Figures
Abstract
The Convention on Biological Diversity (CBD) emphasises the role of biodiversity in delivering benefits essential for all people and, as a result, seeks to safeguard all life-forms. The indices that are used to measure progress towards international conservation and sustainability goals, however, focus solely on the ‘native’ component of biodiversity. A subset of non-native species can cause undesirable economic, social, or biological effects. But non-native species also contribute to regional biodiversity (species richness and biotic interactions) and ecosystem services. In some regions and cities, non-native species make up more than half of all species. Currently, the contributions of these species to biodiversity and ecosystem services are overlooked. Here, I argue that biodiversity and sustainability indices should include all species. This is not only consistent with definitions of biodiversity but also will promote the idea that long-term, sustainable, human well-being is intricately tied to benefits derived from nature.
Citation: Schlaepfer MA (2018) Do non-native species contribute to biodiversity? PLoS Biol 16(4): e2005568. https://doi.org/10.1371/journal.pbio.2005568
Published: April 17, 2018
Copyright: © 2018 Martin A. Schlaepfer. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The author received no specific funding for this work.
Competing interests: The author has declared that no competing interests exist.
Abbreviations: CBD, Convention on Biological Diversity; IPBES, Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services; IUCN, International Union for Conservation of Nature; SDG, Sustainable Development Goal
Provenance: Not commissioned; externally peer reviewed.
Humans have a long history of protecting certain elements of nature. The concepts and values underlying conservation initiatives, however, have changed repeatedly [1]. Conservation efforts in the 20th century focused primarily on preserving landscapes free of human influence and on preventing the erosion of biodiversity, with an emphasis on protecting rare species from extinction. The last 20 years have seen the emergence of additional concepts that emphasise the resilience of nature and the ‘services’ that nature contributes to human well-being [2,3]. These novel approaches are promoted by some conservation leaders under the assumption that they will broaden the social support for conservation goals [4,5]. The advent of more socially inclusive approaches to conservation biology raises interesting and profound questions regarding the dimensions of the living world we seek to preserve and the political process that is used to specify appropriate conservation objectives.
Non-native species, and how they are valued, are at the heart of these ongoing debates. For the last several decades, non-native species have been portrayed by scientists primarily as a threat to society because a subset can cause economic harm, human-health issues, or the loss of native biodiversity [6,7]. The view that non-native species are potentially undesirable persists in indicators used to track progress towards targets of the Convention on Biological Diversity (CBD), where they only appear as a numerical predictor for future invasion events (Aichi Target 9) [8].
More recently, scientists have also documented the potential positive contributions of non-native species to regional species richness [9,10], conservation goals [11], and to the ecosystem services they contribute to certain stakeholders within society [12–14]. In some instances, non-native species are rapidly appreciated for their cultural ecosystem services. For example, citizen groups have lobbied for the protection of non-native Eucalyptus trees in California and non-native dingos in Australia [11]. The potentially positive contributions of non-native species to biodiversity and to the long-term welfare of humans are missing from current biodiversity indicators (Table 1). This raises the following questions: Are non-native species part of ‘nature’ or ‘biodiversity’ that we wish to preserve? If so, can they be integrated into a conservation planning process in a way that recognises their potential for undesirable effects but also captures their potential positive contributions to biodiversity and society?
Biodiversity is a complex notion and the indicators that are used to track it [16] are a reflection of available information, objectives, and values, which all can vary culturally and with time [3,28]. However, it is important to ask under what circumstances it might be scientifically and politically desirable to modify some biodiversity indicators to include all species in light of ongoing preparations for the Post-2020 Strategic Plan of CBD, ongoing assessments by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), and forthcoming national implementation of the Sustainable Development Goals (SDGs).
Non-native species as an integral component of biodiversity
There are several reasons why non-native species should be considered part of biodiversity and included in biodiversity and sustainability indices.
First, the absence of non-native species from biodiversity indices stands in contradiction to the CBD and SDGs. The CBD definition of biodiversity (Article 2) encompasses the biological dimensions of the world (genes, species, ecosystems and their interactions), but it makes no distinction between native and non-native life forms, nor does it refer to notions of ‘intactness’, which forms the basis for excluding non-native species from the Biodiversity Intactness Index (Table 1). Aichi Target 2 and Goal 15.9 of the SDGs require national and local governments to account for ‘the diverse values of biodiversity’.
