Pollution effects on diversity and content of the stable isotope 15N in macroinvertebrates: a study of the impacts on the functional groups from the Maipo River, Chile
María Paz Briones-Alburquenque A , Jorge Cortés-Miranda A and Caren Vega-Retter
A *
A
Abstract
Anthropogenic activities producing nitrogen have affected freshwater ecosystems. The δ15N isotope is a key indicator of these impacts. Macroinvertebrates are vulnerable to pollution. Studying the macroinvertebrate functional feeding groups (FFGs) helps us understand the structure, function and balance of fluvial ecosystems, and how pollution alters ecosystem dynamics. The Maipo River Basin is one of the most polluted in Chile.
This study examines how pollution affects macroinvertebrate family diversity, FFGs, δ15N content and trophic position.
Using a Surber net, five replicates were taken from two polluted and two non-polluted sites to analyse diversity at the family and FFGs levels. Differences in δ15N content and FFGs trophic position were assessed using a permutation Student’s t-test.
Gathering–collectors inhabiting polluted sites showed less richness of taxa than they did in the non-polluted sites. δ15N contents were higher in polluted sites, although gathering–collectors had a lower trophic position.
Our results indicated that greater nitrogen input creates conditions that may affect the diet of studied organisms, potentially explaining the observed trophic position changes.
Pollution alters the composition and structure of macroinvertebrate communities by affecting FFG diversity. This should be considered in future management plans.
Keywords: δ15N content, functional feeding groups, macroinvertebrate, macroinvertebrate family diversity, Maipo River Basin, nitrogen input, pollution, trophic position.
References
Amoatey P, Baawain MS (2019) Effects of pollution on freshwater aquatic organisms. Water Environment Research 91, 1272-1287.
| Crossref | Google Scholar | PubMed |
Ansari AA, Gill SS, Khan FA (2010) Eutrophication: threat to aquatic ecosystems. In ‘Eutrophication: causes, consequences and control’. (Eds A Ansari, S Singh Gill, G Lanza, W Rast) pp. 143–170. (Springer: Dordrecht, Netherlands) 10.1007/978-90-481-9625-8_7
Bertaso TRN, Spies MR, Kotzian CB, Flores MLT (2015) Effects of forest conversion on the assemblages’ structure of aquatic insects in subtropical regions. Revista Brasileira de Entomologia 59, 43-49.
| Crossref | Google Scholar |
Blocksom KA, Flotemersch JE (2005) Comparison of macroinvertebrate sampling methods for nonwadeable streams. Environmental Monitoring and Assessment 102, 243-262.
| Crossref | Google Scholar | PubMed |
Brito EF, Moulton TP, De Souza ML, Bunn SE (2006) Stable isotope analysis indicates microalgae as the predominant food source of fauna in a coastal forest stream, south-east Brazil. Austral Ecology 31, 623-633.
| Crossref | Google Scholar |
Camara IA, Kra MK, Kouadio NK, Konan MK, Edia EO, Doumbia L, Ouattara A, Diomande D (2020) Composition, structure and functional feeding of aquatic entomofauna in Kodjoboué Lake: water quality assessment. Open Journal of Ecology 10, 160-176.
| Crossref | Google Scholar |
Camp AA, Funk DH, Buchwalter DB (2014) A stressful shortness of breath: molting disrupts breathing in the mayfly Cloeon dipterum. Freshwater Science 33, 695-699.
| Crossref | Google Scholar |
Carey RO, Hochmuth GJ, Martinez CJ, Boyer TH, Dukes MD, Toor GS, Cisar JL (2013) Evaluating nutrient impacts in urban watersheds: challenges and research opportunities. Environmental Pollution 173, 138-149.
| Crossref | Google Scholar | PubMed |
Carpenter SR, Stanley EH, Vander Zanden MJ (2011) State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annual Review of Environment and Resources 36, 75-99.
| Crossref | Google Scholar |
Copaja SV, Mauro L, Vega-Retter C, Véliz D (2020) Adsorption–desorption of trace elements in sediments of the Maipo River basin. Journal of the Chilean Chemical Society 65, 4778-4783.
| Crossref | Google Scholar |
Cortés-Miranda J, Rojas-Hernández N, Muñoz G, Copaja S, Quezada-Romegialli C, Veliz D, Vega-Retter C (2024) Biomarker selection depends on gene function and organ: the case of the cytochrome P450 family genes in freshwater fish exposed to chronic pollution. PeerJ 12, e16925.
| Crossref | Google Scholar |
Cummins KW (1973) Trophic relations of aquatic insects. Annual Review of Entomology 18, 183-206.
