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Keywords:

  • biodiversity;
  • experiments;
  • non-indigenous;
  • non-native;
  • risk;
  • species introductions

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

Biological introductions of species to regions outside their known natural distribution are considered a major threat to native marine biodiversity and a key consideration for ecological management. For most invasive species in marine systems, however, little is known about potential impacts. If we are to increase our knowledge of the processes and mechanisms behind the spread of nonindigenous species or determine economic or ecological impacts, manipulative ecological field experiments are the best way to unambiguously ascribe causal relationships. For studies of invasions, such research may result in species spread and the establishment of new viable populations. Is it ethical then, to take the risk of potentially modifying or endangering other species, populations or ecosystems? Is it possible to mitigate the risks? Or should invasion ecologists work under restrictions that limit their ability to fully assess the impact of invaders? Consideration of the ethics of experimentation is rarely carried out. As a consequence, we propose a decision model that includes possible risk of escape/establishment versus the value of the research to allow researchers and/or managers to critically evaluate what type of experimental approach is appropriate.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

Over evolutionary time, there has been much natural interchange of species among and across continents, but in ecological/historical time scales, biological communities have undergone alterations in biodiversity as a result of human exploration, colonisation and urbanisation (Carlton 2009). Anthropogenic introduction of species to regions outside their (known) natural distribution is one such cause of these alterations and is considered a major threat to native biodiversity (Simberloff 2000; Carlton 2009). Many marine, freshwater and terrestrial habitats contain established populations of nonindigenous animals and plants (Ruiz & Carlton 2003).

Nonindigenous species (NIS) have been found inhabiting rocky shores, soft sediments and artificial substrata in almost all marine systems. The rate of reported invasions has increased dramatically over the last 200 years (Ruiz et al. 2000; Fofonoff et al. 2003) and in particular over the latter half of the twentieth century (Fig. 1; Carlton & Geller 1993; Carlton 1996; Cohen & Carlton 1998; Ruiz & Carlton 2003). For example, Cohen and Carlton (1998) estimated that in San Francisco Bay from 1851 to 1960, there was an average of one new introduced species establishing every 55 weeks, which had increased to one every 14 weeks during the period of 1961–1995. In Port Philip Bay, Victoria, Australia an average of one new species establishes every 64 weeks (Hewitt et al. 2004). These increases may be due to more observations, but are largely linked to expansion and globalisation of shipping routes; which in turn has increased the number and area of donor (source) and recipient regions. Thus, there are greater opportunities for transfer of organisms, increased density, overall abundance and survival rates (Carlton 1996; Vitousek et al. 1996; Ruiz et al. 1997, 2000; Fofonoff et al. 2003; Ruiz & Carlton 2003).

image

Figure 1. The cumulative number of established nonindigenous species (NIS) in European marine/estuarine waters (pre 1900–2008). ‘Copyright: European Environment Agency’.

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The majority of introduced marine species fail to establish or spread (Ruiz et al. 1999); however, many successful NIS can have significant ecological or economic impacts on native habitats and ecosystems (Vitousek et al. 1996; Pimentel et al. 2005). For example, negative impacts of invasive aquatic species in Europe were estimated to cost at least 2.2 billion annually (Kettunen et al. 2009). On the US West Coast, the European Green Crab (Carcinus maenas) has had substantial impacts on commercially important native clam species and was estimated to cost the industry US$44 million per year (Lafferty & Kuris 1996). Nonindigenous fish species in the USA were reported to result in economic losses of approximately $1–5.7 billion annually (Pimentel et al. 2005).

In contrast to economic impacts of NIS, ecological and indirect effects (such as altered trophic interactions, predation and competition) are more difficult to quantify and demonstrate (Lafferty & Kuris 1996). Indeed, despite possible threats from introduced species, the effects and potential cumulative impacts of the majority of marine NIS are still either unknown or poorly understood (Carlton & Geller 1993; Vitousek et al. 1996; Cohen & Carlton 1998).

Are all Nonindigenous Marine Species Bad?

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

Marine invasions can profoundly modify native communities, impact conservation strategies, affect human health and the economy (Cohen & Carlton 1998; Byrnes et al. 2007; Rilov 2009), and biotic homogenisation (the widespread replacement of native species with cosmopolitan NIS) is a growing concern (Davis 2003; Simberloff 2005). In a review of global marine biodiversity, Sala and Knowlton (2006) showed that the general trend (in the absence of human disturbance) is an increase in biodiversity. Under persistent human disturbance however, generally global marine biodiversity declines (Sala & Knowlton 2006), but are NIS directly associated with loss of native species?

