Bioindicators and their Applications: A Comprehensive Review
Subject Areas : Journal of Chemical Health Risks
Mohammad Hossein Bahranipour
1
(Department of Biotechnology, Faculty of Converging Sciences and Technologies, Islamic Azad University, Science and Research Branch, Tehran, Iran)
Nazanin Geravand
2
(Department of Biotechnology, Faculty of Converging Sciences and Technologies, Islamic Azad University, Science and Research Branch, Tehran, Iran)
Bahareh Nowruzi
3
(Department of Biology . Science and research Branch . Islamic Azad University . Tehran . Iran)
Keywords: Bio-sensors, Bio-indicators, Environmental change, Eco-systems, Soil eco-system, Marine Eco-system, organisms, Heavy metal, Fresh water,
Abstract :
Biomarkers encompass a diverse range of living organisms, such as plants, plankton, animals, and microorganisms. Biological markers are commonly employed to assess and evaluate the environmental quality and health of ecosystems. Furthermore, these instruments serve as valuable resources for identifying instances of environmental deterioration and assessing its consequences for human civilization. Organisms are influenced by environmental determinants that contribute to environmental change. These organisms, commonly referred to as bio-indicators, serve as a crucial tool in monitoring environmental pollution and are widely recognized as one of the primary methods employed for this purpose. Bioindicators provide scientists with a comprehensive assessment of the present state of various ecosystems. By analyzing this data, scientists are allowed to exercise improved management over ecosystem conditions and subsequently address issues such as pollution and toxic substances. The primary objective of this study is to collect pertinent and extensive data for individuals seeking to acquire knowledge about bioindicators or engage in research about this field, given its substantial role within the ecosystem. The data presented herein is acquired through the examination of bioindicators in diverse ecosystems, drawing upon the research conducted by other scholars.
1. Ho E., Galougahi K.K., Liu C.C., Bhindi R., Figtree G.A., 2013. Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biology. 1, 483-491.
2. Parmar T.K., Rawtani D., Agrawal Y., 2016. Bioindicators: the natural indicator of environmental pollution. Frontiers in Life Science. 9, 110-118.
3. Aronson J.K., 2005. Biomarkers and surrogate endpoints. British Journal of Clinical Pharmacology. 59, 491.
4. Markert B.A., Breure A.M., Zechmeister H.G. 2003. Definitions, strategies and principles for bioindication/biomonitoring of the environment Trace Metals and other Contaminants in the Environment. Elsevier. pp. 3-39.
5. Li L., Song L., Ding S., Zhang X., Qiang L., Han C., Yuan X., Xu D., 2010. Clinical value of CEA and CYFRA21-1 as an assessment indicator of therapeutic efficacy in advanced non-small cell lung cancer patients. Zhonghua Zhong liu za zhi Chinese Journal of Oncology. 32, 850-854.
6. Foissner W., 1997. Global soil ciliate (Protozoa, Ciliophora) diversity: a probability-based approach using large sample collections from Africa, Australia and Antarctica. Biodiversity & Conservation. 6, 1627-1638.
7. Nalecz-Jawecki G., Demkowicz-Dobrzainski K., Sawicki J., 1993. Protozoan Spirostomum ambiguum as a highly sensitive bioindicator for rapid and easy determination of water quality. Science of the Total Environment. 134, 1227-1234.
8. Muñoz-Vera A., Castejón J. M. P., García G., 2016. Patterns of trace element bioaccumulation in jellyfish Rhizostoma pulmo (Cnidaria, Scyphozoa) in a Mediterranean coastal lagoon from SE Spain. Marine Pollution Bulletin. 110, 143-154.
9. Bobrov A., Mazei Y., 2004. Morphological variability of testate amoebae (Rhizopoda: Testacealobosea and Testaceafilosea) in natural populations. Acta Protozoologica. 43, 133-146.
10. Chen Q.H., Xu R.L., Tam N.F., Cheung S.G., Shin P.K., 2008. Use of ciliates (Protozoa: Ciliophora) as bioindicator to assess sediment quality of two constructed mangrove sewage treatment belts in Southern China. Marine Pollution Bulletin. 57, 689-694.
