Article pubs.acs.org/est
Including the Introduction of Exotic Species in Life Cycle Impact Assessment: The Case of Inland Shipping Marlia M. Hanafiah,†,‡ Rob S. E. W. Leuven,‡ Nike Sommerwerk,§ Klement Tockner,§ and Mark A. J. Huijbregts*,‡ †
Department of Environmental Science, School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, National University of Malaysia, 43600 UKM Bangi, Selangor, Malaysia ‡ Department of Environmental Science, Institute for Water and Wetland Research, Radboud University Nijmegen, P.O. Box 9010, 6500 GL Nijmegen, The Netherlands § Leibniz-Institute of Freshwater Ecology and Inland Fisheries, IGB, and Institute of Biology, Freie Universität Berlin, Müggelseedamm 310, 12587 Berlin, Germany S Supporting Information *
ABSTRACT: While the ecological impact of anthropogenically introduced exotic species is considered a major threat for biodiversity and ecosystems functioning, it is generally not accounted for in the environmental life cycle assessment (LCA) of products. In this article, we propose a framework that includes exotic species introduction in an LCA context. We derived characterization factors for exotic fish species introduction related to the transport of goods across the Rhine-Main-Danube canal. These characterization factors are expressed as the potentially disappeared fraction (PDF) of native freshwater fish species in the rivers Rhine and Danube integrated over space and time per amount of goods transported (PDF·m3·yr·kg−1). Furthermore, we quantified the relative importance of exotic fish species introduction compared to other anthropogenic stressors in the freshwater environment (i.e., eutrophication, ecotoxicity, greenhouse gases, and water consumption) for transport of goods through the Rhine-Main-Danube waterway. We found that the introduction of exotic fish species contributed to 70−85% of the total freshwater ecosystem impact, depending on the distance that goods were transported. Our analysis showed that it is relevant and feasible to include the introduction of exotic species in an LCA framework. The proposed framework can be further extended by including the impacts of other exotic species groups, types of water bodies and pathways for introduction.
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INTRODUCTION
Exotic species are introduced intentionally (e.g., via livestock feed, aquaculture, horticulture, pest management, and pet industry) or accidently through the transport of goods, the lifting of dispersal barriers between river basins, and human travel.26,27 The development of a network of navigable rivers and canals, and the transport of goods by shipping are facilitating the rapid spread of exotic species.16 The accelerating introduction of exotic species via interbasin and intercontinental shipping has become an emerging environmental issue of global concern. The spread of exotic species will further increase with increasing continental and intercontinental trade and transportation.28
The introduction of exotic species has increased globally during the past decades affecting biodiversity and ecosystem functioning.1−10 An exotic species is defined as a species that is introduced anthropogenically to areas outside its indigenous range. According to Elliott11 and Arbačiauskas et al.,12 exotic species can be considered as biocontamination due to their impact on ecosystems. Invasive exotic species tolerate wide ranging environmental conditions, have highly effective dispersal abilities, feature a wide geographical range, fast growth rate, high reproductive capacity, and a strong competitive ability.13−18 Invasion by exotic species can result in many ecological consequences, including changes in habitat conditions, displacement of native species, alteration of community structure, and disruption of food webs.6,19,20 In addition, these species may cause major economic impacts21−25 and pose risks to public health.2 © 2013 American Chemical Society
Received: Revised: Accepted: Published: 13934
September 4, 2012 November 14, 2013 November 19, 2013 November 19, 2013 dx.doi.org/10.1021/es403870z | Environ. Sci. Technol. 2013, 47, 13934−13940
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Figure 1. Cause-effect pathway for impact of exotic species introduction on freshwater native species via shipping-related transport.