| Crossref | Google Scholar |
Cummins KW (1974) Structure and function of stream ecosystems. BioScience 24, 631-641.
| Crossref | Google Scholar |
Cummins KW, Klug MJ (1979) Feeding ecology of stream invertebrates. Annual Review of Ecology and Systematics 10, 147-172.
| Crossref | Google Scholar |
di Lascio A, Rossi L, Carlino P, Calizza E, Rossi D, Costantini ML (2013) Stable isotope variation in macroinvertebrates indicates anthropogenic disturbance along an urban stretch of the River Tiber (Rome, Italy). Ecological Indicators 28, 107-114.
| Crossref | Google Scholar |
Dirección General de Aguas de Chile (2004) Diagnóstico y clasificación de los cursos y cuerpos de agua según objetivos de calidad: Cuenca del Rio Maipo, Chile. (Gobierno de Chile, Ministerio de Obras Publicas, Dirección General de Aguas) Available at https://mma.gob.cl/wp-content/uploads/2017/12/Maipo.pdf [In Spanish]
Escenarios Hídricos 2030 (2022) Cuencas regenerativas. De la crisis a la seguridad hídrica. Hoja de ruta Maipo y Maule. (Escenarios Hídricos 2030) Available at https://escenarioshidricos.cl/wp-content/uploads/2023/04/Cuencas-Regenerativas-de-la-crisis-a-la-seguridad-hidrica-hoja-de-ruta-Maipo-y-Maule.pdf [In Spanish]
Farías M, Charrier R, Carretier S, Martinod J, Fock A, Campbell D, Cáceres J, Comte D (2008) Late Miocene high and rapid surface uplift and its erosional response in the Andes of central Chile (33°–35°S). Tectonics 27, TC1005.
| Crossref | Google Scholar |
Friedland KD, Langan JA, Large SI, Selden RL, Link JS, Watson RA, Collie JS (2020) Changes in higher trophic level productivity, diversity and niche space in a rapidly warming continental shelf ecosystem. Science of The Total Environment 704, 135270.
| Crossref | Google Scholar |
Gamboa M, Reyes R, Arrivillaga J (2008) Macroinvertebrados bentónicos como bioindicadores de salud ambiental. Boletín de Malariología y Salud Ambiental 48, 109-120 [In Spanish].
| Google Scholar |
García L, Cross WF, Pardo I, Richardson JS (2017) Effects of landuse intensification on stream basal resources and invertebrate communities. Freshwater Science 36, 609-625.
| Crossref | Google Scholar |
Gomez J, De La Maza C, Melo Ó (2014) Restoring environmental flow: buy-back costs and pollution-dilution as a compliance with water quality standards. Water Policy 16, 864-879.
| Crossref | Google Scholar |
Guo F, Kainz MJ, Sheldon F, Bunn SE (2016) The importance of high-quality algal food sources in stream food webs – current status and future perspectives. Freshwater Biology 61, 815-831.
| Crossref | Google Scholar |
Hanson P, Springer M, Ramirez A (2010) Capítulo 1. Introducción a los grupos de macroinvertebrados acuáticos. Revista de Biologia Tropical 58, 3-37 [In Spanish].
| Google Scholar |
Hepp LU, Milesi SV, Biasi C, Restello RM (2010) Effects of agricultural and urban impacts on macroinvertebrates assemblages in streams (Rio Grande do Sul, Brazil). Zoologia 27, 106-113.
| Crossref | Google Scholar |
Hicks KA, Loomer HA, Fuzzen MLM, Kleywegt S, Tetreault GR, McMaster ME, Servos MR (2017) δ15N tracks changes in the assimilation of sewage-derived nutrients into a riverine food web before and after major process alterations at two municipal wastewater treatment plants. Ecological Indicators 72, 747-758.
| Crossref | Google Scholar |
Kaehler S, Pakhomov EA (2001) Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Marine Ecology Progress Series 219, 299-304.
| Crossref | Google Scholar |
Kasangaki A, Chapman LJ, Balirwa J (2008) Land use and the ecology of benthic macroinvertebrate assemblages of high-altitude rainforest streams in Uganda. Freshwater Biology 53, 681-697.
| Crossref | Google Scholar |
Kuzmanović M, López-Doval JC, De Castro-Català N, Guasch H, Petrović M, Muñoz I, Ginebreda A, Barceló D (2016) Ecotoxicological risk assessment of chemical pollution in four Iberian river basins and its relationship with the aquatic macroinvertebrate community status. Science of The Total Environment 540, 324-333.
