''et al''.<ref>{{Cite journal|date=2016-12-01|title=Indicator species and co-occurrence in communities of arbuscular mycorrhizal fungi at the European scale|url=https://www.sciencedirect.com/science/article/abs/pii/S0038071716303108|journal=Soil Biology and Biochemistry|language=en|volume=103|pages=464–470|doi=10.1016/j.soilbio.2016.09.022|issn=0038-0717|last1=Bouffaud|first1=Marie-Lara|last2=Creamer|first2=Rachel E.|last3=Stone|first3=Dote|last4=Plassart|first4=Pierre|last5=Van Tuinen|first5=Diederik|last6=Lemanceau|first6=Philippe|last7=Wipf|first7=Daniel|last8=Redecker|first8=Dirk|bibcode=2016SBiBi.103..464B |url-access=subscription}}</ref> used Arbuscular Mycorhizzal Fungi (AMF), an asexual clade of fungi that form symbiotic relationships with plant root systems, as indicators to assess soil function and biodiversity in many sites across Europe. They took soil samples in various climatic zones (atlantic, continental, mediterranean, alpine) and three land use regimes (arable, grassland, forestry), and sequenced the DNA of the fungi the soil contained. They found eight indicator species for soil pH: four that were only present when pH was less than 5, three for pH > 5 and one for pH > 7. They found eight indicators of land use: two for forests, five for farm- and grassland, and one for both. They also found one indicator fungus that was present when soil organic carbon was high, and another present when it was low.
==Animal indicators and toxins== [[File:Corvus-brachyrhynchos-001.jpg|thumb|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.<ref>{{Cite report |first1=Jeffrey D. |last1=Grabarkiewicz |first2=Wayne S. |last2=Davis |date=November 2008 |title=An Introduction to Freshwater Fishes As Biological Indicators |url=https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=P1002J1W.TXT |publisher=EPA |id=EPA-260-R-08-016 |page=1}}</ref> 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.<ref>{{Cite journal |last1=Beaulieu |first1=Michaël |last2=Costantini |first2=David |date=2014-01-01 |title=Biomarkers of oxidative status: missing tools in conservation physiology |journal=Conservation Physiology |volume=2 |issue=1 |article-number=cou014 |doi=10.1093/conphys/cou014|pmid=27293635 |pmc=4806730 }}</ref> 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;<ref name="Molluscan">Université Bordeaux et al. [http://molluscan-eye.epoc.u-bordeaux1.fr/index.php?rubrique=accueil&lang=en MolluSCAN ''eye'' project] {{Webarchive|url=https://web.archive.org/web/20161113173444/http://molluscan-eye.epoc.u-bordeaux1.fr/index.php?rubrique=accueil&lang=en |date=2016-11-13 }}</ref> and by assessing changes in individual physiology.<ref>{{Cite journal |last1=França |first1=Filipe |last2=Barlow |first2=Jos |last3=Araújo |first3=Bárbara |last4=Louzada |first4=Julio |date=2016-12-01 |title=Does selective logging stress tropical forest invertebrates? Using fat stores to examine sublethal responses in dung beetles |journal=Ecology and Evolution |volume=6 |issue=23 |pages=8526–8533 |doi=10.1002/ece3.2488|pmid=28031804 |pmc=5167030 |bibcode=2016EcoEv...6.8526F }}</ref>
===Frogs and toads=== Amphibians, particularly anurans (frogs and toads), are increasingly used as bioindicators of contaminant accumulation in pollution studies.<ref name="Simon, E. 2010">Simon, E., Braun, M. & Tóthmérész, B. Water Air Soil Pollut (2010) 209: 467. doi:10.1007/s11270-009-0214-6</ref> Anurans absorb toxic chemicals through their skin and their larval gill membranes and are sensitive to alterations in their environment.<ref name=":0">{{Cite journal |last=Lambert |first=M. R. K. |date=1997-01-01 |title=Environmental Effects of Heavy Spillage from a Destroyed Pesticide Store near Hargeisa (Somaliland) Assessed During the Dry Season, Using Reptiles and Amphibians as Bioindicators |journal=Archives of Environmental Contamination and Toxicology |volume=32 |issue=1 |pages=80–93 |doi=10.1007/s002449900158|pmid=9002438 |bibcode=1997ArECT..32...80L |s2cid=24315472 }}</ref> They have a poor ability to detoxify pesticides that are absorbed, inhaled, or ingested by eating contaminated food.<ref name=":0" /> This allows residues, especially of organochlorine pesticides, to accumulate in their systems.<ref name=":0" /> 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.<ref name=":0" /> 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.<ref name=":1" />
