A Quick Review of the Family Chironomidae (Order Diptera) with Effect on the Environment

authors:

avatar Fatemeh Shahidi-Hakak ORCID 1 , avatar Mohammad Hadi Amid-Motlagh ORCID 2 , avatar Mousa Khosravani ORCID 3 , *

Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
Department of Plant Protection, College of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran
Department of Medical Entomology and Vector Control, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran
Trends in Medical Sciences: Vol.2, issue 2; e129263
published online: August 14, 2022
article type: Review Article
received: June 22, 2022
revised: July 9, 2022
accepted: July 13, 2022
DOI: https://doi.org/10.5812/tms-129263

how to cite: Shahidi-Hakak F, Amid-Motlagh M H, Khosravani M. A Quick Review of the Family Chironomidae (Order Diptera) with Effect on the Environment. J Adv Immunopharmacol. 2022;2(2):e129263. https://doi.org/10.5812/tms-129263.

Abstract

Context:

The Chironomidae family is more sensitive to changes in water environment quality. This taxon is tolerant in stream ecosystems. Thus, it could be used as a bio-indicator of freshwater to recognize the presence of contaminants with deleterious effects on human health.

Evidence Acquisition:

We searched keywords Chironomidae, bioindicator, environment, water stream, water quality, anthropogenic disturbance, pollutant, fossil, industrial waste, and aquatic habitats. Chironomidae was used once in single and again in combination with others. Google Scholar, Scopus, Springer, ScienceDirect, PubMed, ProQuest, JSTOR, EBSCO, BioOne, ResearchGate, Sage, Wiley Online Library, and SID were used as databases or search engines. Then, the results were sorted into four sections: Distribution and ecology, biotic indicators, food, and paleoecological studies.

Results:

The identification key of chironomids should be improved based on morphological and molecular data to determine this family more clearly. Identifying sub-fossil chironomid insects found in the sediments of lakes unravels the range of environments during the history of its aquatic habitat through paleoecological investigations.

Conclusions:

Chironomidae at genera or species has variations in traits in the ecosystems. Each species as a bio-indicator has different tolerable condition in its own habitat .Overall, the role of this family in all types of pollutants is ambiguous. More studies are needed to particularize the importance of Chironomidae based on genera and species.

1. Context

Organics, pathogens, nutrients, agriculture runoff, suspended solids, sediments, inorganic pollutants (salts and metals), and thermal pollution are significant water contaminants (1, 2). Toxic metals in waste streams affect fish life. They harm growth, change liver glycogens and triglycerides, and disrupt metabolic enzyme activities in the catfish (3). Some chemical elements negatively affect embryonic development, hatching, and viability of the mallard (4). Also, they are harmful to human health in either short or long-term exposure. The kidney, pancreas, heart, bones, veins, arteries, liver, and brain would be dysfunctioned by the intake of certain pollutants ingested through drinking water (5).

Bioindicators are sensitivities to the ecological and natural changes caused by anthropogenic disturbance. It affects biodiversity and community of insect (6-8). Aquatic macroinvertebrates such as Baetis sp., Fallceon sp., Leptohyphes sp., Tricorythodes sp., Farrodes sp., Phyllogomphoides sp., Hydroptila sp., Mayatrichia sp., Neotrichia sp., Oxyethira sp., Nectopsyche sp.1, Nectopsyche sp.2, and Oecetis sp. are bioindicators sensitive to water contamination (9).

Chironomidae has been used as a significant insect for the bioassessment of water quality for a long time (10). This study aims to explore Chironomidae as an important bioindicator in all types of water bodies and environments. Furthermore, this macroinvertebrate has a role in the food chain, energy transfer, and paleoecological investigations. This family adapts to environmental conditions and predicts unexpected contamination from human activities or other agents. Studying the Chironomidae traits helps us clarify the dynamic of the species-environment relationship. Moreover, due to its predictability, it demonstrates the effects of stressors on ecosystems.

