Riparian invader: A secondary metabolite of Impatiens glandulifera impairs the development of the freshwater invertebrate key species Chironomus riparius
Authors/Creators
- 1. University of Bayreuth, Bayreuth, Germany
Description
Invasive species represent a significant threat to native biodiversity. The Himalayan Balsam Impatiens glandulifera is an annual plant, which is invasive in Europe and often inhabits the riparian zone. It produces several secondary metabolites causing, for example, growth inhibition of terrestrial plants and invertebrates. One of these metabolites is the quinone 2-methoxy-1,4-naphthoquinone (2-MNQ). The compound gets washed out from the above-ground parts of the plant during precipitation and may then leach into nearby waterbodies. Despite some evidence for the allelopathic effect of plant secondary metabolites on terrestrial invertebrates, little is known about how 2-MNQ affects the survival or development of aquatic dipteran larvae, despite the importance of this functional group in European freshwaters. Here, we investigated the effects of 2-MNQ on larvae of the river keystone species Chironomus riparius in acute and chronic scenarios. The toxicity of 2-MNQ towards the first and the fourth larval stage was determined in a 48-hour acute exposure assay. We show that 2-MNQ has a negative impact on the development, growth and survival of C. riparius. The LC50 of 2-MNQ was 3.19 mg/l for the first instar and 2.09 mg/l for the fourth instar. A ten-day chronic exposure experiment, where the water was spiked with 2-MNQ, revealed that 2-MNQ had a significantly negative impact on larval body size, head capsule size, body weight, development and survival. These results demonstrate the negative impact of the secondary metabolite 2-MNQ from the terrestrial plant I. glandulifera on a crucial macroinvertebrate inhabiting the adjacent stream ecosystem in riverine ecosystems. This may lead to a decline in population size, resulting in cascading effects on the food web.
Files
NB_article_119621.pdf
Files
(851.5 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:4c191ebb1169e5663ba2b5f326e0fd96
|
851.5 kB | Preview Download |
System files
(138.4 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:039c45bc59caec7c0ff435a955e8c7aa
|
138.4 kB | Download |
Linked records
Additional details
References
- Abgrall C, Forey E, Mignot L, Chauvat M (2018) Invasion by Fallopia japonica alters soil food webs through secondary metabolites. Soil Biology & Biochemistry 127: 100–109. https://doi.org/10.1016/j.soilbio.2018.09.016
- Armitage PD, Cranston PS, Pinder LCV (1995) The Chironomidae: The biology and Ecology of Non-Biting Midges. Springer, Dordrecht, 572 pp. https://doi.org/10.1007/978-94-011-0715-0
- Barbas JT, Sigman ME, Buchanan AC III, Chevis EA (1993) Photolysis of substituted naphthalenes on SiO2 and Al2O3. Photochemistry and Photobiology 58(2): 155–158. https://doi.org/10.1111/j.1751-1097.1993.tb09541.x
- Barclay RM (1991) Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. Journal of Animal Ecology 60(1): 165–178. https://doi.org/10.2307/5452
- Beerling DJ, Perrins JM (1993) Impatiens glandulifera Royle (Impatiens roylei Walp.). Journal of Ecology 81(2): 367–382. https://doi.org/10.2307/2261507
- Bieberich J, Lauerer M, Drachsler M, Heinrichs J, Mueller S, Feldhaar H (2018) Species- and developmental stage-specific effects of allelopathy and competition of invasive Impatiens glandulifera on co- occurring plants. PLOS ONE 13(11): e0205843. https://doi.org/10.1371/journal.pone.0205843
- Brett MT, Goldman CR (1997) Consumer versus resource control in freshwater pelagic food webs. Science 275(5298): 384–386. https://doi.org/10.1126/science.275.5298.384
