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Nonnative invasive species are overlooked in biological integrity assessments

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Abstract

Multimetric indices (MMIs) are common tools used to assess the biological status of ecosystems. However, not all the components of biological integrity have been equally addressed, since most of MMIs do not consider nonnative species, which are a great threat to ecosystems integrity. We performed a systematic review of how nonnative species have been considered in MMIs to assess biological conditions worldwide. Using a systematic review of the literature we identified to what extent nonnative species have been included as a disturbance factor for determining reference conditions and if specific metrics related to both nonnative and native species have been taken into account in the MMIs around the world. We also identified the most frequent species origin metrics that have been included in the MMIs. We searched for articles published in English up to 2016 that applied or developed an MMI in the Web of Science database (Clarivate Analytics). Following the PRISMA guidelines, we analyzed 409 articles. We found that only 1.2% of the studies used nonnative species as a disturbance factor in determining reference conditions. About 66% of articles did not test or did not provide the information if they tested metrics on native or nonnative species. Most of the articles (53%) that tested native or nonnative metrics were fish-based MMIs. We found 97 different metrics, of which 69% were related to native species, whereas 31% were related to nonnative ones. Native richness was the most used metric in studies that considered species origin (23.5%). Our main results evidence that nonnative species are overlooked in biomonitoring programs. Owing to the well-known impacts of them on ecosystem integrity, their inclusion in definition of reference conditions and in MMIs metrics should be considered as bioassessment criteria.

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References

  • Angermeier P, Karr JR (2019) Ecological health indicators. In: Fath B (ed) Encyclopedia of ecology, vol 1, 2nd edn. Elsevier, Oxford, pp 391–401

    Chapter  Google Scholar 

  • Barbour MT, Gerritsen J, Snyder BD et al (1999) Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish (EPA 841-B-99-002), 2nd edn. Office of Water, US Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Barbour MT, Swietlik WF, Jackson SK et al (2000) Measuring the attainment of biological integrity in the USA: a critical element of ecological integrity. Hydrobiologia 422/423:453–464

    Article  CAS  Google Scholar 

  • Beck MW, Hatch LK, Vondracek B, Valley RD (2010) Development of a macrophyte-based index of biotic integrity for Minnesota lakes. Ecol Ind 10:968–979

    Article  CAS  Google Scholar 

  • Bezerra LAV, Angelini R, Vitule JRS, Coll M, Sanchez-Botero JI (2018) Food web changes associated with drought and invasive species in a tropical semiarid reservoir. Hydrobiologia 817:475–489

    Article  Google Scholar 

  • Bezerra LAV, Freitas MO, Daga VS et al (2019) A network meta-analysis of threats to South American fish biodiversity. Fish Fish 20:620–639

    Google Scholar 

  • Boon PJ, Clarke SA, Copp GH (2020) Alien species and the EU Water Framework Directive: a comparative assessment of European approaches. Biol Invasions 22:1497–1512

    Article  Google Scholar 

  • Buckley YM, Csergő AM (2017) Predicting invasion winners and losers under climate change. Proc Natl Acad Sci USA 114(16):4040–4041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buss DF, Carlisle D, Chon TS et al (2015) Stream biomonitoring using macroinvertebrates around the globe: a comparison of large-scale programs. Environ Monitor Assess 187:1–21

    Article  Google Scholar 

  • Carniatto N, Thomaz SM, Cunha ER, Fugi R, Ota RR (2013) Effects of an invasive alien Poaceae on aquatic macrophytes and fish communities in a Neotropical reservoir. Biotropica 45:747–754

    Article  Google Scholar 

  • Fausch KD, Lyons JD, Angermeier PL, Karr JR (1990) Fish communities as indicators of environmental degradation. Am Fish Soc Symp 8:123–144

    Google Scholar 

  • Flood PJ, Duran A, Barton M, Mercado-Molina AE, Trexler JC (2020) Invasion impacts on functions and services of aquatic ecosystems. Hydrobiologia 847:1571–1586

    Article  Google Scholar 

  • Gozlan RE, Britton JR, Cowx I, Copp GH (2010) Current knowledge on non-native freshwater fish introductions. J Fish Biol 76:751–786

    Article  Google Scholar 

  • Green PT, O’Dowd DJ, Abbott KL, Jeffery M, Retallick K, Mac Nally R (2011) Invasional meltdown: invader-invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768

