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Aquatic zooremediation: deploying animals to remediate contaminated aquatic environments Scott Gifford1, R. Hugh Dunstan1, Wayne O’Connor2, Claudia E. Koller1 and Geoff R. MacFarlane1 1 2
School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, 2308, Australia NSW Department of Primary Industries, Port Stephens Fisheries Centre, Private Bag 1 Nelson Bay, NSW, 2315, Australia
The ability of animals to act in a bioremediative capacity is not widely known. Animals are rarely considered for bioremediation initiatives owing to ethical or human health concerns. Nonetheless, specific examples in the literature reveal that some animal species are effective remediators of heavy metals, microbial contaminants, hydrocarbons, nutrients and persistent organic pollutants, particularly in an aquatic environment. Recent examples include deploying pearl oysters to remove metals and nutrients from aquatic ecosystems and the harvest of fish to remove polychlorinated biphenyls (PCBs) from the Baltic. It is probable that many animal taxa will possess attributes amenable to bioremediation. We introduce zoological equivalents of the definitions used in phytoremediation literature (zooextraction, zootransformation, zoostabilization and animal hyperaccumulation), to serve as useful benchmarks in the evaluation of candidate animal species for zooremediation initiatives, and propose that recognition of the concept of zooremediation would act to stimulate discussion and future research in this area. Introduction Bioremediation involves the use of living organisms to remove or detoxify pollutants within a given environment. Although bacteria are the most common group of organisms used for bioremediation, the use of plants (phytoremediation) and algae (phycoremediation) is increasing [1–3]. Methods of phytoremediation include: (i) phytostabilization (see Glossary); (ii) phytoextraction (see Glossary); and (iii) phytotransformation or phytodegradation (see Glossary) [2]. Research on the phytoextraction of pollutants has focused on a small group of plants known as hyperaccumulators (see Glossary) [2,3]. Animals are rarely considered for bioremediation owing to ethical concerns or because many of the aquatic organisms currently cultured or harvested commercially are bound for human consumption. Nonetheless, according to the above definitions, many animals in aquatic ecosystems hyperaccumulate, stabilize or degrade pollutants. The use of animals for bioremediation can be achieved Corresponding author: MacFarlane, G.R. (
[email protected]). Available online 14 December 2006. www.sciencedirect.com
in three ways: pollutants can be extracted from an area by harvesting wild populations; through the introduction, culture, and harvest of animals – a form of aquaculture; and supplementation or maintenance of wild animal populations, which might lead to stabilization or degradation of pollutants. Many animal species have simple life histories, are resistant to toxicity and have the ability to generate an economic return following remediation activities. Indeed, the literature reveals that oysters, mussels, clams, fish, polychaetes and sponges are suitable bioremediators [4–10]. Although using animals for bioremediation initiatives has tentatively been termed ‘zooremediation’ (pronounced zo-o-remediation) [11], the concept is poorly developed and not widely recognized. This review outlines zoological analogies to botanical equivalents from the field of phytoremediation and, thus, the potential in aquatic ecosystems for zooextraction (see Glossary), zoostabilization (see Glossary) and/or zoodegradation (see Glossary).
Glossary Phytoremediation Phytoextraction: The harvest and treatment of above ground pollutantcontaining plant biomass. The focus is on plant species that are known to hyperaccumulate pollutants of interest. Phytostabilization: The use of plant roots to inhibit pollutant migration. Phytotransformation or phytodegradation: The use of plants to degrade organic pollutants into less toxic compounds. Plant hyperaccumulator: Plant species known to accumulate >100 mg kg 1 Cd, Cr, Co or Pb; or >1000 mg kg 1 Ni, Cu, Se, As or Al; or >10 000 mg kg 1 Zn or Mn in their above ground biomass (dry weight).