2. Evidence Acquisition

We used keywords such as Chironomidae, bioindicator, environment, water stream, water quality, anthropogenic disturbance, pollutant, fossil, industrial waste, and aquatic habitats. Chironomidae was used once in single and again in combination with others. Google Scholar, Scopus, Springer, ScienceDirect, PubMed, ProQuest, JSTOR, EBSCO, BioOne, ResearchGate, Sage, Wiley Online Library, and SID were used as databases or search engines. Then, the results were sorted into four sections: Distribution and ecology, biotic indicators, food, and paleoecological studies. The obtained articles and scientific documents were often helpful. Few were dropped from our work because of low quality or overlap.

3. Results

3.1. Distribution and Ecology

The family Chironomidae (order: Diptera) comprises predominant insects in freshwater environments. Little studies have been carried out about the lifecycle and ecology of this family. The family has more than 5,000 species worldwide, but the exact number is unclear. A few chironomids have terrestrial habitats (11). This family is categorized into 11 subfamilies and 22 tribes. The subfamilies include Telmatogetoninae, Usambaromyiinae, Aphroteniinae, Chilenomyiinae, Podonominae, Tanypodinae, Buchonomyiinae, Diamesinae, Prodiamesinae, Orthocladiinae, and Chironominae (12). Belgica antarctica, Eretmoptera murphyi (subfamily Orthocladiinae), and Parochlus steinenii (subfamily Podonominae) are the only chironomid species identified in the Antarctica areas (13). The subfamily Chilenomyiinae is restricted to Chile. Buchonomyiinae has two species identified in Europe and Asia. Aphroteniinae, including four genera, has been recognized only in South America, South Africa, and Australia. Subfamilies, including Orthocladiinae, Tanypodinae, and Chironominae, are established more in lake sediments (14). Genus Dicrotendipes Kieffer from China comprises eight species: Dicrotendipes flexus, Dicrotendipes fusconotatus, Dicrotendipes nervosus, Dicrotendipes nudus sp. n., Dicrotendipes pelochloris, Dicrotendipes saetanumerosus sp. n., Dicrotendipes septemmaculatus, and Dicrotendipes tamaviridis (15). This family has four larval instars with around one year of longevity, but pupal and adult stages last about a few days or weeks, depending on species and climate. Males swarm about one hour before sunrise and scatter about one hour after sunset for mating with females (16). The larvae stages of Paratendipes albimanus and Rheotanytarsus curtistylus are remained in the second and third instar in winter (17). Chironomidae are abundant in the organic content of sediments or beds of lakes and rivers (18). For example, macrophytes (Potamogeton pectinatus and Ruppia maritima) or benthic algae (Rhizoclonium hieroglyphicurn) significantly affect the growth of Cricotopus ornatus (Meigen) (Diptera: Chironomidae) (19). Also, it has been found in gravel sediments. Overall, it is limited to the surface layers of soft sediments, but some species habitat more deeply, and the sediment depth may be confining to population density in some instances. Some species ingest wood because of having symbiotic microorganisms in their gut (20). Notably, chironomids larvae use physiological or behavioral strategies to survive in habitats with repeated changes in the situation, such as rain pools, phytotelmata, freshly filled ponds or soil layers, urban rivers, hot springs, and coastal lagoons (21-23).

3.2. Biotic Indicators

Chironomid midges adapt to sites with different water quality streams in the Scioto River basin, Ohio. (1) Stictocbironomus was found in the hard, alkaline unpolluted water; (2) Pentaneura, Cricotopus, and Tanytarsus were observed in the sewage enriched water; (3) Procladius and Dicrotendipes have existed in the high agricultural runoff; (4) Ablabesmyia and Tribelos were adapted to general organic pollution, soft acid water (24). Moreover, Chironomus riparius is an indicator of organic pollution and sediment toxicity monitoring (20, 25). Chironomidae larvae exist in lentic and lotic environments with different taxonomic levels (26-30). This aquatic macroinvertebrate was found at polluted spots of Barbados Stream in Brazil, where pollutants like domestic sewage, plastic materials, root, and slime were sorted (31). Remarkably, riparian vegetation affects Chironomidae assemblage and has a significant role in the composition of aquatic fauna in neotropical streams (32, 33).

