Climate change or tree disease: challenges for diagnosing causes of forest die-off
George Matusick A * , Katinka X. Ruthrof A B , Peter Scott C and Giles E. St. J. Hardy AA
B
C
Australian Journal of Botany - https://doi.org/10.1071/BT23039
Submitted: 14 May 2023 Accepted: 10 October 2023 Published online: 6 November 2023
Abstract
Forest ecosystems experience compositional and structural changes as species’ environmental envelopes shift with climate change. Extreme climate events and pests/pathogens are driving these ecosystem changes. Determining which of the two potential drivers is causing a particular forest die-off can be challenging. In south-western Australia, widespread forest die-off in 2011 coincided with extremely hot and dry conditions. It occurred in a forest ecosystem that has historically experienced Phytophthora cinnamomi root disease (Phytophthora dieback).
To determine whether the causal agent of Phytophthora dieback, P. cinnamomi, was associated with forest die-off in the Northern Jarrah Forest.
A combination of direct (isolation of pathogen) and indirect (survey of susceptible indicator plant species) measurements were taken inside and outside patches of forest experiencing the die-off.
There was no consistent association between die-off patches and the presence of P. cinnamomi. P. cinnamomi was isolated from 3 of 33 control plots and 3 of 33 die-off plots. Although several plant species susceptible to P. cinnamomi were absent from die-off plots, the findings were inconsistent across species. This may be explained by plant tolerance to high temperatures and drought.
P. cinnamomi was not the proximate cause of the observed die-off in the Northern Jarrah Forest in 2011.
Novel disturbance caused by extreme climate events can mimic damage caused by certain pests/pathogens. More research is needed to determine the tolerances of plants to extreme temperature and drought conditions to disentangle abiotic and biotic drivers of tree die-off.
Keywords: climate change, drought, eucalypt dieback, Eucalyptus marginata, extreme climate event, jarrah, Phytophthora cinnamomi, Phytophthora dieback.
References
Aghighi S, Burgess TI, Scott JK, Calver M, Hardy GESJ (2016) Isolation and pathogenicity of Phytophthora species from declining Rubus anglocandicans. Plant Pathology 65, 451-461.
| Crossref | Google Scholar |
Aguayo J, Elegbede F, Husson C, Saintonge F-X, Marçais B (2014) Modeling climate impact on an emerging disease, the Phytophthora alni-induced alder decline. Global Change Biology 20, 3209-3221.
| Crossref | Google Scholar | PubMed |
Anadón JD, Sala OE, Maestre FT (2014) Climate change will increase savannas at the expense of forests and treeless vegetation in tropical and subtropical Americas. Journal of Ecology 102, 1363-1373.
| Crossref | Google Scholar |
Andrew ME, Ruthrof KX, Matusick G, Hardy GESJ (2016) Spatial configuration of drought disturbance and forest gap creation across environmental gradients. PLoS ONE 11, e0157154.
| Crossref | Google Scholar | PubMed |
Andrich MA, Imberger J (2013) The effect of land-water contrast on the sensitivity of the regional climate of south-west Western Australia to changes in background climate conditions. Climate Dynamics 41, 875-895.
| Google Scholar |
Beckage B, Osborne B, Gavin DG, Pucko C, Siccama T, Perkins T (2008) A rapid upward shift of a forest ecotone during 40 years of warming in the Green Mountains of Vermont. Proceedings of the National Academy of Sciences 105, 4197-4202.
| Crossref | Google Scholar |
Bergot M, Cloppet E, Pérarnaud V, Déqué M, Marçais B, Desprez-Loustau M-L (2004) Simulation of potential range expansion of oak disease caused by Phytophthora cinnamomi under climate change. Global Change Biology 10, 1539-1552.
| Crossref | Google Scholar |
Bowman KD, Albrecht U, Graham JH, Bright DB (2007) Detection of Phytophthora nicotianae and P. palmivora in citrus roots using PCR–RFLP in comparison with other methods. European Journal of Plant Pathology 119, 143-158.
| Crossref | Google Scholar |
Bradshaw FJ (1999) Trends in silvicultural practices in the native forests of Western Australia. Australian Forestry 62, 255-264.