Whilst extinctions are reducing the number of predatory species and secondary consumers, introductions are increasing primary filter feeders, detritivores and deposit feeders by a similar percentage (Byrnes et al. 2007). So whilst the structure of the marine food web is changing, there is no evidence at present, which suggests that any extinction of a native marine species is solely due to an introduced species (Briggs 2007). Biological invasions are one of the major threats to changes in biodiversity, but many different processes also contribute to population declines, (habitat change/destruction, overexploitation, pollution and climatic change) which are all likely to interact synergistically (Vitousek et al. 1996; Sala & Knowlton 2006; Didham et al. 2007).

Whilst we know that direct or indirect interactions of NIS can cause native populations to become severely depleted (Rilov 2009), but impacts on native biodiversity and ecosystem processes vary enormously with the NIS in question and the environmental setting (Brown & Sax 2005). Some species appear to have only deleterious effects; the predatory Indo-Pacific lionfish (Pterois spp.) has rapidly expanded its range from an initial introduction and is now firmly established throughout western Atlantic ocean, Caribbean Sea and Gulf of Mexico (Frazer et al. 2012). Reaching densities up to 15 times greater than in its native range and a larger body size, the lionfish consumes 4% of its body weight per day consuming and competing with native species and potentially lowering commercial fisheries yields.

The Pacific Oyster (Crassostrea gigas Thunberg 1793) has been introduced and translocated to many countries since the 1940s, mainly for aquaculture (Ruesink et al. 2005), and has subsequently established highly successful wild populations worldwide. In north-western Europe, native mussel beds could be replaced by extensive nonindigenous oyster reefs with consequences for other trophic levels (Markert et al. 2010; Troost 2010). The oyster reefs may, however, compensate for this loss by replacing the ecological function of the mussel beds, in that the reefs appear to be an alternative habitat for species typically found in former mussel beds (Kochmann et al. 2008; Markert et al. 2010).

In general, it is difficult to determine when, where and which species are likely to be a problem, with direct and indirect effects being highly variable. In economic terms, we may be in a position to assign NIS as good or bad, but for ecological systems such decisions are not so straightforward.

Values and Nonindigenous Species

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

The perception and management of non-native species is an ongoing emotional debate, and currently people appear to place inherent value on the native status of a species (Shackelford et al. 2013). Indeed, most invasion biologists agree that NIS are an intrinsically undesirable component of natural systems (Young & Larson 2011). Value judgements about NIS are made about whether changes induced by them are good or bad and those judgements are different for different people (Lodge & Shrader-Frechette 2003), and the public's concerns are primarily with NIS that threaten resources, health, aesthetic enjoyment, recreational activities or life support processes.

Whilst environmental ethics suggests that we do have some duties to nonhumans, the environment and ecological systems, the exact nature of those duties remains a challenging debate (Minteer & Collins 2005). For example, not everyone cares equally about biodiversity, and people's preferences regarding species can vary temporally depending on a range of factors, from changes in economic circumstances to the portrayal of the species in the media (Sandler 2010). Certainly, people often care more about those species that are cute, cuddly and charismatic. The key question here is – should NIS (or any species outside its natural range) have any consideration within our ethical values? As stated by Sandler (2010) ‘The existence value of species is not determined by their ecological or biological significance; it is determined by what people prefer, independent of why they do so’.

Science can inform society on possible causes and consequences of changes in biodiversity, but ultimately deciding whether an NIS may cause more harm than good (benefit) to society depends on value systems (Brown & Sax 2004), which will be influenced by diverse ecological, economic, aesthetic and moral motivations.

Blurring the Line of the Native/Nonnative Debate

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

As a consequence of global climate change, environmental conditions are becoming less favourable for many species in their native environments and geographic marine range shifts are already occurring (Sorte et al. 2010). Analogous to biological introductions (but not directly human mediated), range shifts are changing the distributions of native marine species faster than in terrestrial environments (Sorte et al. 2010). Increasing sea surface temperatures are already causing poleward shifts of marine fish (Perry et al. 2005; Johnson et al. 2011) affecting shallow-water benthic assemblages in the Antarctic (Aronson et al. 2007) and resulting in shifting biogeographic ranges in all trophic groups (Johnson et al. 2011; Madin et al. 2012).