Neonicotinoid insecticides affect Chironomidae life in all stages. Chironomidae represent high densities of high-affinity nicotinic acetylcholine receptors (34). Also, significant factors influencing Chironomid distribution are temperature associated with O2, Cl-, Al3+, Mg2+, and Na+ ions in lakes of central Yakutia, Russia (35). The chironomid species (i.e., Anatopynia plumipes, Procladius sp., Psectrotanypus rarius, Cricotopus sylvestris, Psectrocladius edwardsi, Chironomus tentans, C. polaris, Chironomus sp. I and II, Einfeldia dissidens, E. pagana, and Glyptotendipes paripés) have shown tolerance to low oxygen pressures and temperature in a frozen lake in northern Sweden (36). Moreover, larval and pupal of Pseudodiamesa arctica were observed in temperatures between 0°C and 4°C of Nettilling lake in Baffin Island, Canada, but 15°C is desirable temperature in small water bodies for larval growth (37). Besides, pH is another environmental parameter. Chironomids species are diverse in pH ranging from 6.4 to 8.3 in small prairie ponds in central Saskatchewan, Canada (38). Chironomus salinarius Kieffer can tolerate a range of salinity levels (39). Baeotendipes noctivagus (Kieffer, 1911) is possibly the most inflexible species to salinity in the world (40). A special subfamily or tribe of chironomids is inhabited in different sampling sites of Swartkops River, south of Africa, by water quality. Dissolved oxygen, electrical conductivity, orthophosphate-phosphorus, total inorganic nitrogen, and turbidity were the critical variables for chironomid communities (41). Hydrocarbon phenanthrene as a chemical substance harms benthic organisms in sediments through acute/chronic exposure. Chironomus sancticaroli larvae frequently have shown susceptibility to this compound (42). Additionally, biodegradation of amorphous carbon was identified in the digestive tract of Chironomidae species (43). Deformities in larvae are reported, often resulting from responding of Chironomidae to anthropogenic and environmental disturbances (44). The deformity rate may be a practicable parameter for biomonitoring (45). This event has been seen in Ablabesmyia sp. and Procladius sp. larvae in acid mine drainage (46). Mouthpart deformities of the Chironomini tribe in response to sediments containing metals such as Pb, Zn, Cu, As, and Cd are recorded from a river in the USA (47).

3.3. Food

Chironomus plumosus larvae are the source of natural substances more beneficial for farm fish diet. For instance, crude protein content is 7.6% and 55.7% in fresh larvae and dry weight, respectively. Amino acids such as Arginine, Histidine, Isoleucine, Leucine, Valine, Lysine, Phenylalanine, Methionine, Threonine, and Tryptophan have been isolated from larvae of this species (48, 49). Other food values of chironomid larvae are carbohydrate 23%, chitin 4%, ash 9%, and caloric content (4.6 to 6.1 kcal.g-1) (50). Dragonfly larvae feed at least 30% of their body weight on midges (51). Similarly, Chironomidae larvae are solely dieted for kind of leech (Erpobdella octoculata) so that leech survives where Chironomidae grow and increase in running water (52). Sometimes, predators like nine-spine stickleback, Pungitius pungitius, and the damselfly, Enallagma clausum, threaten the Cricotopus ornatus population in the fourth instar and pupal phases (19). Chironomids are the main in the early dietary regime of young flightless dabbling ducks after hatching (36). Furthermore, this family, particularly Corynoneura, participates in the trophic cycle and decomposition of plant detritus in subtropical streams. Chemical elements of the detritus assemblage influence the structure of the chironomids community during a long time of exposure (53). Moreover, chironomids with small body sizes have been detected in an environment with high levels of disturbance. Anthropic and climatic factors may cause this morphological trait (54). There is a symbiotic relationship between Chironomidae larvae and benthic animals as follows: Demeijerea rufipes, Chironomidae, a parasite of sponges and bryozoan, Eukiefferiella ancyla, subfamily Orthocladiinae, as commensal of the snail Ancylus fluviatilis, and Symbiocladius rhithrogenae, Orthocladiinae, a true and obligate parasite of Heptageniidae/Ephemeroptera larvae, feeding on the mayfly's hemolymph (55).