11. Efremova S.M., Itskovich V.B., Parfenova V., Drucker V.V., Müller W., Schröder H.C., 2002. Lake Baikal: a unique place to study evolution of sponges and their stress response in an environment nearly unimpaired by anthropogenic perturbation. Cellular and Molecular Biology (Noisy-le-Grand, France). 48, 359-371.
12. Batista D., Tellini K., Nudi A.H., Massone T.P., Scofield A.d.L., de LR Wagener A., 2013. Marine sponges as bioindicators of oil and combustion derived PAH in coastal waters. Marine Environmental Research. 92, 234-243.
13. Mahaut M.L., Basuyaux O., Baudinière E., Chataignier C., Pain J., Caplat C., 2013. The porifera Hymeniacidon perlevis (Montagu, 1818) as a bioindicator for water quality monitoring. Environmental Science and Pollution Research. 20, 2984-2992.
14. Todd B.D., Thornhill D.J., Fitt W.K., 2006. Patterns of inorganic phosphate uptake in Cassiopea xamachana: a bioindicator species. Marine Pollution Bulletin. 52, 515-521.
15. Kushmaro A., Henning G., Hofmann D., Benayahu Y., 1997. Metamorphosis of Heteroxenia fuscescens planulae (Cnidaria: Octocorallia) is inhibited by crude oil: a novel short term toxicity bioassay. Marine Environmental Research. 43, 295-302.
16. White M.L., Strychar K.B., 2011. Coral as environmental bioindicators: ecological and morphological effects of gasoline on gorgonian corals, Leptogorgia virgulata. International Journal of Biology. 3, 63.
17. Knakievicz T., 2014. Planarians as invertebrate bioindicators in freshwater environmental quality: the biomarkers approach. Ecotoxicology and Environmental Contamination. 9, 1-12.
18. Carbayo F., Leal-Zanchet A.M., Vieira E.M., 2002. Terrestrial flatworm (Platyhelminthes: Tricladida: Terricola) diversity versus man-induced disturbance in an ombrophilous forest in southern Brazil. Biodiversity & Conservation. 11, 1091-1104.
19. Oehlmann J., Schulte-Oehlmann U., 2003. Mollusks as bioindicators. Trace Metals and other Contaminants in the Environment. 6, 577-635.
20. Ivan O., 2009. Structure and dynamics of the oribatid mite communities (Acari, Oribatida) in some Quercus forests, in relation with the treatments used in the control of defoliating insects. Annals of Forest Research. 52, 5-10.
21. Boukachabia A., Soucha M., Maamcha O., 2015. Impact of environmental and chemical stress on the activity of the acetylcholinesterase and glutathione S-transferase during reproduction of Scolopendra morsitans (Myriapoda Chilopoda) in the north-east of Algeria. Journal of Entomology and Zoology Studies. 3, 433-439.
22. Rost-Roszkowska M., Vilimová J., Tajovský K., Chachulska-Żymełka A., Sosinka A., Kszuk-Jendrysik M., Ostróżka A., Kaszuba F., 2019. Autophagy and apoptosis in the midgut epithelium of millipedes. Microscopy and Microanalysis. 25, 1004-1016.
23. Jayanti A., Fachrul M., Hendrawan D., 2018Makrozoobentos as Bioindicator Water Quality of Krukut River, Depok, West Java, Indonesia.
24. Paoletti M.G., 1999. The role of earthworms for assessment of sustainability and as bioindicators. Agriculture, Ecosystems & Environment. 74, 137-155.
25. Pearce J., Venier L., 2005. Small mammals as bioindicators of sustainable boreal forest management. Forest Ecology and Management. 208, 153-175.
26. Hirata S.H., Yasuda Y., Urakami S., Isobe T., Yamada T. K., Tajima Y., Amamo M., Miyazaki N., Takahashi S., Tanabe S., 2010. Environmental monitoring of trace elements using marine mammals as bioindicators—species-specific accumulations and temporal trends. Environmental Specimen Bank. 75-79.