PDF·m3·yr per kg of transported goods. The characterization factors for transport-related introduction of exotic species were obtained by multiplying a river basin specific fate factor with a river basin specific effect factor summed over all affected river basins:
Although exotic species are one of the key threats to native biodiversity and ecosystems,29 biocontamination is not yet taken into account in the context of life cycle impact assessment (LCIA) of products. Therefore, including the relationship between transported goods and the introduction of exotic species in the current LCIA framework will provide a more comprehensive picture of environmental impacts in relation to product life cycles. The goal of this paper was to develop a method for assessing the environmental impacts of exotic freshwater species introduction in the context of product life cycles. By focusing on exotic freshwater fish species in relation to the transport of goods via the Rhine-Main-Danube (RMD) waterway, we derived new characterization factors describing the potential disappearance of native freshwater fish species integrated over time per amount of transported goods. A case study of shipping in relation to transported goods is described that demonstrates the applicability of the new characterization factors and assesses the relative importance of introduction of exotic fish species compared with other environmental stressors in freshwater ecosystems.
where CF is the characterization factor for transported goods (PDF·m3·yr·kg−1), FFi is the fate factor of river basin i (fraction of exotic species·yr·kg−1), EFi is the effect factor of river basin i (PDF·m3·exotic species−1), ΔESFi is the change of fraction of exotic freshwater species as part of the total species pool establishment in river basin i (exotic species), ΔTR is the change in yearly transport of goods (kg·yr−1), ΔPDFi is the change in the potentially disappeared fraction of the freshwater native species in river basin i and Vi is the volume of river basin i (m3). Fate Factor. The fate factor was defined as the timeintegrated change in fraction of exotic species due to a change in the transportation of goods. The fate factor (FFi) for river basin i, expressed in units of fraction of exotic species·year·kg−1 of goods transported, can be approximated with empirical data as the change in exotic species occurrence specifically caused by transport-related activities relative to the total species pool in a specific period (ΔESFi) and the yearly average amount of transported goods (ΔTR ) across the new waterway in that time period:
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MATERIALS AND METHODS Framework. Figure 1 illustrates the cause-effect pathway for the potentially disappeared fraction (PDF) of native freshwater species caused by the introduction of exotic species. Depending on the size and nature of goods (raw materials, resources and end products), transportation may take place via land (road or rail), air or water pathways. This study focuses on exotic species that are introduced into river basins by shipping. Cause-effect pathways of exotic species that relate to shipping include ship hull fouling, ballast water discharge and the removal of interbasin dispersal barriers as a result of canal building. Shipping related transport includes different types of cargo vessels such as container, bulk carrier, and tanker ships. In freshwater ecosystems, fish, macroinvertebrates (e.g., molluscs and crustaceans), algae, and aquatic plants (e.g., macrophytes and diatoms) are the most common invasive exotic species.16,17,30 Characterization Factor. Characterization factors that express freshwater ecosystem impact due to the introduction of exotic species can be derived for goods transported by inland shipping. Characterization factors for aquatic exotic species quantify the potentially disappeared fraction (PDF) of freshwater native species due to shipping related transport aggregated over time and water volume, expressed in units of
FFi =
ΔESFi ΔTR
(2)
Bidirectional waterflow of Rhine and Danube river water through staircase locks in the RMD waterway enhances the exchange of exotic species between both river basins. Moreover, exchange of species can be related to shipping vectors (e.g., clocking of fish eggs on ship hulls). The bidirectional flow of Rhine and Danube river water and the number of ships crossing the RMD waterway, considered as causal factors for the exotic fish species propagule pressure on river basins, are directly related to the amount of goods transported across the RMD waterway. However, the correlation between the introduction of exotic species to the number of passing ships could also be considered for inclusion in the fate factor calculation. 13935
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based on Kottelat and Freyhof38 where the newly discovered or described species were added to the 2007 edition of Kottelat and Freyhof in order to provide an overview of the European fish species to mid-2010. The fraction species represented in the World Conservation Union (IUCN) Red List fish species39,40 was used as an approximation for the PDF of native fish species. As a first step, we derived the fraction of IUCN Red List fish species and the fraction of exotic fish species for every river basin, shown as 251 dots in Figure 2
