What lies underneath: Conserving the oceans’ genetic resources

Jesús M. Arrietaa,1, Sophie Arnaud-Haondb, and Carlos M. Duartea aDepartment of Global Change Research, Institut Mediterrani d’Estudis Avançats, Consejo Superior de Investigaciones Científicas (CSIC)- Universitat de les Illes Balears (UIB), 07190 Esporles, Mallorca, Spain; and bInstitut Français de Recherche sur la Mer (IFREMER)-Department “Etude des Ecosystèmes Profonds” - DEEP, Centre de Brest, BP 70, 29280 Plouzané Cedex, France

Edited by Steven D. Gaines, University of California, Santa Barbara, CA, and accepted by the Editorial Board August 10, 2010 (received for review October 29, 2009)

The marine realm represents 70% of the surface of the biosphere and contains a rich variety of organisms, including more than 34 of the 36 living phyla, some of which are only found in the oceans. The number of marine species used by humans is growing at unprecedented rates, including the rapid domestication of marine species for aquaculture and the discovery of natural products and genes of medical and biotechnological interest in marine biota. The rapid growth in the human appropriation of marine genetic resources (MGRs), with over 18,000 natural products and 4,900 patents associated with genes of marine organisms, with the latter growing at 12% per year, demonstrates that the use of MGRs is no longer a vision but a growing source of biotechnological and business opportunities. The diversification of the use of marine living resources by humans calls for an urgent revision of the goals and policies of marine protected areas, to include the protection of MGRs and address emerging issues like biopiracy or benefit sharing. Specific challenges are the protection of these valuable resources in international waters, where no universally accepted legal framework exists to protect and regulate the exploitation of MGRs, and the unresolved issues on patenting components of marine life. Implementing steps toward the protection of MGRs is essential to ensure their sustainable use and to support the flow of future findings of medical and biotechnological interest.

marine protected areas | marine reserves | natural products | gene patents | law of the sea

he protection of marine areas to (MGRs) and the associated emerging organisms at a rate of 0.93% per year (Fig. manage fisheries in a sustainable challenges for the shared use of the oceans 1A). This growth is dwarfed by a rapid Tmanner has been in place for and the conservation of the resources they increase in the inventory of marine natural centuries, since Polynesian cul- contain (7). We do so based on the ex- products and genes of commercial interest tures closed areas to fishing to protect amination of patterns in the use of marine derived from bioprospecting efforts. The breeding grounds and allow recovery from organisms to derive natural products number of natural products described overfishing (1), but the usefulness of no- and gene-associated patents, using data from marine species is growing at a rate of take areas was conclusively demonstrated derived from inventories of natural prod- 4% per year (Fig. 1B and Table 1), which by the recovery of fish stocks in World War ucts (SI Text) and data extracted from is much faster than the rate of species II mine fields in the North Sea closed GenBank (8), respectively. We then dis- discovery, because many species yield to fisheries (2). Marine protected areas cuss the need to regulate the use of these multiple natural products. Indeed, about (MPAs) have since emerged as key instru- emerging marine resources and the lead- 18,000 natural products have been re- ments to protect fish stocks and other living ing role that MPAs could have in the ported from marine organisms belonging resources from overexploitation (3) and protection of MGRs. to about 4,800 named species (16) since have expanded to exceed 5,000 locations, the initial reports in the 1950s. The growth of patents that include genes covering about 0.7% of the oceans (4). Marine Biodiversity and the Ocean’s of marine origin is even faster. The patent The advent of biotechnology has broad- Bounty of Genetic Resources ened human use of biological resources far (PAT) division of GenBank (8) (release Marine species make up about 9.7% of beyond food to include other valuable 165) lists more than 5 million records of total named species (9) (Table 1), a pro- products, such as flavors, fragrances, en- DNA sequences deposited in different portion comparable to the share of re- patent offices worldwide. Most of these se- zymes, and medicines. Although terrestrial search effort on biodiversity allocated to quences belong to a few selected species, plants have been used as medicines for marine systems (10) and the fraction of mainly humans, pathogens, and model or- millennia and still support the needs of marine species among those described ganisms. Although the patent inventory in 80% of the world population (5), the use each year (9). However, the most surpris- GenBank is not exhaustive, the reported of marine biological resources for pur- ing discoveries in biodiversity in the past sequences include DNA from 3,634 named poses other than food is now blooming. decades have taken place in marine sys- species. This register includes 4,928 non- The discovery of organisms containing tems, including the discovery of a whole redundant marine gene sequences derived molecules and genes of commercial in- ecosystem based on chemosynthesis in terest is growing in parallel to the explo- hydrothermal vents in 1977 (11); the de- ration of marine biodiversity. Historically, scription of a previously unnoticed meta- Author contributions: J.M.A., S.A.-H., and C.M.D. designed MPAs have been set up for the conserva- zoan phylum, the Loricifera, discovered in research; J.M.A. and S.A.-H. performed research; J.M.A. tion of general marine biodiversity or for 1983 (12); and the discovery in the 1980s and S.A.-H. analyzed data; J.M.A. wrote the programs; the preservation of fisheries resources (6), and J.M.A., S.A.-H., and C.M.D. wrote the paper. of the marine phototrophic prokaryote fl but the increasing use of marine species Prochlorococcus, which turned out to be The authors declare no con ict of interest. as sources of genetic resources calls for the most abundant photosynthetic organ- This article is a PNAS Direct Submission. S.D.G. is a guest editor invited by the Editorial Board. a reassessment of the scope of MPAs to ism on Earth (13). Recent coordinated 1To whom correspondence should be addressed. E-mail: include the protection of these key international efforts, such as the Census of [email protected]. emerging resources. Marine Life (14) and the World Register This article contains supporting information online at Here, we report on the accelerating rate of Marine Species (15), are propelling the www.pnas.org/lookup/suppl/doi:10.1073/pnas. of discovery of marine genetic resources growth of the inventory of named marine 0911897107/-/DCSupplemental.