| Crossref | Google Scholar | PubMed |
Lapointe BE, Herren LW, Debortoli DD, Vogel MA (2015) Evidence of sewage-driven eutrophication and harmful algal blooms in Florida’s Indian River Lagoon. Harmful Algae 43, 82-102.
| Crossref | Google Scholar |
Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87, 545-562.
| Crossref | Google Scholar | PubMed |
Lee KY, Graham L, Spooner DE, Xenopoulos MA (2018) Tracing anthropogenic inputs in stream foods webs with stable carbon and nitrogen isotope systematics along an agricultural gradient. PLoS ONE 13, e0200312.
| Crossref | Google Scholar |
Merritt RW, Cummins KW (2007) Trophic relationships of macroinvertebrates. In ‘Methods in stream ecology’. (Eds FR Hauer, GA Lamberti) pp. 585–601. (Academic Press) 10.1016/B978-012332908-0.50036-X
Merritt RW, Cummins KW, Berg MB (2017) Trophic relationships of macroinvertebrates. In ‘Methods in stream ecology’, 3rd edn. (Eds FR Hauer, GA Lamberti) pp. 413–433. (Academic Press) 10.1016/B978-0-12-416558-8.00020-2
Mesa LM, Reynaga MC, Correa MV, Sirombra MG (2013) Effects of anthropogenic impacts on benthic macroinvertebrates assemblages in subtropical mountain streams. Iheringia. Serie Zoologia 103, 342-349.
| Crossref | Google Scholar |
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135-1140.
| Crossref | Google Scholar |
Moraes AB, Wilhelm AE, Boelter T, Stenert C, Schulz UH, Maltchik L (2014) Reduced riparian zone width compromises aquatic macroinvertebrate communities in streams of southern Brazil. Environmental Monitoring and Assessment 186, 7063-7074.
| Crossref | Google Scholar | PubMed |
Morin-Crini N, Lichtfouse E, Liu G, Balaram V, Ribeiro ARL, Lu Z, Stock F, Carmona E, Teixeira MR, Picos-Corrales LA, Moreno-Piraján JC, Giraldo L, Li C, Pandey A, Hocquet D, Torri G, Crini G (2022) Worldwide cases of water pollution by emerging contaminants: a review. Environmental Chemistry Letters 20, 2311-2338.
| Crossref | Google Scholar |
Nahmani J, Rossi J-P (2003) Soil macroinvertebrates as indicators of pollution by heavy metals. Comptes Rendus. Biologies 326, 295-303 [In English with abstract in English and French].
| Crossref | Google Scholar | PubMed |
Peña-Guerrero MD, Nauditt A, Muñoz-Robles C, Ribbe L, Meza F (2020) Drought impacts on water quality and potential implications for agricultural production in the Maipo River Basin, Central Chile. Hydrological Sciences Journal 65, 1005-1021.
| Crossref | Google Scholar |
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703-718.
| Crossref | Google Scholar |
Príncipe RE, Gualdoni CM, Oberto AM, Raffaini GB, Corigliano MC (2010) Spatial-temporal patterns of functional feeding groups in mountain streams of Córdoba, Argentina. Ecologia Austral 20, 257-268.
| Google Scholar |
Registro de Emisiones y Transferencias de Contaminantes (2022) Informe Consolidado de Emisiones y Transferencias de Contaminantes del RETC 2005–2020. (Ministerio del Medio Ambiente: Santiago, Chile) Available at https://retc.mma.gob.cl/books/informe-consolidado-de-emisiones-y-transferencias-de-contaminantes-del-retc-2005-2020/ [In Spanish]
Registro de Emisiones y Transferencias de Contaminantes (2023) Informe Consolidado de Emisiones y Transferencias de Contaminantes del RETC 2021. (Ministerio del Medio Ambiente: Santiago, Chile) Available at https://retc.mma.gob.cl/books/informe-consolidado-de-emisiones-y-transferencias-de-contaminantes-del-retc-2021-2/ [In Spanish]
Smucker NJ, Kuhn A, Cruz-Quinones CJ, Serbst JR, Lake JL (2018) Stable isotopes of algae and macroinvertebrates in streams respond to watershed urbanization, inform management goals, and indicate food web relationships. Ecological Indicators 90, 295-304.
| Crossref | Google Scholar | PubMed |
Soriano Y, Carmona E, Renovell J, Picó Y, Brack W, Krauss M, Backhaus T, Inostroza PA (2024) Co-occurrence and spatial distribution of organic micropollutants in surface waters of the River Aconcagua and Maipo basins in Central Chile. Science of The Total Environment 954, 176314.
| Crossref | Google Scholar |
Steffy LY, Kilham SS (2004) Elevated δ15N in stream biota in areas with septic tank systems in an urban watershed. Ecological Applications 14, 637-641.