27. Boulton I., Cooke J., Johnson M., 1994. Fluoride accumulation and toxicity in wild small mammals. Environmental Pollution. 85, 161-167.
28. Booth R.K., 2001. Ecology of testate amoebae (Protozoa) in two Lake Superior coastal wetlands: implications for paleoecology and environmental monitoring. Wetlands. 21, 564-576.
29. Decamp O., Warren A., Sanchez R., 1999. The role of ciliated protozoa in subsurface flow wetlands and their potential as bioindicators. Water Science and Technology. 40, 91-98.
30. García-Gómez J.C., Sempere-Valverde J., González A.R., Martínez-Chacón M., Olaya-Ponzone L., Sánchez-Moyano E., Ostalé-Valriberas E., Megina C., 2020. From exotic to invasive in record time: The extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar. Science of the Total Environment. 704, 135408.
31. Stabili L., Parisi M. G., Parrinello D., Cammarata M., 2018. Cnidarian interaction with microbial communities: from aid to animal’s health to rejection responses. Marine Drugs. 16, 296.
32. González-Duarte M.M., Megina C., Piraino S., 2014. Looking for long-term changes in hydroid assemblages (Cnidaria, Hydrozoa) in Alboran Sea (South-Western Mediterranean): a proposal of a monitoring point for the global warming. Helgoland Marine Research. 68, 511-521.
33. Gouvea R., Santos P., Dutra I., Gouvea V., 1989. Uptake of 210Pb and 210Po by Brazillian Bunodosoma caissarum corrêa, 1964 (Cnidaria, actinidae). Science of the Total Environment. 83, 181-183.
34. Lozano-Bilbao E., Alcázar-Treviño J., Fernández J. J., 2018. Determination of δ15N in Anemonia sulcata as a pollution bioindicator. Ecological Indicators. 90, 179-183.
35. Howe P.L., Reichelt-Brushett A.J., Clark M.W., 2014. Investigating lethal and sublethal effects of the trace metals cadmium, cobalt, lead, nickel and zinc on the anemone Aiptasia pulchella, a cnidarian representative for ecotoxicology in tropical marine environments. Marine and Freshwater Research. 65, 551-561.
36. Pedrosa R., P. Gaudêncio S., Vasconcelos V., MDPI, 2020. XVI International Symposium on Marine Natural Products European Conference on Marine Natural Products. 18, 40.
37. Jiménez S., González-Porto M., Brito A., Almón B., Martín-Sosa P., 2014. Scleractinia off Canary Islands Seamounts. Journal of Geophysical Research-Oceans. 2, 25.
38. Noreña C., Damborenea C., Brusa F., 2015. Phylum Platyhelminthes Thorp and Covich's Freshwater Invertebrates, Elsevier. pp. 181-203.
39. Knakievicz T., Vieira S. M., Erdtmann B., Ferreira H.B., 2006. Reproductive modes and life cycles of freshwater planarians (Platyhelminthes, Tricladida, Paludicula) from southern Brazil. Invertebrate Biology. 125, 212-221.
40. Indeherberg M., Molenberghs G., Moens J., Schockaert E., 1999. Differences in reproductive characteristics among field populations of Polycelis tenuis (Platyhelminthes) in a metal contaminated stream. Bulletin of Environmental Contamination and Toxicology. 62, 130-137.
41. Perera L.R.Y., Wattavidanage J., Nilakarawasam N., 2011. Diversity, abundance and distribution of macroinvertebrates in Colombo canal system and the potential of using them as bioindicators for steam health monitoring. Annual Academic Sessions. 1, 262-265.
42. Duggan I., Green J., Shiel R., Distribution of rotifers in North Island, New Zealand, and their potential use as bioindicators of lake trophic state, 2001. Hydrobiologia. 446, 155-164.
43. McEvoy E.G., Rogers A., Gibson R., 1997. Preliminary investigation of Vibrio alginolyticus-like bacteria associated with marine nemerteans. Hydrobiologia. 365, 287-291.
44. McEvoy E.G., Sundberg P., 1993. Patterns of trace metal accumulation in Swedish marine nemerteans. Hydrobiologia. 266, 273-280.