Second, non-native species should be included in key biodiversity indices because they represent large fractions of modern ecosystems and regional species-pools. Non-native plants and birds can make up 50% or more of species in some urban [29,30], insular [9,31,32], and old-field [33] environments. There is a risk that regional policy makers in areas in which non-native species comprise a significant component of the landscape will perceive biodiversity indices to be irrelevant if they are based solely on native species.
Finally, and perhaps most importantly, society’s motivations for the conservation of biodiversity are evolving and the indicators used to measure the state of the environment and progress towards our goals should too. Biodiversity indices will need to encompass all species if they are to remain socially relevant and illustrate the full gamut of what are now called ecosystem services (and disservices), or nature’s contributions to people [3] (Fig 1).
Left: A bow hunter on the Big Island of Hawaii with his catch, a non-native mouflon (feral sheep, Aries sp.). Mouflon threaten native plant species that have not evolved to resist mammalian herbivory. Right: Introduced goldenrod (Solidago gigantea) population near the city of Geneva, Switzerland. Goldenrod displaces native plants on a local scale and thus is considered invasive in Switzerland. But it is also appreciated for its ornamental and medicinal properties, and it serves as a resource for insects (hymenoptera and diptera, as seen in photograph). Current biodiversity indices and assessments capture the negative aspects of such non-native species (i.e., their potential for harm) but not their contributions to biodiversity (increase in regional species richness, interaction with other species) nor the ecosystem services (provisioning, regulating, cultural, supporting) that are socially and biologically relevant. Photos by author.
Drawbacks of accounting for non-native species
Some will argue that if non-native species are considered as an integral part of biodiversity then, by extension, it will be harder to make the case that non-native species are potentially problematic. Such a change might also be viewed as devaluing conservation efforts that focus on native species. Others have argued that some fraction of the negative impacts of non-native species may be underestimated and will only be known with time [7]. These are legitimate concerns.
Accounting for non-native species does not imply that they are inherently desirable, nor that native and non-native species are biologically or culturally interchangeable. Nor does counting all species as an initial step to describing the environment preclude scientists from conducting risk assessments of different species or groups of species regarding undesirable outcomes [7]. But to exclude non-native species a priori and without justification from indices (Table 1) and assessments of the state of the environment, as is sometimes done [22,34], prevents any subsequent debate about their relative merits.
Moving forward
There are several steps that can be taken to better align future conservation planning with the mission of CBD and the SDGs.
- Data used for biodiversity assessments and conservation planning should, initially, include all species. This will not only ensure that indices are representative of the environments they seek to characterise, but it will also align species richness and identity information with the functional information that is increasingly being measured remotely [35].
- Researchers should continue to investigate the extent to which non-native species influence the flow of ecosystem services and contribute to human well-being. One overlooked area of research is how including non-native species may alter existing biodiversity indices. Including non-native species into the Biodiversity Intactness Index can lead to a 10% improvement in the index score [21], and consideration of non-native populations in International Union for Conservation of Nature (IUCN) protocols will reduce a species’ global risk of extinction [18]. These examples hint that some existing index scores may be overly negative.
- Panels that decide which indicators to use when assessing progress towards global conservation goals, especially those that establish a link with human well-being (e.g., Aichi Targets), should be composed of specialists and laypersons from a range of backgrounds. Some indicators should reflect the preference of certain stakeholders for notions of ‘nativeness’ or ‘pristineness’, while others should capture all species found in modern ecosystems and their contributions to human well-being.
- Biodiversity and sustainability assessments that exclude non-native species [22,36,37,38] should systematically specify that they are tracking ‘native biodiversity’ and not ‘biodiversity’, as these terms are not synonymous.