    Article  PubMed  Google Scholar 

  • Gubiani ÉA, Ruaro R, Ribeiro VR et al (2018) Non-native fish species in Neotropical freshwaters: how did they arrive, and where did they come from? Hydrobiologia 817:57–69

    Article  Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Tren Ecol Evol 19:470–474

    Article  Google Scholar 

  • Hering D, Feld CJ, Moog O et al (2006) Cook book for the development of a Multimetric Index for biological condition of aquatic ecosystems: experiences from the European AQEM and STAR projects and related initiatives. Hydrobiologia 566:311–324

    Article  Google Scholar 

  • Hermoso V, Clavero M (2013) Revisiting ecological integrity 30 years later: non-native species and the misdiagnosis of freshwater ecosystem health. Fish Fish 14:416–423

    Article  Google Scholar 

  • Hermoso V, Clavero M, Blanco-Garrido F, Prenda J (2010) Assessing the ecological status in species-poor systems: a fish-based index for Mediterranean Rivers (Guadiana River, SW Spain). Ecol Ind 10:1152–1161

    Article  Google Scholar 

  • Hughes RM, Kaufmann PR, Herlihy AT et al (1998) A process for developing and evaluating indices of fish assemblage integrity. Can J Fish Aquat Sci 55:1618–1631

    Article  Google Scholar 

  • Karatayev AY, Burlakova LE, Padilla DK (2015) Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia 746:97–112

    Article  CAS  Google Scholar 

  • Karr JR (1981) Assessment of biotic integrity using fish communities. Fisheries 6(6):21–27

    Article  Google Scholar 

  • Karr JR, Chu EW (1999) Restoring life in running waters: better biological monitoring. Island Press, Covelo

    Google Scholar 

  • Karr JR, Chu EW (2000) Sustaining living rivers. Hydrobiologia 422(423):1–4

    Article  Google Scholar 

  • Kleynhans CJ (1999) The development of a fish index to assess the biological integrity of South African rivers. Water SA 25:265–278

    Google Scholar 

  • Kuehne ML, Olden JD, Streecker AL et al (2017) Past, present, and future of ecological integrity assessment for freshwaters. Front Ecol Environ 15:197–205

    Article  Google Scholar 

  • Liu B, Cao S (2018) Comment: averaging statistics of multimetric index leading to an inaccurate evaluation on methods of defining biological condition of streams/rivers in ecological assessment. Sci Total Environ 649:1640–1642

    Article  PubMed  CAS  Google Scholar 

  • Lowry E, Rollinson EJ, Laybourn AJ, Scott TE, Aiello- Lammens ME, Gray SM, Mickley J, Gurevitch J (2013) Biologicalinvasions: a field synopsis, systematic review, and databaseof the literature. Ecol Evol 3:182–196

    Article  PubMed Central  Google Scholar 

  • MacNeil C (2019) Predatory impacts of the invasive “killer shrimp” Dikerogammarus villosus on a resident amphipod and isopod (Crustacea: Malacostraca) are influenced by water quality and habitat type. Hydrobiologia 833:53–64

    Article  CAS  Google Scholar 

  • Magee TK, Blocksom KA, Fennessy MS (2019a) A national-scale vegetation multimetric index (VMMI) as an indicator of wetland condition across the conterminous United States. Environ Monit Assess 191:322

    Article  PubMed  PubMed Central  Google Scholar 

  • Magee TK, Blocksom KA, Herlihy AT et al (2019b) Characterizing nonnative plants in wetlands across the conterminous United States. Environ Monit Assess 191:344

    Article  PubMed  PubMed Central  Google Scholar 

  • Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097

    Article  PubMed  PubMed Central  Google Scholar 

  • Múrria C, Bonada N, Prat N (2008) Effects of the invasive species Potamopyrgus antipodarum (Hydrobiidae, Mollusca) on community structure in a small Mediterranean stream. Fundam Appl Limno 171:131–143

    Article  CAS  Google Scholar 

  • Norris RH, Hawkins CP (2000) Monitoring river health. Hydrobiologia 435:5–17

    Article  Google Scholar 

  • Panetta FD, Gooden B (2017) Managing for biodiversity: impact and action thresholds for invasive plants in natural ecosystems. NeoBiota 34:53–66

    Article  Google Scholar 

  • Paolucci EM, MacIsaac HJ, Ricciardi A (2018) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Div Dist 19:988–995