- Chapelle JP (1974) 2-Methoxy-1,4-naphthoquinone in Impatiens glandulifera and related species. Phytochemistry 13(3): e662. https://doi.org/10.1016/S0031-9422(00)91379-7
- Chapman DS, Gray A (2012) Complex interactions between the wind and ballistic seed dispersal in Impatiens glandulifera (Royle). Journal of Ecology 100(4): 874–883. https://doi.org/10.1111/j.1365-2745.2012.01977.x
- Clements WH (1994) Benthic invertebrate community responses to heavy metals in the Upper Arkansas River Basin, Colorado. Journal of the North American Benthological Society 13(1): 30–44. https://doi.org/10.2307/1467263
- Corpus-Mendoza CI, de Loera D, López-López LI, Acosta B, Vega-Rodríguez S, Navarro-Tovar G (2022) Interactions of antibacterial naphthoquinones with mesoporous silica surfaces: A physicochemical and theoretical approach. Pharmaceuticals 15(12): e1464. https://doi.org/10.3390/ph15121464
- Čuda J, Rumlerová Z, Brůna J, Skálová H, Pyšek P (2017) Floods affect the abundance of invasive Impatiens glandulifera and its spread from river corridors. Diversity & Distributions 23(4): 342–354. https://doi.org/10.1111/ddi.12524
- de Bisthoven LGJ, Timmermans KR, Ollevier F (1992) The concentration of cadmium, lead, copper and zinc in Chironomus gr. thummi larvae (Diptera, Chironomidae) with deformed versus normal menta. Hydrobiologia 239(3): 141–149. https://doi.org/10.1007/BF00007671
- Diller JGP, Drescher S, Hofmann M, Rabus M, Feldhaar H, Laforsch C (2022) The Beauty is a beast: Does leachate from the invasive terrestrial plant Impatiens glandulifera affect aquatic food webs? Ecology and Evolution 12(4): e8781. https://doi.org/10.1002/ece3.8781
- Diller JGP, Hüftlein F, Lücker D, Feldhaar H, Laforsch C (2023) Allelochemical run-off from the invasive terrestrial plant Impatiens glandulifera decreases defensibility in Daphnia. Scientific Reports 13(1): e1207. https://doi.org/10.1038/s41598-023-27667-4
- Dris R, Gasperi J, Rocher V, Saad M, Renault N, Tassin B (2015) Microplastic contamination in an urban area: A case study in Greater Paris. Environmental Chemistry 12(5): 592–599. https://doi.org/10.1071/EN14167
- Dutta PK, Dutta J, Tripathi VS (2004) Chitin and chitosan: Chemistry, properties and applications. Journal of Scientific and Industrial Research 63: 20–31.
- Elendt BP, Bias WR (1990) Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna. Water Research 24(9): 1157–1167. https://doi.org/10.1016/0043-1354(90)90180-E
- Erfmeier A, Bruelheide H (2010) Invasibility or invasiveness? Effects of habitat, genotype, and their interaction on invasive Rhododendron ponticum populations. Biological Invasions 12(3): 657–676. https://doi.org/10.1007/s10530-009-9472-x
- Gelman A, Su YS (2023) arm: Data Analysis Using Regression and Multilevel/Hierarchical Models (R Package Version 1.12-3) [Software]. Comprehensive R Archive Network (CRAN). https://CRAN.R-project.org/package=arm
- Gregory SV, Swanson FJ, Mckee WA, Cummins KW (1991) An ecosystem perspective on riparian zones: Focus on links between land and water. Bioscience 41(8): 540–551. https://doi.org/10.2307/1311607
- Hartig F (2022) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.4.6. http://florianhartig.github.io/DHARMa/
- Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. Journal of Ecology 97(3): 393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x
- Hellawell JM (1986) Biological Indicators of Freshwater Pollution and Environmental Management. In: Melanby K (Ed.) Pollution Monitoring Series. Elsevier Applied Science Publishers, London and New York, 546 pp.