Assisted migration, the controversial conservation strategy proposed to alleviate the effects of novel climate regimes on selected elements of biodiversity (McLachlan et al. 2007; Ricciardi & Simberloff 2009; Minteer & Collins 2010) is also closely aligned with the problems of NIS. This strategy involves a deliberate insertion of NIS into a given system, but the potential risks are unpredictable, and there is concern that the practice may ultimately create more conservation problems than it solves (Ricciardi & Simberloff 2009).

Our understanding of the marine environment is further complicated by a lack of biogeographic and historical data meaning that many marine species cannot be labelled as native or introduced (Carlton 1996, 2009). In a changing environment, it may be more practical to place greater emphasis on ecological values and ecosystem function rather than the origin of the species (Davis et al. 2011; Shackelford et al. 2013). Indeed, many NIS have already been used as ecological substitutes where their functional benefits have been perceived to outweigh the potential risks (for review see Schlaepfer et al. 2011) and may have an important role in providing ecosystem services in the future (Ewel & Putz 2004).

These problems compound the native/non-native debate but highlights the growing need to develop a predictive understanding of invasions and their impacts (Ricciardi & Simberloff 2009), placing an ever increasing pressure on invasion ecologists to provide valuable management information.

Challenges for Invasion Ecologists in Marine Systems

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

The introductions of species to new environments are sometimes considered to be unintentional, uncontrolled experiments that could provide insights into ecological and evolutionary processes affecting biodiversity (Brown & Sax 2004; Sax et al. 2007). Invasion ecologists are, however, increasingly aware of the limitations of using only observational studies (e.g. Ruiz et al. 2000; Johnston et al. 2009), as with any study of ecological mechanisms, manipulative, controlled experimentation is essential to develop our understanding of an invasion process, explain observed patterns or determine any impacts of introduced species on ecosystems or native biodiversity (Hurlbert 1984; Underwood 1997; Simberloff 2004).

Manipulations of biological systems (e.g. removal or addition of species, modifications of densities, transplants and modifications of the environment) are the most powerful way to determine causal factors in ecological contexts (Hurlbert 1984; Underwood 1997), as all variables except the one(s) being manipulated may vary naturally and the factor of environmental variation is therefore randomly sampled as part of the experiment with the hypothesised effect of interest being measured above that of intrinsic natural variation (Underwood 1997).

In studies of marine invasions, there are then major problems. Experimental manipulations of ecological systems where the NIS is already present will be confounded because NIS are often well-established before they are discovered and are consequently already present in ecological systems (Ruiz et al. 1997; Sax et al. 2005). Secondly, the evidence necessary to determine whether there are ecological consequences of introductions of NIS ideally should come from manipulations; therefore, the very experiments needed to allow assessments of a putative impact may themselves be unethical. For example, field transplant experiments (where organisms are moved to different environments) are particularly valuable for explaining causes of ecological patterns. For transplants to provide meaningful information on the effect of NIS in receiving assemblages, it is logically necessary that the receiving system is allowed to operate as naturally as possible. Under this scenario, the experiment is actually a deliberate introduction of a potentially invasive species into a system not previously affected, raising complex ethical issues.

In particular, the dynamic and open nature of marine environments makes it difficult to control dispersion of NIS from experiments. Uncontrollable larval dispersal or the potential of adult escapees may result in species spread and the establishment of new populations and many ecologists agree that it is unethical to take this risk (e.g. Glasby & Creese 2007; Johnston et al. 2009; Simberloff 2009; Sugden et al. 2009). In Australia, for example, there are formal ethical regulations regarding the wellbeing of vertebrates and ‘higher’ invertebrates (Cephalopoda) in biological investigations, there are no formal considerations for other organisms, habitats or ecosystems, in the conduct of ecological research (Minteer & Collins 2010; Parris et al. 2010). The recent emergence of ‘ecological ethics’, proposes an interdisciplinary environmental ethical analysis to fill this gap in ethics literature (Minteer & Collins 2005, 2008), and asserts that ecological research and biodiversity management should incorporate ethical considerations of the impact of ecological study itself and apply the resulting implications to the design, conduct and management of field and laboratory research (Farnsworth & Rosovsky 1993; Marsh & Kenchington 2004; Minteer & Collins 2008). These considerations are perhaps more critical in invasion ecology, when intentional or accidental instructions may have unpredictable, potentially severe consequences. So how can invasion ecologists mitigate the risk of dispersal?

