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The definitive version is available at
http://dx.doi.org/10.1111/gcb.13492
Burgess, T.I., Scott, J.K., McDougall, K.L., Stukely, M.J.C., Crane,
C., Dunstan, W.A., Brigg, F., Andjic, V., White, D., Rudman, T.,
Arentz, F., Ota, N. and Hardy, G.E.St.J. (2017) Current and
projected global distribution of Phytophthora cinnamomi, one of
the world's worst plant pathogens. Global Change Biology,
23 (4). pp. 1661-1674.
http://researchrepository.murdoch.edu.au/34826/
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Accepted Article
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been through the copyediting, typesetting, pagination and proofreading process, which may
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doi: 10.1111/gcb.13492
This article is protected by copyright. All rights reserved.
Received Date : 01-Mar-2016
Accepted Date : 13-Aug-2016
Article type : Primary Research Articles
Title Page
Current and projected global distribution of Phytophthora cinnamomi, one
of the world’s worst plant pathogens
Running Head: Climate change and Phytophthora cinnamomi
TREENA I. BURGESS
1
, JOHN K. SCOTT
2
, KEITH L. McDOUGALL
3
, MICHAEL J. C.
STUKELY
4
, COLIN CRANE
4
, WILLIAM A. DUNSTAN
1
, FRANCES BRIGG
5
, VERA
ANDJIC
1
, DIANE WHITE
1
, TIM RUDMAN
6
, FRANS ARENTZ
7
, NOBORU OTA
8
,
GILES E. St.J. HARDY
1
1
Centre for Phytophthora Science and Management, School of Veterinary and Life Sciences, Murdoch
University, Murdoch, 6150, Australia
2
School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009,
Australia and CSIRO Land and Water, Private Bag 5, P.O. Wembley, W.A. 6913, Australia
3
Department of Ecology, Environment and Evolution, La Trobe University, PO Box 821, Wodonga, Victoria,
3689, Australia
4
Vegetation Health Service, Department of Parks and Wildlife, Locked Bag 104, Bentley Delivery Centre, WA
6983, Australia
5
State Agriculture and Biotechnology Institute, School of Veterinary and Life Sciences, Murdoch University,
Perth, 6150, Australia
6
Department of Primary Industries, Parks, Water and Environment, Hobart, Tas. 7000, Australia
7
RN 23R McLean Rd, Yungaburra, Qld, 4884, Australia
8
CSIRO Agriculture, Private Bag 5, P.O. Wembley, W.A. 6913, Australia
Corresponding author: Treena Burgess, tel. +61 89360 7537, fax. +61 89360 6303, e-mail:
tburgess@murdoch.edu.au
Keywords: climate change, soil pH, high throughput sequencing, plant disease, natural
ecosystem
Type of Paper: Original Research
Accepted Article
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Abstract
Globally, Phytophthora cinnamomi is listed as one of the 100 worst invasive alien species
and active management is required to reduce impact and prevent spread in both horticulture
and natural ecosystems. Conversely, there are regions thought to be suitable for the pathogen
where no disease is observed. We developed a CLIMEX model for the global distribution of
P. cinnamomi based on the pathogen’s response to temperature and moisture and by
incorporating extensive empirical evidence on the presence and absence of the pathogen. The
CLIMEX model captured areas of climatic suitability where P. cinnamomi occurs that is
congruent with all available records. The model was validated by the collection of soil
samples from asymptomatic vegetation in areas projected to be suitable by the model for
which there were few records. DNA was extracted and the presence or absence of P.
cinnamomi determined by high throughput sequencing (HTS). While not detected using
traditional isolation methods, HTS detected P. cinnamomi at higher elevations in eastern
Australia and central Tasmania as projected by the CLIMEX model. Further support for the
CLIMEX model was obtained by using the large dataset from southwest Australia where the
proportion of positive records in an area is related to the Ecoclimatic Index value for the
same area. We provide for the first time a comprehensive global map of the current P.
cinnamomi distribution, an improved CLIMEX model of the distribution, and a projection to
2080 of the distribution with predicted climate change. This information provides the basis
for more detailed regional scale modelling and supports risk assessment for governments to
plan management of this important soil-borne plant pathogen.