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Table 1. Number of described species, species source of patents, and percentage of described species resulting in patents for marine and terrestrial environments Percentage of described species Described species (15, 61) Patented species (8) being a source of patents

Total Terrestrial Marine Total Terrestrial Marine Total Terrestrial Marine

Prokaryotes 7,928 7,173 755 1,619 1,401 218 20.42% 19.53% 28.87% 90.48% 9.52% 86.53% 13.47% Eukaryotes 1,800,000 1,653,045 146,955 2,019 1,679 340 0.11% 0.10% 0.23% 91.84% 8.16% 83.16% 16.84% Total 1,807,928 1,660,218 147,710 3,638 3,080 558 0.20% 0.19% 0.38%

from 558 distinct named marine species cloning and sequencing techniques allow of named species (Table 1). In contrast, (Table S1). Since 1999, the number of ma- description and patenting of genes of spe- the proportion of named marine species rine species with genes associated with cies yet to be named or even discovered. with genes included in patents (28%) far patents has been increasing at an impressive The 18,000 marine natural products exceeds the contribution of marine or- rate of about 12% species per year, which reported in Table 1 comprise about 10% ganisms to the total inventory of named is more than 10 times faster than the rate of total natural products known (17), species (10%) (Table 1). Wild marine of description of marine species (Fig. 1A). which is in good agreement with the share species used as source of natural products This is, however, an underestimate, because of marine species in the total inventory outnumber by up to 18-fold those ever domesticated, while the number of spe- cies included in patent applications is growing almost 4 times faster than the 160,000 A number of domesticated marine species (18) (Fig. 1). Thus, appropriation of MGRs is progressing much faster than the already impressive rate of domestication 140,000 described for aquaculture (19). Taxonomic Provenance of MGRs

120,000 The taxonomic origin of MGRs covers the 5,000 entire breadth of the Tree of Life, from Archaea to vertebrates (Fig. 2 and Fig. S1), as source of MNP in contrast to the limited taxonomic range 4,000 of domesticated species. Although the 600 bulk of the Earth’s metabolic diversity re- number of species sides in prokaryotic organisms (18), natu- as source of gene patents ral products of marine origin are almost 400 entirely (97%) derived from eukaryotic sources. The reason for this apparent paradox is that marine natural products 200 domesticated have been mostly derived from large ses- sile organisms, which are easily collected and provide relatively large amounts of 0 biomass for screening of natural products. Sponges alone are the source of 38% of all B 20,000 6,000 reported marine natural products, fol- cuuae nqeo geneAccumulated of unique

