Supplementary Files
Keywords
Neotropical
water quality
biological monitoring
tolerance values
pupal exuviae
Índice de Integridad Biótica de Chironomidae
Neotropical
calidad de agua
monitoreo biológico
valores de tolerancia
exuvias pupales
How to Cite
Abstract
The family Chironomidae (Diptera) is the most widely distributed, most diverse, and often the most abundant of all families of benthic macroinvertebrates in aquatic ecosystems, including estuaries and other coastal marine ecosystems. Chironomid assemblages are likely to provide a useful measure of biotic integrity in estuaries of Costa Rica, which lack an intensive estuarine bioassessment tool to support environmental monitoring and regulatory programs. We characterized the taxonomic composition of Chironomidae, tested a Chironomidae Index of Biotic Integrity (CIBI) developed from extrinsic pollution tolerance values for its efficacy in evaluating the surface water quality and physical habitat, and made recommendations for increasing the sensitivity of the CIBI to detect differing degrees of stress across a range of estuaries in Costa Rica. Specifically, we selected nine estuaries within six different watersheds across a land use gradient located on the Caribbean coast of Costa Rica and collected Chironomidae surface-floating pupal exuviae (SFPE) samples biannually for two consecutive years (July 2012, Jan. 2013, July 2013, Jan. 2014). We identified 228 morphospecies and 70 genera from 17 071 Chironomidae pupal exuviae collected from nine estuaries, which ranked in the following order from lowest to highest biotic integrity based on CIBI scores: Estero Negro, Laguna Cuatro, Laguna Jalova, Laguna del Tortuguero, Río Parismina, Laguna Barra del Colorado, Río Pacuare, Río Bananito, and Río Estrella. The CIBI successfully differentiated between estuaries with poor versus good biotic integrity, indicating that CIBI could be used to evaluate the surface water quality and physical habitat of Costa Rican estuaries. We recommend that future studies refine our approach by developing regionally accurate genus and corresponding species-level tolerance values to improve the sensitivity of the CIBI for biological monitoring of Costa Rican estuaries.References
Andersen, T., & Mendes, H. F. (2002). New species and records of the Axarus "rogersi-group" from South and Central America (Diptera, Chironomidae). Acta Zoologica Academiae Scientiarum Hungaricae, 48(1), 34-40.
Bailey, R. C., Norris, R. H., & Reynoldson, T. B. (2001). Taxonomic resolution of benthic macroinvertebrate communities in bioassessments. Journal of the North American Benthological Society, 20(2), 280-286.
Barbour, M. T., Gerritsen, J., Snyder, B. D., & Stribling, J. B. (1999). Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish. (EPA 841-B-99-002). Washington, D.C.: U.S. Environmental Protection Agency, Office of Water.
Beck, W. M., & Beck, E. C. (1966). Chironomidae (Diptera) of Florida - I. Pentaneurini (Tanypodinae). Bulletin of the Florida State Museum, Biological Sciences Series, 10(8), 305-379.
Berger, W. H., & Parker, F. L. (1970). Diversity of planktonic foraminifera in deep-sea sediments. Science, 168(3937), 1345-1347.
Boesch, D., Burreson, E., Dennison, W., Houde, E., Kemp, M., Kennedy, V., . . . Ulanowicz, R. (2001). Factors in the Decline of Coastal Ecosystems. Science, 293(5535), 1589c-1591c.
Boesel, M. W. (1974). Observations on the Coelotanypodini of the Northeastern States, with Keys to the Known Stages (Diptera: Chironomidae: Tanypodinae). Journal of the Kansas Entomological Society, 47(4), 417-432.
Borkent, A. (1984). The systematics and phylogeny of the Stenochironomus complex (Xestochironomus, Harrisius, and Stenochironomus) (Diptera: Chironomidae). Memoirs of the Entomological Society of Canada, 128, 1-269.
Bouchard Jr., R. W., & D. Huggins, J. K. (2005). A review of the issues related to taxonomic resolution in biological monitoring of aquatic ecosystems with an emphasis on macroinvertebrates. Retrieved from Lawrence, KS: http://biosurvey.ku.edu/sites/biosurvey.ku.edu/files/publishedworks/pdfs/KBSRept133_TaxResol.pdf
Bouchard Jr., R. W., & Ferrington Jr., L. C. (2011). The effects of subsampling and sampling frequency on the use of surface-floating pupal exuviae to measure Chironomidae (Diptera) communities in wadeable temperate streams. Environmental Monitoring and Assessment, 181(1-4), 205-223.