| Crossref | Google Scholar |
Breshears DD, Fontaine JB, Ruthrof KX, Field JP, Feng X, Burger JR, Law DJ, Kala J, Hardy GESJ (2021) Underappreciated plant vulnerabilities to heat waves. New Phytologist 231, 32-39.
| Crossref | Google Scholar | PubMed |
Brouwers N, Matusick G, Ruthrof K, Lyons T, Hardy G (2013) Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem. Landscape Ecology 28, 69-80.
| Crossref | Google Scholar |
Burgess TI, Webster JL, Ciampini JA, White D, Hardy GESJ, Stukely MJC (2009) Re-evaluation of Phytophthora species isolated during 30 years of vegetation health surveys in Western Australia using molecular techniques. Plant Disease 93, 215-223.
| Crossref | Google Scholar | PubMed |
Burgess TI, Scott JK, McDougall KL, Stukely MJC, Crane C, Dunstan WA, Brigg F, Andjic V, White D, Rudman T, Arentz F, Ota N, Hardy GESJ (2017) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Global Change Biology 23, 1661-1674.
| Crossref | Google Scholar | PubMed |
Burgess TI, López-Villamor A, Paap T, Williams B, Belhaj R, Crone M, Dunstan W, Howard K, Hardy GESJ (2021) Towards a best practice methodology for the detection of Phytophthora species in soils. Plant Pathology 70, 604-614.
| Crossref | Google Scholar |
Cho JJ (1983) Variability in susceptibility of some Banksia species to Phytophthora cinnamomi and their distribution in Australia. Plant Disease 67, 869-871.
| Crossref | Google Scholar |
Close DC, Davidson NJ, Johnson DW, Abrams MD, Hart SC, Lunt ID, Archibald RD, Horton B, Adams MA (2009) Premature decline of Eucalyptus and altered ecosystem processes in the absence of fire in some Australian forests. The Botanical Review 75, 191-202.
| Crossref | Google Scholar |
Colquhoun IJ, Hardy GESJ (2000) Managing the risks of Phytophthora root and collar rot during bauxite mining in the Eucalyptus marginata (Jarrah) forest of Western Australia. Plant Disease 84, 116-127.
| Crossref | Google Scholar | PubMed |
Corcobado T, Cubera E, Juárez E, Moreno G, Solla A (2014) Drought events determine performance of Quercus ilex seedlings and increase their susceptibility to Phytophthora cinnamomi. Agricultural and Forest Meteorology 192-193, 1-8.
| Crossref | Google Scholar |
Cudmore TJ, Björklund N, Carroll AL, Staffan Lindgren B (2010) Climate change and range expansion of an aggressive bark beetle: evidence of higher beetle reproduction in naïve host tree populations. Journal of Applied Ecology 47, 1036-1043.
| Crossref | Google Scholar |
Dakin N, White D, Hardy GESJ, Burgess TI (2010) The opportunistic pathogen, Neofusicoccum australe, is response for crown dieback of peppermint (Agonis flexuosa) in Western Australia. Australasian Plant Pathology 39, 202-206.
| Crossref | Google Scholar |
Davison EM (2015) How Phytophthora cinnamomi became associated with the death of Eucalyptus marginata – the early investigations into jarrah dieback. Australasian Plant Pathology 44, 263-271.
| Crossref | Google Scholar |
Davison EM (2018) Relative importance of site, weather and Phytophthora cinnamomi in the decline and death of Eucalyptus marginata – jarrah dieback investigations in the 1970s to 1990s. Australasian Plant Pathology 47, 245-257.
| Crossref | Google Scholar |
Davison EM, Tay FCS (1985) The effect of waterlogging on seedlings of Eucalyptus marginata. New Phytologist 101, 743-753.
| Crossref | Google Scholar |
Davison EM, Tay FCS (1987) The effect of waterlogging on infection of Eucalyptus marginata seedlings by Phytophthora cinnamomi. New Phytologist 105, 585-594.
| Crossref | Google Scholar |
de Sampaio e Paiva Camilo-Alves C, da Clara MIE, de Almeida Ribeiro NMC (2013) Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. European Journal of Forest Research 132, 411-432.
