in

Using stable isotopes to analyse extinction risks and reintroduction opportunities of native species in invaded ecosystems

  • 1.

    Lovell, S. J., Stone, S. F. & Fernandez, L. The economic impacts of aquatic invasive species: a review of the literature. Agric. Resour. Econ. Rev. 35(1), 195–208 (2006).

    Article  Google Scholar 

  • 2.

    Ehrenfeld, J. G. Ecosystem consequences of biological invasions. Ann. Rev. Ecol. Evol. Syst. 41, 59–80 (2010).

    Article  Google Scholar 

  • 3.

    Dunham, J. B., Adams, S. B., Schroeter, R. E. & Novinger, D. C. Non-native invasions in aquatic ecosystems: toward an understanding of brook trout invasions and potential impacts on inland cutthroat trout in western North America. Rev. Fish Biol. Fish. 12(4), 373–391 (2002).

    Article  Google Scholar 

  • 4.

    Balzani, P. et al. Stable isotope analysis of trophic niche in two co-occurring native and invasive terrapins, Emys orbicularis and Trachemys scripta elegans. Biol. Invasions 18(12), 3611–3621 (2016).

    Article  Google Scholar 

  • 5.

    Haubrock, P. J. et al. Control and eradication efforts of aquatic non-native fish species in Lake Caicedo Yuso-Arreo. Manag. Biol. Invasions 9, 267–278 (2018).

    Article  Google Scholar 

  • 6.

    Preston, D. L., Henderson, J. S. & Johnson, P. T. Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities. Ecology 93(6), 1254–1261 (2012).

    PubMed  Article  Google Scholar 

  • 7.

    Gallardo, B., Clavero, M., Sánchez, M. I. & Vilà, M. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22(1), 151–163 (2016).

    ADS  Article  Google Scholar 

  • 8.

    Pejchar, L. & Mooney, H. A. Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 24(9), 497–504 (2009).

    PubMed  Article  Google Scholar 

  • 9.

    Simberloff, D. & Von Holle, B. Positive interactions of nonindigenous species: invasional meltdown?. Biol. Invasions 1(1), 21–32 (1999).

    Article  Google Scholar 

  • 10.

    Beisel, J. N. The elusive model of a biological invasion process: time to take differences among aquatic and terrestrial ecosystems into account? (2001).

  • 11.

    Ricciardi, A. & Cohen, J. The invasiveness of an introduced species does not predict its impact. Biol. Invasions 9(3), 309–315 (2007).

    Article  Google Scholar 

  • 12.

    Strayer, D. L. Non-native species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw. Biol. 55, 152–174 (2010).

    Article  Google Scholar 

  • 13.

    Früh, D., Stoll, S. & Haase, P. Physicochemical and morphological degradation of stream and river habitats increases invasion risk. Biol. Invasions 14(11), 2243–2253 (2012).

    Article  Google Scholar 

  • 14.

    Höckendorff, S., Früh, D., Hormel, N., Haase, P. & Stoll, S. Biotic interactions under climate warming: temperature-dependent and species-specific effects of the oligochaete Chaetogaster limnaei on snails. Freshw. Sci. 34, 1304–1311 (2015).

    Article  Google Scholar 

  • 15.

    Leung, B. & Mandrak, N. E. The risk of establishment of aquatic invasive species: joining invasibility and propagule pressure. Proc. R. Soc. B Biol. Sci. 274(1625), 2603–2609 (2007).

    Article  Google Scholar 

  • 16.

    Copp, G. H., Garthwaite, R. & Gozlan, R. E. Risk identification and assessment of non-native freshwater fishes: a summary of concepts and perspectives on protocols for the UK. J. Appl. Ichthyol. 21(4), 371–373 (2005).

    Article  Google Scholar 

  • 17.

    Copp, G. H. et al. European non-native species in aquaculture risk analysis scheme—a summary of assessment protocols and decision support tools for use of non-native species in aquaculture. Fish. Manag. Ecol. 23(1), 1–11 (2016).

    Article  Google Scholar 

  • 18.

    Bacher, S. et al. Socio-economic impact classification of non-native taxa (SEICAT). Methods Ecol. Evol. 9(1), 159–168 (2018).

    Article  Google Scholar 

  • 19.

    Roy, H. E. et al. Developing a framework of minimum standards for the risk assessment of non-native species. J. Appl. Ecol. 55(2), 526–538 (2018).

    Article  Google Scholar 

  • 20.

    Moustakas, A. & Katsanevakis, S. Data mining and methods for early detection, horizon scanning, modelling, and risk assessment of invasive species. Front. Appl. Math. Stat. 4, 5 (2018).