We propose a conceptual model to guide researchers as to which type of study (observational/modelling/restoration vs. laboratory/mesocosms/modelling vs. field experimentation) best solves the ethical difficulties inherent in understanding the biological effects of invasions (Fig. 2). The important axis to consider is the dispersal potential of the NIS from any experimental set-up as this will directly affect impact; the weight of this axis will change according to the known or potential invasiveness of the NIS in question; if this is thought to be relatively minor then managers may consider that the risk of escape is of less importance than if the test organism was known to be very damaging in the event of escape/establishment. Should the consequences of dispersal be thought to be small, and the invasiveness of the system considered low; then we suggest that managers may consider doing manipulative field experiments to rigorously assess the impact of the organism in question. Careful procedural design can mitigate associated risks. For example, Clark and Johnston (2005) developed a fully contained larval dosing technique that can be used for any planktonic organism and minimises the potential of dispersal. Creating structural mimics to simulate the effects of an organism providing substrate or habitat for other organisms is an ideal method (Crooks 1998; Holloway & Keough 2002; Byers et al. 2012), but mimics have to be compared with the live habitat and therefore such experiments can only be carried out in areas where the species is already present.

image

Figure 2. A conceptual model of the decision options on what method of study to use to examine the impacts of nonindigenous species (NIS). We suggest that experimental decisions are based on the biotic characteristics of both the invading species (invasiveness) and the recipient community (invasibility) weighted by the current status of the NIS in the proposed region of study (i.e. established or not detected) and the scientific and/or conservation value of the study.

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Mitigation of risk becomes progressively more difficult however when considering experimental transplants. Direct transplants into an uninvaded system are not an ethical option under any circumstances. Although not a movement of a NIS, the following example illustrates the difficulty of a translocation approach. Over 10,000 individuals of a morph of the southern rock lobster (Jasus edwardsii) were moved over hundreds of kilometres and from deep water to inshore sites to enhance depleted populations of the more valuable red morph with a view to improving the yield and sustainability of the fishery (Green et al. 2010). The authors acknowledged that as they were working with invertebrates no ethical approval was required, but they did follow ethical guidelines for the humane treatment of animals in research. There was, however, no mention of any ethical considerations behind the potential effects of the translocation itself.

If the study species is already established, then it is possible to carry out in situ one-way transplants. Researchers can mitigate risk by avoiding transplants outside already invaded areas (Castilla et al. 2004; Willette & Ambrose 2012), and if the test organisms are broadcast spawners, using juveniles to minimise the probability of spread via larval dispersal (Castilla et al. 2004). These methods will limit ecological impacts, but present difficulties in controlling other potentially confounding factors.

If the axis of dispersal potential (weighted by invasiveness) when evaluated against that of invasibility (Fig. 2) is deemed to be high then any research should be directed at quantifying ecosystem/community responses via removal experiments, restoration projects or laboratory and/or mesocosm experiments. The experimental removal of NIS is increasingly used and can be extremely useful in elucidating certain effects of the presence of the NIS in a habitat (Piazzi & Ceccherelli 2006; Klein & Verlaque 2011). For example, removal of the invasive green alga (Caulerpa racemosa var. cylindracea) in the Mediterranean Sea showed that another invasive algal species present recovered more quickly than any native species and subsequently dominated the assemblage (Klein & Verlaque 2011). A targeted removal program in the Caribbean of larger Indo-Pacific lionfish resulted in lower densities and shifted predation pressure away from vulnerable fish species (Frazer et al. 2012). Removals do prevent further introductions, but it is important to note that interpretations of consequences of associated NIS will be confounded unless there is evidence that the remaining assemblage is representative of the assemblage prior to arrival of the NIS, and whether this affects system recovery.

