What lies underneath: Conserving the oceans' genetic resources

Abstract

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.

Full text

What lies underneath: Conserving the oceans’
genetic resources
Jesús M. Arrieta
a,1
, Sophie Arnaud-Haond
b
, and Carlos M. Duarte
a
a
Department 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
b
Institut 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
The protection of marine areas to
manage fisheries in a sustainable
manner has been in place for
centuries, since Polynesian cul-
tures closed areas to fishing to protect
breeding grounds and allow recovery from
overfishing (1), but the usefulness of no-
take areas was conclusively demonstrated
by the recovery of fish stocks in World War
II mine fields in the North Sea closed
to fisheries (2). Marine protected areas
(MPAs) have since emerged as key instru-
ments to protect fish stocks and other living
resources from overexploitation (3) and
have expanded to exceed 5,000 locations,
covering about 0.7% of the oceans (4).
The advent of biotechnology has broad-
ened human use of biological resources far
beyond food to include other valuable
products, such as flavors, fragrances, en-
zymes, and medicines. Although terrestrial
plants have been used as medicines for
millennia and still support the needs of
80% of the world population (5), the use
of marine biological resources for pur-
poses other than food is now blooming.
The discovery of organisms containing
molecules and genes of commercial in-
terest is growing in parallel to the explo-
ration of marine biodiversity. Historically,
MPAs have been set up for the conserva-
tion of general marine biodiversity or for
the preservation of fisheries resources (6),
but the increasing use of marine species
as sources of genetic resources calls for
a reassessment of the scope of MPAs to
include the protection of these key
emerging resources.
Here, we report on the accelerating rate
of discovery of marine genetic resources
(MGRs) and the associated emerging
challenges for the shared use of the oceans
and the conservation of the resources they
contain (7). We do so based on the ex-
amination of patterns in the use of marine
organisms to derive natural products
and gene-associated patents, using data
derived from inventories of natural prod-
ucts (SI Text) and data extracted from
GenBank (8), respectively. We then dis-
cuss the need to regulate the use of these
emerging marine resources and the lead-
ing role that MPAs could have in the
protection of MGRs.
Marine Biodiversity and the Ocean’s
Bounty of Genetic Resources
Marine species make up about 9.7% of
total named species (9) (Table 1), a pro-
portion comparable to the share of re-
search effort on biodiversity allocated to
marine systems (10) and the fraction of
marine species among those described
each year (9). However, the most surpris-
ing discoveries in biodiversity in the past
decades have taken place in marine sys-
tems, including the discovery of a whole
ecosystem based on chemosynthesis in
hydrothermal vents in 1977 (11); the de-
scription of a previously unnoticed meta-
zoan phylum, the Loricifera, discovered in
1983 (12); and the discovery in the 1980s
of the marine phototrophic prokaryote
Prochlorococcus, which turned out to be
the most abundant photosynthetic organ-
ism on Earth (13). Recent coordinated
international efforts, such as the Census of
Marine Life (14) and the World Register
of Marine Species (15), are propelling the
growth of the inventory of named marine
organisms at a rate of 0.93% per year (Fig.
1A). This growth is dwarfed by a rapid
increase in the inventory of marine natural
products and genes of commercial interest
derived from bioprospecting efforts. The
number of natural products described
from marine species is growing at a rate of
4% per year (Fig. 1Band Table 1), which
is much faster than the rate of species
discovery, because many species yield
multiple natural products. Indeed, about
18,000 natural products have been re-
ported from marine organisms belonging
to about 4,800 named species (16) since
the initial reports in the 1950s.
The growth of patents that include genes
of marine origin is even faster. The patent
(PAT) division of GenBank (8) (release
165) lists more than 5 million records of
DNA sequences deposited in different
patent offices worldwide. Most of these se-
quences belong to a few selected species,
mainly humans, pathogens, and model or-
ganisms. Although the patent inventory in
GenBank is not exhaustive, the reported
sequences include DNA from 3,634 named
species. This register includes 4,928 non-
redundant marine gene sequences derived
Author contributions: J.M.A., S.A.-H., and C.M.D. designed
research; J.M.A. and S.A.-H. performed research; J.M.A.
and S.A.-H. analyzed data; J.M.A. wrote the programs;
and J.M.A., S.A.-H., and C.M.D. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. S.D.G. is a guest
editor invited by the Editorial Board.