Bricker, S. B., Longstaff, B., Dennison, W., Jones, A., Boicourt, K., Wicks, C., & Woerner, J. (2008). Effects of nutrient enrichment in the nation's estuaries: A decade of change. Harmful Algae, 8(1), 21-32.
Caldwell, B. A. (1993). The immature stages of Ablabesmyia cinctipes (Johannsen) with comments on ecology. Spixiana, 16(1), 49-52.
Cañedo-Argüelles, M., Boix, D., Sánchez-Millaruelo, N., Sala, J., Caiola, N., Nebra, A., & Rieradevall, M. (2012). A rapid bioassessment tool for the evaluation of the water quality of transitional waters. Estuarine, Coastal and Shelf Science, 111(0), 129-138.
Casas, J. J., & Vilchez-Quero, A. (1996). Chironomid assemblages of three endoreic karstic lagoons (southern Spain) determined by collection of pupal exuviae: importance of the water mineralization and sediment characteristics. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 81(4), 529-539.
Castillo, L. E., de la Cruz, E., & Ruepert, C. (1997). Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environmental Toxicology and Chemistry, 16(1), 41-51.
Castillo, L. E., Martinez, E., Ruepert, C., Savage, C., Gilek, M., Pinnock, M., & Solis, E. (2006). Water quality and macroinvertebrate community response following pesticide applications in a banana plantation, Limon, Costa Rica. Science of The Total Environment, 367(1), 418-432.
Castillo, L. E., Ruepert, C., & Solis, E. (2000). Pesticide residues in the aquatic environment of banana plantation areas in the North Atlantic Zone of Costa Rica. Environmental Toxicology and Chemistry, 19(8), 1942-1950.
Chao, A. (1984). Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270.
Coffman, W. P., & de la Rosa, C. (1998). Taxonomic composition and temporal organization of tropical and temperate assemblages of lotic Chironomidae. Journal of the Kansas Entomological Society, 71, 388-406.
Coffman, W. P., de la Rosa, C., Cumming, K., & Wilzbach, M. A. (1992). Species richness in some Neotropical (Costa Rica) and Afrotropical (West Africa) lotic communities of Chironomidae (Diptera). Netherlands Journal of Aquatic Ecology, 26, 229-237.
Colbo, M. H. (1996). Chironomidae from marine coastal environments near St. John's, Newfoundland, Canada. Hydrobiologia, 318(1), 117-122. doi:10.1007/bf00014137
Colwell, R. K. (2013). EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application published at: http://purl.oclc.org/estimates
Da Silva, F. L., Fonseca-Gessner, A. A., & Ekrem, T. (2014). A taxonomic revision of genus Labrundinia Fittkau, 1962 (Diptera: Chironomidae: Tanypodinae). Zootaxa, 3769, 1-185.
De Oliveira, C. S. N., Da Silva, M. A. N., & Gessner, A. A. F. (2013). Neotropical Ablabesmyia Johannsen (Diptera: Chironomidae, Tanypodinae)–Part I. 2013, 3733(1), 123.
Diepens, N. J., Pfennig, S., Van den Brink, P. J., Gunnarsson, J. S., Ruepert, C., & Castillo, L. E. (2014). Effect of pesticides used in banana and pineapple plantations on aquatic ecosystems in Costa Rica. Journal of Environmental Biology, 35(1), 73-84.
Dimitriadis, S., & Cranston, P. S. (2007). From the mountains to the sea: assemblage structure and dynamics in Chironomidae (Insecta: Diptera) in the Clyde River estuarine gradient, New South Wales, south-eastern Australia. Australian Journal of Entomology, 46(3), 188-197.
Donato, M., Siri, A., Massaferro, J., & Brooks, S. J. (2015). Apedilum griseistriatum comb. nov., placement of Chironomus (Polypedilum) griseistriatum (Diptera, Chironomidae). Iheringia. Série Zoologia, 105, 5-11.