Zooremediation equivalents Zooextraction: The harvest and treatment of pollutant-containing animal biomass. The focus rests on animal species known to accumulate pollutants of interest. Zoostabilization: The use of animals to inhibit pollutant migration. This involves the maintenance or supplementation of wild animal populations without the harvesting of animal biomass. Zootransformation or zoodegradation: The use of animals to degrade organic pollutants to less toxic compounds. This involves the maintenance or supplementation of wild animal populations without the harvesting of animal biomass. Animal metal-hyperaccumulator: Those animal species known to accumulate >100 mg kg 1 Cd, Cr, Co or Pb; or >1000 mg kg 1 Ni, Cu, Se, As or Al; or >10 000 mg kg 1 Zn or Mn. This field would probably be limited to invertebrates for ethical reasons.
0167-7799/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tibtech.2006.12.002
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Zooremediation of pollutants Zooextraction of nutrients and microorganisms The cultivation and harvest of animals to remediate nutrient and pathogenic microorganism pollution in aquatic systems is the most common form of zooremediation. The practice has a long history in aquaculture, where polyculture can reduce nutrient and microorganism pollution from some monocultures. The most common group of animals used are bivalve molluscs, as demonstrated by the co-culture of salmon with mussels or oysters to reduce nutrient pollution from waste salmon feed [12,13]. Oysters reduced the levels of nitrogen and phosphorus in shrimp effluent by 72% and 86%, respectively [14]; similarly, turbidity and chlorophyll a concentrations in fish farm effluent were reduced by 68% and 79%, respectively [15]. At an estuary level, the cultivation and harvest of pearl oysters (Pinctada imbricata) can balance the nitrogen input of a sewage treatment plant. Gifford et al. [4] estimated that an annual harvest of 499 tonnes per year of pearl oyster material would balance the annual input of 3741 kg nitrogen entering the estuary from a small sewage treatment plant located on its southern shores. Similarly, the deployment and harvest of shellfish has been proposed in Sweden [5] and America [16], to mitigate anthropogenic nutrient input to coastal waters. Moreover, there has been recent interest regarding the use of sponges for bioremediation of aquatic microorganism pollution [7,17]. Sponges have a renowned filtering capacity and in large communities filter the overlying water column in as little as 24 h [18], with high particle-retention rates [7] and potential for economic gains through their use as bath sponges [19] or the production of novel metabolites, for example, the cytotoxin latrunculin B for pharmaceutical use [20]. A recent European study reported a successful trial of the marine sponge Chondrilla nucula as an environmental remediator of bacteria [7]. This study estimated that a 1 m2 patch of this sponge can retain up to 7 1010 E. coli cells and filter 14 l of water per hour. A similar Chinese study investigated the potential of the marine sponge Hymeniacidon perleve to remediate E. coli and Vibrio anguillarum II, with the sponges filtering up to 8 107 E. coli cells h 1 g fresh sponge 1 [17]. Recently, the successful use of polychaetes as environmental remediators of microbial pollution has also been reported, with Sabella spallanzanii and Branchiomma luctuosum demonstrating retention efficiencies of Vibrio alginolyticus of 70% and 98%, respectively [21]. It has been estimated that a standing stock of 250 000 worms (Sabella spallanzanii), with aging worms harvested and younger worms cultured, could be used to remediate the suspended-particulate waste matter from a 50 tonne per year fish farm, producing 50 kg dry weight of worm material annually [10]. Zoostabilization or degredation of nutrients and microorganisms Many filter-feeding animals act as benthic–pelagic couplers – they actively transfer energy and nutrients from the water column to the benthos (an aggregation of the organisms living on or at the bottom of a body of water). Newell [8] proposed that large-scale ecological changes in Chesapeake Bay (the largest estuary in the USA) due to eutrophication www.sciencedirect.com