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Introduction
Worldwide, Phytophthora cinnamomi Rands is one of the most devastating plant pathogens,
infecting a wide range of trees, woody shrubs and herbs (Cahill et al., 2008; Weste & Marks,
1987; Zentmyer, 1980). The Global Invasive Species Database (http://www.issg.org) lists it
as one of the 100 worst invasive alien species, and it is the only Oomycete, and one of only
three plant pathogens listed (Lowe et al., 2000). Although, the origin of P. cinnamomi
remains uncertain, most evidence points to a natural distribution in mountainous regions in
south-east Asia, i.e. in a temperate climate within the tropics (Arentz & Simpson, 1986; Jung
et al., 2016; Ko et al., 1978; Martin & Coffey, 2012). Phytophthora cinnamomi was first
described as the causal agent of stripe canker of cinnamon (Cinnamomum burmannii) in
Sumatra (Rands, 1922). However, it is now known to have been the causal agent of ink
disease of European chestnut, first reported in 1860 (Grente, 1961), and also of American
chestnuts (Castanea dentata) prior to 1910 (Anagnostakis, 2001; Crandall et al., 1945).
While P. cinnamomi can be a destructive pathogen globally in tropical and sub-tropical
agriculture (Drenth & Guest, 2004), it is in ecosystems with a Mediterranean-type climate
where it has its biggest impact. Phytophthora cinnamomi causes root rot and decline in the
fynbos in the Cape Floristic Region of South Africa (Nagel et al., 2013; Von Broembsen &
Kruger, 1985). It is the dominant causal biotic agent in oak decline in Mediterranean Europe
(Brasier et al., 1993; Robin et al., 1998; Vettraino et al., 2002) and is also associated with
oak disease in California (Garbelotto et al., 2006). In the South-West Botanical Province of
Western Australia (WA), an estimated 40% of the 5710 plant species, are susceptible to P.
cinnamomi, including 14% considered highly susceptible (Shearer et al., 2007). Given that P.
cinnamomi is an Oomycete and free water is required for infection by zoospores, it is perhaps
surprising that Mediterranean ecosystems are the most affected. However, the relatively
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warm and wet winter and spring conditions are ideal for zoospore proliferation and host
infection, while the long dry summers place plants, with compromised root or vascular
systems, at risk of drought-induced mortality (Brasier, 1996; Desprez-Loustau et al., 2006;
Shearer & Tippett, 1989).
As P. cinnamomi has been transported globally with horticultural (perennial fruit, spice and
nut crops), and has subsequently become invasive in many natural ecosystems, it would be
very useful to predict parts of the globe where it might occur now and into the future. This
would enable preventative measures to be implemented. Species distribution models (SDM)
of invasive species can be poor if the organism is capable of invading new environments
extending beyond the known niche of the species in its native range (Gallien et al., 2010;
Webber et al., 2011). Additionally, as demonstrated for Phytophthora ramorum, an invasive
species in North America and Europe, SDMs generated early in an invasion (2001) are less
accurate than later models after the pathogen was closer to equilibrium (2009) (Václavík &
Meentemeyer, 2012). However, the biology of P. cinnamomi is well known, and the species
has a global distribution where it has been invasive for at least 100 years (Anonymous, 2015).
Additionally, there are extensive distribution records available, especially across a wide range
of climates in Australia where pathogen distribution has been well delineated, and is stable,
representing an equilibrium situation. For these reasons, it is possible to develop a robust
global species distribution model for P. cinnamomi.
Various modelling approaches have been used previously to estimate the potential
distribution of P. cinnamomi in Europe (Brasier & Scott, 1994), France (Bergot et al., 2004;
Desprez-Loustau et al., 2007), south-western Spain and south-western Australia (Duque-
Lazo et al., 2016) and south-western USA (Thompson et al., 2014). Here we produce, for the
first time, a global niche model for P. cinnamomi using a large empirical data set on the