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|date=December 2019|reason=removed citation to predatory publisher content}} 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|date=December 2019|reason=removed citation to predatory publisher content}} Decline of anurans and malformations could also suggest increased exposure to ultra-violet light and parasites.<ref name=":1">Center for Global Environmental Education. What are the frogs trying to tell us? OR Malformed Amphibians. Retrieved from http://cgee.hamline.edu/frogs/archives/corner3.html {{Webarchive|url=https://web.archive.org/web/20220305232717/https://cgee.hamline.edu/frogs/archives/corner3.html |date=2022-03-05 }}</ref> 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.<ref>(Herek et al., 2020)</ref>
Pond-breeding anurans are especially sensitive to pollution because of their complex life cycles, which could consist of terrestrial and aquatic living.<ref name="Simon, E. 2010"/> During their embryonic development, morphological and behavioral alterations are the effects most frequently cited in connection with chemical exposures.<ref>Venturino, A., Rosenbaum, E., De Castro, A. C., Anguiano, O. L., Gauna, L., De Schroeder, T. F., & De D'Angelo, A. P. (2003). Biomarkers of effect in toads and frogs. Biomarkers, 8(3/4), 167.</ref> Effects of exposure may result in shorter body length, lower body mass and malformations of limbs or other organs.<ref name="Simon, E. 2010"/> The slow development, late morphological change, and small metamorph size result in increased risk of mortality and exposure to predation.<ref name="Simon, E. 2010"/>
===Crustaceans=== Crayfish have also been hypothesized as being suitable bioindicators, under the appropriate conditions.<ref>{{Cite journal|last1=Füreder|first1=L.|last2=Reynolds|first2=J. D.|date=2003|url=https://www.kmae-journal.org/articles/kmae/abs/2003/02/kmae2003370p157/kmae2003370p157.html|journal=Bulletin Français de la Pêche et de la Pisciculture|language=en|issue=370–371|pages=157–163|doi=10.1051/kmae:2003011|issn=0767-2861|title=Is Austropotamobius Pallipes a Good Bioindicator?|doi-access=free}}</ref> 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.<ref>{{Cite web |last=Baxter |first=Samantha |date=2023-09-15 |title=Research Brief: Using Red Swamp Crayfish as Bioindicators of Microplastic Pollution |url=https://www.lakescientist.com/research-brief-using-red-swamp-crayfish-as-bioindicators-of-microplastic-pollution/ |access-date=2024-01-18 |website=Lake Scientist |language=en-US}}</ref>
=== Bats === Bats respond noticeably to environmental changes and have therefore been suggested as potentially valuable bioindicators.<ref>{{Cite journal |last1=Jones |first1=G |last2=Jacobs |first2=DS |last3=Kunz |first3=TH |last4=Willig |first4=MR |last5=Racey |first5=PA |date=2009-07-09 |title=Carpe noctem: the importance of bats as bioindicators |journal=Endangered Species Research |volume=8 |pages=93–115 |doi=10.3354/esr00182 |issn=1863-5407}}</ref> Although the number of studies is still relatively small, existing evidence suggests that bats are likely to be excellent indicators in environments like rivers, forests, and urban areas.<ref name=":5">{{Cite journal |last1=Russo |first1=Danilo |last2=Salinas-Ramos |first2=Valeria B. |last3=Cistrone |first3=Luca |last4=Smeraldo |first4=Sonia |last5=Bosso |first5=Luciano |last6=Ancillotto |first6=Leonardo |date=2021-07-21 |title=Do We Need to Use Bats as Bioindicators? |journal=Biology |volume=10 |issue=8 |page=693 |doi=10.3390/biology10080693 |doi-access=free |pmid=34439926 |issn=2079-7737 |pmc=8389320 |bibcode=2021Biol...10..693R }}</ref> Nevertheless, further research across large geographic regions is necessary, and building research networks is essential to achieve this. There are also some challenges in using bats as bioindicators, including the difficulty of distinguishing cryptic species and identifying flying bats through their calls. Additionally, it is often challenging to determine which environmental factors shape bat distribution and behaviour.<ref name=":5" />
=== Indicator helminth eggs === thumb|Identification and quantification of helminth eggs at UNAM university in Mexico City, Mexico The eggs from helminths (parasitic worms) are a commonly used indicator organism to assess the safety of sanitation and wastewater reuse systems (such schemes are also called reuse of human excreta).<ref name="Marcos2">{{Cite journal|last=Von Sperling|first=M.|date=2015|title=Wastewater Characteristics, Treatment and Disposal|url=https://iwaponline.com/ebooks/book/72/|journal=Water Intelligence Online|language=en|volume=6|article-number=9781780402086|doi=10.2166/9781780402086|issn=1476-1777|doi-access=free|url-access=subscription}}</ref>{{rp|55}} This is because they are the most resistant pathogens of all types of pathogens (pathogens can be viruses, bacteria, protozoa and helminths).