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could be a result of overharvesting of oyster biomass. Newell calculated that the 1880 standing stock of oysters would have taken 3.6 days to filter the entire water column of the Bay, whereas in 1988 it would have taken 228 days. This finding has led to a concerted effort to re-establish oyster bars for ecological reasons in many areas of the USA [22,23], with the largest, the Chesapeake 2000 Agreement, committing various stakeholders to a tenfold increase in native oysters in the Chesapeake Bay by 2010, at a cost of US$100 million [24]. Further examples of the potential for filter feeders to act as ‘ecological engineers’ include the zebra mussel (Dreissenia polymorpha) and the Asiatic clam (Corbicula fluminea). Between 1988 and 1989, following the introduction of the zebra mussel, turbidity in Lake Erie decreased markedly. Additionally, chlorophyll a concentrations reduced by 43%, and mean sechi disc transparencies (a measure of turbidity, assessed by lowering a patterned disc that lies on the end of a rope over the side of a boat and recording the depth at which the observer loses sight of the disc) increased by 1.24 m [25]. Meanwhile, Phelps [26] reported that following establishment of the Asiatic clam in the Potomac River estuary in the early 1980s, water quality improved substantially, with submerged aquatic vegetation that had been absent for 50 years reappearing; subsequent fish and bird surveys revealed large increases in their respective populations. Following reductions in clam biomass, water quality declined and fish, bird and aquatic vegetation populations contracted. Evidence such as this has supported recent calls for the deliberate introduction of exotic bivalve mollusc species to aquatic ecosystems [27]. However, to avoid the problems associated with the introduction of invasive species, the use of native species is generally preferable unless it is certain that exotic candidate species are non-invasive. In addition to bivalve molluscs, zoostabilization of nutrient and microorganism pollution using polychaetes, sponges and a variety of filter feeding invertebrates is conceivable; here, maintenance or supplementation of wild populations of these organisms could be used to manage nutrient or microbial pollution in aquatic ecosystems. Recognition of the importance of these ecosystem services might aid in the conservation of these communities [28]. However, research in this area remains poorly developed in comparison to oyster reef conservation and would profit from increased endeavours. Zooextraction of heavy metals Although no definition has been proposed for an animal metal-hyperaccumulator (see Glossary), we propose the use of plant definitions as a useful reference. A recent review by Gifford et al. [29], focusing on bivalve molluscs, identified species that satisfy the plant definition of a hyperaccumulator for Cu (Crassostrea virginica [2013 mg Cu kg 1]), Pb (Mytilus edulis [506 mg Pb kg 1]), Cd (Pinctada albina albina [108 mg Cd kg 1]) and Al (Crassostrea rhizophorae [2240 mg Al kg 1]) and approached this status for Zn (Crassostrea virginica [9077 mg Zn kg 1]). This phenomenon is well known, and many such animals are presently used in various large-scale environmental monitoring programs [30]. Das and Jana [31,32] investigated the potential for the freshwater bivalve Lamellidens
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marginalis as a biofilter of cadmium pollution in India, demonstrating a bioconcentration factor (BCF – the ratio of concentration within the organism to the exposure concentration) for Cd of up to 347 and a dry weight Cd concentration >500 mg kg 1. Some metal-hyperaccumulating animals offer non-food economic returns. Gifford et al. [4] demonstrated that each tonne of pearl oyster harvested resulted in 703 g metals removed from an estuary on the east coast of Australia. However, this does not give an indication of the remediation potential of pearl oysters because the farm was located in a relatively pristine estuary. Further work by our research group (S. Gifford, PhD thesis, University of Newcastle, 2006) investigated the uptake of Pb and Zn by pearl oysters under controlled laboratory conditions. Pearl oysters exposed to 90 mg l 1 of each metal accumulated 601 mg kg 1 and 209 mg kg 1 Pb as well as 4421 mg kg 1 and 54 mg kg 1 Zn in the soft tissue and shell, respectively. On-going work will assess the effects of selected pollutants on pearl quality, with the aim of developing a model that optimizes environmental and economic outcomes. A vast group of animals