The idea of considering non-native species in biodiversity assessments remains controversial [39] in part because it runs against decades of studies alerting policy makers and the public to the potential dangers associated with these species. Scientifically and politically, however, it may be the best thing to do, as it will ultimately ensure that indices and the databases that underlie them cover all dimensions of the living world and remain relevant to groups of stakeholders that extend beyond conservation biologists. The discussion about how to best integrate non-native species into biodiversity indicators will need to take place not only within a scientific debate about the contributions of these species to society but also a broader social debate about what type of nature we need to ensure a good life for present and future generations.
Acknowledgments
Stefanie Deinet and Louise McRae kindly provided data on the number of non-native populations in the Living Planet Index. I also thank A. Lehmann and L. Gallagher for their constructive feedback on earlier versions of this manuscript.
References
- 1. Mace GM. Whose conservation? Science. 2014;345(6204):1558–60. pmid:25258063
- 2. Costanza R, de Groot R, Braat L, Kubiszewski I, Fioramonti L, Sutton P, et al. Twenty years of ecosystem services: How far have we come and how far do we still need to go? Ecosystem Services. 2017;28:1–16.
- 3. Díaz S, Pascual U, Stenseke M, Martín-López B, Watson RT, Molnár Z, et al. Assessing nature’s contributions to people. Science. 2018;359(6373):270–2. pmid:29348221
- 4. Kareiva P, Lalasz R, Marvier M. Conservation in the Anthropocene. Breakthrough Journal. 2011;Fall 2011:29–37.
- 5.
Daily GC. Nature’s Services: Societal Dependence on Natural Ecosystems. Washington, DC: Island Press; 1997.
- 6.
Mooney HA, Hobbs RJ. Invasive Species in a Changing World. Washington DC: Island Press; 2000.
- 7. Simberloff D. Biological invasions: What’s worth fighting and what can be won? Ecological Engineering. 2014;65:112–21.
- 8.
Convention on Biological Diversity (CBD). Decision adopted by the conference of the parties to the convention on biological diversity at its tenth meeting. X/2. The Strategic Plan for Biodiversity 2011–2020 and the Aichi Biodiversity Targets2010. [cited 2018 apr 4]. https://www.cbd.int/doc/decisions/cop-10/cop-10-dec-02-en.pdf.
- 9. Sax DF, Gaines SD, Brown JH. Species invasions exceed extinctions on islands worldwide: A comparative study of plants and birds. Am Nat. 2002;160(6):766–83. pmid:18707464
- 10. Thomas CD, Palmer G. Non-native plants add to the British flora without negative consequences for native diversity. Proc Natl Acad Sci U S A. 2015;112(14):4387–92. Epub 2015/04/02. pmid:25831537
- 11. Schlaepfer MA, Sax DF, Olden JD. The potential conservation value of non-native species. Conserv Biol. 2011;25:428–37. pmid:21342267
- 12. Russo L, Nichol C, Shea K. Pollinator floral provisioning by a plant invader: quantifying beneficial effects of detrimental species. Diversity and Distributions. 2016;22(2):189–98.
- 13. Ramus AP, Silliman BR, Thomsen MS, Long ZT. An invasive foundation species enhances multifunctionality in a coastal ecosystem. Proc Natl Acad Sci U S A. 2017;114(32):8580–5. Epub 2017/07/19. pmid:28716918
- 14. Cameron RW, Blanusa T. Green infrastructure and ecosystem services—is the devil in the detail? Ann Bot. 2016;118(3):377–91. Epub 2016/07/23. pmid:27443302
- 15. Loh J, Green RE, Ricketts T, Lamoreux J, Jenkins M, Kapos V, et al. The Living Planet Index: using species population time series to track trends in biodiversity. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005;360(1454):289–95. pmid:15814346
- 16. Tittensor DP, Walpole M, Hill SLL, Boyce DG, Britten GL, Burgess ND, et al. A mid-term analysis of progress toward international biodiversity targets. Science. 2014;346(6206):241–4. pmid:25278504
- 17.
IUCN. IUCN Red List of Threatened Species. Version 2015–2. http://www.iucnredlist.org (IUCN: Gland, Switzerland, 2015). 2015.
- 18. Gibson L, Yong DL. Saving two birds with one stone: solving the quandary of introduced, threatened species. Frontiers in Ecology and the Environment. 2017;15(1):35–41.