<ref name=":5a">{{Cite journal |last1=Koné |first1=Doulaye |last2=Cofie |first2=Olufunke |last3=Zurbrügg |first3=Christian |last4=Gallizzi |first4=Katharina |last5=Moser |first5=Daya |last6=Drescher |first6=Silke |last7=Strauss |first7=Martin |date=2007 |title=Helminth eggs inactivation efficiency by faecal sludge dewatering and co-composting in tropical climates |url=https://linkinghub.elsevier.com/retrieve/pii/S0043135407004009 |journal=Water Research |language=en |volume=41 |issue=19 |pages=4397–4402 |doi=10.1016/j.watres.2007.06.024|pmid=17624391 |bibcode=2007WatRe..41.4397K |url-access=subscription }}</ref> It means they are relatively hard to destroy through conventional treatment methods. They can survive for 10–12 months in tropical climates.<ref name=":5a" /> These eggs are also called ''ova'' in the literature.<ref name=":6" />
Helminth eggs that are found in wastewater and sludge stem from soil-transmitted helminths (STHs) which include ''Ascaris lumbricoides'' (Ascaris), ''Anclostoma duodenale'', ''Necator americanus'' (hookworm), and ''Trichuris trichiura'' (whipworm).<ref>{{Cite web|last=Prevention|first=CDC-Centers for Disease Control and|date=2021-01-13|title=CDC - Soil-Transmitted Helminths|url=https://www.cdc.gov/parasites/sth/index.html|access-date=2021-04-27|website=www.cdc.gov|language=en-us}}</ref> Ascaris and whipworm that are identified in reusable wastewater systems can cause certain diseases and complications if ingested by humans and pigs.<ref>{{Cite journal|last1=Navarro|first1=I.|last2=Jiménez|first2=B|date=2011-04-01|title=Evaluation of the WHO helminth eggs criteria using a QMRA approach for the safe reuse of wastewater and sludge in developing countries|url=https://iwaponline.com/wst/article/63/7/1499/14213/Evaluation-of-the-WHO-helminth-eggs-criteria-using|journal=Water Science and Technology|language=en|volume=63|issue=7|pages=1499–1505|doi=10.2166/wst.2011.394|pmid=21508556|bibcode=2011WSTec..63.1499N |issn=0273-1223|url-access=subscription}}</ref> Hookworms will plant and hatch their larvae into the soil where they grow until maturity. Once the hookworm eggs are fully developed, they infect organisms by crawling through the organism's skin.<ref name=":0a">{{Cite journal|last1=Jiménez|first1=B.|last2=Maya|first2=C.|last3=Galván|first3=M.|date=2007-09-01|title=Helminth ova control in wastewater and sludge for advanced and conventional sanitation|url=https://iwaponline.com/wst/article/56/5/43/14049/Helminth-ova-control-in-wastewater-and-sludge-for|journal=Water Science and Technology|language=en|volume=56|issue=5|pages=43–51|doi=10.2166/wst.2007.555|pmid=17881836|issn=0273-1223|doi-access=free|bibcode=2007WSTec..56...43J |url-access=subscription}}</ref>
The presence or absence of viable helminth eggs ("viable" meaning that a larva would be able to hatch from the egg) in a sample of dried fecal matter, compost or fecal sludge is often used to assess the efficiency of diverse wastewater and sludge treatment processes in terms of pathogen removal.<ref name="Marcos2" />{{rp|55}} In particular, the number of viable Ascaris eggs is often taken as an indicator for all helminth eggs in treatment processes as they are very common in many parts of the world and relatively easy to identify under the microscope. However, the exact inactivation characteristics may vary for different types of helminth eggs.<ref name=":22">{{cite journal |author=Maya C., Torner-Morales F.J., Lucario E.S., Hernández E., Jiménez B. |year=2012 |title=Viability of six species of larval and non-larval helminth eggs for different conditions of temperature, pH and dryness |journal=Water Research |volume=46 |issue=15 |pages=4770–4782 |doi=10.1016/j.watres.2012.06.014 |pmid=22794801|bibcode=2012WatRe..46.4770M }}</ref>thumb|Various microscopic images of different types of helminth eggs The technique used for testing depends on the type of sample.<ref name=":6">{{Cite journal|last1=Maya|first1=C.|last2=Jimenez|first2=B.|last3=Schwartzbrod|first3=J.|date=2006|title=Comparison of Techniques for the Detection of Helminth Ova in Drinking Water and Wastewater|url=https://onlinelibrary.wiley.com/doi/abs/10.2175/106143005X89571|journal=Water Environment Research|language=en|volume=78|issue=2|pages=118–124|doi=10.2175/106143005X89571|pmid=16566519|bibcode=2006WaEnR..78..118M |s2cid=46046758 |issn=1554-7531|url-access=subscription}}</ref> When the helminth ova are in sludge, processes such as alkaline-post stabilization, acid treatment, and anaerobic digestion are used to reduce the amount of helminth ova in areas where there is a large amount. These methods make it possible for helminth ova to be within the healthy requirements of ≤1 helminth ova per liter. Dehydration is used to inactivate helminth ova in fecal sludge. This type of inactivation occurs when feces is stored between 1-2 years, a high total solids content (>50-60%) is present, items such as leaves, lime, earth, etc. are added, and at a temperature of 30°C or higher.<ref name=":0a" />