45. Marneffe Y., Comblin S., Thomé J.P., Ecological water quality assessment of the Bütgenbach lake (Belgium) and its impact on the River Warche using rotifers as bioindicators. 1998. Hydrobiologia. 387, 459-467.
46. Saksena D., 1987. Rotifers as indicators of water quality. Acta Hydrochimica et Hydrobiologica. 15, 481-485.
47. Ji G., Wang X., Wang L., 2013. Planktonic rotifers in a subtropical shallow lake: succession, relationship to environmental factors, and use as bioindicators. The Scientific World Journal. 2013, 14.
48. Ezz S.M.A., Aziz N.E.A., Abou Zaid M.M., El Raey M., Abo-Taleb H.A., 2014. Environmental assessment of El-Mex Bay, Southeastern Mediterranean by using Rotifera as a plankton bio-indicator. The Egyptian Journal of Aquatic Research. 40, 43-57.
49. Bongers T., Ferris H., 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution. 14 (6), 224-228.
50. Li Y., Hyde K. D., Jeewon R., Cai L., Vijaykrishna D., Zhang K., 2005. Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia. 97, 1034-1046.
51. Biswal D., 2023. Soil nematodes as the silent sufferers of climate-induced toxicity: Analysing the outcomes of their interactions with climatic stress factors on land cover and agricultural production. Applied Biochemistry and Biotechnology. 195, 2519-2586.
52. Neher D.A., 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology. 33, 161.
53. Šalamún P., Renčo M., Kucanová E., Brázová T., Papajová I., Miklisová D., Hanzelová V., 2012. Nematodes as bioindicators of soil degradation due to heavy metals. Ecotoxicology. 21, 2319-2330.
54. Rose F., 1970. Lichens as pollution indicators. Your Environ.;(United Kingdom). 1.
55. Oertel N., 1998. Molluscs as bioindicators of heavy metals in a side-arm system of the River Danube disturbed by engineering activity. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen. 26, 2120-2124.
56. Karmakar P., Pal S., Mishra M., 2022. Arthropods: An Important Bio-Indicator to Decipher the Health of the Water of South Asian Rivers. River Health and Ecology in South Asia: Pollution, Restoration, and Conservation. 9-38.
57. Dionisio-da-Silva W., de Araujo Lira A.F., de Albuquerque C.M.R., 2018. Distinct edge effects and reproductive periods of sympatric litter-dwelling scorpions (Arachnida: Scorpiones) in a Brazilian Atlantic forest. Zoology. 129, 17-24.
58. Marc P., Canard A., Ysnel F., 1999. Spiders (Araneae) useful for pest limitation and bioindication. Agriculture, Ecosystems & Environment. 74, 229-273.
59. Hajeb P., Christianus A., Ismail A., Zadeh S.S., Saad C., 2009. Heavy metal concentration in horseshoe crab (Carcinoscorpius rotundicauda and Tachypleus gigas) eggs from Malaysian coastline. Biology and Conservation of Horseshoe Crabs. 455-463.
60. Al-Shami S.A., Rawi C.S.M., HassanAhmad A., Nor S.A.M., 2010. Distribution of Chironomidae (Insecta: Diptera) in polluted rivers of the Juru River Basin, Penang, Malaysia. Journal of Environmental Sciences. 22, 1718-1727.
61. Lowry J., Stoddart H., 2002. The Amaryllididae of Australia (Crustacea: Amphipoda: Lysianassoidea). Records-Australian Museum. 54, 129-214.
62. Väinölä R., Witt J., Grabowski M., Bradbury J.H., Jazdzewski K., Sket B., 2008. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia. 595, 241-255.
63. Barut I.F., Nazik A., Balkıs N., Aksu A., Erşan M.S., 2015. Ostracoda as bioindicators of anthropogenic impact in salt lakes, saltpans, and a lagoon: A case study from the Gulf of Saros coast (NE Aegean Sea), Turkey. Revue de Micropaléontologie. 58, 351-367.