1
To whom correspondence should be addressed. E-mail:
txetxu@imedea.uib-csic.es.
This article contains supporting information online at
www.pnas.org/lookup/suppl/doi:10.1073/pnas.
0911897107/-/DCSupplemental.
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from 558 distinct named marine species
(Table S1). Since 1999, the number of ma-
rine species with genes associated with
patents has been increasing at an impressive
rate of about 12% species per year, which
is more than 10 times faster than the rate
of description of marine species (Fig. 1A).
This is, however, an underestimate, because
cloning and sequencing techniques allow
description and patenting of genes of spe-
cies yet to be named or even discovered.
The 18,000 marine natural products
reported in Table 1 comprise about 10%
of total natural products known (17),
which is in good agreement with the share
of marine species in the total inventory
of named species (Table 1). In contrast,
the proportion of named marine species
with genes included in patents (28%) far
exceeds the contribution of marine or-
ganisms to the total inventory of named
species (10%) (Table 1). Wild marine
species used as source of natural products
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
number of domesticated marine species
(18) (Fig. 1). Thus, appropriation of
MGRs is progressing much faster than the
already impressive rate of domestication
for aquaculture (19).
Taxonomic Provenance of MGRs
The taxonomic origin of MGRs covers the
entire breadth of the Tree of Life, from
Archaea to vertebrates (Fig. 2 and Fig. S1),
in contrast to the limited taxonomic range
of domesticated species. Although the
bulk of the Earth’s metabolic diversity re-
sides in prokaryotic organisms (18), natu-
ral products of marine origin are almost
entirely (97%) derived from eukaryotic
sources. The reason for this apparent
paradox is that marine natural products
have been mostly derived from large ses-
sile organisms, which are easily collected
and provide relatively large amounts of
biomass for screening of natural products.
Sponges alone are the source of 38% of all
reported marine natural products, fol-
lowed by cnidarians (20%), tunicates
(under Chordata, 20%), and red algae
(Rhodophyta, 9%). However, a major
prokaryotic contribution is compatible
with these estimates, because a significant
fraction of sponge biomass, for example, is
composed of symbiotic microbes, which
are increasingly identified as the source of
the secondary metabolites contributing the
natural products attributed to their host
(20, 21). The share of marine natural
products of microbial origin may expand
rapidly in the future, as demonstrated by
the 600% increase in the number of ma-
rine natural products of microbial origin
reported in 2007 relative to the average
figure for the period 1965–2005 (22).
The taxonomic provenance of the ma-
rine sequences in patents is quite different
0
200
400
600
4,000
5,000
120,000
140,000
160,000
dom est icated
as source of
g
ene
p
atents
described
as source of MNP
A
number of species
1980 1990 2000 2010
0
5,000
10,000
15,000
20,000
0
2,000
4,000
6,000
natural
p
roducts describ ed
distinct se
q
uences
p
atented
B
Year
Accumu lated umber of marin e
natural products
Accumulated unique of gene
sequences of marine origin
Fig. 1. (A) Time course of the accumulated number of marine species described (black line), those do-
mesticated for food (red line), those having sequences associated with patents in GenBank (blue line), and
the total number of species reported as sources of natural products in the marine realm by 2006 (green
column). Note the broken scale along the yaxis. (B) Accumulated number of distinct natural products
(green line) and sequences associated with patents reported in GenBank (blue line) over time.
Table 1. Number of described species, species source of patents, and percentage of described species resulting in patents for marine
and terrestrial environments
Described species (15, 61) Patented species (8)
Percentage of described species
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%
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SPECIAL FEATURE: PERSPECTIVE

from that of marine natural products, be-
cause more than a third (39%) of the
marine species in the PAT division of
GenBank are prokaryotes (bacteria and
Archaea), contributing 42% of the marine
genes included in patents, in contrast to the
ample dominance of eukaryotes among the
marine species domesticated for food or
used to derive natural products. Moreover,
the percentage of described species being
a source of patents is much larger for pro-
karyotes as compared with eukaryotes for
both terrestrial and marine organisms
(Table 1). Chordates (mainly fish), mol-
lusks, and cnidarians are the major eukary-
otic sources of gene sequences in patents,
contributing, respectively, 17%, 15%, and
9% of the marine species yielding patented
gene applications (Fig. 2 and Fig. S1).
