APS – IPPC Joint Meeting, Honolulu 2011. Symposium: “The
Developing Crisis. International Movement of Insects and
Pathogens in Commercial Trade”
Flaws in international protocols
for preventing entry and spread
of plant pathogens via ‘plants
for planting’
Clive Brasier, Forest Research
Agency UK
Disclaimer
The views expressed in this talk are solely those of the author.
They are based on > 40 years personal experience researching the
behaviour of plant pathogens and on the observations of many
scientific colleagues.
The permissions of scientific colleagues to use their data or
photographs in this talk are gratefully acknowledged.
For a fuller account of the issues raised and detailed references see:
Brasier C M (2008). The biosecurity threat to the UK and global plant
heritage from international trade in plants. Plant Pathology 57, 792808.
Webber J (2010). Pest risk analysis and invasion pathways for plant
pathogens. New Zealand Journal of Forest Science 40, suppl., S45S56 (and online at www.scionresearch.com/nzjfs)
A. The problem
B. Why the growing threat?
C. [Solutions]
I will be talking mainly about ‘plants for
planting’ - nursery stock - and its impact on
the environment
Going to use examples of forest pathogens and in particular Phytophthora pathogens
(fungi) because
Phytophthora is arguably the most
damaging genus of fungal plant pathogens
(a well known example is potato blight)
Phytophthoras are well suited to
transmission via international trade in
plants
I’m also going to take many of my examples
from the present situation in Europe
Because Europe nicely represents
the problem worldwide
Because Europe, regrettably, has an
increasingly poor record in keeping
exotic pathogens out
A. The problem
Europe is currently experiencing a stream of
imported pathogens and pests –
– a growing threat to the long term biosecurity
and sustainability of European forests and natural
ecosystems, egs ..
Pitch canker of pine, Horse chestnut bleeding canker,
Plane wilt, Ash dieback, Pine wood nematode, Asian
longhorn beetle, Pine lappet moth, Oak processionary
moth, Chestnut gall wasp…
Especially Phytophthora pathogens – eg. Phytophthora
dieback of alder, Phytophthora ramorum dieback (SOD,
SLD), Phytophthora kernoviae dieback, Phytophthora
dieback of Nothofagus, Phytophthora collar rot of
almond, Phytophthora lateralis cedar mortality…
Mainly introduced primary
pathogens ie likely to cause
serious disease irrespective of
climate or other environmental
changes
Examples of destructive pathogens causing
recent major tree and natural environment
disease events in the UK alone:
Cumulative major events trees and natural
environment UK
xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx
Cumulative incidence of disease outbreak over time
Cumulative outbreaks
Cumulative incidence of disease outbreak
12
10
8
6
4
2
Sandra Denman Forest Research
2009
2005
2001
1997
Year
Year
1993
1989
1985
1981
1970
1977
1973
1969
1965
0
2009
Cumulative major events UK
xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx
Cumulative incidence of disease outbreak over time
Cumulative outbreaks
Cumulative incidence of disease outbreak
12
Phytophthora lateralis. Lawson’s cypress
Phytophthora ramorum. Larch
10
Phytophthora pseudosyringae. Native heath, Nothofagus
Phytophthora kernoviae. Native heath
8
Phytophthora pseudosyringae. Beech, hornbeam
Pseudomonas syringae pv aesculi. Horse chestnut
6
Phytophthora kernoviae. Beech, rhododendron etc
Phytophthora ramorum. Larch, rhododendron etc
4
Dothiostroma septosporum. Pines
Ophiostoma
novo-ulmi. Elm
2
Phytophthora alni. Alder
Sandra Denman Forest Research
2009
2005
2001
1997
Year
Year
1993
1989
1985
1981
1970
1977
1973
1969
1965
0
2009
Cumulative major events UK
xxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxxx
Cumulative incidence of disease outbreak over time
Cumulative outbreaks
Cumulative incidence of disease outbreak
12
Phytophthora lateralis. Lawson’s cypress
Phytophthora ramorum. Larch
10
Phytophthora pseudosyringae. Native heath, Nothofagus
Phytophthora kernoviae. Native heath
8
Phytophthora pseudosyringae. Beech, hornbeam
Pseudomonas syringae pv aesculi. Horse chestnut
6
Phytophthora kernoviae. Beech, rhododendron etc
Phytophthora ramorum. Larch, rhododendron etc
4
Dothiostroma septosporum. Pines
Ophiostoma
novo-ulmi. Elm
2
Phytophthora alni. Alder
Sandra Denman Forest Research
2009
2005
2001
1997
Year
Year
1993
1989
1985
1981
1970
1977
1973
1969
1965
0
2009
This phenomenon is not confined to
Europe –
Europe is simply representative
A similar pattern of pathogen
invasion is occurring in forests and
natural ecosystems worldwide
P. cinnamomi
Jarrah forest Australia
P. taxon agathis
P. lateralis
Kauri pine New Zealand
Chamaecyparis USA
P. austrocedrae
Austrocedrus Argentina
P. ramorum
Tanoak USA
P. pinifolia
Radiata pine Chile
Photos top, l to r : CMB; Giles Hardy ; Don Goheen. Centre: Alina Greslebin; Bottom, l to r: CMB; FABI ZA.