Downing, J. A., Mcclain, M., Twilley, R., Melack, J. M., Elser, J., Rabalais, N. N., . . . Howarth, R. W. (1999). The impact of accelerating land-use change on the N-Cycle of tropical aquatic ecosystems: Current conditions and projected changes. Biogeochemistry, 46(1), 109-148.
Echeverría-Sáenz, S., Mena, F., Pinnock, M., Ruepert, C., Solano, K., de la Cruz, E., . . . Barata, C. (2012). Environmental hazards of pesticides from pineapple crop production in the Río Jiménez watershed (Caribbean Coast, Costa Rica). Science of The Total Environment, 440(0), 106-114.
Ekrem, T. (2007). A taxonomic revision of the genus Stempellinella (Diptera: Chironomidae). Journal of Natural History, 41(21-24), 1367-1465.
Epler, J. H. (1988). Biosystematics of the genus Dicrotendipes Kieffer, 1913 (Diptera: Chironomidae) of the world. Memoirs of the American Entomology Society, 36, 1-214.
Epler, J. H., & Janetzky, W. J. (1998). A New Species of Monopelopia (Diptera: Chironomidae) from Phytotelmata in Jamaica, with Preliminary Ecological Notes. Journal of the Kansas Entomological Society, 71(3), 216-225.
Fagan, M. E. (2014). The Changing Matrix: Reforestation and Connectivity in a Tropical Habitat Corridor. (PhD), Columbia University.
Ferrington Jr., L. C. (2008). Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. In E. V. Balian, C. Lévêque, H. Segers, & K. Martens (Eds.), Freshwater animal diversity assessment (pp. 447-455). Netherlands: Springer Netherlands.
Ferrington Jr., L. C., Berg, M. B., & Coffman, W. P. (2008). Chironomidae. In R. W. Merritt, K. W. Cummins, & M. B. Berg (Eds.), An Introduction To The Aquatic Insects Of North America (4th ed., pp. 847-989). Dubuque, IA: Kendall/Hunt Publishing Company.
Ferrington Jr., L. C., Blackwood, M. A., Wright, C. A., Crisp, N. H., Kavanaugh, J. L., & Schmidt, F. J. (1991). A protocol for using surface-floating pupal exuviae of Chironomidae for rapid bioassessment of changing water-quality. Sediment and Stream Water Quality in a Changing Environment: Trends and Explanation, 203, 181-190.
Ferrington Jr., L. C., Buzby, K. M., & Masteller, E. C. (1993). Composition and Temporal Abundance of Chironomidae Emergence from a Tropical Rainforest Stream at El Verde, Puerto Rico. Journal of the Kansas Entomological Society, 66(2), 167-180.
Ferrington Jr., L. C., & Saether, O. A. (2011). A revision of the genera Pseudosmittia Edwards, 1932, Allocladius Kieffer, 1913, and Hydrosmittia gen. n. (Diptera : Chironomidae, Orthocladiinae). Zootaxa, 2849, 1-314.
Gotelli, N. J., & Colwell, R. K. (2011). Estimating species richness. In A. E. Magurran & B. J. McGill (Eds.), Frontiers in measuring biodiversity. (pp. 39–54). New York: Oxford University Press.
Grant, P. B. C., Woudneh, M. B., & Ross, P. S. (2013). Pesticides in blood from spectacled caiman (Caiman crocodilus) downstream of banana plantations in Costa Rica. Environmental Toxicology and Chemistry, 32(11), 2576-2583.
Gutierrez-Fonseca, P. E., & Lorion, C. M. (2014). Application of the BMWP-Costa Rica biotic index in aquatic biomonitoring: sensitivity to collection method and sampling intensity. Revista de Biología Tropical, 62(2), 275-289.
Herman, M. R., & Nejadhashemi, A. P. (2015). A review of macroinvertebrate- and fish-based stream health indices. Ecohydrology & Hydrobiology, 15(2), 53-67.
Hestenes, T. C., & Saether, O. A. (2000). Three new Nearctic Thienemanniella Kieffer species with a review of the Nearctic species. Paper presented at the Late 20th Century Research on Chironomidae: an Anthology from the 13th International Symposium on Chironomidae, Aachen, Germany.
Hilsenhoff, W. L. (1977). Use of Arthropods to Evaluate Water Quality of Streams. Madison, Wisconsin: Department of Natural Resources.