==Microbial indicators==
=== Indicator bacteria === {{main|Indicator bacteria}} Certain bacteria can be used as indicator organisms in particular situations, such as when present in bodies of water. Indicator bacteria themselves may not be pathogenic but their presence in waste may indicate the presence of other pathogens.<ref>{{Cite journal|last1=Noble|first1=R.T|last2=Moore|first2=D.F|last3=Leecaster|first3=M.K|last4=McGee|first4=C.D|last5=Weisberg|first5=S.B|date=April 2003|title=Comparison of total coliform, fecal coliform, and enterococcus bacterial indicator response for ocean recreational water quality testing|journal=Water Research|volume=37|issue=7|pages=1637–1643|doi=10.1016/s0043-1354(02)00496-7|pmid=12600392|bibcode=2003WatRe..37.1637N |issn=0043-1354}}</ref> Similar to how there are various types of indicator organisms, there are also various types of indicator bacteria. The most common indicators are total coliforms, fecal coliforms, ''E. coli'', and enterococci.<ref name=":1a">{{Cite book|title=Chapter 17: Bacteria Indicators of Potential Pathogens. Volunteer Estuary Monitoring: A Methods Manual|publisher=United States Environmental Protection Agency|year=2006}}</ref> The presence of bacteria commonly found in human feces, termed coliform bacteria (e.g. ''E. coli''), in surface water is a common indicator of faecal contamination. The means by which pathogens found in fecal matter can enter recreational bodies of water include, but are not limited to, sewage, septic systems, urban runoff, coastal recreational waste, and livestock waste.<ref name=":1a" />
For this reason, sanitation programs often test water for the presence of these organisms to ensure that drinking water systems are not contaminated with feces. This testing can be done using several methods which generally involve taking samples of water, or passing large amounts of water through a filter to sample bacteria, then testing to see if bacteria from that water grow on selective media such as MacConkey agar. MacConkey agar will only allow the growth of gram-negative bacteria and the bacteria will grow differently according to how it metabolizes lactose or its lack of ability to metabolize it.<ref>{{Citation|last1=Jung|first1=Benjamin|title=MacConkey Medium|date=2021|url=https://www.ncbi.nlm.nih.gov/books/NBK557394/|work=StatPearls|place=Treasure Island (FL)|publisher=StatPearls Publishing|pmid=32491326|access-date=2021-04-26|last2=Hoilat|first2=Gilles J.}}</ref> Alternatively, the sample can be tested to see if it utilizes various nutrients in ways characteristic of coliform bacteria.<ref name="WHO13">{{cite book|url=https://www.who.int/water_sanitation_health/dwq/iwachap13.pdf |access-date=16 July 2016 |title=Assessing Microbial Safety of Drinking Water |publisher=World Health Organization |chapter=13: Indicators of microbial water quality |vauthors=Ashbolt NJ, Grabow WO, Snozzi M |pages=293–295}}</ref>
Coliform bacteria selected as indicators of faecal contamination must not persist in the environment for long periods of time following efflux from the intestine, and their presence must be closely correlated with contamination by other faecal organisms. Indicator organisms need not be pathogenic.<ref>{{cite web |url=http://des.nh.gov/organization/commissioner/pip/factsheets/wwt/documents/web-18.pdf |title=Fecal Coliform as an Indicator Organism |access-date=2007-11-30 |date=2003 |work=Wastewater treatment environmental fact sheet |publisher=New Hampshire Department of Environmental Services |archive-date=4 July 2009 |archive-url=https://web.archive.org/web/20090704133105/http://des.nh.gov/organization/commissioner/pip/factsheets/wwt/documents/web-18.pdf }}</ref>
Non-coliform bacteria, such as ''Streptococcus bovis'' and certain clostridia, may also be used as an index of faecal contamination.<ref>{{cite book |last=Gerardi |first=Michael H. |author2=Mel C. Zimmerman |editor=Michael H. Gerardi |title=Wastewater Pathogens |series=Wastewater Microbiology Series |date= January 2005 |publisher=John Wiley & Sons, Inc. |location=Hoboken, NJ |isbn=978-0-471-20692-7 |page=147 }}</ref>