that is still unexplored as metal bioremediators that have the potential for non-food economic returns are the sponges. Sponges are exposed to many metal pollutants within aquatic ecosystems and, owing to their filtration capacity, they are known metal bioaccumulators [33,34] with a history of use as reliable biomonitors of marine pollution [35,36]. Indeed, the little work carried out on sponges indicates that they meet the definition of hyperaccumulators for Cd (Halichondria panicea [271 mg Cd kg 1]) [34]. These characteristics, combined with recent interest in sponges as a source of novel pharmaceuticals and bioactive compounds [20], indicate the possibility for a self-financing remediation program (Box 1). Conceivably, other animals, such as bryozoans, polychaetes, and ascidians (which are known to accumulate V [37]), could be used as environmental remediators of metals and might also offer the potential for the farming of novel chemical compounds (Box 1). As with phytoremediation, there is a need for adequate treatment of harvested metal-laden animal biomass. One system that is presently in use is the recovery of Cd in waste scallop tissue: in scallops, only the muscle and the gonad are eaten, whereas the remainder of the organism preferentially accumulates natural sources of Cd from marine waters and thus is removed and discarded from the animal before sale (http://www.unirex-jp.com/ engcadmium/engcadmium.htm). As such, there has been a need to develop systems to handle properly the estimated 400 000 tonnes of cadmium-contaminated scallop waste generated in Japan through scallop processing [38,39]. The Cd is harvested from the scallop waste before being re-used in a nearby car battery plant, whereas the scallop tissue, now free of Cd, is used for fertilizer. Zooextraction of organic pollutants Although the deployment and harvest of animals that hyperaccumulate organic pollutants is still undergoing trials, the use of pearl oysters [29] and sponges is indicated by past studies. Spongia officinalis is known to concentrate many organic contaminants, including polychlorinated www.sciencedirect.com
Box 1. Self-financing zooremediation models The cost of environmental remediation programs can often be prohibitive; thus, the development of ‘profitable’ remediation programs would enhance their use. Several specialized animals have been identified that could function as a remediation model while, at the same time, produce a valuable economic product. Pearl oysters The pearls produced by pearl oysters are an ideal economic offset against the costs of remediation. They are easily stored, are not food products and have a high market value. Pearl oysters are effective nutrient remediators; however, further work is necessary to determine the effects of metals and organic pollutants on pearl quality before deployment against these pollutants. Sponges As with pearl oysters, sponges provide an ideal opportunity for profitable zooremediation. Many sponge metabolites are in global demand and fetch high prices. For certain sponge taxa, bath sponge material offers an alternative economic return for programs aimed at nutrient and microorganism pollution (the use of chemically exposed bath sponge material is unlikely to be accepted in the market). However, the culture of sponges is not as advanced as mollusc culture, and further work is required to demonstrate whether any effects exist on the metabolites of economic interest following pollutant exposure. Sponges have been successfully deployed as zooremediators of microbial pollution. Edible molluscs Edible molluscs are well established as zooremediators of nutrient pollution. However, as products of human consumption, great care needs to be maintained, either to depurate them of pollutants before sale or to culture the organisms in estuarine locations not impacted by other pollution sources such as microorganisms or metals. Nonetheless, increasing mollusc culture in estuaries is an economically advantageous method of nutrient stabilization and/or reduction in estuaries suffering from eutrophication. Gastropod molluscs, Bryozoans, Ascidians There is a current interest within the bioprospecting field for investigating the pharmaceutical value of novel gastropod secondary metabolites [44,45]. It is possible that some of these economic molluscs might possess attributes amenable to concomitant bioremediation, such as the ability to accumulate or breakdown pollutants.