eune fmarinesequences origin of lowed by cnidarians (20%), tunicates (under Chordata, 20%), and red algae 15,000 natural products described (Rhodophyta, 9%). However, a major 4,000 prokaryotic contribution is compatible with these estimates, because a significant 10,000 fraction of sponge biomass, for example, is composed of symbiotic microbes, which 2,000 fi natural products are increasingly identi ed as the source of 5,000 the secondary metabolites contributing the natural products attributed to their host Accumulated umber of marine distinct sequences patented (20, 21). The share of marine natural 0 0 1980 1990 2000 2010 products of microbial origin may expand rapidly in the future, as demonstrated by Year the 600% increase in the number of ma- Fig. 1. (A) Time course of the accumulated number of marine species described (black line), those do- rine natural products of microbial origin reported in 2007 relative to the average mesticated for food (red line), those having sequences associated with patents in GenBank (blue line), and fi – the total number of species reported as sources of natural products in the marine realm by 2006 (green gure for the period 1965 2005 (22). column). Note the broken scale along the y axis. (B) Accumulated number of distinct natural products The taxonomic provenance of the ma- (green line) and sequences associated with patents reported in GenBank (blue line) over time. rine sequences in patents is quite different

Arrieta et al. PNAS | October 26, 2010 | vol. 107 | no. 43 | 18319 Downloaded by guest on September 23, 2021 Number of described marine species agriculture or aquaculture (26%), food (17%), or cosmetics (7%) industry and an with one or more described natural products emerging and growing number of applica- tions in the fields of ecotoxicology, bio-

185 , with one or more patented DNA sequences 1 remediation, and biofuel production (Fig. 3). Many of the patents are related to the domesticated production of enzymes and other reagents for molecular and cell biology applica- 642 287 563 121 tions (29%) and to the genetic engineering

19 134 16 4 0 4

0 fi 2 48 (modi cation) of organisms (48%).

2 0 11 94 Current applications of patents associ- 6 356 1 ated with genes of marine origin are mostly Viridiplantae 18 0 based on a few specific properties of ma- 15 Rhodophyta 301

Fungi rine organisms. About 8% of the patents 643 Other protists 32 6 5 4 relate to the use of polyunsaturated fatty

Other metazoa 445 84 acids, which are present in high quantity 177 Stramenopiles Porifera 83 Cnidaria 1 and diversity in marine organisms. These Chordata 148 are components of dietary supplements Echinodermata Bacteria 57 fi 28 that deliver health bene ts to humans and Mollusca 39 can alleviate a broad range of diseases (24). 0 Arthropoda 40 Archaea Another major cluster of marine patents 0 involves fluorescent proteins with appli- Fig. 2. Phylogenetic affiliation of marine species as sources of DNA sequences in patents, natural cations in biomedical research and cell products, and domesticated for food. Bar lengths correspond to the percentage of species in each and molecular biology (25). Their impor- taxonomic group relative to the total number of species for that particular use (natural products, se- tance is illustrated by the 2008 Nobel Prize quences, or domesticated). The numbers show the actual number of species. in Chemistry awarded to Shimomura, Chalfie, and Tsien for the discovery and development of GFPs, originally described from that of marine natural products, be- 9% of the marine species yielding patented from the jellyfish Aequorea victoria. Many cause more than a third (39%) of the gene applications (Fig. 2 and Fig. S1). of the patents are associated with genes marine species in the PAT division of Applications and Prospects for MGRs of marine organisms inhabiting extreme GenBank are prokaryotes (bacteria and environments, such as hydrothermal vents Archaea), contributing 42% of the marine Marine ecosystems are particularly suited and polar oceans. The adaptation of en- genes included in patents, in contrast to the for bioprospecting. Our survey indicates zymes of hydrothermal vent organisms to ample dominance of eukaryotes among the that marine species are about twice as likely very high operating ranges of temperature marine species domesticated for food or to yield at least one gene in a patent than (>80 °C) and pressure (>100 bar) allow used to derive natural products. Moreover, their terrestrial counterparts (Table 1), the use of these “extremozymes” in the the percentage of described species being and it is estimated that the success rate in fi transformation of substrates of biotech- a source of patents is much larger for pro- nding previously undescribed active nological interest to proceed under the karyotes as compared with eukaryotes for chemicals in marine organisms is 500 times harsh conditions imposed by some in- both terrestrial and marine organisms higher than that for terrestrial species (23). fi dustrial processes. Applications of ther- (Table 1). Chordates (mainly sh), mol- The applications of genes of marine mophilic and barophilic (pressure-loving) lusks, and cnidarians are the major eukary- organisms patented thus far range widely, enzymes include the liquefaction of starch otic sources of gene sequences in patents, with a prevalence of applications in the for biofuel production, the use of inteins contributing, respectively, 17%, 15%, and pharmacology and human health (55%), for the safe production of toxic proteins, and the use of thermostable enzymes in molecular biology (26). Marine organisms 60 from polar areas are the source of psy- chrophilic (cold-loving) enzymes, which present high activity at low temperatures. 40 These enzymes allow processing of heat- sensitive substrates and products, such as food, or the avoidance of expensive heating 20 steps in some processes. Some applications % of patents of psychrophilic enzymes include the use of proteases, amylases, and lipases in the formulation of detergents active at low 0 temperatures or the use of cod pepsins for the production of caviar and descaling of Biofuel fish. Other applications of cold-adapted Cosmetics enzymes include proteases for meat ten- Environment Human health Food industry Bioremediation derizing or for the efficient skinning of Biotechnologies β Genetic engineering squid and the use of -galactosidases for the elimination of lactose from milk (27). Application MolecularAgriculture and cell biology & aquaculture The blooming of marine patents and Fig. 3. Synthesis of the uses proposed in the claims or description of 460 patents deposited at the In- patent applications associated with MGRs ternational Patent Office and associated with genes isolated in marine organisms. Because each patent is largely a result of recent technological claim can belong to several categories, the sum is larger than 100%. advances in exploring the ocean and the