3.4. Paleoecological Studies

Climate affects chironomid fauna composition and their morphological structures (56). Surficial sediments sampling upon altitudinal range can be helpful. It means we can trace chemistry among lakes according to lake depth. On the other hand, Chironomid fauna presents the past condition of the environment in different depths. Heterotrissocladius was predominant in deep lakes rather than shallow ponds. In contrast, Cladopelma was limited to shallow lakes as warmer habitats in summer (57). Analysis of deposits has approved that more chironomid taxa were discovered at low elevations in the southern Canadian Cordillera lakes (58). In a study using the larval head capsule fossils from surface sediment samples of 50 lakes, 7,771 chironomids were identified, following 13 species, 10 species groups, four subgenera, 41 genera, four genus groups, five types, and three with unknown taxonomic affiliation. Taxon richness was described with physical, chemical, and biological variables such as water temperature, lake depth, pH, conductivity, alkalinity, calcium, magnesium, sodium, potassium, total organic carbon, latitude, longitude, and altitude (59).

4. Conclusions

Chironomids are a favorable candidate to use in bioassessment approaches in toxicity tests and paleolimnology. Detailed life-history information of some species is available from laboratory studies. In contrast, they might be disqualified as biochemical and physiological indicators of environmental stress resulting from taxonomic problems with larvae and small size (60). However, the role of this family in all types of pollutants is ambiguous. More studies are needed to particularize the importance of Chironomidae based on genera and species.

References

  • 1.

    Ghangrekar MM, Chatterjee P. Water Pollutants Classification and Its Effects on Environment. In: Das R, editor. Carbon Nanotubes for Clean Water. Cham, Switzerland: Springer; 2018. p. 11-26. https://doi.org/10.1007/978-3-319-95603-9_2.

  • 2.

    Blasco C, Picó Y. Prospects for combining chemical and biological methods for integrated environmental assessment. Trends Analyt Chem. 2009;28(6):745-57. https://doi.org/10.1016/j.trac.2009.04.010.

  • 3.

    El-Sheekh M. River Nile Pollutants and Their Effect on Life Forms and Water Quality. In: Dumont HJ, editor. The Nile: Origin, Environments, Limnology and Human Use. Dordrecht, Netherlands: Springer; 2009. p. 395-405. https://doi.org/10.1007/978-1-4020-9726-3_19.

  • 4.

    Kertész V, Fáncsi T. Adverse effects of (surface water pollutants) Cd, Cr and Pb on the embryogenesis of the mallard. Aquat Toxicol. 2003;65(4):425-33. https://doi.org/10.1016/S0166-445X(03)00155-3.

  • 5.

    Chhipa DRRC. Health hazards as slow poison and risk assessment on human health caused by water pollutants. Environmental Pollution Hazards, Mitigation and Quality of Life. India. Academia; 2009.

  • 6.

    Parmar TK, Rawtani D, Agrawal YK. Bioindicators: the natural indicator of environmental pollution. Front Life Sci. 2016;9(2):110-8. https://doi.org/10.1080/21553769.2016.1162753.

  • 7.

