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The Nagoya Protocol and historical collections
of plants
Keeping pace with food demand and climate change requires continuous genetic improvement of crops that,
in turn, relies on the availability of genetic resources. Access to these resources is complicated by the need to
establish benefit-sharing arrangements when accessing and using such genetic resources.
Brad Sherman and Robert James Henry
Benefit-sharing arrangements have
been a key part of recent efforts to
ensure that benefits that arise from
the use of genetic resources are shared more
equitably1,2. While these arrangements work
well for some plants, in other situations,
access to established genetic collections is
hindered or blocked by these requirements.
This particularly affects historical
collections, where the provenance and
origin of plants are unclear or unknown.
The fate of plants in historical collections
is important given that they may contain
valuable genetic material that is no longer
available insitu. In these cases, it is crucial
that researchers and breeders are able to
access and use this historical material
to develop new plants3. Solutions that
facilitate access and benefit sharing for these
historical species are urgently required.
The international regulation of plant
genetic resources changed dramatically in
1992 when the Convention on Biological
Diversity (CBD) introduced the principal
that states have sovereignty over the
biological resources located within their
borders4. This was in contrast to the
situation previously, where biological
resources were the ‘common heritage’ of
humankind and freely available for use
without restriction. One of the aims of the
CBD is to promote the conservation and
sustainable use of biodiversity as well
as the fair and equitable sharing of the
benefits arising from the utilization of
genetic resources.
The push towards a more equitable
sharing of benefits under the CBD took an
important turn when the Nagoya Protocol
came into effect in 2014 (ref. 5). The
protocol, which provides member states
with guidance on how the CBD is to be
implemented, reaffirms the sovereign rights
of states over their natural resources6. One
of the goals of the Nagoya Protocol is to
establish a standardized global framework
that governs how users of genetic resources
access and utilize such resources. It also
aims to ensure that any benefits derived
from that utilization are shared fairly and
equitably with the providers. The protocol
does this by requiring member states to
adopt measures which ensure that there is
prior informed consent from the authorities
and providers of biological material and
that benefit-sharing agreements are in
place between users and providers of
biological material.
Unlike some international legal
agreements which only apply in the country
where they are enacted, Nagoya regulates
behaviour outside of the countries where it
has been adopted. This is because countries
that have ratified the protocol are not only
under an obligation to ensure that biological
material used in the country is Nagoya
compliant, but are also required to ensure
that biological material imported into
the country was collected, used and/or
developed in compliance with the protocol.
Specifically, they are required to ensure
that biological material imported into
the country is accompanied by relevant
documentary evidence, including:
• access permits from the relevant
authorities
• prior informed consent from the
authorities and providers of biological
material
• benet-sharing agreements between users
and providers of biological material5
Because the protocol applies to people
who want to export material into a country
that has implemented the Nagoya Protocol,
this means that for a company in the USA
(which is neither a member of the CBD nor
Nagoya) to export biological material to
France (which has adopted Nagoya), they
will have to show that the biological material
is ‘Nagoya compliant’.
Historical plant
material
Annex 1 of
the Plant Treaty
Covered by special
international access
and benefit-sharing
instrument
Not covered by special
international access
and benefit-sharing
instrument
In the multilateral
system
Countries where Nagoya
is retrospective
Countries where Nagoya
is prospective
Non-state actors
Fig. 1 | Nagoya compliance for historical plant material. Historical collections may or may not be
covered by the FAO treaty. If not covered by the treaty, it becomes important to consider if the Nagoya
protocol is retrospective or prospective in the jurisdiction.
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The global reach of Nagoya has been
extended by a number of non-state actors,
such as universities, herbaria and scientific
journals, who have made Nagoya compliance
a pre-condition of dealing with biological
materials. For example, even though the
USA is neither a party to the CBD nor a
signatory to the protocol, the University of
California (or parts thereof) has adopted
Nagoya as best practice when dealing with
biological resources. This means that for a
researcher in Queensland to export a plant
to a colleague at the University of California,
they need to be able to show that the plant
was Nagoya compliant. Similarly, a number
of scientific journals, such as Nature journals,
require contributors writing about biological
material to make these materials available to
readers without restriction or show that the
plants being studied were collected with the
necessary approvals, such as BMC journals.
What it means for historical material
to be Nagoya compliant
One of criticisms made of the CBD
access and benefit-sharing regimes is
that they create bureaucratic barriers
that hinder research. While this needs
to be addressed, we are concerned here
with a different problem that arises when
implementing Nagoya at the national level:
different countries have taken different
interpretations of what Nagoya requires.