18320 | www.pnas.org/cgi/doi/10.1073/pnas.0911897107 Arrieta et al. Downloaded by guest on September 23, 2021 genetic diversity it contains. Advances in would require a few kilograms per year of samples (36). Impressive as they are, these technologies for the direct observation and the active principle. Matching such de- numbers are likely gross underestimates sampling of the deep ocean, including mand would require harvesting about 106– of the true potential for discoveries because the development of submersibles and re- 107 kg (31) of the corresponding organism, the inclusion of rare and normally un- motely operated vehicles, opened the deep which is clearly unsustainable, given their detected prokaryotes may increase present and hitherto unexplored areas in the high limited distribution. However, commercial estimates of marine microbial diversity by seas to bioprospecting. Parallel develop- extraction of wild resources may be possi- one to two orders of magnitude (37). ments in molecular biology, including high- ble in some instances. The pseudopterosins throughput sequencing, metagenomics, and found in the Caribbean octocoral Pseu- MPAs and the Conservation of MGRs bioinformatics, are greatly accelerating dopterogorgia elisabethae are used in the Very little is known about the conservation our capacities to explore and make use of cosmetic industry for their antiinflam- status of most of the species used so far the genetic resources of the ocean, even matory and analgesic properties. Large as sources of MGRs. The Red List of before the source organisms are discovered wild harvests of P. elisabethae, estimated at Endangered Species of the International in some cases. The continued improvement 13–20 tons per year, have been conducted Union for Conservation of Nature (IUCN) in these technologies is facilitating the hu- in the Bahamas for over a decade (32). (38), one of the foundations for de- man appropriation of the genetic resources The successful exploitation of these octo- termining and validating conservation of the oceans, which is already evident in the corals has been made possible by a combi- priorities, contains data about only 36 of very rapid growth of patents that include nation of two factors: (i) a careful the 340 marine eukaryotic species re- genes and natural products of marine collection strategy that involves manually ported as a source of genes included in organisms presented here (Fig. 1B). clipping part of the coral and allowing the patents, of which 10 appear as “data de- Bioprospecting of marine resources only central branches to recover for 2–3 y and ficient,” 2as“endangered,” 6as“vulner- requires the collection of a very limited (ii) regulation by means of an export able,” and 7 as “near threatened.” Thus, 8 amount of biomass for the initial gene limit set by the Bahamas Department of of the 36 marine species assessed so far or product discovery. Therefore, bio- Marine Resources (32). are threatened, and 7 of them are close to prospecting does not generally involve Wild harvests of marine organisms are qualifying as threatened or likely to be threats to biodiversity comparable to the undesirable from a conservational point of threatened in the near future. Although large biomass removals involved in har- view because it is not always possible to current Red List coverage of marine spe- vesting of marine resources for food (28). predict their impact accurately. Anyway, cies is biased toward fish and other large This is especially true for gene finding, many of these large biomass collections can metazoans, efforts are in progress to ex- where a small amount of biomass can be avoided when alternative production pand coverage from the actual number provide enough DNA for endless replica- schemes are developed. Cost-effective of 2,331 (38) to about 20,000 species by tion by cloning or PCR. However, in the commercial scale production in aquacul- 2012 (39), which will likely result in a case of natural products, when a promising ture has been demonstrated for E. turbi- greater number of threatened species drug candidate is found, a second more nate, B. neritina, and several sponges (31). among those listed as a source