64. Guerra-García J., Koonjul M., 2005. Metaprotella sandalensis (Crustacea: Amphipoda: Caprellidae): a bioindicator of nutrient enrichment on coral reefs? A preliminary study at Mauritius Island. Environmental monitoring and assessment. 104, 353-367.
65. Correa-Araneda F., Delosrios RÍOS P., 2010. Amphipoda and decapoda as potential bioindicators of water quality in an urban stream (38 S, Temuco, Chile). Crustaceana. 897-902.
66. Guerra García J.M., Corzo J., García Asencio I., García Gómez J.C., 2001. Seasonal fluctuations of Phtisica marina Slabber (Crustacea: Amphipoda: Caprellidea) in estuarine zone of southwest Spain. Polskie Archiwum Hydrobiologii. 47, 527-531
67. Conradi M., López‐González P., García‐Gómez C., 1997. The amphipod community as a bioindicator in Algeciras Bay (southern Iberian Peninsula) based on a spatio‐temporal distribution. Marine Ecology. 18, 97-111.
68. Longo G., Trovato M., Mazzei V., Ferrante M., Conti G.O., 2013. Ligia italica (Isopoda, Oniscidea) as bioindicator of mercury pollution of marine rocky coasts. PloS one. 8, e58548.
69. Shuhaimi-Othman M., Yakub N., Ramle N.A., Abas A., 2011. Sensitivity of the freshwater prawn, Macrobrachium lanchesteri (Crustacea: Decapoda), to heavy metals. Toxicology and Industrial Health. 27, 523-530.
70. Licciano M., Stabili L., Giangrande A., Cavallo R.A., 2007. Bacterial accumulation by Branchiomma luctuosum (Annelida: Polychaeta): a tool for biomonitoring marine systems and restoring polluted waters. Marine Environmental Research. 63, 291-302.
71. Muys B., Granval P., 1997. Earthworms as bio-indicators of forest site quality. Soil Biology and Biochemistry. 29, 323-328.
72. Fernández Rodríguez V., Londoño Mesa M., 2015. Polychaetes (Annelida: Polychaeta) as biological indicators of marine pollution: Colombian cases. Gestión y Ambiente. 18, 189-204.
73. Suthar S., Singh S., 2008. Vermicomposting of domestic waste by using two epigeic earthworms (Perionyx excavatus and Perionyx sansibaricus). International Journal of Environmental Science & Technology. 5, 99-106.
74. Macova S., Harustiakova D., Kolarova J., Machova J., Zlabek V., Vykusova B., Randak T., Velisek J., Poleszczuk G., Hajslova J., 2009. Leeches as sensor-bioindicators of river contamination by PCBs. Sensors. 9, 1807-1820.
75. Abubakr A., Gojar A. A., Balkhi M., Malik R., 2018. Macro-invertebrates (Annelida; Oligochaeta) as bio-Indicator of water quality under temperate climatic conditions. Int J Pure App Biosci. 6, 726-737.
76. Zaccone G., Dabrowski K., Hedrick M.S., Fernandes J.M., Icardo J.M. 2015. Phylogeny, anatomy and physiology of ancient fishes. CRC Press
77. Mitchell C.D., Criscitiello M.F., 2020. Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture. Fish & Shellfish Immunology. 107, 435-443.
78. Cooper M.D., Alder M.N., 2006. The evolution of adaptive immune systems. Cell. 124, 815-822.
79. Yu D., Chen M., Zhou Z., Eric R., Tang Q., Liu H., 2013. Global climate change will severely decrease potential distribution of the East Asian coldwater fish Rhynchocypris oxycephalus (Actinopterygii, Cyprinidae). Hydrobiologia. 700, 23-32.
80. Beatty G.L., Chiorean E.G., Fishman M.P., Saboury B., Teitelbaum U.R., Sun W., Huhn R.D., Song W., Li D., Sharp L.L., 2011. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science. 331, 1612-1616.
81. Beatty S., Morgan D., 2010. Teleosts, agnathans and macroinvertebrates as bioindicators of ecological health in a south-western Australian river. Journal of the Royal Society of Western Australia. 93, 65-79.