    Article  Google Scholar 

  • 21.

    Dick, J. T. et al. Invader relative impact potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive non-native species. J. Appl. Ecol. 54(4), 1259–1267 (2017).

    Article  Google Scholar 

  • 22.

    Cuthbert, R. N., Dickey, J. W., Coughlan, N. E., Joyce, P. W. & Dick, J. T. The functional response ratio (FRR): advancing comparative metrics for predicting the ecological impacts of invasive non-native species. Biol. Invasions 1–5 (2019).

  • 23.

    Haubrock, P. J. et al. Predatory functional responses under increasing temperatures of two life stages of an invasive gecko. Sci. Rep. 10(1), 1–10 (2020).

    Article  CAS  Google Scholar 

  • 24.

    Vonesh, J., McCoy, M., Altwegg, R., Landi, P. & Measey, J. Functional responses can’t unify invasion ecology. Biol. Invasions 19(5), 1673–1676 (2017).

    Article  Google Scholar 

  • 25.

    Dick, J. T. et al. Fictional responses from Vonesh et al. Biol. Invasions 19(5), 1677–1678 (2017).

    Article  Google Scholar 

  • 26.

    Vander Zanden, M. J., Casselman, J. M. & Rasmussen, J. B. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401(6752), 464 (1999).

    ADS  Article  CAS  Google Scholar 

  • 27.

    Haubrock, P. J. et al. Shared histories of co-evolution may affect trophic interactions in a freshwater community dominated by non-native species. Front. Ecol. Evol. 7, 355 (2019).

    Article  Google Scholar 

  • 28.

    Stellati, L. et al. Living with non-natives: suboptimal ecological condition in semiaquatic snakes inhabiting a hot spot of allodiversity. Acta Oecol. 100, 103466 (2019).

    Article  Google Scholar 

  • 29.

    Huckembeck, S. et al. Feeding ecology and basal food sources that sustain the Paradoxal frog Pseudis minuta: a multiple approach combining stomach content, prey availability, and stable isotopes. Hydrobiologia 740(1), 253–264 (2014).

    Article  Google Scholar 

  • 30.

    Middelburg, J. J. Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences. 11, 2357–2371 (2014).

    ADS  Article  Google Scholar 

  • 31.

    Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER–stable isotope bayesian ellipses in R. J. Anim. Ecol. 80(3), 595–602 (2011).

    Article  Google Scholar 

  • 32.

    Parnell, A. C. et al. Bayesian stable isotope mixing models. Environmetrics 24(6), 387–399 (2013).

    MathSciNet  Google Scholar 

  • 33.

    Haubrock, P. J. et al. Predicting the effects of reintroducing a native predator (European eel, Anguilla anguilla) into a freshwater community dominated by non-native species using a multidisciplinary approach. Manag. Biol. Invasions 10(1), 171–191 (2019).

    Article  Google Scholar 

  • 34.

    Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3), 703–718 (2002).

    Article  Google Scholar 

  • 35.

    Füreder, L., Gherardi, F., Holdich, D., Reynolds, J., Sibley, P. & Souty-Grosset, C. Austropotamobius pallipes. The IUCN Red List of Threatened Species. e.T2430A9438817. https://doi.org/10.2305/IUCN.UK.2010-3.RLTS.T2430A9438817.en. (2010).

  • 36.

    Pike, C., Crook, V. & Gollock, M. Anguilla anguilla. The IUCN Red List of Threatened Species e.T60344A152845178. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T60344A152845178.en. (2020).

  • 37.

    González-Mozo, M. E., Chicote, A., Rico, E. & Montes, C. Limnological characterization of an evaporite karstic lake in Spain (Arreo Lake). Trends Ecol. Evol. 19(9), 470–474 (2004).

    Article  Google Scholar 

  • 38.

    Asensio, R. Actuaciones de descaste de cangrejos alóctonos en el lago de Caicedo Yuso – Arreo para los años 2014 y 2015. PROYECTO TREMEDAL “LIFE11 NAT/ES/707”. URA/Arabako Foru Aldundia/HAZI. (2015).

  • 39.

    Alonso de Santocildes, G., Criado, A., Manzanos, A. & A.P. Monteoliva. Fish sampling in inland lakes: methodological approach and case study, Arreo Lake (Álava). IV Jornadas Ibéricas de Ictiología (2012).

  • 40.

    Losos, J. B. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 11(10), 995–1003 (2008).

    PubMed  Article  Google Scholar 

  • 41.

    Pauli, J. N., Steffan, S. A. & Newsome, S. D. It is time for IsoBank. BioScience 65(3), 229–230 (2015).