- 19. Brooks TM, Akçakaya HR, Burgess ND, Butchart SHM, Hilton-Taylor C, Hoffmann M, et al. Analysing biodiversity and conservation knowledge products to support regional environmental assessments. Scientific Data. 2016;3:160007. pmid:26881749
- 20. Scholes RJ, Biggs R. A biodiversity intactness index. Nature. 2005;434(7029):45–9. pmid:15744293
- 21. Newbold T, Hudson LN, Arnell AP, Contu S, De Palma A, Ferrier S, et al. Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science. 2016;353(6296):288–91. pmid:27418509
- 22. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, et al. Global biodiversity scenarios for the Year 2100. Science. 2000;287(5459):1770–4. pmid:10710299
- 23. Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW, Almond REA, et al. Global Biodiversity: Indicators of Recent Declines. Science. 2010;328(5982):1164–8. pmid:20430971
- 24.
Department for Environment Food & Rural Affaires (DEFRA). Wild bird populations in the UK, 1970–2016. 2017.
- 25.
Chan L, Hillel O, Elmquist T, Werner P, Holman N, Mader A, et al. User’s Manual on the Singapore Index on Cities’ Biodiversity (also known as the City Biodiversity Index). Singapore: 2014.
- 26.
European Bird Census Council (EBCC). 2017 [cited 2017]. http://www.ebcc.info/index.php?ID=617.
- 27.
IUCN. Guidelines for Application of IUCN Red List Criteria at Regional and National Levels: Version 4.0. IUCN, editor. Gland, Switzerland and Cambridge, UK 2012.
- 28. Maris V, Béchet A. From adaptive management to adjustive management: a pragmatic account of biodiversity values. Conserv Biol. 2010;24(4):966–73. pmid:20151986
- 29. Pysek P. Alien and native species in Central European urban floras: a quantitative comparison. Journal of Biogeography. 1998;25(1):155–63.
- 30. Zerbe S, Maurer U, Schmitz S, Sukopp H. Biodiversity in Berlin and its potential for nature conservation. Landscape and Urban Planning. 2003;62(3):139–48.
- 31. Kueffer C, Daehler CC, Torres-Santana CW, Lavergne C, Meyer JY, Otto R, et al. A global comparison of plant invasions on oceanic islands. Perspectives in Plant Ecology Evolution and Systematics. 2010;12(2):145–61.
- 32. Case TJ. Global patterns in the establishment and distribution of exotic birds. Biol Conserv. 1996;78(1–2):69–96.
- 33. Cleland EE, Smith MD, Andelman SJ, Bowles C, Carney KM, Claire Horner-Devine M, et al. Invasion in space and time: non-native species richness and relative abundance respond to interannual variation in productivity and diversity. Ecology Letters. 2004;7(10):947–57.
- 34. Di Minin E, Soutullo A, Bartesaghi L, Rios M, Szephegyi MN, Moilanen A. Integrating biodiversity, ecosystem services and socio-economic data to identify priority areas and landowners for conservation actions at the national scale. Biol Conserv. 2017;206:56–64.
- 35. Vihervaara P, Auvinen A-P, Mononen L, Törmä M, Ahlroth P, Anttila S, et al. How Essential Biodiversity Variables and remote sensing can help national biodiversity monitoring. Global Ecology and Conservation. 2017;10:43–59.
- 36.
Hayhow DB, Burns F, Eaton MA, Al Fulaij N, August TA, Babey L, et al. State of Nature 2016. 2016.
- 37. Gregory RD, Strien Av. Wild Bird Indicators: Using composite population trends of birds as measures of environmental health. Ornithological Science. 2010;9(1):3–22.
- 38.
Lachat T, Pauli D, Gonseth Y, Klaus G, Scheidegger C, Vittoz P, et al. Evolution de la biodiversité en Suisse depuis 1900. Avons-nous touché le fond? Collection Bristol, vol 25, editor: Haupt Verlag; 2011. 433 p.
- 39. Schlaepfer MA, Sax DF, Olden JD. Towards a more balanced view of non-native species. Conserv Biol. 2012;26(6):1156–8. pmid:23082954