| Crossref | Google Scholar |
Dell B, Bartle JR, Tacey WH (1983) Root occupation and root channels of jarrah forest subsoils. Australian Journal of Botany 31(6), 615-627.
| Crossref | Google Scholar |
Dell B, Hardy GESJ, Vear K (2005) History of Phytophthora cinnamomi management in Western Australia. In ‘A Forest Conscienceness: Proceedings 6th National Conference of the Australian Forest History Society’. (Eds MC Calver, H Bigler-Cole, G Bolton, J Dargavel, A Gaynor, P Horwitz, J Mills, G Wardell-Johnston) pp. 391–406. (Millpress Science Publishers: Rotterdam, Netherlands)
Delworth TL, Zeng F (2014) Regional rainfall decline in Australia attributed to anthropogenic greenhouse gases and ozone levels. Nature Geoscience 7, 583-587.
| Crossref | Google Scholar |
Dukes JS, Pontius J, Orwig D, Garnas JR, Rodgers VL, Brazee N, Cooke B, Theoharides KA, Stange EE, Harrington R, Ehrenfeld J, Gurevitch J, Lerdau M, Stinson K, Wick R, Ayres M (2009) Responses of insect pests, pathogens, and invasive plant species to climate change in the forests of northeastern North America: what can we predict? Canadian Journal of Forest Research 39, 231-248.
| Crossref | Google Scholar |
Dunstan WA, Rudman T, Shearer BL, Moore NA, Paap T, Calver MC, Dell B, Hardy GESJ (2010) Containment and spot eradication of a highly destructive, invasive plant pathogen (Phytophthora cinnamomi) in natural ecosystems. Biological Invasions 12, 913-925.
| Crossref | Google Scholar |
Foster SD, Griffin DA, Dunstan PK (2014) Twenty years of high-resolution sea surface temperature imagery around Australia: inter-annual and annual variability. PLoS ONE 9, e100762.
| Crossref | Google Scholar |
Groves E, Hollick P, Hardy G, McComb J (2009) Appendix 2 Western Australian natives susceptible to Phytophthora cinnamomi. Murdoch University, WA, Australia. Available at https://www.cpsm-phytophthora.org/downloads/natives_susceptible.pdf [Accessed 28 October 2023]
Hansen EM (2015) Phytophthora species emerging as pathogens of forest trees. Current Forestry Reports 1, 16-24.
| Crossref | Google Scholar |
Hardy GEStJ, Vear K, O’Gara E, Williams NM (2007) Detection, diagnosis and mapping of native areas infested by Phytophthora species in Western Australia. Brazilian Phytopathology 32, S45-S46.
| Google Scholar |
Hill TCJ (1990) Dieback diseases and other Phytophthora spp. in the Northern Kwongon. In ‘Nature, conservation, landscape and recreational values of the Lesueur area. A report to the Environmental Protection Authority from the Department of Conservation and Land Management’. (Eds A Burbidge, SD Hopper, S van Leeuwen) pp. 89–97. (EPA: WA, Australia)
Homet P, González M, Matías L, Godoy O, Pérez-Ramos IM, García LV, Gómez-Aparicio L (2019) Exploring interactive effects of climate change and exotic pathogens on Quercus suber performance: damage caused by Phytophthora cinnamomi varies across contrasting scenarios of soil moisture. Agricultural and Forest Meteorology 276-277, 107605.
| Crossref | Google Scholar |
Hooper RJ, Sivasithamparam K (2005) Characterization of damage and biotic factors associated with the decline of Eucalyptus wandoo in southwest Western Australia. Canadian Journal of Forest Research 35, 2589-2602.
| Crossref | Google Scholar |
Hope P, Abbs D, Bhend J, Chiew F, Church J, Ekström M, Kirono D, Lenton A, Lucas C, McInnes K, Moise A, Monselesan D, Mpelasoka F, Timbal B, Webb L, Whetton P (2015) Southern and south-western flatlands cluster report, climate change in Australia projections for Australia’s natural resource management regions: cluster reports. CSIRO and Bureau of Meteorology, Australia.