82. Lima A.R., Torres R.A., Jacobina U.P., Pinheiro M.A., Adam M.L., 2019. Genomic damage in Mugil curema (Actinopterygii: Mugilidae) reveals the effects of intense urbanization on estuaries in northeastern Brazil. Marine Pollution Bulletin. 138, 63-69.
83. Zhelev Z.M., Tsonev S.V., Boyadziev P.S., 2018. Significant changes in morpho-physiological and haematological parameters of Carassius gibelio (Bloch, 1782)(Actinopterygii: Cyprinidae) as response to sporadic effusions of industrial wastewater into the Sazliyka River, Southern Bulgaria. Acta Zoologica Bulgarica. 70, 547-556.
84. Morris T.C., van der Ploeg J., Awa S.B., van der Lingen C.D., Reed C.C., 2019. Parasite community structure as a predictor of host population structure: An example using Callorhinchus capensis. International Journal for Parasitology: Parasites and Wildlife. 8, 248-255.
85. Adel M., Conti G. O., Dadar M., Mahjoub M., Copat C., Ferrante M., 2016. Heavy metal concentrations in edible muscle of whitecheek shark, Carcharhinus dussumieri (elasmobranchii, chondrichthyes) from the Persian Gulf: a food safety issue. Food and Chemical Toxicology. 97, 135-140.
86. Dural M., Genc E., Sangun M.K., Güner Ö., 2011. Accumulation of some heavy metals in Hysterothylacium aduncum (Nematoda) and its host sea bream, Sparus aurata (Sparidae) from North-Eastern Mediterranean Sea (Iskenderun Bay). Environmental Monitoring and Assessment. 174, 147-155.
87. Flewelling L.J., Adams D.H., Naar J.P., Atwood K.E., Granholm A.A., O’Dea S.N., Landsberg J.H., 2010. Brevetoxins in sharks and rays (Chondrichthyes, Elasmobranchii) from Florida coastal waters. Marine Biology. 157, 1937-1953.
88. Ozmen M., Güngördü A., Kucukbay F.Z., Güler R.E., 2006. Monitoring the effects of water pollution on Cyprinus carpio in Karakaya Dam Lake, Turkey. Ecotoxicology. 15, 157-169.
89. Silva V., Valenzuela A., Ruiz P., Oyarzún C., 2005. Trypanosoma humboldti en Schroederichthys chilensis (Chondrichthyes, Elasmobranchii, Scyliorhinidae) como indicador no destructivo de contaminación. Gayana (Concepción). 69, 160-165.
90. Ueno D., Inoue S., Takahashi S., Ikeda K., Tanaka H., Subramanian A., Fillmann G., Lam P., Zheng J., Muchtar M., 2004. Global pollution monitoring of butyltin compounds using skipjack tuna as a bioindicator. Environmental Pollution. 127, 1-12.
91. Ueno D., Kajiwara N., Tanaka H., Subramanian A., Fillmann G., Lam P.K., Zheng G.J., Muchitar M., Razak H., Prudente M., 2004. Global pollution monitoring of polybrominated diphenyl ethers using skipjack tuna as a bioindicator. Environmental Science & Technology. 38, 2312-2316.
92. Tsygankov V.Y., Boyarova M.D., Lukyanova O.N., Khristoforova N.K., 2017. Bioindicators of organochlorine pesticides in the Sea of Okhotsk and the Western Bering Sea. Archives of Environmental Contamination and Toxicology. 73, 176-184.
93. Beebee T.J., Griffiths R.A., 2005. The amphibian decline crisis: a watershed for conservation biology? Biological Conservation. 125, 271-285.
94. Welsh Jr H.H., Lind A.J., 1996. Habitat correlates of the southern torrent salamander, Rhyacotriton variegatus (Caudata: Rhyacotritonidae), in northwestern California. Journal of Herpetology. 385-398.
95. Saber S., Tito W., Said R., Mengistou S., Alqahtani A., 2017. Amphibians as bioindicators of the health of some wetlands in Ethiopia. The Egyptian Journal of Hospital Medicine. 66, 66-73.