    Article  Google Scholar 

  • 42.

    Pauli, J. N. et al. Opinion: Why we need a centralized repository for isotopic data. Proc. Natl. Acad. Sci. 114(12), 2997–3001 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Gratwicke, B. & Marshall, B. E. The relationship between the exotic predators Micropterus salmoides and Serranochromis robustus and native stream fishes in Zimbabwe. J. Fish Biol. 58(1), 68–75 (2001).

    Article  Google Scholar 

  • 44.

    Maezono, Y. & Miyashita, T. Community-level impacts induced by introduced largemouth bass and bluegill in farm ponds in Japan. Biol. Conserv. 109(1), 111–121 (2003).

    Article  Google Scholar 

  • 45.

    Yonekura, R., Kita, M. & Yuma, M. Species diversity in native fish community in Japan: comparison between non-invaded and invaded ponds by exotic fish. Ichthyol. Res. 51(2), 176–179 (2004).

    Article  Google Scholar 

  • 46.

    Maezono, Y., Kobayashi, R., Kusahara, M. & Miyashita, T. Direct and indirect effects of exotic bass and bluegill on exotic and native organisms in farm ponds. Ecol. Appl. 15(2), 638–650 (2005).

    Article  Google Scholar 

  • 47.

    Almeida, D., Gomes-Lopes, A., Muñoz-López, M., Merino-Aquirre, R. & Miranda, R. Ecología de la agresión interespecífica en el pez sol Lepomis gibbosus y efectos sobre la fauna autóctona. In Posters from the Symposium on non-native freshwater species introduction in the Iberian Peninsula, Pamplona, Spain. http://www.unav.es/centro/especiesinvasoras/ (2009).

  • 48.

    Froese, R., & Pauly, D. (2010). www.FishBase.de. Accessed November 19th, 2019.

  • 49.

    Oficialdegui, F. J., Sánchez, M. I. & Clavero, M. One century away from home: how the red swamp crayfish took over the world. Rev. Fish Biol. Fish. 1–15 (2020).

  • 50.

    Fletcher, A. R., Morison, A. K. & Hume, D. J. Effects of carp, Cyprinus carpio L., on communities of aquatic vegetation and turbidity of waterbodies in the lower Goulburn River basin. Mar. Freshw. Res. 36(3), 311–327 (1985).

    Article  Google Scholar 

  • 51.

    Pompei, L., Franchi, E., Giannetto, D. & Lorenzoni, M. Growth and reproductive properties of Tench, Tinca tinca Linnaeus, 1758 in Trasimeno Lake (Umbria, Italy). Knowl. Manag. Aquat. Ecosyst. 406 (2012).

  • 52.

    Angeler, D. G., Sánchez-Carrillo, S., García, G. & Alvarez-Cobelas, M. The influence of Procambarus clarkii (Cambaridae, Decapoda) on water quality and sediment characteristics in a Spanish floodplain wetland. Hydrobiologia 464(1–3), 89–98 (2001).

    Article  Google Scholar 

  • 53.

    Jastrebski, C. J. & Robinson, B. W. Natural selection and the evolution of replicated trophic polymorphisms in pumpkinseed sunfish (Lepomis gibbosus). Evol. Ecol. Res. 6(2), 285–305 (2004).

    Google Scholar 

  • 54.

    Gherardi, F. & Barbaresi, S. Feeding opportunism of the red swamp crayfish Procambarus clarkii, an invasive species. Freshw. Crayfish 16, 77–85 (2008).

    Google Scholar 

  • 55.

    Wolfram-Wais, A., Wolfram, G., Auer, B., Mikschi, E. & Hain, A. Feeding habits of two introduced fish species (Lepomis gibbosus, Pseudorasbora parva) in Neusiedler See (Austria), with special reference to chironomid larvae (Diptera: Chironomidae). Shallow Lakes 98, 123–129 (1999).

    Article  Google Scholar 

  • 56.

    Fell, P. E. et al. Does invasion of oligohaline tidal marshes by reed grass, Phragmites australis (Cav.) Trin. ex Steud., affect the availability of prey resources for the mummichog, Fundulus heteroclitus L.?. J. Exper. Mar. Biol. Ecol. 222(1–2), 59–77 (1998).

    Article  Google Scholar 

  • 57.

    Bedford, A. P. & Powell, I. Long-term changes in the invertebrates associated with the litter of Phragmites australis in a managed reedbed. Hydrobiologia 549(1), 267–285 (2005).

    Article  Google Scholar 

  • 58.