    Article  Google Scholar 

  • Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19

    Article  Google Scholar 

  • Pelicice FM, Agostinho AA (2009) Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biol Invasions 11:1789–1801

    Article  Google Scholar 

  • Pereira PS, Souza NF, Baptista DF et al (2016) Incorporating natural variability in the bioassessment of stream condition in the Atlantic Forest biome, Brazil. Ecol Ind 69:606–616

    Article  Google Scholar 

  • Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species' traits and environment. Glob Chang Biol 18(5):1725–1737

    Article  PubMed Central  Google Scholar 

  • Ribeiro VR, da Silva PRL, Gubiani ÉA, Faria L, Daga VS, Vitule JRS (2017) Imminent threat of the predator fish invasion Salminus brasiliensis in a Neotropical ecoregion: eco-vandalism masked as an environmental project. Perspect Ecol Conser 15:132–135

    Google Scholar 

  • Roset N, Grenouillet G, Goffaux D, Pont D, Kestemont P (2007) A review of existing fish assemblage indicators and methodologies. Fish Manag Ecol 14:393–405

    Article  Google Scholar 

  • Ruaro R, Gubiani ÉA (2013) A scientometric assessment of 30 years of the Index of Biotic Integrity in aquatic ecosystems: applications and main flaws. Ecol Ind 29:105–110

    Article  Google Scholar 

  • Ruaro R, Mormul RP, Gubiani ÉA et al (2018) Non-native fish species are related to the loss of ecological integrity in Neotropical streams: a multimetric approach. Hydrobiologia 817:413–430

    Article  Google Scholar 

  • Ruaro R, Gubiani ÉA, Cunico AM et al (2019) Unified multimetric index for the evaluation of the biological condition of streams in Southern Brazil based on fish and macroinvertebrate assemblages. Environ Manag 64:661–673

    Article  Google Scholar 

  • Ruaro R, Gubiani ÉA, Hughes RM, Mormul RP (2020a) Global trends and challenges in multimetric indices of biological condition. Ecol Ind 110:105862

    Article  Google Scholar 

  • Ruaro R, Gubiani ÉA, Padial AA, Mormul (2020b) Use of Multimetric indices of ecological condition: a meta-analysis (in preparation)

  • Silva DRO, Herlihy AT, Hughes RM, Callisto M (2017) An improved macroinvertebrate multimetric index for assessment of wade-able streams in the neotropical savanna, Brazil. Ecol Ind 81:514–525

    Article  Google Scholar 

  • Simberloff D, von Holle B (1999) Positive interactions of nonindigenous species. Biol Invasions 1:21–32

    Article  Google Scholar 

  • Simberloff D, Martin JL, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Article  PubMed  Google Scholar 

  • Sofaer HR, Jarnevich CS, Pearse IS (2018) The relationship between invader abundance and impact. Ecosphere 9(9):e02415

    Article  Google Scholar 

  • Stevenson RJ, Tang T, Infante DM (2018) Advancing evaluation of bioassessment methods: a reply to Liu and Cao. Sci Total Environ 645:895–900

    Article  CAS  PubMed  Google Scholar 

  • Stoddard JL, Larsen DP, Hawkins CP et al (2006) Setting expectations for the ecological condition of running waters: the concept of reference condition. Ecol Appl 16:1267–1276

    Article  PubMed  Google Scholar 

  • Stoddard JL, Herlihy AT, Peck DV, Hughes RM, Whittier TR, Tarquino E (2008) A process for creating multimetric indices for large-scale aquatic surveys. J N Am Benthol Soc 27(4):878–891

    Article  Google Scholar 

  • Stribling JB, Dressing SA (2015) Technical memorandum 4: applying benthic macroinvertebrate multimetric indexes to stream condition assessments, October 2015. Developed for U.S. Environmental Protection Agency by Tetra Tech, Inc., Fairfax, VA, 14 p. Available online at https://www.epa.gov/polluted-runoff-nonpoint-source-pollution/watershed-approach-technical-resources. Accessed 10 August 2019

  • Suter GW (1993) A critique of ecosystem health concepts and indexes. Environ Toxicol Chem 12:1533–1539

    Article  Google Scholar 

  • Tang TR, Stevenson RJ, Infante D (2016) Accounting for regional variation in both natural environment and human disturbance to improve performance of multimetric indices of lotic benthic diatoms. Sci Total Environ 568:1124–1134