Effect Factor. The effect factor reflects the impact of exotic species on native freshwater species richness (in PDF·m3·exotic species−1):
EFi =
ΔPDFi ·Vi ΔESFi
(3)
The effect factor for species disappearance can be derived if an exotic species introductionnative species response relationship can be established. In this study, the effect factor is expressed as the PDF of native fish species divide by the river volume affected, per fraction of exotic species introduced (ESF) (m3). River volume (m3) was used as a weighting factor in order to make the effect factor consistent with that of other impact categories such as greenhouse gases and water consumption.31 This allows for comparison between different types of impacts. The river volume was used as a proxy for the actual species richness indicating that the larger the river volume, the more important the fraction of species disappearance. RMD Waterway. To demonstrate how to calculate characterization factors of exotic species introduction by shipping activities, we applied these factors for goods transported via the Rhine-Main-Danube (RMD) waterway. The Main-Danube canal was constructed in 1992 to enhance shipping transport between western, central and southeastern Europe via the rivers Rhine, Main and Danube. The RMD waterway is an important corridor for dispersal of exotic species between rivers in Western Europe and the Ponto-Caspian area (i.e., southern corridor).12,16,32 The rivers Rhine and Danube are among the largest rivers of Europe and are regarded as important economic pathways for shipping between various European regions.33,34 The river Rhine runs for over 1320 km from its sources in Switzerland and Austria to its estuary in The Netherlands.33 The river Danube is located in Central Europe and has a total length of 2780 km.34 For the calculation of the fate factor, we obtained data on the yearly average of transported goods over the period 1992−2009 through the RMD waterway, and the change in percentage of exotic species introduced via passive dispersal by inland shipping or active dispersal using the RMD waterway in both the rivers Rhine and Danube. The average yearly amount of transported goods via the RMD waterway over the period 1992−2009 was 6.45 Megatons·yr−1.35 The data on the cumulative number of exotic fish species introduced via passive dispersal with inland ships or active dispersal using the RMD waterway was obtained from various references.17,33,34,36,37 A total of 81 fish species were found in the river Rhine (45 native and 36 exotic).33 For the river Danube, a total of 145 fish species were recorded (115 native and 30 exotic).34 Over the period 1992−2009, a total of nine exotic fish species dispersed from the river Danube to the river Rhine and one exotic fish species from the river Rhine to the river Danube. A list of exotic fish species related to shipping activities and the yearly average amount of goods transported through the RMD waterway can be found in the Supporting Information (Tables S1 and S2, respectively). To be able to derive an effect factor, we established an empirical stressor-response relationship between the fraction of exotic species introduced and the fraction of native species threatened. For this purpose, we used a database of fish occurrences in 251 European river basins.38 This database is
Figure 2. Potentially disappeared fraction (PDF) of IUCN red list species in relation to the fraction of exotic fish species introduction (ESF), based on data for 251 European river basins. The blue open dots represent the data for the individual river basins, while the red closed dots are the lowest fraction of IUCN Red list fish species per bin of 0.01 unit of fraction of exotic species introduced.
(open blue dots). Next, we divided the fraction of exotic fish species introduced into bins of 0.01 unit (e.g., from 0.025 to 0.035) and identified per bin the river basin with the lowest fraction of IUCN Red list fish species. We limited our analysis to the lowest fractions per bin only, as we considered that the higher fractions of IUCN Red list fish species within a bin can be caused by one or more unidentified stress factors (red closed dots in Figure 2). Finally, we performed a linear regression analysis to correlate the fraction of exotic fish species introduced to the lowest fraction of IUCN Red List fish species observed per bin. Leprieur et al.40 used a similar statistical approach to elucidate the effects of exotic fish species on native species. The slope of the linear relationship between the fraction of IUCN Red List fish species and the fraction of exotic fish species introduced was 0.60 (95% CFI: 0.33−0.88; P < 0.001; N = 23 bins) and an explained variance of 49% (see Figure 2). The derivative of the linear regression represented the ΔPDF/ ΔESF-part of the effect factor (eq 3) and equals 0.60. The water volumes of the rivers Rhine and Danube (2.88 × 108 and 1.55 × 109 m3, respectively), also required in the calculation of the effect factor, were taken from Hanafiah et al.31 Case Study. The relative importance of exotic species introduction in LCIA freshwater impact calculations was evaluated with a case study on goods transported via the RMD waterway from the port of Rotterdam to Budapest (about 1500 km transport distance) and to the Black Sea (about 3000 km transport distance), and vice versa. We calculated the freshwater ecosystem impact (in PDF·m3·yr) of one ton of goods transported from Rotterdam to Budapest and the Black Sea per barge, respectively. The impact categories included were exotic species introduction, water consumption, and emissions of greenhouse gases, toxic pollutants, and nutrients. 13936