biphenols (PCBs), to higher concentrations than bivalve molluscs, with a BCF of 105 [40]. Thus, substantial quantities of PCBs could potentially be removed from aquatic environments upon harvest of sponge tissue. Recently, fish have been proposed for zooextraction of PCBs and DDT [6]: the authors propose that by not discarding fish waste, such as cod liver, overboard Baltic Sea fisheries could remove 31 kg per year of PCBs from the Baltic ecosystem. This amount compares with an annual influx of some 260 kg of PCBs; therefore, it would remove more from the ecosystem than all other alternative methods (such as degradation in the water column). Zoostabilization and/or degradation of organic pollutants Several examples exist in the literature of the use of animals to degrade organic contaminants to less toxic by-products. Gudimov [11] reported that degradation of oil was accelerated 10–20 times in the presence of Mytilus edulis. Alternatively, the sponge Spongia officinalis can degrade the surfactant 1-( p-sulfophenyl)nonane to its
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main degradation products, 3-( p-sulfophenyl)propionic acid and p-sulfobenzoic acid, ten times more rapidly than marine bacteria [41]: the first evidence of pollutant degradation by a sponge. In addition, there is some evidence that this sponge can degrade the PCB CB138 (International Union of Pure and Applied Chemistry, IUPAC) [40]. It is probable that many sponges are able to breakdown organic pollutants, particularly given their ability to produce and safely store many halogenated biomolecules within the cell. In addition, the differential accumulation of organic pollutants observed in the gastropod Austrocochlea constricta [42] could be used for zoostabilization: short-chain aliphatic hydrocarbons (C14–C18) accumulated in the soft tissue, whereas longer-chain aliphatic hydrocarbons (C20–C30) tended to accumulate in the shell. The authors proposed that those compounds that are more resistant to cellular degradation (longer chain) were isolated from metabolically active tissue and stored in the shell of the organism. As such, it is conceivable that certain contaminants could be remediated through isolation from trophic transfer through sequestration in the shell. Future directions and concluding remarks Animals can be used to extract or stabilize nutrient, microbial, heavy metal and organic pollution. This can be achieved by the harvesting of wild populations of animals to extract pollutants, supplementation or maintenance of wild populations to stabilize pollutants, or the introduction, culture and harvest of animals to extract pollutants – a form of aquaculture. However, many questions need to be addressed before zooremediation can be optimized. The successful harvest of wild animal taxa for the zooextraction of pollutants requires a clear understanding of the population dynamics of candidate taxa, to ensure a sustainable harvest. The successful supplementation of wild animal populations with introduced species for zoostabilization requires an understanding of the risk of the candidate taxa perturbing local ecological communities. In addition, specific care must be exercised when contemplating the addition of exotic species, to avoid the risk of introducing invasive species. The use of animal taxa for zooremediation is likely to trigger substantial community and governmental interest. To formulate sound decisions, quality scientific data must be available. A suitable model is the current debate surrounding the introduction of the non-native Asian oyster
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Box 2. The ethics of employing animals for zooremediation The use of animals for bioremediation initiatives is likely to trigger greater ethical concern from the community and decision-makers than the use of plants or microorganisms. In this context, it is important to recognize that all use of animals for zooremediation initiatives must be based on sound ethical principles. In many jurisdictions, the term animals refers to ‘all live non-human vertebrates’; thus, most guidelines do not relate to invertebrate species [46]. It is probable that the use of invertebrate animal species, such as polychaetes, sponges and molluscs, will meet little resistance and satisfy community ethical standards. However, this does not preclude the use of vertebrate species such as fish if it can be demonstrated that the ethics of such zooremediation programs conform to current best-practice animal husbandry guidelines.