    Chambers, R. M., Meyerson, L. A. & Saltonstall, K. Expansion of Phragmites australis into tidal wetlands of North America. Aquat. Bot. 64(3–4), 261–273 (1999).

    Article  Google Scholar 

  • 59.

    Gratton, C. & Denno, R. F. Restoration of arthropod assemblages in a Spartina salt marsh following removal of the invasive plant Phragmites australis. Restoration Ecology. 13(2), 358–372 (2005).

    Article  Google Scholar 

  • 60.

    Gherardi, F. et al. A review of allodiversity in Lake Naivasha, Kenya: developing conservation actions to protect East African lakes from the negative impacts of non-native species. Biol. Conserv. 144(11), 2585–2596 (2011).

    Article  Google Scholar 

  • 61.

    Stiers, I., Crohain, N., Josens, G. & Triest, L. Impact of three aquatic invasive species on native plants and macroinvertebrates in temperate ponds. Biol. Invasions 13(12), 2715–2726 (2011).

    Article  Google Scholar 

  • 62.

    Barbaresi, S., Tricarico, E. & Gherardi, F. Factors inducing the intense burrowing activity of the red-swamp crayfish, Procambarus clarkii, an invasive species. Naturwissenschaften 91(7), 342–345 (2004).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 63.

    Britton, J. R. et al. From introduction to fishery dominance: the initial impacts of the invasive carp Cyprinus carpio in Lake Naivasha, Kenya, 1999 to 2006. J. Fish Biol. 71, 239–257. https://doi.org/10.1111/j.1095-8649.2007.01669.x (2007).

    Article  Google Scholar 

  • 64.

    Anton-Pardo, M., Hlaváč, D., Másílko, J., Hartman, P. & Adámek, Z. Natural diet of mirror andscaly carp (Cyprinus carpio) phenotypes in earth ponds. Folia Zool. 63, 229–237. https://doi.org/10.25225/fozo.v63.i4.a1.2014 (2014).

    Article  Google Scholar 

  • 65.

    Hauser, C. E. & McCarthy, M. A. Streamlining ‘search and destroy’: cost-effective surveillance for invasive species management. Ecol. Lett. 12(7), 683–692 (2009).

    PubMed  Article  Google Scholar 

  • 66.

    Rinella, M. J., Maxwell, B. D., Fay, P. K., Weaver, T. & Sheley, R. L. Control effort exacerbates invasive-species problem. Ecol. Appl. 19(1), 155–162 (2009).

    PubMed  Article  Google Scholar 

  • 67.

    Jourdan, J. et al. Reintroduction of freshwater macroinvertebrates: challenges and opportunities. Biol. Rev. 94(2), 368–387 (2019).

    PubMed  Article  Google Scholar 

  • 68.

    Haase, P., & Pilotto, F. A method for the reintroduction of entire benthic invertebrate communities in formerly degraded streams. Limnologica, 77, 125689 (2019).

    Article  Google Scholar 

  • 69.

    Feunteun, E. Management and restoration of European eel population (Anguilla anguilla): an impossible bargain. Ecol. Eng. 18(5), 575–591 (2002).

    Article  Google Scholar 

  • 70.

    Clavero, M. & Hermoso, V. Historical data to plan the recovery of the European eel. J. Appl. Ecol. 52(4), 960–968 (2015).

    Article  Google Scholar 

  • 71.

    Benndorf, J. Possibilities and limits for controlling eutrophication by biomanipulation. Int. Rev. Hydrobiol. 80, 519–534. https://doi.org/10.1002/iroh.19950800404 (1995).

    CAS  Article  Google Scholar 

  • 72.

    Aquiloni, L. et al. Biological control of invasive populations of crayfish: the European eel (Anguilla anguilla) as a predator of Procambarus clarkii. Biol. Invasions 12, 3817–3824. https://doi.org/10.1007/s10530-010-9774-z (2010).

    Article  Google Scholar 

  • 73.

    McCord JW American eel. South Carolina State Documents Depository (2005)

  • 74.

    Schiphouwer, M. E. et al. Risk assessment of the alien smallmouth bass (Micropterusdolomieu). Rep. Environ. Sci. 527, 1–60 (2017).

    Google Scholar 

  • 75.

    Costantini, M. L. et al. The role of alien fish (the centrarchid Micropterus salmoides) in lake food webs highlighted by stable isotope analysis. Freshw. Biol. 63, 1130–1142. https://doi.org/10.1111/fwb.13122 (2018).

    CAS  Article  Google Scholar 

  • 76.