- Hladyz S, Åbjörnsson K, Giller PS, Woodward G (2011) Impacts of an aggressive riparian invader on community structure and ecosystem functioning in stream food webs. Journal of Applied Ecology 48(2): 443–452. https://doi.org/10.1111/j.1365-2664.2010.01924.x
- Hothorn T, Bretz F, Westfall P (2008) Simultaneous Inference in General Parametric Models. Biometrical Journal 50(3): 346–363. https://doi.org/10.1002/bimj.200810425
- Hulme PE (2009) Trade, transport and trouble: Managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46(1): 10–18. https://doi.org/10.1111/j.1365-2664.2008.01600.x
- Jackson BK, Stock SL, Harris LS, Szewczak JM, Schofield LN, Desrosiers MA (2020) River food chains lead to riparian bats and birds in two mid‐order rivers. Ecosphere 11(6): e03148. https://doi.org/10.1002/ecs2.3148
- Jiang W, Pan B, Jiang X, Shi P, Zhu P, Zhang L, Wu N (2021) A comparative study on the indicative function of species and traits structure of stream macroinvertebrates to human disturbances. Ecological Indicators 129: e107939. https://doi.org/10.1016/j.ecolind.2021.107939
- Jones GL, Scullion J, Worgan H, Gwynn-Jones D (2019) Litter of the invasive shrub Rhododendron ponticum (Ericaceae) modifies the decomposition rate of native UK woodland litter. Ecological Indicators 107: e105597. https://doi.org/10.1016/j.ecolind.2019.105597
- Keller VD, Williams RJ, Lofthouse C, Johnson AC (2014) Worldwide estimation of river concentrations of any chemical originating from sewage‐treatment plants using dilution factors. Environmental Toxicology and Chemistry 33(2): 447–452. https://doi.org/10.1002/etc.2441
- Kisielius V, Hama JR, Skrbic N, Hansen HCB, Strobel BW, Rasmussen LH (2020) The invasive butterbur contaminates stream and seepage water in groundwater wells with toxic pyrrolizidine alkaloids. Scientific Reports 10(1): e19784. https://doi.org/10.1038/s41598-020-76586-1
- Kubo I, Uchida M, Klocke JA (1983) An insect ecdysis inhibitor from the african medicinal plant, Plumbago capensis (Plumbaginaceae); a naturally occurring chitin synthetase inhibitor. Agricultural and Biological Chemistry 47(4): 911–913. https://doi.org/10.1080/00021369.1983.10865746
- Lake PS (2000) Disturbance, patchiness, and diversity in streams. Journal of the North American Benthological Society 19(4): 573–592. https://doi.org/10.2307/1468118
- Leitner P, Borgwardt F, Birk S, Graf W (2021) Multiple stressor effects on benthic macroinvertebrates in very large European rivers – A typology-based evaluation of faunal responses as a basis for future bioassessment. The Science of the Total Environment 756: e143472. https://doi.org/10.1016/j.scitotenv.2020.143472
- Lobstein A, Brenne X, Feist E, Metz N, Weniger B, Anton R (2001) Quantitative determination of naphthoquinones of Impatiens species. Phytochemical Analysis 12(3): 202–205. https://doi.org/10.1002/pca.574
- Logan P, Brooker MP (1983) The macroinvertebrate faunas of riffles and pools. Water Research 17(3): 263–270. https://doi.org/10.1016/0043-1354(83)90179-3
- Macneale KH, Spromberg JA, Baldwin DH, Scholz NL (2014) A modeled comparison of direct and food web-mediated impacts of common pesticides on Pacific salmon. PLOS ONE 9(3): e92436. https://doi.org/10.1371/journal.pone.0092436
- Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity; separating nest site and parental activity effects. Proceedings. Biological Sciences 267(1459): 2287–2293. https://doi.org/10.1098/rspb.2000.1281
- Meyer GW, Bahamon Naranjo MA, Widhalm JR (2021) Convergent evolution of plant specialized 1, 4-naphthoquinones: Metabolism, trafficking, and resistance to their allelopathic effects. Journal of Experimental Botany 72(2): 167–176. https://doi.org/10.1093/jxb/eraa462
- Millane M, Caffrey JM (2014) Risk assessment of Impatiens glandulifera Royle – Himalayan Balsam. Report prepared for Inland Fisheries Ireland and the National Biodiversity Data Centre.
- Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: A history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research 19(1): 1–54. https://doi.org/10.1016/S0380-1330(93)71197-1
- Mitchell MJ, Crooks JR, Keogh DP, Smith SL (1999) Ecdysone 20‐monooxygenase activity during larval‐pupal‐adult development of the tobacco hornworm, Manduca sexta. Archives of Insect Biochemistry and Physiology 41(1): 24–32. https://doi.org/10.1002/(SICI)1520-6327(1999)41:1<24::AID-ARCH5>3.0.CO;2-R
- Mitchell MJ, Brescia AI, Smith SL, Morgan ED (2007) Effects of the compounds 2-methoxynaphthoquinone, 2-propoxynaphthoquinone, and 2-isopropoxy-naphthoquinone on ecdysone 20-monooxygenase activity. Archives of Insect Biochemistry and Physiology 66(1): 45–52. https://doi.org/10.1002/arch.20196
- Monk AB, Kanmukhla V, Trinder K, Borkow G (2014) Potent bactericidal efficacy of copper oxide impregnated non-porous solid surfaces. BMC Microbiology 14(1): e57. https://doi.org/10.1186/1471-2180-14-57
- Muzzarelli RAA, Littarru G, Muzzarelli C, Tosi G (2003) Selective reactivity of biochemically relevant quinones towards chitosans. Carbohydrate Polymers 53(1): 109–115. https://doi.org/10.1016/S0144-8617(03)00006-7
- Naiman RJ, Décamps H (1997) The ecology of interfaces: Riparian zones. Annual Review of Ecology and Systematics 28(1): 621–658. https://doi.org/10.1146/annurev.ecolsys.28.1.621
- Naiman RJ, Decamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecological Applications 3(2): 209–212. https://doi.org/10.2307/1941822
- Park K, Kwak IS (2018) Disrupting effects of antibiotic sulfathiazole on developmental process during sensitive life-cycle stage of Chironomus riparius. Chemosphere 190: 25–34. https://doi.org/10.1016/j.chemosphere.2017.09.118
- Patil I (2021) Visualizations with statistical details: The 'ggstatsplot' approach. Journal of Open Source Software 6(61): e3167. https://doi.org/10.21105/joss.03167
- Pattison Z, Rumble H, Tanner RA, Jin L, Gange AC (2016) Positive plant – soil feedbacks of the invasive Impatiens glandulifera and their effects on above‐ground microbial communities. Weed Research 56(3): 198–207. https://doi.org/10.1111/wre.12200
- Pereyra CE, Dantas RF, Ferreira SB, Gomes LP, Paes Jr FS (2019) The diverse mechanisms and anticancer potential of naphthoquinones. Cancer Cell International 19(1): 1–20. https://doi.org/10.1186/s12935-019-0925-8
- Pinder LCV (1986) Biology of freshwater Chironomidae. Annual Review of Entomology 31(1): 1–23. https://doi.org/10.1146/annurev.en.31.010186.000245
- Pyšek P (1994) Ecological aspects of invasion by Heracleum mantegazzianum in the Czech Republic. In: de Waal LC, Child LE, Wade PM, Brock JH (Eds) Ecology and Management of Invasive Riverside Plants. J. Wiley and Sons, Chichester, 45–54.
- Pysek P, Prach K (1995) Invasion dynamics of Impatiens glandulifera – a century of spreading reconstructed. Biological Conservation 74(1): 41–48. https://doi.org/10.1016/0006-3207(95)00013-T
- Richardson JS (1993) Limits to productivity in streams: Evidence from studies of macroinvertebrates. Canadian Special Publication of Fisheries and Aquatic Sciences 118: 9–15.
- Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLOS ONE 10(12): e0146021. https://doi.org/10.1371/journal.pone.0146021
- Ruckli R, Hesse K, Glauser G, Rusterholz H-P, Baur B (2014a) Inhibitory potential of naphthoquinones leached from leaves and exuded from roots of the invasive plant Impatiens glandulifera. Journal of Chemical Ecology 40(4): 371–378. https://doi.org/10.1007/s10886-014-0421-5
- Ruckli R, Rusterholz HP, Baur B (2014b) Invasion of an annual exotic plant into deciduous forests suppresses arbuscular mycorrhiza symbiosis and reduces performance of sycamore maple saplings. Forest Ecology and Management 318: 285–293. https://doi.org/10.1016/j.foreco.2014.01.015
- R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
- Serra SRQ, Graça MAS, Dolédec S, Feio MJ (2017) Chironomidae traits and life history strategies as indicators of anthropogenic disturbance. Environmental Monitoring and Assessment 189(7): 1–16. https://doi.org/10.1007/s10661-017-6027-y
- Smith SL (1985) Regulation of ecdysteroid titer: synthesis. In: Kerkut GA, Gilbert LI (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, Oxford, 295–341.