Hilsenhoff, W. L. (1987). An improved biotic index of organic stream pollution. Great Lakes Entomologist, 20(1), 31-39.
Howarth, R., Chan, F., Conley, D. J., Garnier, J., Doney, S. C., Marino, R., & Billen, G. (2011). Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment, 9(1), 18-26.
Huang, D., & Cheng, L. (2011). The flightless marine midge Pontomyia (Diptera: Chironomidae): ecology, distribution, and molecular phylogeny. Zoological Journal of the Linnean Society, 162(2), 443-456. doi:10.1111/j.1096-3642.2010.00680.x
Instituto Meteorológico Nacional. (2016). Climatic data: Limón (1941-2015). Retrieved from https://www.imn.ac.cr
Jacobsen, R. E. (2008). A Key to the Pupal Exuviae of the Midges (Diptera: Chironomidae) of Everglades National Park, Florida (Scientific Investigations Report 2008-5082). Retrieved from https://pubs.er.usgs.gov/publication/sir20085082
Jacobsen, R. E., & Perry, S. A. (2000). A review of Beardius Reiss & Sublette, with description of a new species from Everglades National Park, Florida (Insecta, Diptera, Chironomidae). Spixiana, 23, 129-144.
James, K. R., Cant, B., & Ryan, T. (2003). Responses of freshwater biota to rising salinity levels and implications for saline water management: A review. Australian Journal of Botany, 51(6), 703-713.
Kafle, A. (2013). Chironomidae Contributions to the Macroinvertebrate Assemblage, Index of Biotic Integrity and Relationships to Water Quality Impairment for Eastern South Dakota Streams. (Master of Science), South Dakota State University.
Karr, J. R. (1981). Assessment of Biotic Integrity Using Fish Communities. Fisheries, 6(6), 21-27.
Karr, J. R., Fausch, K. D., Angermeier, P. L., Yant, P. R., & Schlosser, I. J. (1986). Assessing biological integrity in running waters: A method and its rationale. Champaign, IL: Illinois Natural History Survey.
Kennish, M. J., & Townsend, A. R. (2007). Nutrient Enrichment and Estuarine Eutrophication. Ecological Applications, 17(5), S1-S2.
King, R. S., & Richardson, C. J. (2002). Evaluating subsampling approaches and macroinvertebrate taxonomic resolution for wetland bioassessment. Journal of the North American Benthological Society, 21(1), 150-171.
Kranzfelder, P. (2012). Comparison of emergence and taxanomic composition of Chironomidae (Insecta: Diptera) in Tortuguero National Park, Costa Rica. (Master's Thesis), University of Minnesota, University of Minnesota.
Kranzfelder, P., Anderson, A. M., Egan, A. T., Mazack, J. E., Bouchard, R. W., & Ferrington, L. C. (2015). Use of Chironomidae (Diptera) surface-floating pupal exuviae as a rapid bioassessment protocol for water bodies. Journal of Visualized Experiments (JoVE), 101, e52558.
Kranzfelder, P., Corcoran, J. M., Rampi, L. P., Knight, J. F., & Ferrington, L. C. (in review). Land use and land cover change in six watersheds on the Caribbean coast of Costa Rica with implications for estuarine monitoring. Journal of Coastal Conservation.
Kranzfelder, P., Ekrem, T., & Stur, E. (2017). DNA barcoding for species identification of insect skins: A test on Chironomidae (Diptera) pupal exuviae. Journal of Insect Science, 17(6), 1-7.
Kranzfelder, P., & Ferrington Jr., L. C. (2016). Temporal and spatial variability of Chironomidae (Insecta: Diptera) species emergence in a Neotropical estuary. Freshwater Science, 35(2), 631-643.
Kress, N., Coto, S. L., Brenes, C. L., Brenner, S., & Arroyo, G. (2002). Horizontal transport and seasonal distribution of nutrients, dissolved oxygen and chlorophyll-a in the Gulf of Nicoya, Costa Rica: A tropical estuary. Continental Shelf Research, 22(1), 51-66.
Langton, P. H. (1991). A key to pupal exuviae of West Palearctic Chironomidae. Huntingdon, Cambridgeshire, England: P. H. Langton.
Lenat, D. R., & Resh, V. H. (2001). Taxonomy and stream ecology - The benefits of genus- and species-level identifications. Journal of the North American Benthological Society, 20(2), 287-298.