96. Lambert M., 1997. Environmental effects of heavy spillage from a destroyed pesticide store near Hargeisa (Somaliland) assessed during the dry season, using reptiles and amphibians as bioindicators. Archives of Environmental Contamination and Toxicology. 32, 80-93.
97. Zhelev Z., Arnaudov A., Boyadzhiev P., 2014. Colour polymorphism, sex ratio and age structure in the populations of Pelophylax ridibundus and Pseudepidalea viridis (Amphibia: Anura) from anthropogenically polluted biotopes in southern Bulgaria and their usage as bioindicators. Trakia Journal of Sciences. 12, 1.
98. Townsend J.M., Driscoll C.T., Rimmer C.C., McFarland K.P., 2014. Avian, salamander, and forest floor mercury concentrations increase with elevation in a terrestrial ecosystem. Environmental toxicology and chemistry. 33, 208-215.
99. Gauthier J.A., 1994. The diversification of the amniotes. Short Courses in Paleontology. 7, 129-159.
100. Ezcurra M. D., Scheyer T. M., Butler R. J., 2014. The origin and early evolution of Sauria: reassessing the Permian saurian fossil record and the timing of the crocodile-lizard divergence. PloS One. 9, e89165.
101. Burgin C.J., Colella J.P., Kahn P.L., Upham N.S., 2018. How many species of mammals are there? Journal of Mammalogy. 99, 1-14.
102. Marsili L., Casini S., Mori G., Ancora S., Bianchi N., D'Agostino A., Ferraro M., Fossi M., 2009. The Italian wall lizard (Podarcis sicula) as a bioindicator of oil field activity. Science of the Total Environment. 407, 3597-3604.
103. Singh S., Mohan L., 2013. Biological control of mosquitoes by insectivorous flycatcher birds. Journal of Entomological Research. 37, 359-364.
104. Gong L., Shi B., Wu H., Feng J., Jiang T., 2021. Who’s for dinner? Bird prey diversity and choice in the great evening bat, Ia io. Ecology and Evolution. 11, 8400-8409.
105. Križanauskienė A., Hellgren O., Kosarev V., Sokolov L., Bensch S., Valkiūnas G., 2006. Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome B gene sequences. Journal of Parasitology. 92, 1319-1324.
106. Bostan N., Ashraf M., Mumtaz A. S., Ahmad I., 2007. Diagnosis of heavy metal contamination in agro-ecology of Gujranwala, Pakistan using cattle egret (Bubulcus ibis) as bioindicator. Ecotoxicology. 16, 247-251.
107. Rutkowska M., Płotka-Wasylka J., Lubinska-Szczygeł M., Różańska A., Możejko-Ciesielska J., Namieśnik J., 2018. Birds' feathers–suitable samples for determination of environmental pollutants. TrAC Trends in Analytical Chemistry. 109, 97-115.
108. Frederick P.C., Spalding M.G., Dusek R., 2002. Wading birds as bioindicators of mercury contamination in Florida, USA: annual and geographic variation. Environmental Toxicology and Chemistry: An International Journal. 21, 163-167.
109. Piratelli A., Sousa S., Corrêa J., Andrade V., Ribeiro R., Avelar L., Oliveira E., 2008. Searching for bioindicators of forest fragmentation: passerine birds in the Atlantic forest of southeastern Brazil. Brazilian Journal of Biology. 68, 259-268.
110. Hahn E., Hahn K., Stoeppler M., 1993. Bird feathers as bioindicators in areas of the German environmental specimen bank-bioaccumulation of mercury in food chains and exogenous deposition of atmospheric pollution with lead and cadmium. Science of the Total Environment. 139, 259-270.
111. Fernández J.M., Selma M.A.E., Aymerich F.R., Sáez M.T.P., Fructuoso M.F.C., 2005. Aquatic birds as bioindicators of trophic changes and ecosystem deterioration in the Mar Menor lagoon (SE Spain). Hydrobiologia. 550, 221-235.