Applications and Prospects for MGRs
Marine ecosystems are particularly suited
for bioprospecting. Our survey indicates
that marine species are about twice as likely
to yield at least one gene in a patent than
their terrestrial counterparts (Table 1),
and it is estimated that the success rate in
finding previously undescribed active
chemicals in marine organisms is 500 times
higher than that for terrestrial species (23).
The applications of genes of marine
organisms patented thus far range widely,
with a prevalence of applications in the
pharmacology and human health (55%),
agriculture or aquaculture (26%), food
(17%), or cosmetics (7%) industry and an
emerging and growing number of applica-
tions in the fields of ecotoxicology, bio-
remediation, and biofuel production (Fig.
3). Many of the patents are related to the
production of enzymes and other reagents
for molecular and cell biology applica-
tions (29%) and to the genetic engineering
(modification) of organisms (48%).
Current applications of patents associ-
ated with genes of marine origin are mostly
based on a few specific properties of ma-
rine organisms. About 8% of the patents
relate to the use of polyunsaturated fatty
acids, which are present in high quantity
and diversity in marine organisms. These
are components of dietary supplements
that deliver health benefits to humans and
can alleviate a broad range of diseases (24).
Another major cluster of marine patents
involves fluorescent proteins with appli-
cations in biomedical research and cell
and molecular biology (25). Their impor-
tance is illustrated by the 2008 Nobel Prize
in Chemistry awarded to Shimomura,
Chalfie, and Tsien for the discovery and
development of GFPs, originally described
from the jellyfish Aequorea victoria. Many
of the patents are associated with genes
of marine organisms inhabiting extreme
environments, such as hydrothermal vents
and polar oceans. The adaptation of en-
zymes of hydrothermal vent organisms to
very high operating ranges of temperature
(>80 °C) and pressure (>100 bar) allow
the use of these “extremozymes”in the
transformation of substrates of biotech-
nological interest to proceed under the
harsh conditions imposed by some in-
dustrial processes. Applications of ther-
mophilic and barophilic (pressure-loving)
enzymes include the liquefaction of starch
for biofuel production, the use of inteins
for the safe production of toxic proteins,
and the use of thermostable enzymes in
molecular biology (26). Marine organisms
from polar areas are the source of psy-
chrophilic (cold-loving) enzymes, which
present high activity at low temperatures.
These enzymes allow processing of heat-
sensitive substrates and products, such as
food, or the avoidance of expensive heating
steps in some processes. Some applications
of psychrophilic enzymes include the use
of proteases, amylases, and lipases in the
formulation of detergents active at low
temperatures or the use of cod pepsins for
the production of caviar and descaling of
fish. Other applications of cold-adapted
enzymes include proteases for meat ten-
derizing or for the efficient skinning of
squid and the use of β-galactosidases for the
elimination of lactose from milk (27).
The blooming of marine patents and
patent applications associated with MGRs
is largely a result of recent technological
advances in exploring the ocean and the
Archaea
Bacteria
Stramenopiles
Other protists
Rhodophyta
Viridiplantae
Fungi
Other metazoa
Porifera
Cnidaria
Chordata
Echinodermata
Mollusca
Arthropoda
177
148
1
40
0
0
643
32
5
18
15
0
563
11
6
287
16
2
19
4
0
134
4
0
2
1185
0
48
642
1
94
356
121
301
6
4
83
445
84
28
57
39
with one or more patented DNA sequences
with one or more described natural products
domesticated
Number of described marine species
,
Fig. 2. Phylogenetic affiliation of marine species as sources of DNA sequences in patents, natural
products, and domesticated for food. Bar lengths correspond to the percentage of species in each
taxonomic group relative to the total number of species for that particular use (natural products, se-
quences, or domesticated). The numbers show the actual number of species.
Human health
Genetic engineering
Molecular and cell biology
Agriculture & aquaculture
Food industry
Cosmetics
Environment
Biotechnologies
Bioremediation
Biofuel
0
20
40
60
Application
% of patents
Fig. 3. Synthesis of the uses proposed in the claims or description of 460 patents deposited at the In-
ternational Patent Office and associated with genes isolated in marine organisms. Because each patent
claim can belong to several categories, the sum is larger than 100%.