    Laffaille, P., Caraguel, J. M. & Legault, A. Temporal patterns in the upstream migration of European glass eels (Anguilla anguilla) at the Couesnon estuarine dam. Estuarine Coast. Shelf Sci. 73(1–2), 81–90 (2007).

    ADS  Article  Google Scholar 

  • 77.

    Prigge, E. Factors challenging the European eel (Anguilla anguilla) stock recovery in continental waters (Doctoral dissertation, Christian-Albrechts Universität Kiel) (2013).

  • 78.

    Catford, J. A., Jansson, R. & Nilsson, C. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers. Distrib. 15(1), 22–40 (2009).

    Article  Google Scholar 

  • 79.

    Marchi, M. et al. Resistance and re-organization of an ecosystem in response to biological invasion: some hypotheses. Ecol. Modell. 222(16), 2992–3001 (2011).

    Article  Google Scholar 

  • 80.

    Martínez-Torres, L., Gonzáles-Tapia, J. R. & Ramóm-Luch, C. Batimetría y propuesta de cartografía geológica del lago de Arreo (Diapiro de salinas de Añana, Álava) Eusko Jkaskuntza. Cuadernos de Sección. Historia 20, 123–134 (1992).

    Google Scholar 

  • 81.

    Camacho, A., Borja, C., Valero-Garcés, B., Sahuquillo, M., Cirujano, S., Soria, J. M., Rico, E., De la Hera, A., Santamans, A. C., García deDomingo, A., Chicote, A. & Gosálvez, R. U. 3190 Lagos ylagunas kársticas sobre yesos. In: Ministerio de Medio Ambiente,y Medio Rural y Marino Bases ecológicas preliminares para laconservación de los tipos de hábitat de interés comunitario en España. Madrid, Spain, 37 pp (2009).

  • 82.

    Vitoria-Gasteiz, L. Biodiversity Strategy of the Basque Autonomous Community 2030 and First Action Plan 2020; Servicio Central de Publicaciones del Gobierno Vasco (2016).

  • 83.

    Choi, W. J., Ro, H. M. & Chang, S. X. Carbon isotope composition of Phragmites australis in a constructed saline wetland. Aquat. Bot. 82(1), 27–38 (2005).

    Article  Google Scholar 

  • 84.

    Bergamino, L., Dalu, T. & Richoux, N. B. Evidence of spatial and temporal changes in sources of organic matter in estuarine sediments: stable isotope and fatty acid analyses. Hydrobiologia 732(1), 133–145 (2014).

    CAS  Article  Google Scholar 

  • 85.

    Kullman, M. A., Kidd, K. A., Podemski, C. L., Paterson, M. J. & Blanchfield, P. J. Assimilation of freshwater salmonid aquaculture waste by native aquatic biota. Can. J. Fish. Aquat. Sci. 66(11), 1965–1975 (2009).

    CAS  Article  Google Scholar 

  • 86.

    Tonn, W. M., Klatt, P. H., Paszkowski, C. A., Gingras, B. A. & Wilcox, K. Trophic Relations of the Red-Necked Grebe on Lakes in the Western Boreal Forest: A Stable-Isotope Analysis (2004).

  • 87.

    Jardine, T. D. et al. Understanding and overcoming baseline isotopic variability in running waters. River Res. Appl. 30(2), 155–165 (2014).

    Article  Google Scholar 

  • 88.

    Tran, T. N. Q., Jackson, M. C., Sheath, D., Verreycken, H. & Britton, J. R. Patterns of trophic niche divergence between invasive and native fishes in wild communities are predictable from mesocosm studies. J. Anim. Ecol. 84(4), 1071–1080 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 89.

    Dörner, H. et al. Piscivory and trophic position of Anguilla anguilla in two lakes: importance of macrozoobenthos density. J. Fish Biol. 74(9), 2115–2131 (2009).

    PubMed  Article  Google Scholar 

  • 90.

    Quezada-Romegialli, C. et al. tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol. Evol. 9(6), 1592–1599 (2018).

    Article  Google Scholar 

  • 91.

    Layman, C. A. et al. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol. Rev. 87(3), 545–562 (2012).

    PubMed  Article  Google Scholar 

  • 92.

    Layman, C. A., Arrington, D. A., Montaña, C. G. & Post, D. M. Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology 88(1), 42–48 (2007).

    Article  Google Scholar 

  • 93.

    Swanson, H. K. et al. A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology 96(2), 318–324 (2015).

    PubMed  Article  Google Scholar 


  • Source: Ecology - nature.com

    Amanda Hubbard honored with Secretary of Energy’s Appreciation Award

    Quantifying and addressing the prevalence and bias of study designs in the environmental and social sciences