While this has occurred in a number of
areas, we focus on an issue particularly
important for food security — namely,
the question of the temporal scope of the
protocol and its impact on our ability to
access historical plant collections (Fig. 1).
During the Nagoya Protocol negotiations,
there were differing opinions about whether
the protocol should be limited to material
collected after it came into force or whether
it should regulate material irrespective of
when it was collected. Because the parties
could not agree on the temporal scope
of Nagoya, the protocol leaves it up to
individual countries to decide whether the
law should be prospective or retrospective
when they implement the protocol into
their national law7,8.
One of the consequences of the gradual
adoption of Nagoya globally is that it’s
changing the way researchers work with
plant material9,10. While this is relatively
straightforward regarding material that
has been collected recently, the position is
more complicated with historical materials
(that is, material collected before the CBD
came into operation in 1992). In part, this is
because researchers working with historical
materials may find that the provenance
of the material is unknown or unclear:
there may be no information about where
and when the material was collected, who
the access provider was or whether it
was collected with permission. This lack
of information is important because the
CBD presupposes that researchers are able
to negotiate with the party who initially
provided the material. While this makes
sense under the CBD, which only applies to
material accessed after the laws came into
force, the shift from ‘access’ to ‘use’ that
occurred under Nagoya means this is now
much more problematic11,12.
In this situation, the following question
arises: what does it mean for a researcher
who utilizes material from a historical
collection to be ‘Nagoya compliant’? The
answer to this question will depend on
whether the material falls within the special
exception established by Article 4 of the
Nagoya Protocol.
Where the Article 4 exception applies
Article 4 of the Nagoya Protocol creates
an exception whereby certain plants are
taken outside of the remit of Nagoya to
be governed by the 2001 International
Treaty on Plant Genetic Resources (‘Plant
Treaty’) and its Standard Material Transfer
Agreement (SMTA). While it is clear that
plant material falling under Article 4 of
Nagoya will be governed by the Plant Treaty
rather than the Nagoya Protocol, what is less
clear is when this occurs. This is because
there are competing interpretations about
when the exception applies.
On one reading, the Article 4 exception
only applies to the 64 plants listed in
Annex 1 of the Plant Treaty. With these
materials, compliance with the SMTA
should suffice. This means that an
Australian researcher working on native
sorghum (which is listed in Annex 1)
obtained from an historical collection would
be Nagoya compliant if they can show the
material was acquired under the SMTA.
On another reading, the Article 4
exception also applies to those materials that
are part of the Plant Treaty’s multilateral
system rather than those merely listed in
Annex 1. This would extend beyond the
scope of Annex 1 material to include plants
placed in the multilateral system, such
as Consultative Group on International
Agricultural Research (CGIAR) collections.
Under this reading, where materials are part
of the multilateral system and supplied with
the SMTA, they would be Nagoya compliant.
Where the Article 4 exception does
not apply
Questions about Nagoya compliance also
arise when plant materials fall outside the
scope of Article 4 (Table 1). The question of
whether plants not covered by Article 4 are
Nagoya compliant will change depending on
whether the relevant domestic law applies
to historical collections. It may also change
when Nagoya compliance is required by a
non-state actor.
In implementing the Nagoya Protocol
into domestic law, a number of countries
have limited the operation of Nagoya to
genetic resources collected after the Protocol
came into force. This was the approach
adopted by the European Union (EU). As a
result, if someone is using historical material
in the EU, or if they are in a non-EU country
and want to export material to one of the EU
member states, as the material is outside the
remit of the EU–Nagoya law, it would not be
necessary for them to show that the material
was Nagoya compliant13–15.
An alternative reading provides that
because the protocol is triggered whenever
genetic material is ‘utilized’, this means
that it applies retrospectively to material
collected before the protocol or, indeed,
the CBD came into operation. If someone
was using material in, or wanted to
export material to, a country that had
Table 1 | 2017 Production of some
high-value crops not listed in Annex 1 of
the FAO treaty
Crop Global production
in 2017 (millions
of tons)
Soybean 352
Sugarcane 1,842
Grapes 74
Mangos, magosteens
and guavas 51
Coffee 9
Onions 98
Peanuts 47
Olives 21
Almonds 2
Walnuts 4
Chillies and peppers 36
Rubber 14
Tea 6
Cucumber 84
Peaches and nectarines 25
Lettuce and chicory 27
Cacao (chocolate) 5
Chestnuts 2
Hazelnuts 1
Crops in Table 1 are not listed in Annex 1 of the FAO treaty;
because of this, it may be very difficult to establish Nagoya
compliance for historical collections of these species. Other
crops for which similar data is not available, including oil palm
and cotton seed oil, can be accessed via ref. 21.