    Burgeot T, Bocquené G, His E, Vincent F, Geffard O, Beiras R, et al. Monitoring of Biological Effects of Pollutants : Field Application. In: Garrigues P, Barth H, Walker CH, Narbonne JF, editors. Biomarkers in Marine Organisms. Amsterdam, Netherlands: Elsevier Science; 2001. p. 179-213. https://doi.org/10.1016/b978-044482913-9/50009-2.

  • 8.

    Asif N, Malik M, Chaudhry FN. A review of on environmental pollution bioindicators. Pollution. 2018;4(1):111-8. https://doi.org/10.22059/poll.2017.237440.296.

  • 9.

    Rizo-Patrón V F, Kumar A, McCoy Colton MB, Springer M, Trama FA. Macroinvertebrate communities as bioindicators of water quality in conventional and organic irrigated rice fields in Guanacaste, Costa Rica. Ecol Indic. 2013;29:68-78. https://doi.org/10.1016/j.ecolind.2012.12.013.

  • 10.

    Shimba MJ, Jonah FE. Macroinvertebrates as bioindicators of water quality in the Mkondoa River, Tanzania, in an agricultural area. Afr J Aquat Sci. 2016;41(4):453-61. https://doi.org/10.2989/16085914.2016.1230536.

  • 11.

    Cranston PS, Yule CM, Sen YH. The freshwater invertebrates of the Malaysia region. Kuala Lampur, Malaysia: Academy of Sciences Malaysia; 2004.

  • 12.

    Ferrington LC. Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. In: Balian EV, Lévêque C, Segers H, Martens K, editors. Freshwater Animal Diversity Assessment. Dordrecht, Netherlands: Springer; 2008. p. 447-55. https://doi.org/10.1007/978-1-4020-8259-7_45.

  • 13.

    Allegrucci G, Carchini G, Todisco V, Convey P, Sbordoni V. A molecular phylogeny of Antarctic Chironomidae and its implications for biogeographical history. Polar Biol. 2006;29(4):320-6. https://doi.org/10.1007/s00300-005-0056-7.

  • 14.

    Walker IR. Chironomidae (Diptera) in paleoecology. Quat Sci Rev. 1987;6(1):29-40. https://doi.org/10.1016/0277-3791(87)90014-X.

  • 15.

    Qi X, Lin XL, Wang XH. Review of dicrotendipes kieffer from china (Diptera, chironomidae). Zookeys. 2012;(183):23-36. [PubMed ID: 22573947]. [PubMed Central ID: PMC3332026]. https://doi.org/10.3897/zookeys.183.2834.

  • 16.

    Hilsenhoff WL. The biology of Chironomus plumosus (Diptera: Chironomidae) in Lake Winnebago, Wisconsin. Ann Entomol Soc Am. 1966;59(3):465-73. https://doi.org/10.1093/aesa/59.3.465.

  • 17.

    Ward G, Cummins KW. Life History and Growth Pattern of Paratendipes albimanus in a Michigan Headwater Stream1,2. Ann Entomol Soc Am. 1978;71(2):272-84. https://doi.org/10.1093/aesa/71.2.272.

  • 18.

    Rosa BJ, Rodrigues LF, de Oliveira GS, da Gama Alves R. Chironomidae and Oligochaeta for water quality evaluation in an urban river in southeastern Brazil. Environ Monit Assess. 2014;186(11):7771-9. [PubMed ID: 25130902]. https://doi.org/10.1007/s10661-014-3965-5.

  • 19.

    Swanson SM, Hammer UT. Production of Cricotopus ornatus (Meigen) (Diptera: Chironomidae) in Waldsea Lake, Saskatchewan. Hydrobiologia. 1983;105(1):155-63. https://doi.org/10.1007/BF00025185.

  • 20.

    Pinder LCV. Biology of Freshwater Chironomidae. Annu Rev Entomol. 1986;31:1-23. https://doi.org/10.1146/annurev.en.31.010186.000245.