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genetic diversity it contains. Advances in
technologies for the direct observation and
sampling of the deep ocean, including
the development of submersibles and re-
motely operated vehicles, opened the deep
and hitherto unexplored areas in the high
seas to bioprospecting. Parallel develop-
ments in molecular biology, including high-
throughput sequencing, metagenomics, and
bioinformatics, are greatly accelerating
our capacities to explore and make use of
the genetic resources of the ocean, even
before the source organisms are discovered
in some cases. The continued improvement
in these technologies is facilitating the hu-
man appropriation of the genetic resources
of the oceans, which is already evident in the
very rapid growth of patents that include
genes and natural products of marine
organisms presented here (Fig. 1B).
Bioprospecting of marine resources only
requires the collection of a very limited
amount of biomass for the initial gene
or product discovery. Therefore, bio-
prospecting does not generally involve
threats to biodiversity comparable to the
large biomass removals involved in har-
vesting of marine resources for food (28).
This is especially true for gene finding,
where a small amount of biomass can
provide enough DNA for endless replica-
tion by cloning or PCR. However, in the
case of natural products, when a promising
drug candidate is found, a second more
substantial harvest may be needed to col-
lect the several grams needed to test the
drug’s suitability in clinical studies. Ex-
amples of these needs for large biomass
collections are the anticancer drug ectei-
nascidin 743, obtained from the tunicate
Ecteinascidia turbinate (1 g in 1,000 kg wet
weight), the cytostatic halichondrin B
from Lissodendoryx sp. (300 mg in 1,000 kg)
(29), or the bryostatins from the bryozoan
Bugula neritina (1.5 g in 1,000 kg) (30).
Although total synthesis of these substan-
ces has been successfully demonstrated, it
was deemed economically unviable (29),
resulting in the need for large collections of
wild biomass. A survey on the feasibility of
Lissodendoryx sp. harvests revealed that
only small quantities of this sponge can be
collected despite its relatively good pop-
ulation recovery after dredging. On the
other hand, more than 12,000 kg of
B.neritina, enough to support all pre-
clinical and clinical trials, were recovered
from docks and pilings where this fouling
organism is commonly found, with no de-
tectable impact on the populations (30).
These results demonstrate the need for
careful assessment of the impact of har-
vesting and the capacity of the species for
postharvesting recovery before attempting
large biomass harvest. Although these
large collections may be feasible at the re-
search stage, successful launch of any of
these substances as therapeutical agents
would require a few kilograms per year of
the active principle. Matching such de-
mand would require harvesting about 10
6
–
10
7
kg (31) of the corresponding organism,
which is clearly unsustainable, given their
limited distribution. However, commercial
extraction of wild resources may be possi-
ble in some instances. The pseudopterosins
found in the Caribbean octocoral Pseu-
dopterogorgia elisabethae are used in the
cosmetic industry for their antiinflam-
matory and analgesic properties. Large
wild harvests of P. elisabethae, estimated at
13–20 tons per year, have been conducted
in the Bahamas for over a decade (32).
The successful exploitation of these octo-
corals has been made possible by a combi-
nation of two factors: (i) a careful
collection strategy that involves manually
clipping part of the coral and allowing the
central branches to recover for 2–3 y and
(ii) regulation by means of an export
limit set by the Bahamas Department of
Marine Resources (32).
Wild harvests of marine organisms are
undesirable from a conservational point of
view because it is not always possible to
predict their impact accurately. Anyway,
many of these large biomass collections can
be avoided when alternative production
schemes are developed. Cost-effective
commercial scale production in aquacul-
ture has been demonstrated for E. turbi-
nate,B. neritina, and several sponges (31).
Moreover, a dinoflagellate symbiont of
P. elisabethae has been found to be the
source of pseudopterosin (33), and bryos-
tatins have recently been attributed to an
uncultured bacterial symbiont of B. ner-
itina, indicating that production in simple
microbial cultures may be possible in the
future. Also, the limitations in the supply
of halichondrin B have been resolved by
the synthesis of simplified artificial ana-
logues (34). These developments indicate
that the exploitation of scarce MGRs
can be pursued in a sustainable manner
with little impact on the populations of
the source organism in many cases.