Crassostrea ariakensis to Chesapeake Bay, USA. Here, the government commissioned a report from the National Academy of Sciences [43] that recommended that too little is known about the biology of C. ariakensis to assert confidently that its introduction to US waters would be successful. Thus, in reality, it is probable that the research burden of introducing non-native species for zoostabilization programs will support the use of native animal taxa in this role. The introduction, culture and harvest of animal taxa for zooremediation programs requires detailed knowledge of the biological requirements for successful husbandry practices. In addition, knowledge of the factors governing optimal carrying capacity, disease and parasitic risks, and impacts on the surrounding ecology are necessary, to establish successful zooextractive aquaculture operations. A sound understanding of temporal accumulation dynamics (accumulation, equilibration and depuration) is paramount for optimizing deployment and extraction efficiencies. Some general desirable traits for zooremediation are listed in Table 1. Furthermore, it is generally preferable to focus zooremediation initiatives on invertebrate taxa to minimize ethical concerns (Box 2), although specialized examples using non-invertebrate species, such as existing fishing operations, do exist [6]. The identification of suitable animal taxa for zooremediation could involve surveys of polluted aquatic habitats and subsequent bioprospecting for individuals that are able to stabilize, transform, degrade, or hyperaccumulate pollutants. For metal zooextraction, the definitions from the literature for hyperaccumulating plants serve as a useful benchmark in the evaluation of candidate
Table 1. Checklist for candidate zooremediation species Trait Accumulate pollutant Resistant to toxicity Non-invasive Rapid growth rate Relatively sedentary Ease of culture Population dynamics known Uptake dynamics known Knowledge of carrying capacity Disease risks understood
Zoostabilisation Nutrients * * * * *
Metals * * * * *
Organics * * * * *
* * * *
* * * *
* * * *
*Indicates that trait is required for sustainable zooremediation www.sciencedirect.com
Zooextraction Nutrients * * * * * *
Metals * * * * * *
Organics * * * * * *
* * *
* * *
* * *
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animal species. Selective breeding and/or transgenic technology could be applied to optimize zooremediation, and research into the appropriate management of pollutant-laden biomass would be profitable. Furthermore, an economic return upon the harvest of animal material is highly desirable. Finally, the optimal zooremediation model is context-specific for both the estuary of interest and the candidate zooremediator species, requiring carefully planned preliminary research programmes to maximize remediative benefits against any potential negative ecological impacts. Acknowledgements SG acknowledges the support of the University of Newcastle Barker Foundation in providing financial assistance in the preparation of this manuscript. Aspects of this work were presented at the 3rd European Bioremediation conference in 2005, and discussions with conference participants assisted in the development of this work. The assistance of two anonymous referees improved this manuscript.
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44 Benkendorff, K. et al. (2001) Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 molluscs and 4 polychaetes. J. Invertebr. Pathol. 78, 109–118 45 Mendola, D. (2003) Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: process developments and economics. Biomol. Eng. 20, 441–458 46 New South Wales Animal Research Act, 1985 An act to protect the welfare of animals used in connection with animal research. (http://www.austlii.edu.au/cgi-bin/download.cgi/download/au/legis/ nsw/consol_act/ara1985134.rtf)
Articles of Interest Articles of interest in other Trends and Current Opinion journals DNA tumor viruses and human cancer Blossom Damania Trends in Microbiology doi:10.1016/j.tim.2006.11.002 Emerging concepts in molecular MRI David E. Sosnovik and Ralph Weissleder Current Opinion in Biotechnology doi:10.1016/j.copbio.2006.11.001 Targeting ischemic memory Omar Aras and Vasken Dilsizian Current Opinion in Biotechnology doi:10.1016/j.copbio.2006.11.002 Mechanisms of nucleic acid translocases: lessons from structural biology and single-molecule biophysics Karl-Peter Hopfner and Jens Michaelis Current Opinion in Structural Biology doi:10.1016/j.sbi.2006.11.003 Gene regulatory network models for plant development Elena R. Alvarez-Buylla, Mariana Benı´tez, Enrique Balleza Da´vila, A´lvaro Chaos, Carlos Espinosa-Soto and Pablo Padilla-Longoria Current Opinion in Plant Biology doi:10.1016/j.pbi.2006.11.008 Characterization of histones and their post-translational modifications by mass spectrometry Benjamin A. Garcia, Jeffrey Shabanowitz and Donald F. Hunt Current Opinion in Chemical Biology doi:10.1016/j.cbpa.2006.11.022 www.sciencedirect.com
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