  • 21.

    Drake P, Arias AM. Distribution and production ofChironomus salinarius (Diptera: Chironomidae) in a shallow coastal lagoon in the Bay of Cádiz. Hydrobiologia. 1995;299(3):195-206. https://doi.org/10.1007/BF00767326.

  • 22.

    Frouz J, Matena J, Ali A. Survival strategies of chironomids (Diptera: Chironomidae) living in temporary habitats: a review. Eur J Entomol. 2003;100(4):459-66. https://doi.org/10.14411/eje.2003.069.

  • 23.

    Lin CT, Chiu MC, Kuo MH. Effects of anthropogenic activities on microplastics in deposit-feeders (Diptera: Chironomidae) in an urban river of Taiwan. Sci Rep. 2021;11(1):400. [PubMed ID: 33432041]. [PubMed Central ID: PMC7801685]. https://doi.org/10.1038/s41598-020-79881-z.

  • 24.

    Rae JG. Chironomid midges as indicators of organic pollution in the Scioto River Basin, Ohio. Ohio J Sci. 1989;89(1):5-9.

  • 25.

    Watts MM, Pascoe D. Use of the freshwater macroinvertebrate (Diptera: Chironomidae) in the assessment of sediment toxicity. Water Sci Technol. 1996;34(7-8):101-7. https://doi.org/10.2166/wst.1996.0607.

  • 26.

    Molineri C, Tejerina EG, Torrejón SE, Pero EJI, Hankel GE. Indicative value of different taxonomic levels of Chironomidae for assessing the water quality. Ecol Indic. 2020;108:105703. https://doi.org/10.1016/j.ecolind.2019.105703.

  • 27.

    Krosch MN, Baker AM, Mather PB, Cranston PS. Systematics and biogeography of the Gondwanan Orthocladiinae (Diptera: Chironomidae). Mol Phylogenet Evol. 2011;59(2):458-68. [PubMed ID: 21402162]. https://doi.org/10.1016/j.ympev.2011.03.003.

  • 28.

    Porinchu DF, Cwynar LC. The Distribution of Freshwater Chironomidae (Insecto: Diptera) across Treeline near the Lower Lena River, Northeast Siberia, Russia. Arct Antarct Alp Res. 2018;32(4):429-37. https://doi.org/10.1080/15230430.2000.12003387.

  • 29.

    Serra SRQ, Cobo F, Graca MAS, Doledec S, Feio MJ. Synthesising the trait information of European Chironomidae (Insecta: Diptera): Towards a new database. Ecol Indic. 2016;61(2):282-92. https://doi.org/10.1016/j.ecolind.2015.09.028.

  • 30.

    Sæther OA. Zoogeographical patterns in Chironomidae (Diptera). SIL Proceedings, 1922-2010. 2000;27(1):290-302. https://doi.org/10.1080/03680770.1998.11901242.

  • 31.

    Machado NG, Nassarden DCS, Santos FD, Boaventura ICG, Perrier G, Souza FSCD, et al. Chironomus larvae (Chironomidae: Diptera) as water quality indicators along an environmental gradient in a neotropical urban stream. Rev Ambient Água. 2015;10(2):298-309. https://doi.org/10.4136/ambi-agua.1533.

  • 32.

    Sensolo D, Hepp LU, Decian V, Restello RM. Influence of landscape on assemblages of Chironomidae in Neotropical streams. Ann Limnol Int J Lim. 2012;48(4):391-400. https://doi.org/10.1051/limn/2012031.

  • 33.

    Lencioni V, Rossaro B. Microdistribution of chironomids (Diptera: Chironomidae) in Alpine streams: an autoecological perspective. Hydrobiologia. 2005;533(1-3):61-76. https://doi.org/10.1007/s10750-004-2393-x.

  • 34.