of genes substantial harvest may be needed to col- Moreover, a dinoflagellate symbiont of and natural products. Nevertheless, the lect the several grams needed to test the P. elisabethae has been found to be the data shown here illustrate the need to drug’s suitability in clinical studies. Ex- source of pseudopterosin (33), and bryos- identify threats and determine conserva- amples of these needs for large biomass tatins have recently been attributed to an tion priorities for MGRs. collections are the anticancer drug ectei- uncultured bacterial symbiont of B. ner- We are not aware of any conservation nascidin 743, obtained from the tunicate itina, indicating that production in simple measures ever taken to protect prokaryotes, Ecteinascidia turbinate (1 g in 1,000 kg wet microbial cultures may be possible in the which comprise a large share of the MGRs weight), the cytostatic halichondrin B future. Also, the limitations in the supply described in this paper. The most extended from Lissodendoryx sp. (300 mg in 1,000 kg) of halichondrin B have been resolved by view is that microbes, in general, are not (29), or the bryostatins from the bryozoan the synthesis of simplified artificial ana- likely to be endangered because of their Bugula neritina (1.5 g in 1,000 kg) (30). logues (34). These developments indicate sheer numbers, fast growth, and potential Although total synthesis of these substan- that the exploitation of scarce MGRs global dispersion (40, 41). However, some ces has been successfully demonstrated, it can be pursued in a sustainable manner microbes are constrained to very particu- was deemed economically unviable (29), with little impact on the populations of lar environments, which make them sensi- resulting in the need for large collections of the source organism in many cases. tive to the same threats faced by their wild biomass. A survey on the feasibility of Many potential sources of genes and milieu. Examples include symbiotic mi- Lissodendoryx sp. harvests revealed that natural products become available every crobes, which are likely to perish along with only small quantities of this sponge can be year, because the rate of discovery of pre- their hosts, or the obligate psychrophiles collected despite its relatively good pop- viously undescribed marine species remains dwelling in Arctic Sea ice and its sur- ulation recovery after dredging. On the high (Fig. 1A). A complete inventory of rounding waters, which are unable to cope other hand, more than 12,000 kg of marine species may require a further 250– with warmer temperatures, and are there- B. neritina, enough to support all pre- 1,000 y at current rates of discovery (9), fore threatened by global warming. Thus, clinical and clinical trials, were recovered projecting opportunities for discovery of some of the prokaryotes sourcing natural from docks and pilings where this fouling MGRs well into the future. The prospect products and genes of economic interest organism is commonly found, with no de- for unique findings is huge, particularly may be confronting a much higher risk for tectable impact on the populations (30). in the microbial realm, as illustrated by extinction than hitherto assumed (40, 41). These results demonstrate the need for recent studies reporting 1.2 million previ- The exploitation of MGRs has the po- careful assessment of the impact of har- ously undescribed gene sequences using tential to be a sustainable process de- vesting and the capacity of the species for cultivation-independent sequencing tech- livering considerable wealth and business postharvesting recovery before attempting niques on a single cubic meter of water from opportunities. The global market for large biomass harvest. Although these the Sargasso Sea (35) and 6 million pre- marine biotechnology was estimated at large collections may be feasible at the re- viously undescribed proteins and 811 dis- US $2.1 billion in 2002, increasing at search stage, successful launch of any of tinct prokaryotic ribotypes (a proxy for a rapid 9.4% from the previous year (23). these substances as therapeutical agents species) from a series of 45 surface seawater However, these practices will only be