Hüberli D, Tommerup IC, Hardy GESJ (2000) False-negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Australasian Plant Pathology 29, 164-169.
| Crossref | Google Scholar |
Ikegami M, Jenkins TAR (2018) Estimate global risks of a forest disease under current and future climates using species distribution model and simple thermal model – Pine Wilt disease as a model case. Forest Ecology and Management 409, 343-352.
| Crossref | Google Scholar |
Jurskis V, Turner J (2002) Eucalypt dieback in eastern Australia: a simple model. Australian Forestry 65, 87-98.
| Crossref | Google Scholar |
Koch JM (2007) Alcoa’s mining and restoration process in south western Australia. Restoration Ecology 15, S11-S16.
| Crossref | Google Scholar |
La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, Von Weissenberg K (2008) Forest pathogens with higher damage potential due to climate change in Europe. Canadian Journal of Plant Pathology 30, 177-195.
| Crossref | Google Scholar |
Liu N, Harper RJ, Smettem KRJ, Dell B, Liu S (2019) Responses of streamflow to vegetation and climate change in southwestern Australia. Journal of Hydrology 572, 761-770.
| Crossref | Google Scholar |
Matusick G, Ruthrof KX, Hardy GSJ (2012) Drought and heat triggers sudden and severe dieback in a dominant mediterranean-type woodland species. Open Journal of Forestry 2, 183-186.
| Crossref | Google Scholar |
Matusick G, Ruthrof KX, Brouwers NC, Dell B, Hardy GSJ (2013) Sudden forest canopy collapse corresponding with extreme drought and heat in a mediterranean-type eucalypt forest in southwestern Australia. European Journal of Forest Research 132, 497-510.
| Crossref | Google Scholar |
Matusick G, Ruthrof KX, Kala J, Brouwers NC, Breshears DD, Hardy GESJ (2018) Chronic historical drought legacy exacerbates tree mortality and crown dieback during acute heatwave-compounded drought. Environmental Research Letters 13, 095002.
| Crossref | Google Scholar |
McCredie TA, Dixon KW, Sivasithamparam K (1985) Variability in the resistance of Banksia L. f. species to Phytophthora cinnamomi Rands. Australian Journal of Botany 33, 629-637.
| Crossref | Google Scholar |
McDougall KL, Hardy GESJ, Hobbs RJ (2002) Distribution of Phytophthora cinnamomi in the northern jarrah (Eucalyptus marginata) forest of Western Australia in relation to dieback age and topography. Australian Journal of Botany 50, 107-114.
| Crossref | Google Scholar |
McDougall KL (2005) The responses of native Australian plant species to Phytophthora cinnamomi. Appendix 4. In ‘Management of Phytophthora cinnamomi for biodiversity conservation in Australia: Part 2. National best practice’. (Eds E O’Gara, K Howard, B Wilson, GESJ Hardy) pp. 1–52. (Department of the Environment and Heritage: Canberra, ACT, Australia)
McFarlane D, George R, Ruprecht J, Charles S, Hodgson G (2020) Runoff and groundwater responses to climate change in South West Australia. Journal of the Royal Society of Western Australia 103, 9-27.
| Google Scholar |
McGrath G, Fontaine JB, Van Dongen R, Hyde J, Leopold M, Matusick G, Ruthrof KX (2023) Geophysics reveals forest vulnerability to drought. Ecohydrology
| Crossref | Google Scholar |
Mitton JB, Ferrenberg SM (2012) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. The American Naturalist 179, E163-E171.
| Crossref | Google Scholar | PubMed |
Navarro-Cerrillo RM, González-Moreno P, Ruiz-Gómez FJ, Sánchez-Cuesta R, Gazol A, Camarero JJ (2022) Drought stress and pests increase defoliation and mortality rates in vulnerable Abies pinsapo forests. Forest Ecology and Management 504, 119824.
| Crossref | Google Scholar |
Negrón JF, McMillin JD, Anhold JA, Coulson D (2009) Bark beetle-caused mortality in a drought-affected ponderosa pine landscape in Arizona, USA. Forest Ecology and Management 257, 1353-1362.