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Table 1. Characterization Factors for Shipping Related Transport of Goods in the Rivers Rhine and Danube (PDF·m3·yr·kg−1) Fate factor Effect factor Characterization factor
Unit
River Rhine
River Danube
Total
exotic species·yr·kg−1 PDF·m3·exotic species−1 PDF·m3·yr·kg−1
1.7 × 10−11 1.7 × 10−8 3.0 × 10−3
1.1 × 10−12 9.4 × 10−8 1.0 × 10−3
na na 4.0 × 10−3
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Inventory data were taken from the ecoinvent database v.2.2.41 Characterization factors for greenhouse gas emissions and water consumption were taken from Hanafiah et al.,31 for ecotoxicity from Van Zelm et al.42 and Goedkoop et al.,43, and for eutrophication from Helmes et al.44 Further information on inventory data and characterization factors can be found in the Supporting Information (Table S3).
DISCUSSION The development and application of a framework to evaluate the relative change in freshwater species richness per unit of transported goods due to the introduction of exotic species show that it is feasible and relevant to include introductions of exotic species by interbasin shipping transport in the LCIA of goods. Fate Factor. The river Danube contained only one exotic fish species directly or indirectly introduced by shipping via the RMD waterway, compared to nine species in the river Rhine. The difference in shipping related species introductions of these two rivers may be explained by two factors: (1) the differing availability of open niches, and (2) the dominant water flow in the RMD waterway from the Danube to Rhine basin. The river Danube harbors a higher native fish species richness (115 species) than the river Rhine (45 species).34 A river with a low species richness may contain open niches that favor the establishment of exotic species. Apart from the differing availability of open niches, the bidirectional flow regime of the staircase locks in the RMD waterway may also contribute to the greater dispersal of exotic species from the Danube to the Rhine. The inlet of the RMD waterway is dominated by water originating from the river Danube.45 Uncertainty in the fate factors can emerge from the lack of completeness and accuracy in the information on exotic species introduction. In this study, information on exotic species introduction was based on various data sources. The combination of data from multiple data sources can decrease the data consistency and lead to underestimations in the calculation of fate factors. Exotic species can be introduced into new areas through multiple pathways and vectors. Therefore, it is important to carefully identify the vectors and pathways of exotic species introductions in river basins; in the present case only inland shipping transport-related species introductions are considered. A key factor affecting fate factors is the lag period between interbasin spread and establishment of exotic species in a new river basin. Time lags occur due to (i) the opening of the canal and the subsequent dispersal of species, (ii) dispersal of species and date of first record, and (iii) date of first record, establishment of viable populations and impact on native species. It is very likely that in the near future more exotic species will disperse via the RMD waterway. Different species lag periods could affect the number of native species present because it could lead to species pool saturation and exoticnative species turnover in both rivers. Therefore, exclusion of the lag period implies an underestimation of fate factors. Effect Factor. We elucidated a relationship between the fraction of exotic fish species introduction and the fraction of potentially disappeared native fish species, without explicitly considering the mechanisms that caused the disappearance (see Figure 1). For instance, the ratio of exotic species to invasive species is not explicitly included, as it is very difficult to predict whether an exotic species will become invasive.46 Only a fraction of exotic species become invasive, however, once a viable population of exotic species is established, it may spread
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RESULTS Characterization Factors. Table 1 contains the fate factors, effect factors and characterization factors for transport of goods through the RMD waterway. The characterization factor of the river Rhine is a factor of 3 higher compared to that of the river Danube. The fate factor of the river Rhine is a factor of 16 higher compared to that of the river Danube, whereas the effect factor is about a factor of 5 higher for the river Danube than for the river Rhine. This can be explained by the Danube’s larger river volume in comparison with the river Rhine. Case Study. Figure 3 shows the relative contribution of five impact categories (exotic species introduction, eutrophication,
Figure 3. The relative contribution of five impact categories (exotic species introduction, eutrophication, ecotoxicity, greenhouse gases, and water consumption) to the freshwater ecosystem impact by transport of one ton of goods from Rotterdam to Budapest (1500 km) and the Black Sea (3000 km).