The presence of indicator bacteria is measured in a variety of ecosystems and sometimes alongside other measurements. In the Great Lakes, a study was conducted testing for both fecal indicator bacteria (FIB) concentrations and pathogen gene markers.<ref name=":2a">Brennan, A. K., Johnson, H. E., Totten, A. R., Duris, J. W., Geological Survey (U.S.), & Great Lakes Restoration Initiative (U.S.). (2015). Occurrence and distribution of fecal indicator bacteria and gene markers of pathogenic bacteria in great lakes tributaries, march-october 2011 (Ser. Open-file report, 2015-1013). U.S. Department of the Interior, U.S. Geological Survey. https://permanent.fdlp.gov/gpo55630/ofr2015-1013.pdf</ref> The FIB measured in this study included fecal coliform bacteria, ''E. coli'', and enterococci.<ref name=":2a" /> FIB were collected via membrane filtration and serial dilution methods, producing samples which could be cultured and used to run PCR and amplify the pathogenic genes in question.<ref name=":2a" /> Among the 22 sampling locations, 165 samples were analyzed and ''E. coli'' concentrations were found to range from less than 2 to 26,000 CFU/100mL, enterococci ranged from less than 2 to 31,000 CFU/100mL, and fecal coliform bacteria ranged from less than 2 to 950 CFU/100mL.<ref name=":2a" />
Another example of indicator bacteria being measured for safety purposes is in Malibu, CA. The state of California requires that beaches with greater than 50,000 visitors a year be monitored for FIB.<ref name=":32">Izbicki, J., Geological Survey (U.S.), & Malibu (Calif.). (2011). Distribution of fecal indicator bacteria along the malibu, california, coastline (Ser. Open-file report, 2011-1091). U.S. Department of the Interior, U.S. Geological Survey. https://permanent.fdlp.gov/gpo138800/ofr20111091.pdf</ref> High FIB concentrations, exceeding what is considered acceptable by the EPA were observed in Malibu Lagoon and other Malibu beaches.<ref name=":32" /> Measurement of high levels of FIB leads to a search to determine what the source(s) is/are. Potential sources of FIB in the Malibu area include waste from sewage treatment systems, runoff from local developments, and wildlife waste.<ref name=":32" /> Common FIB were measured including enterococci which presented itself in levels as high as 242,000 MPN/100mL within onsite wastewater treatment systems.<ref name=":32" /> The measurement of FIB is widespread and used for the purpose of providing safe waters.
In Texas, the occurrence and distribution of FIB, in particular fecal coliforms and ''E. coli'', were measured in streams that receive discharge from the Dallas Fort Worth International Airport and the surrounding area.<ref name=":3a">Harwell, G. R., Mobley, C. A., Mobley, C. A., Dallas-Fort Worth International Airport, Geological Survey (U.S.), Dallas-Fort Worth International Airport, & Geological Survey (U.S.). (2009). Occurrence and distribution of fecal indicator bacteria, and physical and chemical indicators of water quality in streams receiving discharge from dallas/fort worth international airport and vicinity, north-central texas, 2008 (Ser. Scientific investigations report, 2009-5103). U.S. Geological Survey. https://pubs.usgs.gov/sir/2009/5103/pdf/sir2009-5103.pdf</ref> These streams receiving the waste are home to aquatic life, used for recreational purposes, and as fishing sites.<ref name=":3a" /> Various standards exist in order to ensure the safety of all organisms present in the ecosystem, including humans. ''E. coli'' is used as an indicator of unsafe or below standard water quality for recreational use in Texas.<ref name=":4a">Texas Commission on Environmental Quality, 2008a, 2000 Texas surface water quality standards: accessed November 4, 2008, at http://www.tceq.state.tx.us/permitting/water_ quality/wq_assessment/standards/WQ_standards_2000.html</ref> The standards for ''E. coli'' levels that declare contact recreation unsafe are a geometric mean of over 126 cfu/100mL or over a fourth of the samples measuring levels greater than 394cfu/100mL.<ref name=":4a" /> Various sites were tested, some found to exceed acceptable levels of ''E. coli'' and therefore did not support recreational use.<ref name=":3a" /> This is yet another example of how testing for indicator bacteria is used to determine whether bodies of water are safe for various uses, particularly recreational use.
===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|date=March 2024}}
===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|date=March 2024}} 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.<ref>{{cite journal |last1=Rasheed |first1=M. A.|display-authors=et al |title=Application of geo-microbial prospecting method for finding oil and gas reservoirs |journal=Frontiers of Earth Science |date=2015 |volume=9 |issue=1 |pages=40–50 |doi=10.1007/s11707-014-0448-5 |bibcode=2015FrES....9...40R|s2cid=129440067}}</ref>
===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.