Some researchers suggest that strictly controlled laboratory and/or mesocosm experiments are the only ethical approach to the study of NIS (Vermeij 1996; Trowbridge 2002), but there are limitations to the interpretation and applicability of laboratory results due to isolation from potential influencing factors in the field, and possible alteration of the target species’ behaviour (Chapman 2000). Whilst these may be less representative of truly natural systems, the ability to control for escapes and to construct the system of choice will allow meaningful interpretations. Laboratory experiments should, however, also be subject to ethical considerations, and mitigation methods applied should be discussed. For example, when examining fertilisation success of an nonindigenous ascidian the authors stated explicitly, that to avoid accidental introduction (and comply with Chilean laws) that ‘the waste seawater was mixed with tap water, and drained through PVC pipes into a hole in the ground 30 m away from high tide level’ (Manriquez & Castilla 2010). This approach acknowledged that despite the experiment being carried out in a controlled laboratory situation, dispersal risk was high for this known highly invasive species and as such a mitigation method was employed to minimise further introductions.

Ecological restoration projects may offer an ideal opportunity to study impacts of NIS on native species (Byers 2002). As a system recovers to something approximating the previous/target state, the impacts should be reduced compared with nonrestored control sites, although the author acknowledged that a second control (NIS absent) may be required, to control for direct effects of the systems recovery on native species. If replacing a niche left vacant by the extirpation of a native species by a NIS to maintain declining ecosystem services, a restoration can also be an intentional introduction (Sandler 2010). In this case, the relative risks and benefits will be quite different, and it will be important to demonstrate that the value of the translocation justifies associated relatively low ecological risk. For an excellent example of a thorough ecological risk assessment on oyster restoration options in Chesapeake Bay, see Menzie et al. (2013).

If both axes are high and the NIS is not already established then we propose that the best option for researchers is to utilise observational investigations or modelling studies (Fig. 2), accepting the fact that although these approaches cannot unambiguously assign causality, they may be the most ethical approach to examining the effects of NIS. The use and value of both these approaches will likely increase, as new knowledge and longer term data sets become available (e.g. Edelist et al. 2013).

Of course, modifying all these considerations is the scientific value of the study (Fig. 2), which is likely to be greatly influenced by management and policy makers. For example, research may be considered more valuable when proposing the introduction of a species for restoration of ecological processes or the conservation of a unique species. The need to provide relevant information for management may compel researchers to take a greater experimental risk, it will be important to balance the potential power of the data and the practical utility of the new information that data may provide (Parris et al. 2010), whilst acknowledging and discussing relevant ethical problems as they arise (Farnsworth & Rosovsky 1993).

Conclusion

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

Public policy, science and conflicting value systems strongly intersect on the issue of NIS (Lodge & Shrader-Frechette 2003) raising complex ethical decisions. If we are to meet the research and management challenges of global change, unprecedented levels of research effort will be required, integrating multiple disciplines as well as multiple approaches, across multiple spatial and temporal scales (Larson 2007).

Invasion ecologists will need to not only present the facts, but communicate value judgments to managers, policy makers and different stakeholders with conflicting interests to facilitate trade-offs and management actions (Larson 2007; Young & Larson 2011).

Applying a decision framework to research carried out on the impacts of NIS that can be integrated with relevant risk and management tools will aid how invasion ecologists provide the research required for society and managers to make informed ecologically ethical decisions.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies

This work was funded by a Northcote Graduate Scholarship to Denise Bunting, with additional support from the Centre for Research on Ecological Impacts of Coastal Cities (EICC). We thank colleagues at the EICC for critical comment and advice. The manuscript was much improved by critical commentary by three anonymous reviewers and members of the EMR editorial board.

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  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies
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Biographies

  1. Top of page
  2. Summary
  3. Introduction
  4. Are all Nonindigenous Marine Species Bad?
  5. Values and Nonindigenous Species
  6. Blurring the Line of the Native/Nonnative Debate
  7. Challenges for Invasion Ecologists in Marine Systems
  8. Conclusion
  9. Acknowledgements
  10. References
  11. Biographies
  • Denise Bunting carried out her PhD research at the Centre for Research on the Ecological Impacts of Coastal Cities (EICC), School of Biological Sciences, Marine Ecology Laboratories (A11), The University of Sydney (Science Road, Sydney, NSW 2006, Australia ). This paper arose from Denise's PhD studies, in particular on how to design experiments to examine the ecology of our ‘pet’ invasive organism, Cirolana harfordi.

  • Ross A. Coleman is an Associate Professor at the University of Sydney and Director of the EICC Centre for Research on Ecological Impacts of Coastal Cities, School of Biological Sciences, Marine Ecology Laboratories (A11), The University of Sydney (Science Road, Sydney, NSW 2006, Australia ).