112. Stanhope M.J., Waddell V.G., Madsen O., De Jong W., Hedges S.B., Cleven G.C., Kao D., Springer M.S., 1998. Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proceedings of the National Academy of Sciences. 95, 9967-9972.
113. Boros Á., Pankovics P., Reuter G., 2014. Avian picornaviruses: molecular evolution, genome diversity and unusual genome features of a rapidly expanding group of viruses in birds. Infection, Genetics and Evolution. 28, 151-166.
114. Rubeš J., Pokorna Z., Borkovec L., Urbanova J., Strnadova V., 1997. Dairy cattle as a bioindicator of exposure to genotoxic substances in a heavily polluted area in Northern Bohemia. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 391, 57-70.
115. Metcheva R., Beltcheva M., Chassovnikarova T., 2008. The snow vole (Chionomys nivalis) as an appropriate environmental bioindicator in alpine ecosystems. Science of the Total Environment. 391, 278-283.
116. Wilkening J.L., Ray C., Varner J., 2015. Relating sub-surface ice features to physiological stress in a climate sensitive mammal, the American pika (Ochotona princeps). PloS one. 10, e0119327.
117. McLean C.M., Koller C.E., Rodger J.C., MacFarlane G.R., 2009. Mammalian hair as an accumulative bioindicator of metal bioavailability in Australian terrestrial environments. Science of the Total Environment. 407, 3588-3596.
118. Ma W.C., 1989. Effect of soil pollution with metallic lead pellets on lead bioaccumulation and organ/body weight alterations in small mammals. Archives of Environmental Contamination and Toxicology. 18, 617-622.
119. Al Sayegh Petkovšek S., Kopušar N., Kryštufek B., 2014. Small mammals as biomonitors of metal pollution: a case study in Slovenia. Environmental Monitoring and Assessment. 186, 4261-4274.
120. Lazarus M., Sekovanić A., Orct T., Reljić S., Kusak J., Jurasović J., Huber Đ., 2017. Apex predatory mammals as bioindicator species in environmental monitoring of elements in Dinaric Alps (Croatia). Environmental Science and Pollution Research. 24, 23977-23991.
121. Zukal J., Pikula J., Bandouchova H., 2015. Bats as bioindicators of heavy metal pollution: history and prospect. Mammalian Biology. 80, 220-227.
122. Marques A., Piló D., Carvalho S., Araújo O., Guilherme S., Santos M.A., Vale C., Pereira F., Pacheco M., Pereira P., 2018. Metal bioaccumulation and oxidative stress profiles in Ruditapes philippinarum–insights towards its suitability as bioindicator of estuarine metal contamination. Ecological Indicators. 95, 1087-1099.
123. Marcheselli M., Sala L., Mauri M., 2010. Bioaccumulation of PGEs and other traffic-related metals in populations of the small mammal Apodemus sylvaticus. Chemosphere. 80, 1247-1254.
124. Tanabe S., Mori T., Tatsukawa R., Miyazaki N., 1983. Global pollution of marine mammals by PCBs, DDTs and HCHs (BHCs). Chemosphere. 12, 1269-1275.
125. Alonso Alcalá Jáuregui J., Rodríguez Ortiz J.C., Filippini M.F., Martínez Carretero E., Hernández Montoya A., Rojas Velázquez Á. N., Méndez Cortés H., Beltrán Morales F. A., 2022. Metallic elements in foliar material and fruits of three tree species as bioindicators. Revista de la Facultad de Ciencias Agrarias. Universidad Nacional de Cuyo. 54, 61-72.
126. Sánchez-Chardi A., Peñarroja-Matutano C., Borrás M., Nadal J., 2009. Bioaccumulation of metals and effects of a landfill in small mammals Part III: structural alterations. Environmental Research. 109, 960-967.
127. Gago-Ferrero P., Alonso M. B., Bertozzi C.P., Marigo J., Barbosa L., Cremer M., Secchi E.R., Azevedo A., Lailson-Brito Jr J., Torres J.P., 2013. First determination of UV filters in marine mammals. Octocrylene levels in Franciscana dolphins. Environmental Science & Technology. 47, 5619-5625.