Sudden oak death
P. ramorum Tanoak USA
2008
P. ramorum Larch
UK 2010
Sudden larch death
Many of these damaging invasive pathogens
are new to science
e.g. P. ramorum, P. alni, P. kernoviae, P.
niederhauseri , P. pinifolia, P. austrocedrae …
Many of them are introduced by the
international plant trade – via rooted plants plants for planting -for horticulture and forestry
Phytophthoras are especially suited to spread
on nursery stock
So – look further at the Phytophthora nursery
issue as exemplified by Europe -
Recent surveys of European nurseries show stock
is often infested with Phytophthora species
e.g. Moralejo et al Plant Pathology 2008 :
Found 17 different Phytophthora species
from 37 hosts in nurseries in Balearic
islands and north east Spain:
“An example of unnoticed spread via the
ornamental plant trade in Europe ...
.. several of the Phytophthoras now
confined to nurseries may pose a threat
to local natural ecosystems“
And similarly in the USA:
Schwingle & Blanchette Plant Disease (2007) :
Found 11 Phytophthora species on ornamentals
in Minnesota nurseries..
Yakabe et al Plant Disease (2009) :
Found 13 Phytophthora species causing foliar
disease of ornamentals in Californian nurseries..
Surveys by Thomas Jung and colleagues
on Phytophthoras in European nurseries
and forests show :
A strong link between high levels
of infestation in nurseries and
Phytophthora disease in forestry
plantations
Phytophthora alni on alder, spreading across Europe.
Origin – recent hybridization event in a nursery?
Alnus glutinosa
Photos: Thomas Jung, Germany John Gibbs, UK
Bavarian river system
Diseased
alders
P. alni first
appeared
ca 1995
Germany
By 2003,
80% of
Bavarian
river system
infested
Jung & Blashke
Plant Pathology
2004
In Bavaria Jung and colleagues have
shown:
Initial P. alni damage almost exclusively
linked to introduction of infested stock from
nurseries into forest alder plantations
The pathogen then spread from the alder
plantations to the riparian alders along
Bavarian rivers
Similar surveys oak, beech and maple. Show spread of
Phytophthoras from nurseries to young plantations
Infested beech
seedlings
root
symptoms
from
nursery
to
plantation
Photos: Thomas Jung, Gunter Hartmann, Germany
To summarise (Phytophthoras only) – in Europe:
Many dangerous Phytophthoras ( .. P. ramorum,
P. kernoviae, P. lateralis, P. alni, P. niederhauseri, P.
inundata, P. citrophthora, P. hibernalis, P. tropicalis, P.
palmivora, P. hadraiandra, P. bisheria…) being
imported into Europe from other continents by
the international plant trade
Spread around Europe by the nursery industry
Introduced into gardens, forests and natural
ecosystems
Planting stock for forests often leaves
European nurseries already contaminated
by Phytophthoras (Jung et al, in press)
To summarise (Phytophthoras only) – in Europe:
Many dangerous Phytophthoras such as P. ramorum,
P. kernoviae, P. lateralis, P. alni, P. niederhauseri, P.
inundata, P. citrophthora, P. hibernalis, P. tropicalis, P.