| Crossref | Google Scholar |
Sterling JL, Rosemond AD, Wenger SJ (2016) Watershed urbanization affects macroinvertebrate community structure and reduces biomass through similar pathways in Piedmont streams, Georgia, USA. Freshwater Science 35, 676-688.
| Crossref | Google Scholar |
Vega-Retter C, Muñoz-Rojas P, Vila I, Copaja S, Véliz D (2014) Genetic effects of living in a highly polluted environment: the case of the silverside Basilichthys microlepidotus (Jenyns) (Teleostei: atherinopsidae) in the Maipo River Basin, central Chile. Population Ecology 56, 569-579.
| Crossref | Google Scholar |
Vega-Retter C, Vila I, Véliz D (2015) Signatures of directional and balancing selection in the silverside Basilichthys microlepidotus (Teleostei: Atherinopsidae) inhabiting a polluted river. Evolutionary Biology 42, 156-168.
| Crossref | Google Scholar |
Vega-Retter C, Rojas-Hernandez N, Vila I, Espejo R, Loyola DE, Copaja S, Briones M, Nolte AW, Véliz D (2018) Differential gene expression revealed with RNA-Seq and parallel genotype selection of the ornithine decarboxylase gene in fish inhabiting polluted areas. Scientific Reports 8, 4820.
| Crossref | Google Scholar |
Vega-Retter C, Rojas-Hernández N, Cortés-Miranda J, Véliz D, Rico C (2024) Genome scans reveal signals of selection associated with pollution in fish populations of Basilichthys microlepidotus, an endemic species of Chile. Scientific Reports 14, 15727.
| Crossref | Google Scholar |
Veliz D, Rojas-Hernández N, Copaja SV, Vega-Retter C (2020) Temporal changes in gene expression and genotype frequency of the ornithine decarboxylase gene in native silverside Basilichthys microlepidotus: impact of wastewater reduction due to implementation of public policies. Evolutionary Applications 13, 1183-1194.
| Crossref | Google Scholar | PubMed |
Wilkinson JL, Boxall ABA, Kolpin DW, Leung KMY, Lai RWS, Galban-Malagón C, Adell AD, Mondon J, Metian M, Marchant RA, Bouzas-Monroy A, Cuni-Sanchez A, Coors A, Carriquiriborde P, Rojo M, Gordon C, Cara M, Moermond M, Luarte T, Petrosyan V, Perikhanyan Y, Mahon CS, McGurk CJ, Hofmann T, Kormoker T, Iniguez V, Guzman-Otazo J, Tavares JL, Gildasio De Figueiredo F, Razzolini MTP, Dougnon V, Gbaguidi G, Traore O, Blais JM, Kimpe LE, Wong M, Wong D, Ntchantcho R, Pizarro J, Ying G-G, Chen C-E, Paez M, Martínez-Lara J, Otamonga J-P, Poté J, Ifo SA, Wilson P, Echeverría-Sáenz S, Udikovic-Kolic N, Milakovic M, Fatta-Kassinos D, Ioannou-Ttofa L, Belusova V, Vymazal J, Cardenas-Bustamante M, Kassa BA, Garric J, Chaumot A, Gibba P, Kunchulia I, Seidensticker S, Lyberatos G, Halldorsson HP, Melling M, Shashidhar T, Lamba M, Nastiti A, Supriatin A, Pourang N, Abedini A, Abdullah O, Gharbia SS, Pilla F, Chefetz B, Topaz T, Yao KM, Aubakirova B, Beisenova R, Olaka L, Mulu JK, Chatanga P, Ntuli V, Blama NT, Sherif S, Aris AZ, Looi LJ, Niang M, Traore ST, Oldenkamp R, Ogunbanwo O, Ashfaq M, Iqbal M, Abdeen Z, O’Dea A, Morales-Saldaña JM, Custodio M, de la Cruz H, Navarrete I, Carvalho F, Gogra AB, Koroma BM, Cerkvenik-Flajs V, Gombac M, Thwala M, Choi K, Kang H, Ladu JLC, Rico A, Amerasinghe P, Sobek A, Horlitz G, Zenker AK, King AC, Jiang J-J, Kariuki R, Tumbo M, Tezel U, Onay TT, Lejju JB, Vystavna Y, Vergeles Y, Heinzen H, Perez-Parada A, Sims DB, Figy M, Good D, Teta C (2022) Pharmaceutical pollution of the world’s rivers. Proceedings of the National Academy of Sciences of the United States of America 119, e2113947119.
| Crossref | Google Scholar |