Arrieta et al. PNAS | October 26, 2010 | vol. 107 | no. 43 | 18321 Downloaded by guest on September 23, 2021 sustainable if based on sound in- networks of MPAs (49). These criteria On a more global scale, the General ternationally accepted governance and are well suited for the protection of MGRs Assembly established a United Nations conservation mechanisms, which are lack- because they target, among other things, “Open-Ended Informal Consultative Pro- ing as yet and must be urgently developed. the protection of rare, vulnerable, natural, cess on Oceans and the Law of the Sea,” Prospects are indeed jeopardized by the or extreme environments and diversity with an “Ad-Hoc Open-Ended Informal global deterioration of marine ecosystems hotspots. MPAs with general conservation Working Group” to study issues relating to by direct and indirect human pressures goals are suitable for the preservation of the conservation and sustainable use of conducive to biodiversity loss (9, 38, 42) MGRs because they target both known marine biological diversity and genetic and the associated loss of potential genetic and yet to be discovered species. How- resources beyond areas of national juris- resources. The unresolved legal and ethi- ever, there is a perception of an inherent diction (52, 53). Despite the establishment cal issues associated with bioprospecting trade-off between conservation and other of regional fisheries management organ- and the global protection of biological goals, such as fisheries management, izations, about two-thirds of fish stocks are resources allocated beyond national juris- which must be addressed (6). Although no either depleted or overexploited (54); dictions also represent major obstacles for single MPA design is likely to provide therefore, there is a growing need to establish the sustainable exploitation of MGRs. the perfect conditions for the preservation high seas MPAs for the protection of fisheries MGRs of economic interest are deemed of all species, the emerging evidence in- resources (55) that converges with the need to be particularly abundant in biodiversity dicates that carefully designed MPA net- for protection of general biodiversity, in- hot spots, such as coral reefs and sea works are probably the best tool to meet cluding MGRs. In addition, the imple- mounts, and in extreme environments, such both fishery and conservation goals (6). mentation of high seas MPAs covering the as polar and hydrothermal vent ecosys- Although the scientific aspects involved in water column, the sea floor, or both, and tems. Unfortunately, coral reefs, sea expanding and networking marine reserves targeting specific environments, such as sea mounts, and marine polar environments are moving forward, the economic and mounts and hydrothermal vents, will benefit are threatened. Coral reefs are experi- governance structures required for the the protection of MGRs in areas beyond na- encing a steep global decline, which is global protection of marine biodiversity tional jurisdictions. Additional regulations, forecasted to be aggravated further by remain ill-defined. such as the requirement for environmental climate change and ocean acidification (43, At the present state, MPAs encompass impact assessment of bioprospecting activi- 44). Polar ecosystems experience some of an area 10-fold lower than that of terres- ties, would be desirable in some cases, par- the fastest warming rates on the planet, trial protected areas (4), with most of these ticularly when large biomass collections or particularly in the Arctic (45), leading to areas located within economic exclusive harsh techniques like trawling are required. a loss of sea ice and warming of seawater zones (EEZs) under national jurisdictions. However, enforcing a compulsory environ- above the thresholds for psychrophilic However, 65% of the ocean lies beyond mental impact assessment would require an organisms, one of the reservoirs of useful the EEZs, including many of the potential international agreement on access and own- genes. Sea mounts are facing increasing hot spots for MGRs, such as sea mounts ership of MGRs in areas beyond national pressure by deep-sea fisheries, which is and hydrothermal vents, which are mainly jurisdictions, which is currently lacking. likely to result in high environmental im- distributed in areas beyond national juris- Bioprospecting technologies are vul- pacts and extinctions (46). Little is known diction, thereby lacking a global gover- nerable to biopiracy practices, wherein about the potential impacts of mining nance framework to ensure their pro- individuals or corporations from techno- for sulfide deposits rich in gold and other tection. Regarding the international wa- logically advanced countries may secure metals located near hydrothermal vent ters outside the EEZs, the first article of the intellectual property of resources de- ecosystems, but they are likely to be severe the United Nations Convention on the rived from unique ecosystems in de- because these sites support the highest Law of the Sea (UNCLOS) (50) defines veloping countries lacking the financial and biomass concentrations in the deep sea the “area” as “the seabed and ocean floor technological resources to compete in this (46). Other future threats include gas ex- and subsoil thereof, beyond the limits race. Thus, MPAs may help to reduce ploitation or mining near the summits of of national jurisdiction,” thereby clearly biopiracy by implementing clear policies sea mounts, ridges, and other areas where distinguishing it from the water column regarding the use and sharing of the ben- sediment does not accumulate. Their dis- referred to as “high seas” in the areas efits generated by the resources they pro- tribution often coincides with hot spots beyond national jurisdiction. Freedom of tect. Within national EEZs, biopiracy of deep marine biodiversity, which are also the high seas is warranted under conditions can be addressed by specific policies on located on hard substrates, away from of part VII of the Convention. Cooperation genetic resources clearly defining the the typical deep sea soft sediment (46). is also promoted for the conservation of conditions for bioprospecting and access Finally, projects of massive CO2 sequestra- living resources, research, and resource ex- and benefit sharing. More explicit and tion in the sea floor, with pilot studies al- ploitation in the high seas, with govern- robust national laws may also add to the ready ongoing, also raise concern as a ments being responsible for activities of ongoing efforts of the CBD toward an in- potential threat to deep sea biodiversity (47). ships carrying their country flag. Although ternational regime on access and benefit As agreed at the World Summit on many MGRs are extracted from benthic sharing that should at least apply to EEZs Sustainable Development in Johannes- organisms, part XI of the UNCLOS dedi- (56). These access and benefit sharing burg, a global network of MPAs should be cated to the area is clearly restricted to policies should also accommodate other effective by 2012. There are ongoing efforts the exploitation of mineral resources, under needs for access, such as basic academic to reach an international consensus on the management of the International Sea- research. Increasingly difficult access pro- the scientific criteria and guidelines un- bed Authority. The conservation of MGRs cedures have been reported to deter basic derpinning this network. Also, the Con- in the area can only be addressed by the scientific research in the terrestrial envi- ference of Parties to the Convention on International Seabed Authority under the ronment (57) and could also condition Biological Diversity (CBD) (48) has re- framework of mineral exploitation, which basic marine research, biasing sampling cently made a significant step toward will therefore manage limited and scattered efforts toward sites beyond national juris- achieving this goal by adopting scientific protection zones in the area beyond na- dictions. Limitations to basic research on criteria for identifying ecologically or bi- tional jurisdiction, such as the one being biodiversity could be detrimental, imped- ologically significant marine areas in need implemented for nodule mining in the ing the collection of the data that are of protection and designing representative Clarion–Clipperton zone (51). needed for the implementation of the pro-