palmivora, P. hadraiandra, P. bisheria… are being
imported into Europe from other continents by the
international plant trade
Then spread around Europe on infested stock by the
nursery industry
Then introduced into gardens, forests and natural
ecosystems
Planting stock for forests
often
leaves
Bottom
line
is: European
nurseries already contaminated by Phytophthoras
These
Phytopthoras
should
not
be
present
(Jung information)
in Europe at all
Each of them represents a failure
of International - and European plant biosecurity
Basically Europe - meaning
especially the ‘older’ EU countries is now acting as an import,
distribution and export centre for
Phytophthora pathogens
But the European nursery situation is
a symptom
not the cause
and the problem is world wide
B. Why the growing threat?
Primarily an international biosecurity
protocol problem
Linked to the fact that when current
International Plant Health / IPPC / WTO
(now the ‘SPS’ agreement) regulations
were devised in the 1950s - the plant trade was not highly globalised.
Today the market is highly globalised Now, like some other global markets, the
protocols governing international plant trade
need a major overhaul –
to align them with modern scientific knowledge
to make them effective in the context of
expanding global trade
to control the growing environmental damage
Critiques – the scientific issue -
2003
2008
2004
My case is essentially an argument for science based International Plant Health (~SPS)
protocols
With caveats that in many countries Current SPS protocols are regulated and
operated to a good standard
The trade generally adhere to the
protocols
It’s the protocols themselves that are flawed
Look at some of the scientific and
operational flaws in International
Plant Health (~SPS) protocols:
Current SPS protocols are scientifically
flawed
1. Because they cover only named organisms
Yet - a significant proportion of current fungal
invaders of forests are organisms previously
unknown to science. (eg’s : Phytophthora
ramorum, P. alni, P. kernoviae, P. pinifolia ..)
Such ‘unknowns’ are not covered by the current
SPS protocols
How ‘big’ is the unknown pathogen problem?
eg. Phytophthoras?
How ‘big’ is the unknown pathogen problem?
eg. Phytophthoras?
From Brasier (2009)
?
140
130
120
Described species
110
100
90
Described Phytophthora
species over time
IUFRO
2007
80
70
60
Erwin & Ribeiro 1996
50
40
30
20
10
Waterhouse1963
Tucker 1931
DeBary
1876
0
1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010 2020
Year
Known species doubled since 1996 ..
I have estimated the number of extant
Phytophthora species to be 200 – 600
(Brasier 2009)
Taking the ~100 currently known species –
This suggests 100 - 500 unknown
Phytophthora species may still exist in
underexplored forests and natural
ecosystems …
Say 300 unknown species
The ‘Phytophthora invasives in waiting’ ?
Bla bla bla bla bla bla bla
Current SPS protocols scientifically
flawed
2. Because we usually regulate a pathogen
only after it has escaped its geographic
centre of origin and is causing damage in
a susceptible plant community
Whereas, scientifically, what we should do
is to prevent it from escaping in the first
place.
The 1950s SPS protocols were grew out of a
1780s ‘Linnean list-making’ taxonomic culture
They did not encompass the large numbers of
unescaped ‘unknown pathogens’ that, through
Darwinian co-evolution, were causing little
damage in their centres of origin.
Ergo: The SPS protocols are not biologically
- or evolutionary - process based:
They are non Darwinian
Not very smart 200 years after Darwin’s
birth?
A consequence is –
The ‘door’ is wide open to introduction and
spread, largely by the plant trade, of
scientifically unknown pathogens, such as
Phytophthoras, into nurseries
and then from nurseries into horticulture,
agriculture, or into the natural environment
Fundamentally, a recipe for bioinsecurity?
Problems with implementation of
regulations (EU)
Consignments often arrive with ‘pest free’
certificates yet are visibly infected
Weakest link syndrome –states with less
effective inspection regimes put other states
at risk
States do not report incursions by listed
pathogens
Or report too late, sometimes deliberately to
‘protect trade’.
We rely largely on visual inspection at
ports but –
We inspect only a tiny proportion of
imports (APHIS ~2%)
And even visually healthy looking plants
can have symptomless, dangerous
infections -
Both Phytophthora ramorum and P. kernoviae
exhibit asymptomatic sporulation on nursery stock
Sporangia of P.
ramorum on
asymptomatic
rhododendron
leaf
Photo – Sandra Denman Forest Research UK
Chlamydospore
of P. ramorum
in asymptomatic
rhododendron
root
Photo Marco Riedel, BBA Braunschweig, Germany
Infected but asymptomatic nursery stock
will be imported in this way And exported to uninfested areas
This could be how P. ramorum recently entered
the US. Or P. lateralis entered the UK ..