Many potential sources of genes and
natural products become available every
year, because the rate of discovery of pre-
viously undescribed marine species remains
high (Fig. 1A). A complete inventory of
marine species may require a further 250–
1,000 y at current rates of discovery (9),
projecting opportunities for discovery of
MGRs well into the future. The prospect
for unique findings is huge, particularly
in the microbial realm, as illustrated by
recent studies reporting 1.2 million previ-
ously undescribed gene sequences using
cultivation-independent sequencing tech-
niques on a single cubic meter of water from
the Sargasso Sea (35) and 6 million pre-
viously undescribed proteins and 811 dis-
tinct prokaryotic ribotypes (a proxy for
species) from a series of 45 surface seawater
samples (36). Impressive as they are, these
numbers are likely gross underestimates
of the true potential for discoveries because
the inclusion of rare and normally un-
detected prokaryotes may increase present
estimates of marine microbial diversity by
one to two orders of magnitude (37).
MPAs and the Conservation of MGRs
Very little is known about the conservation
status of most of the species used so far
as sources of MGRs. The Red List of
Endangered Species of the International
Union for Conservation of Nature (IUCN)
(38), one of the foundations for de-
termining and validating conservation
priorities, contains data about only 36 of
the 340 marine eukaryotic species re-
ported as a source of genes included in
patents, of which 10 appear as “data de-
ficient,”2as“endangered,”6as“vulner-
able,”and 7 as “near threatened.”Thus, 8
of the 36 marine species assessed so far
are threatened, and 7 of them are close to
qualifying as threatened or likely to be
threatened in the near future. Although
current Red List coverage of marine spe-
cies is biased toward fish and other large
metazoans, efforts are in progress to ex-
pand coverage from the actual number
of 2,331 (38) to about 20,000 species by
2012 (39), which will likely result in a
greater number of threatened species
among those listed as a source of genes
and natural products. Nevertheless, the
data shown here illustrate the need to
identify threats and determine conserva-
tion priorities for MGRs.
We are not aware of any conservation
measures ever taken to protect prokaryotes,
which comprise a large share of the MGRs
described in this paper. The most extended
view is that microbes, in general, are not
likely to be endangered because of their
sheer numbers, fast growth, and potential
global dispersion (40, 41). However, some
microbes are constrained to very particu-
lar environments, which make them sensi-
tive to the same threats faced by their
milieu. Examples include symbiotic mi-
crobes, which are likely to perish along with
their hosts, or the obligate psychrophiles
dwelling in Arctic Sea ice and its sur-
rounding waters, which are unable to cope
with warmer temperatures, and are there-
fore threatened by global warming. Thus,
some of the prokaryotes sourcing natural
products and genes of economic interest
may be confronting a much higher risk for
extinction than hitherto assumed (40, 41).
The exploitation of MGRs has the po-
tential to be a sustainable process de-
livering considerable wealth and business
opportunities. The global market for
marine biotechnology was estimated at
US $2.1 billion in 2002, increasing at
a rapid 9.4% from the previous year (23).
However, these practices will only be
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sustainable if based on sound in-
ternationally accepted governance and
conservation mechanisms, which are lack-
ing as yet and must be urgently developed.
Prospects are indeed jeopardized by the
global deterioration of marine ecosystems
by direct and indirect human pressures
conducive to biodiversity loss (9, 38, 42)
and the associated loss of potential genetic
resources. The unresolved legal and ethi-
cal issues associated with bioprospecting
and the global protection of biological
resources allocated beyond national juris-
dictions also represent major obstacles for
the sustainable exploitation of MGRs.