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decided to extend the Nagoya access and
benefit-sharing scheme to include material
collected before the national law came
into effect (such as Norway16,17 or South
Africa18,19), the fate of material not covered
by Article 4 would depend on what the
local laws allowed. In the absence of a
due-diligence ‘defence’ allowing someone to
use historical material when they have made
reasonable efforts to locate the provider
of the genetic material, it may simply not
be possible for someone to plant genetic
material with unknown lineage and still be
Nagoya compliant.
A third situation where questions about
Nagoya compliance arise is when someone
is dealing with non-state actors who have
made Nagoya compliance a condition of
working with them. Because Nagoya is silent
regarding whether it applies to historical
materials, and because different countries
have responded to this silence differently,
it is not clear what Nagoya compliance
means in this context. Thus, when a journal
asks a potential author working with
historical material whether the material
they are writing about is Nagoya compliant,
it might be legitimate for them to reply:
which Nagoya?
Uncertainty about the scope and
operation of the Nagoya Protocol is a
problem that needs to be avoided. At best,
it might slow or hamper access to biological
materials. At worst, it might mean that
access is blocked completely. There are a
number of potential options that might be
adopted to avoid these problems.
One option is to revise Nagoya to
expressly deal with plants in historical
collections. Given the different approaches
taken by member countries to the question
of whether the protocol should apply to
historical material, it is unlikely that there
would be the consensus needed to amend
Nagoya in this way.
Another option, which was rejected at
the Plant Treaty’s Governing Body 2019
meeting, would be to broaden Annex 1 of
the Plant Treaty to include all crops. Given
that the interests of countries in this matter
differ greatly (for example, some countries
favour expanding the treaty while others
are opposed because it would mean a loss
of control over crops of national interest),
we are sceptical about the possibility of
there being an international agreement to
extend Annex 1 to include all plants in the
foreseeable future.
Yet another option would be to increase
the material that is part of the multilateral
system. This could be done by building
on previous work of the Plant Treaty’s
governing body to reach agreement with
institutions for their materials to become
part of the multilateral system. The
effectiveness of this solution would depend
on there being consensus, which there
currently isn’t, about when the Article 4
exception applies.
While these options would improve
access to historical collections, given
the fractured nature of the international
law-making community, it is highly unlikely
that any will be adopted, at least in the near
future. Given this, perhaps the best option is
for scientists, breeders, universities, journals,
research organizations, herbaria, seed banks,
funding bodies and other non-state actors to
develop a common understanding of what
Nagoya compliance means. Rather than
waiting for reform at the international level,
this option could be developed through
micro-level collaborative interaction and
partner engagement.
If adopted, a common and shared
understanding of what Nagoya compliance
means would increase legal certainty,
reduce costs and facilitate timely access to
biological material that is so important for
the breeding of new plants and food security.
In developing a shared understanding of
what Nagoya compliance means, it would be
important to decide whether the Article 4
exception comes into play when the material
is listed in Annex 1 of the Plant Treaty or
when the material forms part of the Plant
Treaty multilateral system. It would also
be useful to decide whether Nagoya was
retrospective and, if so, what could be done
where the provenance of an historical plant
was unknown. Where a historical plant is
used, it is important that benefits flow back
to origin communities. Given that it may not
be possible to identify the origin or provider
of some historical plants, one option might
be to utilize the Plant Treaty SMTA20,
which directs benefits to the third-party
beneficiary fund and thus indirectly to
the origin community. While these are
challenging issues, the stakes are too high
for us not to attempt to find a solution that
ensures ongoing access to the historical
collections that are so important for
food security. ❐
Brad Sherman1,2 and
Robert James Henry 1,3 ✉
1ARC Centre of Excellence for Plant Success in
Nature and Agriculture, University of Queensland,
Brisbane, Queensland, Australia. 2Law School,
University of Queensland, Brisbane, Queensland,
Australia. 3Queensland Alliance for Agriculture
and Food Innovation, University of Queensland,
Brisbane, Queensland, Australia.
✉e-mail: robert.henry@uq.edu.au
Published online: 15 May 2020
https://doi.org/10.1038/s41477-020-0657-8
References
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Author contributions
B.S. and R.J.H. conceived and conducted the study and
wrote the manuscript.
Competing interests
The authors declare no competing interests.
NATURE PLANTS | VOL 6 | MAY 2020 | 430–432 | www.nature.com/natureplants