[[File:Gravitactism Euglena.png|thumb|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.<ref>{{cite journal |last1=Azizullah |first1=Azizullah |last2=Murad |first2=Waheed |last3=Muhammad |first3=Adnan |last4=Waheed |first4=Ullah |last5=Häder |first5=Donat-Peter |title=Gravitactic orientation of Euglena gracilis - a sensitive endpoint for ecotoxicological assessment of water pollutants |journal=Frontiers in Environmental Science |date=2013 |volume=1 |issue=4 |pages=1–4 |doi=10.3389/fenvs.2013.00004|doi-access=free |bibcode=2013FrEnS...1....4A }}</ref><ref>{{cite journal |last1=Tahedl |first1=Harald |last2=Donat-Peter |first2=Haeder |title=Automated Biomonitoring Using Real Time Movement Analysis of Euglena gracilis |journal=Ecotoxicology and Environmental Safety |volume=48 |issue=2 |pages=161–169 |doi=10.1006/eesa.2000.2004 |pmid=11161690 |year=2001|bibcode=2001EcoES..48..161T }}</ref> Other species such as ''Paramecium biaurelia'' (see ''Paramecium aurelia'') also use gravitactic orientation.<ref>{{cite journal |last1=Hemmersbach |first1=Ruth |last2=Simon |first2=Anja |last3=Waßer |first3=Kai |last4=Hauslage |first4=Jens |last5=Christianen |first5=Peter C.M. |last6=Albers |first6=Peter W. |last7=Lebert |first7=Michael |last8=Richter |first8=Peter |last9=Alt |first9=Wolfgang |last10=Anken |first10=Ralf |title=Impact of a High Magnetic Field on the Orientation of Gravitactic Unicellular Organisms—A Critical Consideration about the Application of Magnetic Fields to Mimic Functional Weightlessness |journal=Astrobiology |date=2014 |volume=14 |issue=3 |doi=10.1089/ast.2013.1085 |pmid=24621307 |pages=205–215 |pmc=3952527|bibcode=2014AsBio..14..205H }}</ref>
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 EC<sub>50</sub> (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).<ref name="ReferenceA">{{cite journal |last1=Tahedl |first1=Harald |last2=Hader |first2=Donat-Peter |title=Fast examination of water quality using the automatic biotest ECOTOX based on the movement behavior of a freshwater flagellate |journal=Water Research | date=1999 |volume=33 |issue=2 |pages=426–432 |doi=10.1016/s0043-1354(98)00224-3|bibcode=1999WatRe..33..426T }}</ref><ref>{{cite journal |last1=Ahmed |first1=Hoda |last2=Häder |first2=Donat-Peter |title=Monitoring of Waste Water Samples Using the ECOTOX Biosystem and the Flagellate Alga Euglena gracilis |journal=Water, Air, & Soil Pollution |date=2011 |volume=216 |issue=1–4 |pages=547–560 |doi=10.1007/s11270-010-0552-4|bibcode=2011WASP..216..547A |s2cid=98814927 }}</ref>
==Macroinvertebrates==
Macroinvertebrates are useful and convenient indicators of the ecological health of water bodies<ref name =waterbug>{{cite book |title=The Waterbug Book: A Guide to the Freshwater Macroinvertebrates of Temperate Australia |last1= Gooderham |first1= John |last2= Tsyrlin |first2= Edward |year=2002 |publisher=CSIRO Publishing |location=Collingswood, Victoria |isbn=0-643-06668-3 |url=https://books.google.com/books?id=0_Paklse3XcC&pg=PP1 }}</ref> and terrestrial ecosystems.<ref>{{Cite journal |last1=Bicknell |first1=Jake E. |last2=Phelps |first2=Simon P. |last3=Davies |first3=Richard G. |last4=Mann |first4=Darren J. |last5=Struebig |first5=Matthew J. |last6=Davies |first6=Zoe G. |title=Dung beetles as indicators for rapid impact assessments: Evaluating best practice forestry in the neotropics |journal=Ecological Indicators |volume=43 |pages=154–161 |doi=10.1016/j.ecolind.2014.02.030|year=2014 |bibcode=2014EcInd..43..154B }}</ref><ref>{{Cite journal |url=http://www.aloki.hu/indvol12_2.htm |title=Structure and composition of edaphic arthropod community and its use as bioindicators of environmental disturbance |last1=Beiroz |first1=W. |last2=Audino |first2=L. D. |date=2014 |journal=Applied Ecology and Environmental Research |issn=1785-0037 |access-date=2017-08-02 |last3=Rabello |first3=A. M. |last4=Boratto |first4=I. A. |last5=Silva |first5=Z |last6=Ribas |first6=C. R.|volume=12 |issue=2 |pages=481–491 |doi=10.15666/aeer/1202_481491 |doi-access=free |bibcode=2014ApEER..12..481B }}</ref> 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.<ref name=":3" /> 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.<ref name=":3" /> 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.