    Maloney EM, Taillebois E, Gilles N, Morrissey CA, Liber K, Servent D, et al. Binding properties to nicotinic acetylcholine receptors can explain differential toxicity of neonicotinoid insecticides in Chironomidae. Aquat Toxicol. 2021;230:105701. [PubMed ID: 33249296]. https://doi.org/10.1016/j.aquatox.2020.105701.

  • 35.

    Nazarova LB, Pestryakova LA, Ushnitskaya LA, Hubberten HW. Chironomids (Diptera: Chironomidae) in lakes of central Yakutia and their indicative potential for paleoclimatic research. Contemp Probl Ecol. 2008;1(3):335-45. https://doi.org/10.1134/s1995425508030089.

  • 36.

    Danell K, Sjöberg K. Seasonal emergence of chironomids in relation to egglaying and hatching of ducks in a restored lake (northern Sweden). Wildfowl. 1977;28:129-35.

  • 37.

    Oliver DR. Adaptations of arctic Chironomidae. Ann Zool Fenn. 1968;5(1):111-8.

  • 38.

    Driver EA. Chironomid communities in small prairie ponds: some characteristics and controls. Freshw Biol. 1977;7(2):121-33. https://doi.org/10.1111/j.1365-2427.1977.tb01663.x.

  • 39.

    Cartier V, Claret C, Garnier R, Franquet E. How salinity affects life cycle of a brackish water species, Chironomus salinarius KIEFFER (Diptera:Chironomidae). J Exp Mar Biol Ecol. 2011;405(1-2):93-8. https://doi.org/10.1016/j.jembe.2011.05.019.

  • 40.

    Shadrin NV, Anufriieva EV, Belyakov VP, Bazhora AI. Chironomidae larvae in hypersaline waters of the Crimea: diversity, distribution, abundance and production. Eur Zool J. 2017;84(1):61-72. https://doi.org/10.1080/11250003.2016.1273974.

  • 41.

    Odume ON, Muller WJ. Diversity and structure of Chironomidae communities in relation to water quality differences in the Swartkops River. Phys Chem Earth. 2011;36(14-15):929-38. https://doi.org/10.1016/j.pce.2011.07.063.

  • 42.

    Richardi VS, Vicentini M, Morais GS, Rebechi D, da Silva TA, Favaro LF, et al. Effects of phenanthrene on different levels of biological organization in larvae of the sediment-dwelling invertebrate Chironomus sancticaroli (Diptera: Chironomidae). Environ Pollut. 2018;242(Pt A):277-87. [PubMed ID: 29990935]. https://doi.org/10.1016/j.envpol.2018.06.091.

  • 43.

    Chaika V, Pikula K, Vshivkova T, Zakharenko A, Reva G, Drozdov K, et al. The toxic influence and biodegradation of carbon nanofibers in freshwater invertebrates of the families Gammaridae, Ephemerellidae, and Chironomidae. Toxicol Rep. 2020;7:947-54. [PubMed ID: 32793424]. [PubMed Central ID: PMC7415770]. https://doi.org/10.1016/j.toxrep.2020.07.011.

  • 44.

    Al-Shami S, Rawi CS, Nor SA, Ahmad AH, Ali A. Morphological deformities in Chironomus spp. (Diptera: Chironomidae) larvae as a tool for impact assessment of anthropogenic and environmental stresses on three rivers in the Juru river system, Penang, Malaysia. Environ Entomol. 2010;39(1):210-22. [PubMed ID: 20146859]. https://doi.org/10.1603/EN09109.

  • 45.

    Wiederholm T. Incidence of deformed chironomid larvae (Diptera: Chironomidae) in Swedish lakes. Hydrobiologia. 1984;109(3):243-9. https://doi.org/10.1007/BF00007742.

  • 46.

    De Bisthoven LJ, Gerhardt A, Soares AMVM. Chironomidae larvae as bioindicators of an acid mine drainage in Portugal. Hydrobiologia. 2005;532(1-3):181-91. https://doi.org/10.1007/s10750-004-1387-z.