MGRs of economic interest are deemed
to be particularly abundant in biodiversity
hot spots, such as coral reefs and sea
mounts, and in extreme environments, such
as polar and hydrothermal vent ecosys-
tems. Unfortunately, coral reefs, sea
mounts, and marine polar environments
are threatened. Coral reefs are experi-
encing a steep global decline, which is
forecasted to be aggravated further by
climate change and ocean acidification (43,
44). Polar ecosystems experience some of
the fastest warming rates on the planet,
particularly in the Arctic (45), leading to
a loss of sea ice and warming of seawater
above the thresholds for psychrophilic
organisms, one of the reservoirs of useful
genes. Sea mounts are facing increasing
pressure by deep-sea fisheries, which is
likely to result in high environmental im-
pacts and extinctions (46). Little is known
about the potential impacts of mining
for sulfide deposits rich in gold and other
metals located near hydrothermal vent
ecosystems, but they are likely to be severe
because these sites support the highest
biomass concentrations in the deep sea
(46). Other future threats include gas ex-
ploitation or mining near the summits of
sea mounts, ridges, and other areas where
sediment does not accumulate. Their dis-
tribution often coincides with hot spots
of deep marine biodiversity, which are also
located on hard substrates, away from
the typical deep sea soft sediment (46).
Finally, projects of massive CO
2
sequestra-
tion in the sea floor, with pilot studies al-
ready ongoing, also raise concern as a
potential threat to deep sea biodiversity (47).
As agreed at the World Summit on
Sustainable Development in Johannes-
burg, a global network of MPAs should be
effective by 2012. There are ongoing efforts
to reach an international consensus on
the scientific criteria and guidelines un-
derpinning this network. Also, the Con-
ference of Parties to the Convention on
Biological Diversity (CBD) (48) has re-
cently made a significant step toward
achieving this goal by adopting scientific
criteria for identifying ecologically or bi-
ologically significant marine areas in need
of protection and designing representative
networks of MPAs (49). These criteria
are well suited for the protection of MGRs
because they target, among other things,
the protection of rare, vulnerable, natural,
or extreme environments and diversity
hotspots. MPAs with general conservation
goals are suitable for the preservation of
MGRs because they target both known
and yet to be discovered species. How-
ever, there is a perception of an inherent
trade-off between conservation and other
goals, such as fisheries management,
which must be addressed (6). Although no
single MPA design is likely to provide
the perfect conditions for the preservation
of all species, the emerging evidence in-
dicates that carefully designed MPA net-
works are probably the best tool to meet
both fishery and conservation goals (6).
Although the scientific aspects involved in
expanding and networking marine reserves
are moving forward, the economic and
governance structures required for the
global protection of marine biodiversity
remain ill-defined.
At the present state, MPAs encompass
an area 10-fold lower than that of terres-
trial protected areas (4), with most of these
areas located within economic exclusive
zones (EEZs) under national jurisdictions.
However, 65% of the ocean lies beyond
the EEZs, including many of the potential
hot spots for MGRs, such as sea mounts
and hydrothermal vents, which are mainly
distributed in areas beyond national juris-
diction, thereby lacking a global gover-
nance framework to ensure their pro-
tection. Regarding the international wa-
ters outside the EEZs, the first article of
the United Nations Convention on the
Law of the Sea (UNCLOS) (50) defines
the “area”as “the seabed and ocean floor
and subsoil thereof, beyond the limits
of national jurisdiction,”thereby clearly
distinguishing it from the water column
referred to as “high seas”in the areas
beyond national jurisdiction. Freedom of
the high seas is warranted under conditions
of part VII of the Convention. Cooperation
is also promoted for the conservation of
living resources, research, and resource ex-
ploitation in the high seas, with govern-
ments being responsible for activities of
ships carrying their country flag. Although
many MGRs are extracted from benthic
organisms, part XI of the UNCLOS dedi-
cated to the area is clearly restricted to
the exploitation of mineral resources, under
the management of the International Sea-
bed Authority. The conservation of MGRs
in the area can only be addressed by the
International Seabed Authority under the
framework of mineral exploitation, which
will therefore manage limited and scattered
protection zones in the area beyond na-
tional jurisdiction, such as the one being
implemented for nodule mining in the
Clarion–Clipperton zone (51).
On a more global scale, the General
Assembly established a United Nations
“Open-Ended Informal Consultative Pro-
cess on Oceans and the Law of the Sea,”
with an “Ad-Hoc Open-Ended Informal
Working Group”to study issues relating to
the conservation and sustainable use of
marine biological diversity and genetic
resources beyond areas of national juris-
diction (52, 53). Despite the establishment
of regional fisheries management organ-
izations, about two-thirds of fish stocks are
either depleted or overexploited (54);
therefore, there is a growing need to establish
high seas MPAs for the protection of fisheries
resources (55) that converges with the need
for protection of general biodiversity, in-
cluding MGRs. In addition, the imple-
mentation of high seas MPAs covering the
water column, the sea floor, or both, and
targeting specific environments, such as sea
mounts and hydrothermal vents, will benefit
the protection of MGRs in areas beyond na-
tional jurisdictions. Additional regulations,
such as the requirement for environmental
impact assessment of bioprospecting activi-
ties, would be desirable in some cases, par-
ticularly when large biomass collections or
harsh techniques like trawling are required.