Lindegaard, C. (1989). A review of secondary production of zoobenthos in freshwater ecosystems with special reference to Chironomidae (Diptera). Acta Biologica Debrecen, Oecologica Hungarica, 3, 231-240.
Lovelock, C. E., Feller, I. C., McKee, K. L., Engelbrecht, B. M. J., & Ball, M. C. (2004). The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panamá. Functional Ecology, 18(1), 25-33.
Lunde, K. B., & Resh, V. H. (2012). Development and validation of a macroinvertebrate index of biotic integrity (IBI) for assessing urban impacts to Northern California freshwater wetlands. Environmental Monitoring and Assessment, 184(6), 3653-3674.
Magurran, A. E., & McGill, B. J. (2011). Biological Diversity: Frontiers in Measurement and Assessment: OUP Oxford.
Maue, T., & Springer, M. (2008). Effect of methodology and sampling time on the taxa richness of aquatic macroinvertebrates and subsequent changes in the water quality index from three tropical rivers, Costa Rica. Revista de Biología Tropical, 56(4), 257-271.
Mendes, H. F., Marcondes, C. B., & Pinho, L. C. D. (2003). A new phytotelmatic species of Monopelopia Fittkau, 1962 (Insecta: Diptera: Chironomidae: Tanypodinae) from South Brazil. Zootaxa, 262, 1-10.
Ministerio del Ambiente y Energia y la Ministra de Salud. (2007). Reglamento Reglamento para la Evaluación y Clasificación de la Calidad de Cuerpos de Agua Superficiales No. 33903-MINAE-S. La Gaceta, 178.
Nicacio, G., & Juen, L. (2015). Chironomids as indicators in freshwater ecosystems: an assessment of the literature. Insect Conservation and Diversity, 8(5), 393-403.
Nixon, S. W. (1995). Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia, 41(1), 199-219.
Oliveira, C. S. N. D., Mendes, H. F., & Silva, M. A. N. D. (2010). A New Species Of The Genus Monopelopia From South Brazil, With Keys To The Neotropical – Nearctic Species (Diptera: Chironomidae: Tanypodinae). Zootaxa, 2420, 53-62.
Oliveira, C. S. N. D., & Silva, F. L. (2011). Two new species of Larsia Fittkau, 1962 (Diptera: Chironomidae: Tanypodinae) from Neotropical Region, with a checklist of Larsia species of the world. Zootaxa, 2786, 27-41.
Paerl, H. W., Hall, N. S., Peierls, B. L., & Rossignol, K. L. (2014). Evolving Paradigms and Challenges in Estuarine and Coastal Eutrophication Dynamics in a Culturally and Climatically Stressed World. Estuaries and Coasts, 37(2), 243-258.
Paggi, A. C. (1977). Imaginal and preimaginal forms of chironomids (Diptera) II. Parachironomus longistilus sp. nov. Limnobios, 1(6).
Palmégn, E., & Lindeberg, B. (1959). The Marine Midge, Clunio Marinus Hal. (Dipt., Chironomidae), Found in Brackish Water In The Northern Baltic. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 44(1‐4), 383-394. doi:10.1002/iroh.19590440120
Pinder, L. C. V. (1986). Biology of freshwater Chironomidae. Annual Review of Entomology, 31, 1-23.
Pringle, C. M., Anderson, E. P., Ardón, M., Bixby, R. J., Connelly, S., Duff, J. H., . . . Triska, F. J. (2016). Rivers of Costa Rica. In M. Kappelle (Ed.), Costa Rican Ecosystems (pp. 621-655). Chicago: University of Chicago Press.
Pringle, C. M., & Hamazaki, T. (1998). The role of omnivory in a Neotropical stream: separating diurnal and nocturnal effects. Ecology, 79(1), 269-280.
Rizo-Patrón V, F., Kumar, A., McCoy Colton, M. B., Springer, M., & Trama, F. A. (2013). Macroinvertebrate communities as bioindicators of water quality in conventional and organic irrigated rice fields in Guanacaste, Costa Rica. Ecological Indicators, 29, 68-78.
Roback, S. S. (1980). The immature chironomids of the eastern United States IV. Tanypodinae-Procladiini. Proceedings of the Academy of Natural Sciences of Philadelphia, 132, 1-63.