18322 | www.pnas.org/cgi/doi/10.1073/pnas.0911897107 Arrieta et al. Downloaded by guest on September 23, 2021 tection goals set by the CBD (57), partic- a universally accepted legal framework for realm requires (i) halting the widespread ularly in developing countries. This sit- the protection and equitable exploitation loss of marine biodiversity, for which uation could be eased by ensuring the of the genetic resources of 65% of the MPAs are key instruments, and (ii) the transfer of knowledge and development ocean represents a 21st century techno- urgent development of international leg- tools necessary to build the capacity to logically sophisticated version of the islation regulating the conservation of “ ” fi conduct research on biodiversity in de- tragedy of the commons, affecting sh- these resources as well as access and veloping countries. Fear of biopiracy could eries in international ocean waters (59). benefit sharing for the vast economic and also be alleviated by a clear mandate to In summary, the data reported here social benefits still to emerge. More spe- disclose the origin of patented biological portray the appropriation of MGRs as cifically, high and deep seas MPAs must be resources, a requirement that does not a major recent development, with a huge created and international laws explicitly exist at present. Detailed information prospect for scientific discovery and crea- about the geographical and phylogenetic tion of wealth during the 21st century. The regulating the use and protection of bi- origins of MGRs would help states to unfathomable biological diversity of the ological resources beyond EEZs must be settle disputes over intellectual property oceans offers a vast repertoire of poten- urgently agreed on for the effective pro- rights after a patent claim is made. tially useful biological molecules with no tection of the vast pool of marine bio- Whereas the issue of biopiracy has been comparable equivalent in terrestrial envi- diversity and MGRs yet to be discovered addressed by the CBD, this convention ronments (60). Most importantly, whereas in the in the high seas and the area. applies strictly to the resources from the use of marine organisms for food has EEZs, excluding the area and the high often caused major ecological damage, ACKNOWLEDGMENTS. We thank Sara Teixeira for seas, which are by far the largest marine the appropriation of their genetic re- technical help and Joël Querrelou and Elie Jarm- spaces to be explored and exploited, and sources is a potentially sustainable process ache for useful discussions. This is a contribution to fi the MALASPINA 2010 project, funded by the where very pro table genes have already but also requires conservation measures. CONSOLIDER-Ingenio 2010 program of the Spanish been isolated (58). The unregulated ex- Realization of the ample opportunities Ministry of Science and Technology (Reference ploitation of MGRs in the absence of for science and business in the oceanic CSD2008-00077).

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