Modern plant trade is enhancing the risk
Increasing globalisation of trade ‘sucking in’ high
volume imports of plants
Modern plant trade is enhancing the risk
3 billion p a
- 3.0
Value $ millions
US imports
plants for
planting
1967
Year
Courtesy Kerry Briton USDA Forest Service. Briton et al in press
2009
Imported plants in billions
Increasing globalisation of trade ‘sucking in’ high
volume imports of plants
Modern plant trade is enhancing the risk
Many nurseries seriously infested eg.
Phytophthoras in EU, US. Already discussed.
Fungicides / pesticides often used to suppress
symptoms eg Phytophthora again.
‘Re-badging’ of stock, concealing country of
origin
Demand for instant woody landscapes
Current fashion for ‘instant landscaping’ –
resulting in inter- state shipment of semi
mature trees and shrubs
e.g. Large plane trees, olives, oaks,
cypresses, alders, figs, pines being
imported into UK from the EU and across
the world -
Alder
Cypress
Platanus
Olives
Photo PHSI Fera UK
Such large trees, often in original soil,
cannot be adequately inspected without
prolonged quarantine and a detailed
microbial analysis
Biologically, a highly irresponsible trade
In my view best prohibited as soon as
possible
Consequences for world plant heritage
Damaging, long term impact on the worlds
forests and plant heritage ..
Currently developed countries most affected
In future will affect the plant heritage of
developing countries –
e.g.
The unique plant floras of Yunnan, Chile
The forests of Nepal ..
We have sampled Nepalese forests, two expeditions -
2005: sampled remote
forests in western Nepal
Photos Forest Research UK
and University of Viterbo, Italy
2005: Sampled remote
forests in western Nepal
Found only two Phytophthora species.
A previously unknown forest
Phytophthora, P. himalsilva sp. nov.
– an “invasive in waiting”.
And P. plurivora.
Photos Forest Research UK and
University of Viterbo, Italy
Annapurna range
Everest range
Photos Forest
Research UK and
University of Viterbo, forests
Italy
2007:
Sampled
degraded
near Kathmandu
2007: Sampled degraded forests near Kathmandu
Photos Forest Research UK and University of Viterbo, Italy
2007: Sampled degraded forests near Kathmandu
Nine Phytophthora species found.
Including P. himalsilva and P. plurivora.
Plus: P. cinnamomi, P. drechsleri, P.cryptogea,
P. katsurae .. classic exotic, invasive
Phytophthoras
The growing environmental cost of introducing
contaminated nursery stock into Nepal;
and of increasing human disturbance
C. Solutions?
On a percentage scale I suggest the ‘risk level’
associated with importing plants under current
international protocols is 60 -100%.
We need to reduce this ‘risk’ to say 10% or
less.
How?
I am a researcher not a regulator. But I can
suggest some approaches.
1. Improving diagnosis at ports of entry, even with
molecular technology is, I believe, unlikely to be
the answer.
Just an attractive ‘figleaf’ for regulators.
We could still only inspect ~2% of imports.
And what about all those “unknown
pathogens” ?
We need to prevent escape of unknown pathogens
from their centres of origin
2. There is only one simple, scientifically low risk,
approach:
Import only small numbers of rooted plants or
cuttings under licence, quarantine them and
use them as “safe propagation” material
Allow licenced importation of seed or tissue
culture.
A “zero tolerance” approach that should
have been implemented in the 1950s?
3. Education blitz
Politicians, public, nursery men, plant
importers, horticulturalists, journalists,
foresters, conservationists, regulators
4. Improve publicity:
Publicise the true environmental and economic
costs of invasive pests and pathogens
Apply the ‘polluter pays’ principle
Certify plants in retail outlets as disease
free. Label with true geographic source and
method of production (cf. food labelling)
5. Improve biosecurity intelligence:
Search for unknown pathogens in
underexplored ecosystems.
6. Make plant biosecurity a two-way process
Currently, nation states are fixated on
preventing pathogen entry
They should be required to be equally
fixated on preventing export of pathogens
Thank
You