Roback, S. S. (1986). The Immature Chironomids of the Eastern United States. VII. Pentaneurini-Genus Monopelopia, with Redescription of the Male Adults and Description of Some Neotropical Material. Proceedings of the Academy of Natural Sciences of Philadelphia, 138(2), 350-365.
Roback, S. S., & Coffman, W. P. (1983). Results of the Catherwood Bolivian- Peruvian Altiplano Expedition part II. Aquatic Diptera including montane Diamesinae and Orthocladiinae (Chironomidae) from Venezuela. Proceedings of the Academy of Natural Sciences of Philadelphia, 135, 9-79.
Rosenberg, D. (1992). Freshwater biomonitoring and Chironomidae. Netherland Journal of Aquatic Ecology, 26(2-4), 101-122.
Ruse, L. (2002). Chironomid pupal exuviae as indicators of lake status. Archiv fur Hydrobiologie, 153(3), 367-390.
Ruse, L. (2010). Classification of nutrient impact on lakes using the chironomid pupal exuvial technique. Ecological Indicators, 10(3), 594-601.
Sæther, O., & Cranston, P. (2012). New World Stictocladius Edwards (Diptera: Chironomidae). Neotropical Entomology, 41(2), 124-149.
Saether, O. A. (2011). Notes On Canadian Ablabesmyia Johannsen, With Keys To Known Nearctic Immatures Of The Genus (Diptera: Chironomidae). Zootaxa.
Sæther, O. A. (2004). A Review of Orthocladius subgen. Symposiocladius Cranston (Diptera: Chironomidae). Aquatic Insects, 25(4), 281-317.
Sawedal, L. (1984). The cururui-group of the genus Stempellina Thienemann & Bause. Amazonian Tanytarsini II. (Diptera: Chironomidae). Entomologica Scandinavica, 15, 141-149.
Serrano, M. A. S., & Nolte, U. (1996). A sit-and-wait predatory chironomid from tropical Brazil- Fittkauimyia crypta sp. n. (Diptera: Chironomidae). Insect Systematics & Evolution, 27(3), 251-258.
Shapiro, J., Lamarra, V. A., & Lynch, M. (1975). Biomanipulation: An Ecosystem Approach to Lake Restoration: Limnological Research Center, University of Minnesota.
Silva, F. L. D., & Ekrem, T. (2016). Phylogenetic relationships of nonbiting midges in the subfamily Tanypodinae (Diptera: Chironomidae) inferred from morphology. Systematic Entomology, 41(1), 73-92.
Siqueira, T., De Oliveira Roque, F., & Trivinho-Strixino, S. (2008). Phenological patterns of neotropical lotic chironomids: Is emergence constrained by environmental factors? Austral Ecology, 33(7), 902-910.
Soponis. (1987). Paranilothauma and Neelamia, New Genera of Chironomini (Diptera: Chironomidae) from Brazil. Studies on Neotropical Fauna and Environment, 22(1), 11-24.
Souza, M., Moulton, T., Silveira, R., Krsulovic, F., & Brito, E. (2007). Responses of Chironomidae (Diptera; Insecta) to the exclusion of shrimps and Ephemeroptera in a coastal forest stream, Rio de Janeiro, Brazil. Brazilian Journal of Biology, 67, 47-51.
Spies, M., Andersen, T., Epler, J. H., & Watson, C. N. (2009). Chironomidae (non-biting midges). In B. V. Brown (Ed.), Manual of Central American Diptera (Vol. 1, pp. 437-480). Ottawa: NRC Research Press.
Spies, M., & Reiss, F. (1996). Catalog and bibliography of Neotropical and Mexican Chironomidae (Insecta, Diptera). Spixiana Supplement, 22, 61-119.
Stein, H., Springer, M., & Kohlmann, B. (2008). Comparison of two sampling methods for biomonitoring using aquatic macroinvertebrates in the Dos Novillos River, Costa Rica. Ecological Engineering, 34(4), 267-275.
Sublette, J. E., & Sasa, M. (1994). Chironomidae collected in Onchocerciasis endemic areas of Guatemala (Insecta, Diptera). Spixiana Supplement, 20, 1-60.