<ref name=":2a" /> Tolerance values are commonly used to assess ecological effects of water pollution<ref>{{cite journal |author= Chang, F.C. |author2=J.E. Lawrence |author5=B. Rios-Touma |author6=V.H. Resh |name-list-style=amp |title= Tolerance Values of Benthic Macroinvertebrates for Stream Biomonitoring: Assessment of Assumptions Underlying Scoring Systems Worldwide |journal= Environmental Monitoring and Assessment |year=2014 |volume=186 |issue= 4 | pages=2135–2149 |doi=10.1007/s10661-013-3523-6 |pmid= 24214297 |bibcode=2014EMnAs.186.2135C |s2cid=39590510 }}</ref> such as pesticide contamination with the SPEAR system<ref>{{Cite journal |last1=Liess |first1=Matthias |last2=Liebmann |first2=Liana |last3=Vormeier |first3=Philipp |last4=Weisner |first4=Oliver |last5=Altenburger |first5=Rolf |last6=Borchardt |first6=Dietrich |last7=Brack |first7=Werner |last8=Chatzinotas |first8=Antonis |last9=Escher |first9=Beate |last10=Foit |first10=Kaarina |last11=Gunold |first11=Roman |last12=Henz |first12=Sebastian |last13=Hitzfeld |first13=Kristina L. |last14=Schmitt-Jansen |first14=Mechthild |last15=Kamjunke |first15=Norbert |date=2021-08-01 |title=Pesticides are the dominant stressors for vulnerable insects in lowland streams |url=https://linkinghub.elsevier.com/retrieve/pii/S0043135421004607 |journal=Water Research |language=en |volume=201 |article-number=117262 |doi=10.1016/j.watres.2021.117262|pmid=34118650 |bibcode=2021WatRe.20117262L |url-access=subscription }}</ref> and environmental degradation, such as human activities (e.g. selective logging and wildfires) in tropical forests.<ref>{{Cite journal |last1=Barlow |first1=Jos |last2=Lennox |first2=Gareth D. |last3=Ferreira |first3=Joice |last4=Berenguer |first4=Erika |last5=Lees |first5=Alexander C. |last6=Nally |first6=Ralph Mac |last7=Thomson |first7=James R. |last8=Ferraz |first8=Silvio Frosini de Barros |last9=Louzada |first9=Julio |title=Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation |journal=Nature |volume=535 |issue=7610 |pages=144–147 |doi=10.1038/nature18326|pmid=27362236 |year=2016 |bibcode=2016Natur.535..144B |s2cid=4405827 |url=https://e-space.mmu.ac.uk/617293/11/author%20accepted%281%29.pdf }}</ref><ref>{{Cite journal |last1=França |first1=Filipe |last2=Louzada |first2=Julio |last3=Korasaki |first3=Vanesca |last4=Griffiths |first4=Hannah |last5=Silveira |first5=Juliana M. |last6=Barlow |first6=Jos |s2cid=67849288 |date=2016-08-01 |title=Do space-for-time assessments underestimate the impacts of logging on tropical biodiversity? An Amazonian case study using dung beetles |journal=Journal of Applied Ecology |volume=53 |issue=4 |pages=1098–1105 |doi=10.1111/1365-2664.12657 |issn=1365-2664|doi-access=free |bibcode=2016JApEc..53.1098F }}</ref>
=== 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.<ref name=":2" /> 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.<ref>{{cite web |title=Aquatic Macroinvertebrates |url=https://extension.usu.edu/waterquality/learnaboutsurfacewater/propertiesofwater/aquaticmacros |website=Water Quality |publisher=Utah State University Extension |location=Logan, UT |access-date=2020-10-11}}</ref> 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.<ref name=":2" /> 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.<ref name=":2" /> Benthic indicators are the most frequently used water quality test within the United States.<ref name=":2" /> 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.<ref>{{Cite journal |last1=Smith |first1=A. J. |last2=Duffy |first2=B. T. |last3=Onion |first3=A. |last4=Heitzman |first4=D. L. |last5=Lojpersberger|first5=J. L.|last6=Mosher|first6=E. A.|last7=Novak|first7=M. A .|date=2018 |title=Long-term trends in biological indicators and water quality in rivers and streams of New York State (1972–2012)|journal=River Research and Applications |volume=34 |issue=5 |pages=442–450 |doi=10.1002/rra.3272 |bibcode=2018RivRA..34..442S |s2cid=133650984 |issn=1535-1467}}</ref>
=== Global context === In Europe, the Water Framework Directive (WFD) went into effect on October 23, 2000.<ref>{{Cite web |url=https://ec.europa.eu/environment/water/water-framework/index_en.html |title=The EU Water Framework Directive - integrated river basin management for Europe |website=Environment |publisher=European Commission |date=2020-08-04}}</ref> 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<ref name=":4" /> 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).<ref name="Molluscan" />