However, enforcing a compulsory environ-
mental impact assessment would require an
international agreement on access and own-
ership of MGRs in areas beyond national
jurisdictions, which is currently lacking.
Bioprospecting technologies are vul-
nerable to biopiracy practices, wherein
individuals or corporations from techno-
logically advanced countries may secure
the intellectual property of resources de-
rived from unique ecosystems in de-
veloping countries lacking the financial and
technological resources to compete in this
race. Thus, MPAs may help to reduce
biopiracy by implementing clear policies
regarding the use and sharing of the ben-
efits generated by the resources they pro-
tect. Within national EEZs, biopiracy
can be addressed by specific policies on
genetic resources clearly defining the
conditions for bioprospecting and access
and benefit sharing. More explicit and
robust national laws may also add to the
ongoing efforts of the CBD toward an in-
ternational regime on access and benefit
sharing that should at least apply to EEZs
(56). These access and benefit sharing
policies should also accommodate other
needs for access, such as basic academic
research. Increasingly difficult access pro-
cedures have been reported to deter basic
scientific research in the terrestrial envi-
ronment (57) and could also condition
basic marine research, biasing sampling
efforts toward sites beyond national juris-
dictions. Limitations to basic research on
biodiversity could be detrimental, imped-
ing the collection of the data that are
needed for the implementation of the pro-
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tection goals set by the CBD (57), partic-
ularly in developing countries. This sit-
uation could be eased by ensuring the
transfer of knowledge and development
tools necessary to build the capacity to
conduct research on biodiversity in de-
veloping countries. Fear of biopiracy could
also be alleviated by a clear mandate to
disclose the origin of patented biological
resources, a requirement that does not
exist at present. Detailed information
about the geographical and phylogenetic
origins of MGRs would help states to
settle disputes over intellectual property
rights after a patent claim is made.
Whereas the issue of biopiracy has been
addressed by the CBD, this convention
applies strictly to the resources from
EEZs, excluding the area and the high
seas, which are by far the largest marine
spaces to be explored and exploited, and
where very profitable genes have already
been isolated (58). The unregulated ex-
ploitation of MGRs in the absence of
a universally accepted legal framework for
the protection and equitable exploitation
of the genetic resources of 65% of the
ocean represents a 21st century techno-
logically sophisticated version of the
“tragedy of the commons,”affecting fish-
eries in international ocean waters (59).
In summary, the data reported here
portray the appropriation of MGRs as
a major recent development, with a huge
prospect for scientific discovery and crea-
tion of wealth during the 21st century. The
unfathomable biological diversity of the
oceans offers a vast repertoire of poten-
tially useful biological molecules with no
comparable equivalent in terrestrial envi-
ronments (60). Most importantly, whereas
the use of marine organisms for food has
often caused major ecological damage,
the appropriation of their genetic re-
sources is a potentially sustainable process
but also requires conservation measures.
Realization of the ample opportunities
for science and business in the oceanic
realm requires (i) halting the widespread
loss of marine biodiversity, for which
MPAs are key instruments, and (ii) the
urgent development of international leg-
islation regulating the conservation of
these resources as well as access and
benefit sharing for the vast economic and
social benefits still to emerge. More spe-
cifically, high and deep seas MPAs must be
created and international laws explicitly
regulating the use and protection of bi-
ological resources beyond EEZs must be
urgently agreed on for the effective pro-
tection of the vast pool of marine bio-
diversity and MGRs yet to be discovered
in the in the high seas and the area.
ACKNOWLEDGMENTS. We thank Sara Teixeira for
technical help and Joël Querrelou and Elie Jarm-
ache for useful discussions. This is a contribution to
the MALASPINA 2010 project, funded by the
CONSOLIDER-Ingenio 2010 program of the Spanish
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