    Article  CAS  PubMed  Google Scholar 

  • Thomas CD (2010) Climate, climate change and range boundaries. Divers Distrib 16:488–495

    Article  Google Scholar 

  • Turbelin AJ, Malamud BD, Francis RA (2016) Mapping the global state of invasive alien species: Patterns of invasion and policy responses. Glob Ecol Biogeogr 26:78–92

    Article  Google Scholar 

  • USEPA (United States Environmental Protection Agency) (1996) Biological Criteria: Technical Guidance for Streams and Small Rivers, EPA 822-B-96-001. U.S. Environmental Protection Agency, Office of Water, Washington, DC

    Google Scholar 

  • USEPA (United States Environmental Protection Agency) (2016a) A Practitioner’s Guide to the Biological Condition Gradient: A Framework to Describe Incremental Change in Aquatic Ecosystems. EPA-842-R-16-001. U.S. Environmental Protection Agency, Washington, DC. https://www.epa.gov/sites/production/files/2016-02/documents/bcg-practioners-guide-report.pdf

  • USEPA (United States Environmental Protection Agency) (2016b) National Rivers and Streams Assessment 2008–2009: A Collaborative Survey. EPA 841/R-16/007, Office of Water and Office of Research and Development, US Environmental Protection Agency, Washington, DC. https://www.epa.gov/national-aquatic-resource-surveys/national-rivers-and-streams-assessment-2008-2009-report

  • Vitule JRS, Freire CA, Simberloff D (2009) Introduction of non-native freshwater fish can certainly be bad. Fish Fish 10:98–108

    Article  Google Scholar 

  • Whittier TR, Van Sickle J (2010) Macroinvertebrate tolerance levels and an assemblage tolerance index (ATI) for western USA streams and rivers. J N Am Benthol Soc 29:852–866

    Article  Google Scholar 

  • Whittier TR, Hughes RM, Stoddard JL et al (2007) A structured approach for developing indices of biotic integrity: three examples from streams and rivers in the western USA. Trans Am Fish Soc 136:718–735

    Article  Google Scholar 

  • Winterbourn MJ, Gregson KLD, Dolphin CH (2006) Guide to the aquatic insects of New Zealand. Fourth Edition. Bull Entomol Soc New Zealand 14

  • Wood KA, O’Hare MT, McDonald C, Searle KR, Daunt F, Stillman RA (2017) Herbivory regulation of plant abundance in aquatic ecosystems. Biol Rev 92:1128–1141

    Article  PubMed  Google Scholar 

  • Wurtzebach Z, Schultz C (2016) Measuring ecological integrity: history, practical applications, and research opportunities. Bioscience 66(6):446–457

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded partially by the Coordination of Superior Level Staff Improvement - Finance Code 001. We acknowledge two anonymous referees whose comments helped to improve considerably the first version of this work. We thank the National Council for Scientific and Technological Development (CNPq) for a scholarship granted to RR (141371/2016-1). RPM, ÉAG and SMT are Productivity Researchers funded by CNPq and thanks to this agency for grants. We thank MSR Arita (University of Maringá, Brazil) for help in obtaining articles.

Funding

Funding was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Grand Number 001), Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grand Number 308578/2017-1).

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  1. Ecology of Inland Water Ecosystems, State University of Maringá, Av. Colombo 5790, Bloco H-90, Maringá, Paraná, CEP 87020-900, Brazil

    Renata Ruaro, Sidinei Magela Thomaz & Roger Paulo Mormul

  2. Federal University of Technology – Paraná (UTFPR), Câmpus Curitiba - Sede Ecoville, Rua Deputado Heitor de Alencar Furtado 5000, Curitiba, Paraná, CEP 81280-340, Brazil

    Renata Ruaro

  3. Group of Research in Fisheries Resources and Limnology (Gerpel), Graduate Course in Fishing Resources and Fisheries Engineering, State University of Western Paraná, Toledo, Paraná, Brazil

    Éder André Gubiani

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  1. Renata Ruaro
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Ruaro, R., Gubiani, É.A., Thomaz, S.M. et al. Nonnative invasive species are overlooked in biological integrity assessments. Biol Invasions 23, 83–94 (2021). https://doi.org/10.1007/s10530-020-02357-8

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