- Smith SL, Bollenbacher WE, Cooper DY, Schleyer H, Wielgus JJ, Gilbert LI (1979) Ecdysone 20-monooxygenase: Characterization of an insect cytochrome P-450 dependent steroid hydroxylase. Molecular and Cellular Endocrinology 15(3): 111–133. https://doi.org/10.1016/0303-7207(79)90033-9
- Sugie S, Okamoto K, Rahman KMW, Tanaka T, Kawai K, Yamahara J, Mori H (1998) Inhibitory effects of plumbagin and juglone on azoxymethane-induced intestinal carcinogenesis in rats. Cancer Letters 127(1–2): 177–183. https://doi.org/10.1016/S0304-3835(98)00035-4
- Taenzler V, Bruns E, Dorgerloh M, Pfeifle V, Weltje L (2007) Chironomids: Suitable test organisms for risk assessment investigations on the potential endocrine disrupting properties of pesticides. Ecotoxicology 16(1): 221–230. https://doi.org/10.1007/s10646-006-0117-x
- Tandon VK, Maurya HK (2009) 'On water': Unprecedented nucleophilic substitution and addition reactions with 1, 4-quinones in aqueous suspension. Tetrahedron Letters 50(43): 5896–5902. https://doi.org/10.1016/j.tetlet.2009.07.149
- Tassou KT, Schulz R (2009) Ecotoxicology and Environmental Safety Effects of the insect growth regulator pyriproxyfen in a two-generation test with Chironomus riparius. Ecotoxicology and Environmental Safety 72(4): 1058–1062. https://doi.org/10.1016/j.ecoenv.2009.02.001
- Thiboldeaux RL, Lindroth RL, Tracy JW (1994) Differential toxicity of juglone (5-hydroxy-1, 4-naphthoquinone) and related naphthoquinones to saturniid moths. Journal of Chemical Ecology 20(7): 1631–1641. https://doi.org/10.1007/BF02059885
- Urgenson L, Reichard SH (2007) The ecological consequences of giant knotweed invasion into riparian forests. US Forest Service Pacific Northwest Research Station General Technical Report PNW-GTR 694: 63–64.
- Verling E, Ruiz GM, Smith LD, Galil B, Miller AW, Murphy KR (2005) Supply-side invasion ecology: Characterizing propagule pressure in coastal ecosystems. Proceedings of the Royal Society B, Biological Sciences 272(1569): 1249–1257. https://doi.org/10.1098/rspb.2005.3090
- Vermeulen AC, Liberloo G, Dumont P, Ollevier F, Goddeeris B (2000) Exposure of Chironomus riparius larvae (diptera) to lead, mercury and β-sitosterol: Effects on mouthpart deformation and moulting. Chemosphere 41(10): 1581–1591. https://doi.org/10.1016/S0045-6535(00)00033-3
- Vitousek PM (1990) Biological Invasions and Ecosystem Processes: Towards an Integration of Population Biology and Ecosystem Studies. Oikos 57(1): 7–13. https://doi.org/10.2307/3565731
- Watts MM, Pascoe D (2000) A comparative study of Chironomus riparius Meigen and Chironomus tentans Fabricius (Diptera: Chironomidae) in aquatic toxicity tests. Archives of Environmental Contamination and Toxicology 39(3): 299–306. https://doi.org/10.1007/s002440010108
- Wright DA, Dawson R, Cutler SJ, Cutler HG (2006) Use of quinones as biocides for treatment of ballast water on ships. Environmental Technology 28: 309–319. https://doi.org/10.1080/09593332808618790