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.<ref name="EPA=RBP" /><ref>{{cite web |url=http://www.iwla.org/index.php?ht=display/ContentDetails/i/1479/pid/1976 |title=Biological Stream Monitoring |author=<!--Staff writer(s); no by-line.--> |publisher=Izaak Walton League of America |access-date=2010-08-14 |archive-url=https://web.archive.org/web/20150421203157/http://www.iwla.org/index.php?ht=display%2FContentDetails%2Fi%2F1479%2Fpid%2F1976 |archive-date=2015-04-21 }}</ref><ref>{{cite report |date=November 1997 |title=Volunteer Stream Monitoring: A Methods Manual |url=https://www.epa.gov/sites/default/files/2015-06/documents/stream.pdf |publisher=EPA |id=EPA 841-B-97-003}}</ref>
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.<ref name=":3">{{cite journal | last1 = Dickens | first1 = CWS | last2 = Graham | first2 = PM | year = 2002 | title = The Southern Africa Scoring System (SASS) version 5 rapid bioassessment for rivers | url = http://www.dwa.gov.za/iwqs/rhp/methods/dickens%20and%20graham.pdf | journal = African Journal of Aquatic Science | volume = 27 | pages = 1–10 | doi = 10.2989/16085914.2002.9626569 | s2cid = 85035010 | access-date = 2011-11-16 | archive-url = https://web.archive.org/web/20160328153218/https://www.dwa.gov.za/iwqs/rhp/methods/dickens%20and%20graham.pdf | archive-date = 2016-03-28 }}</ref> 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|date=October 2023}}
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.<ref name=CobImposex>{{cite journal |last=Cob |first=Z. C. |author2=Arshad, A. |author3=Bujang, J. S. |author4= Ghaffar, M. A. |title=Description and evaluation of imposex in ''Strombus canarium'' Linnaeus, 1758 (Gastropoda, Strombidae): a potential bio-indicator of tributyltin pollution |journal=Environmental Monitoring and Assessment |year=2011 |volume=178 |issue=1–4 |pages=393–400 |doi=10.1007/s10661-010-1698-7 |pmid=20824325|bibcode=2011EMnAs.178..393C |s2cid=207130813 |url=http://psasir.upm.edu.my/id/eprint/23629/1/Description%20and%20evaluation%20of%20imposex%20in%20Strombus%20canarium%20Linnaeus.pdf }}</ref>
==See also== {{div col|colwidth=30}} * Biological integrity * Biological monitoring working party (a measurement procedure) * Biosignature * Ecological indicator * Environmental indicator * Indicator value * Sentinel species {{div col end}}
==References== {{Reflist|30em}}
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
==Further reading== * {{cite book |last1=Caro |first1=Tim |title=Conservation by proxy: indicator, umbrella, keystone, flagship, and other surrogate species |date=2010 |publisher=Island Press |location=Washington, DC |isbn=978-1-59726-192-0|author-link=Tim Caro}}
==External links== {{Commons category|Bioindicators}} * [https://web.archive.org/web/20070608035034/http://biomarkers.pnl.gov/ Environmental Biomarkers Initiative at Pacific Northwest National Laboratory] – U.S. Department of Energy, Richland, WA * [https://www.epa.gov/nps/nonpoint-source-volunteer-monitoring Volunteer Monitoring Program] – U.S. EPA * [https://web.archive.org/web/20180311062607/http://www.dwa.gov.za/iwqs/rhp/index.html The National River Health Programme] – South Africa * [http://isebindia.com/09-12/10-01-3.html ''Pyxine cocoes'' Nyl. – A Foliose Lichen as a Potential Bio-indicator/Bio-monitor of Air Pollution in Philippines: An Update] {{Webarchive|url= https://web.archive.org/web/20170810164449/http://isebindia.com/09-12/10-01-3.html |date=2017-08-10 }} by Isidro A. T. Savillo * [https://www.protakscientific.com/biological-indicators ''Biological Indicators for Sterilization''] {{Webarchive|url=https://web.archive.org/web/20190207015759/https://www.protakscientific.com/biological-indicators |date=2019-02-07 }} – Protak Scientific
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Category:Bioindicators Category:Community ecology Category:Conservation biology Category:Ecology terminology Category:Ecotoxicology Category:Habitat Category:Measurement of biodiversity Category:Water quality indicators Category:Water pollution Category:Indicators Category:Environmental and ecological indicators