Tang, H. (2016). Paralauterborniella from Oriental China (Diptera: Chironomidae). Oriental Insects, 50(4), 160-170.
Tejerina, E. G., & Paggi, A. C. (2009). A new Neotropical species of Oliveiriella Wiedenbrug & Fittkau (Diptera: Chironomidae) from Argentina, with description of all its life stages. Aquatic Insects, 31(2), 91-98.
Thorne, R., & Williams, P. (1997). The response of benthic macroinvertebrates to pollution in developing countries: a multimetric system of bioassessment. Freshwater Biology, 37(3), 671-686.
Trivinho-Strixino, S., Da Silva, F. L., & Roque, F. O. (2010). A new species of Parachironomus Lenz, 1921 (Diptera: Chironomidae: Chironominae), and description of immature stages of two other species from the Neotropical Region. Zootaxa, 2689, 1-14. doi:10.5281/zenodo.199500
Watson, C. N., & Heyn, M. W. (1992). A preliminary survey of the Chironomidae (Diptera) of Costa Rica, with emphasis on the lotic fauna. Netherland Journal of Aquatic Ecology, 26(2-4), 257-262.
Weisberg, S. B., Ranasinghe, J. A., Dauer, D. M., Schaffner, L. C., Diaz, R. J., & Frithsen, J. B. (1997). An estuarine benthic index of biotic integrity (B-IBI) for Chesapeake Bay. Estuaries, 20(1), 149.
Wiedenbrug, S., & Andersen, T. (2002). New Species of Parakiefferiella Thienemann, 1936 from South America (Chironomidae, Orthocladiinae). Studies on Neotropical Fauna and Environment, 37(2), 119-132.
Wiedenbrug, S., & Fittkau, E. J. (1997). Oliveiriella almeidai (Oliveira, 1946), gen. nov., comb. nov., from South America with description of the pupae (Insecta, Diptera, Chironomidae, Orthocladiinae). Spixiana, 20, 167-172.
Wiedenbrug, S., Lamas, C. E., & Trivinho-Strixino, S. (2012). A review of the genus Corynoneura Winnertz (Diptera: Chironomidae) from the Neotropical region. Zootaxa, 3574, 1-61.
Wiedenbrug, S., & Ospina-Torres, R. (2005). A key to pupal exuviae of Neotropical Tanytarsini (Diptera: Chironomidae). Amazoniana, 18(3), 317-371.
Wiedenburg, S., Lamas, C. E., & Trivinho-Strixino, S. (2013). A review of Neotropical species in Thienemanniella Kieffer (Diptera, Chironomidae). Zootaxa, 3670, 215-237.
Wiedenburg, S., Mendes, H. F., Pepinelli, M., & Trivinho-Strixino, S. (2009). Review of the genus Onconeura Andersen et Sæther (Diptera: Chironomidae), with the description of four new species from Brazil. Zootaxa, 2265, 1-26.
Wiedenburg, S., & Trivinho-Strixino, S. (2009). Ubatubaneura, a new genus of the Corynoneura group (Diptera: Chironomidae: Orthocladiinae) from the Brazilian Atlantic Forest. Zootaxa, 1993, 41-52.
Wiedenburg, S., & Trivinho-Strixino, S. (2011). New species of the genus Corynoneura Winnertz (Diptera, Chironomidae) from Brazil. Zootaxa, 2822, 1-40.
Wiederholm, T. (1986). Chironomidae of the Holarctic region. Part 2. Pupae (Vol. 28). Sandby, Sweden: Entomologica Scandinavica Supplement.
Williams, D. D., & Hamm, T. (2002). Insect community organisation in estuaries: the role of the physical environment. Ecography, 25(3), 372-384.
Williams, D. D., & Williams, N. E. (1998). Aquatic insects in an estuarine environment: densities, distribution and salinity tolerance. Freshwater Biology, 39(3), 411-421.
Williams, W. D. (1998). Salinity as a determinant of the structure of biological communities in salt lakes. Hydrobiologia, 381(1-3), 191-201.
Wilson, R. S., & Ruse, L. P. (2005). A guide to the identification of genera of chironomid pupal exuviae occurring in Britain and Ireland (including common genera from Northern Europe) and their use in monitoring lotic and lentic fresh waters. Ambleside, Cumbria, UK.: Freshwater Biological Association.
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