ecotoxicity, greenhouse gases and water consumption) to impacts on the freshwater ecosystem caused by the transport of one ton goods by shipping from the port of Rotterdam via the RMD waterway to Budapest, and finally to the Black Sea. The newly derived characterization factors for exotic fish species introduction were used in the calculations. For the shipping of 1500 km and 3000 km of one ton of goods, the introduction of exotic species contributes to 72% and 84% of the total environmental impact, respectively. The relative contribution of exotic species introduction changes with the transport distance due to the fact that the impact of exotic species introduction only scales with the amount of goods transported, while the other impacts such as ecotoxicity, water consumption and greenhouse gas emission scale with the amount of goods transported and with travel distance. 13937
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invaders can be predicted from the total number of invaders in an area, after controlling for species−area effects. These two variables are positively correlated in a set of 16 invaded freshwater and marine systems from around the world. The relationship is a simple linear function; there is no evidence of synergistic or antagonistic effects of invaders across systems. A similar relationship is found for introduced freshwater fish across 149 regions. In both data sets, high-impact invaders comprise approximately 10% of the total number of invaders. So, the indicator total number of exotic fish species can be regarded as a surrogate for the number of invasive species/high impact invaders. The scope of our study was limited to freshwater exotic fish species. Exotic fish not only displace native fish species but also affect other freshwater taxonomic groups (e.g., macroinvertebrates and plankton) and ecosystem functioning.51 However, effects on other aquatic freshwater taxonomic groups and ecosystem functioning could not be included due to a lack of solid data. In addition, shipping transport and development of the European network of waterways also result in the introduction of exotic species that belong to other taxonomical groups than fish, in particular macroinvertebrates such as molluscs and crustaceans. 16 Including the impacts of introduction of other taxonomical groups is recommended for future study, as several macroinvertebrate species may also cause local and regional species extinction.16,51 In previous studies, the relative contributions of impact categories (i.e., greenhouse gases and water consumption) to impacts on the freshwater ecosystem were also related to fish species occurrence.31 The impact of ecotoxicity covers a wide range of taxonomic groups (algae, invertebrates, and fish species).42,43 For eutrophication, impact to the freshwater ecosystem was derived from invertebrate species occurrences.44 Furthermore, a recent study on the species richness-phosphorus relationships for freshwater showed that the stressor response curves for fish and invertebrates toward phosphorus were approximately the same.52 This implies that the results of the case study are likely to be most representative for relative fish species richness. Implications. The method developed in this paper makes it possible to compare the relative importance of exotic fish species introduction with other stressors for relative fish species richness in freshwater. We have shown that the introduction of exotic fish species may be responsible for an important share (>70%) of the freshwater ecosystem impact (i.e., PDF) related to the transport of goods through the RMD waterway. This implies that neglecting exotic species introduction during current life cycle impact assessments of inland shipping transport-related activities can substantially underestimate the overall impact to freshwater ecosystems. The influence of other interbasin connections and intercontinental transport related introductions of exotic species was not dealt with in this study. Native freshwater species in freshwater bodies are increasingly affected by exotic species that are introduced from other continents by ballast water or via other inland dispersal corridors.16 Including impacts caused by exotic species introduction via other interbasin or continental routes is a constructive step and will improve LCIA. Inclusion will provide a more complete picture of the consequences of exotic species on freshwater ecosystems in an LCA context.