  • 47.

    Martinez EA, Moore BC, Schaumloffel J, Dasgupta N. The potential association between menta deformities and trace elements in Chironomidae (Diptera) taken from a heavy metal contaminated river. Arch Environ Contam Toxicol. 2002;42(3):286-91. [PubMed ID: 11910456]. https://doi.org/10.1007/s00244-001-0190-0.

  • 48.

    Bogut I, Has-Schön E, Adámek Z, Rajković V, Galović D. Chironomus plumosus larvae-a suitable nutrient for freshwater farmed fish. Poljoprivreda. 2007;13(1):159-62.

  • 49.

    Hirabayashi K, Wotton RS. Organic matter processing by chironomid larvae (Diptera: Chironomidae). Hydrobiologia. 1998;382(1/3):151-9. https://doi.org/10.1023/a:1003472329603.

  • 50.

    Armitage PD. Chironomidae as food. In: Armitage PD, Cranston PS, Pinder LCV, editors. The Chironomidae. Dordrecht, Netherlands: Springer; 1995. p. 423-35. https://doi.org/10.1007/978-94-011-0715-0_17.

  • 51.

    Benke AC. Dragonfly Production and Prey Turnover. Ecology. 1976;57(5):915-27. https://doi.org/10.2307/1941057.

  • 52.

    Elliott JM. The Diel Activity Pattern, Drifting and Food of the Leech Erpobdella octoculata (L.) (Hirudinea: Erpobdellidae) in a Lake District Stream. J Anim Ecol. 1973;42(2):449-59. https://doi.org/10.2307/3297.

  • 53.

    Biasi C, Tonin AM, Restello RM, Hepp LU. The colonisation of leaf litter by Chironomidae (Diptera): The influence of chemical quality and exposure duration in a subtropical stream. Limnologica. 2013;43(6):427-33. https://doi.org/10.1016/j.limno.2013.01.006.

  • 54.

    Gomes WIA, Jovem-Azevêdo DDS, Paiva FF, Milesi SV, Molozzi J. Functional attributes of Chironomidae for detecting anthropogenic impacts on reservoirs: A biomonitoring approach. Ecol Indic. 2018;93:404-10. https://doi.org/10.1016/j.ecolind.2018.05.006.

  • 55.

    Schiffels S. Commensal and parasitic Chironomidae. Denisia. 2014;33:393-407.

  • 56.

    Antczak-Orlewska O, Płóciennik M, Sobczyk R, Okupny D, Stachowicz-Rybka R, Rzodkiewicz M, et al. Chironomidae morphological types and functional feeding groups as a habitat complexity vestige. Front Ecol Evol. 2021;8:583831. https://doi.org/10.3389/fevo.2020.583831.

  • 57.

    Walker IR, MacDonald GM. Distributions of Chironomidae (Insecta: Diptera) and other freshwater midges with respect to treeline, Northwest Territories, Canada. Arct Antarct Alp Res. 1995;27(3):258-63. https://doi.org/10.2307/1551956.

  • 58.

    Walker IR, Mathewes RW. Chironomidae (Diptera) remains in surficial lake sediments from the Canadian Cordillera: analysis of the fauna across an altitudinal gradient. J Paleolimnol. 1989;2(1):61-80. https://doi.org/10.1007/BF00156985.

  • 59.

    Nyman M, Korhola A, Brooks SJ. The distribution and diversity of Chironomidae (Insecta: Diptera) in western Finnish Lapland, with special emphasis on shallow lakes. Glob Ecol Biogeogr. 2005;14(2):137-53. https://doi.org/10.1111/j.1466-822X.2005.00148.x.

  • 60.

    Rosenberg DM. Freshwater biomonitoring and Chironomidae. Neth J Aquat Ecol. 1992;26(2):101-22. https://doi.org/10.1007/BF02255231.