and can dominate freshwater native species. Global data show that this fraction appears to be linearly related to the number of introduced exotic species. Factors enabling successful invasion, establishment and spread of exotic species include complex invasion processes, such as the number and frequency of introductions of exotic species into a new area (propagule pressure), minimum viable population size, and the delay between the introduction of an exotic species and its successful spread in a new region (lag period).47 If sufficient information on species invasiveness is available, it is recommended that the more mechanistic details are included in the LCIA framework. The mechanisms contained within the invasion process are subject to further research that will provide a more complete picture of the consequences of exotic species invasion to aquatic ecosystems. The impacts of exotic species on native biodiversity differ with species and ecosystem type and depend on species life history traits and habitat suitability. Besides negative effects, invasion by some exotic species can potentially have positive effects, for example, an increase in the local or regional number of aquatic species48 or predation of other exotic species leading to control of their population size. Whether these effects are considered to be positive or negative, however, is a subjective value judgment.49 In this study, we only considered the effects of exotic fish species introduction on the extinction of native fish species. Uncertainty in the effect factor arises from uncertainties in the stressor-response model that links exotic fish introduction with threatened native fish species. We used the fraction of exotic species as a proxy for potential impacts in our life cycle assessment study. The response curve for deriving the PDF was based on the number of threatened native species from the IUCN Red List.39 However, the data used for status assessments of species is still incomplete and can lead to an underestimation of the fraction of threatened fish species. The relationship between the fraction of exotic fish species and the fraction of threatened fish species was based on empirical observations in a large number of European river basins. We tried to isolate the impacts of exotic fish species introductions on native fish species richness by dividing the fraction of exotic fish species introduced in 251 European river basins in bins and by using minimum values of threatened species per bin. The relationship derived, however, cannot be directly interpreted as a causal “impact” relationship due to the empirical nature of the regression analysis. Indeed, many human-related factors, such as hydrological changes and urbanization, directly affect native species but are indirectly also related to the successful establishment of exotic species (or indicators such exotic species richness and the fraction of exotic species). 40 This also explains the variability between endangered species in drainage basins with a similar area or number of exotic species. By applying the bin-minimum approach we were able to derive a conservative statistical relationship that prevents an overestimation of impacts related to exotic species. Unfortunately, we could not distinguish invasive exotic species (with known negative impacts) and noninvasive exotic species (with no recorded negative impacts). This approach is currently not feasible due to lack of data for European river basins. However, macro ecological analyses of other biogeographical regions elucidate that the number of high impact invaders shows a significant linear relationship with the number of exotic fish species introductions (e.g., Ricciardi and Kipp).50 These authors show that the number of high-impact 13938
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ASSOCIATED CONTENT
S Supporting Information *
Information on exotic fish species related to shipping activities from 1992 until 2009 (Tables S1), amount of goods transported via the RMD waterway (Table S2) and inventory data of five impact categories (exotic species introduction, eutrophication, ecotoxicity, greenhouse gases and water consumption) related to the freshwater ecosystem and the distance of shipping voyages (Table S3). This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*(M.A.J.H.) Phone: +31 243652835; e-mail: m.huijbregts@ science.ru.nl. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS M.M.H. was financed by the National University of Malaysia (UKM) and the UKM research grant (GGPM-2012-078; INDUSTRI-2013-028). M.H. was partly funded by the European Commission under the seventh framework program on environment; ENV.2009.3.3.2.1: LC-IMPACTdevelopment and application of environmental Life Cycle Impact assessment Methods for imProved sustAinability Characterization of Technologies, grant agreement 243827. K.T. and N.S. received support through the EU-funded project BioFresh (www.freshwaterbiodiversity.eu). We thank Rick Veenhof for providing information on shipping transport and exotic species in The Netherlands, and Jon Matthews for English proofreading. We thank Dr. M. Dorenbosch for permission to use his photo of the Kessler’s goby in our TOC graphic. We thank David Strayer and one anonymous reviewer for critical remarks on an earlier version of this manuscript and constructive suggestions for improvements to our paper.
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dx.doi.org/10.1021/es403870z | Environ. Sci. Technol. 2013, 47, 13934−13940
Environmental Science & Technology
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dx.doi.org/10.1021/es403870z | Environ. Sci. Technol. 2013, 47, 13934−13940