| Crossref | Google Scholar |
Paap T, Brouwers NC, Burgess TI, Hardy GESJ (2017) Importance of climate, anthropogenic disturbance and pathogens (Quambalaria coyrecup and Phytophthora spp.) on marri (Corymbia calophylla) tree health in southwest Western Australia. Annals of Forest Science 74, 62.
| Crossref | Google Scholar |
Podger FD (1972) Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology 62, 972-981.
| Crossref | Google Scholar |
Ritchie AL, Svejcar LN, Ayre BM, Bolleter J, Brace A, Craig MD, Davis B, Davis RA, van Etten EJB, Fontaine JB, Fowler WM, Froend RH, Groom C, Hardy GESJ, Hooper P, Hopkins AJM, Hughes M, Krauss SL, Leopold M, Miller BP, Miller RG, Ramalho CE, Ruthrof KX, Shaw C, Stevens JC, Tangney R, Valentine LE, Veneklaas EJ, Hobbs RJ (2021) A threatened ecological community: research advances and priorities for Banksia woodlands. Australian Journal of Botany 69, 53-84.
| Crossref | Google Scholar |
Ruthrof KX, Breshears DD, Fontaine JB, Froend RH, Matusick G, Kala J, Miller BP, Mitchell PJ, Wilson SK, van Keulen M, Enright NJ, Law DJ, Wernberg T, Hardy GESJ (2018) Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses. Scientific Reports 8, 13094.
| Crossref | Google Scholar | PubMed |
Schut AGT, Wardell-Johnson GW, Yates CJ, Keppel G, Baran I, Franklin SE, Hopper SD, Van Niel KP, Mucina L, Byrne M (2014) Rapid characterization of vegetation structure to predict refugia and climate change impacts across a global biodiversity hotspot. PLoS ONE 9, e82778.
| Crossref | Google Scholar | PubMed |
Sena K, Crocker E, Vincelli P, Barton C (2018) Phytophthora cinnamomi as a driver of forest change: implications for conservation and management. Forest Ecology and Management 409, 799-807.
| Crossref | Google Scholar |
Shaw JD, Steed BE, DeBlander LT (2005) Forest inventory and analysis (FIA) annual inventory answers the question: what is happening to Pinyon–Juniper woodlands? Journal of Forestry 103, 280-285.
| Google Scholar |
Shearer BL, Crane CE (2014) Phytophthora cinnamomi disease expression and habitat suitability of soils on a topographic gradient across a coastal plain from dunes to forested peneplain. Australasian Plant Pathology 43, 131-142.
| Crossref | Google Scholar |
Shearer BL, Dillon M (1995) Susceptibility of plant species in Eucalyptus marginata forest to infection by Phytophthora cinnamomi. Australian Journal of Botany 43, 113-134.
| Crossref | Google Scholar |
Shearer BL, Dillon M (1996) Impact and disease centre characteristics of Phytophthora cinnamomi infestations of Banksia woodlands on the Swan Coastal Plain, Western Australia. Australian Journal of Botany 44, 79-90.
| Crossref | Google Scholar |
Shearer BL, Crane CE, Cochrane A (2004) Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Australian Journal of Botany 52, 435-443.
| Crossref | Google Scholar |
Shearer BL, Crane CE, Barrett S, Cochrane A (2007) Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55, 225-238.
| Crossref | Google Scholar |
Spencer RD (1984) Detecting dieback in native eucalypt forests using aerial photographs. Australian Forestry 47, 243-249.
| Crossref | Google Scholar |
Steel EJ, Fontaine JB, Ruthrof KX, Burgess TI, Hardy GESJ (2019) Changes in structure of over- and midstory tree species in a Mediterranean-type forest after an extreme drought-associated heatwave. Austral Ecology 44, 1438-1450.
| Crossref | Google Scholar |
Sturrock RN, Frankel SJ, Brown AV, Hennon PE, Kliejunas JT, Lewis KJ, Worrall JJ, Woods AJ (2011) Climate change and forest diseases. Plant Pathology 60, 133-149.
| Crossref | Google Scholar |
Taylor AR, Boulanger Y, Price DT, Cyr D, McGarrigle E, Rammer W, Kershaw JA, Jr. (2017) Rapid 21st century climate change projected to shift composition and growth of Canada’s Acadian Forest Region. Forest Ecology and Management 405, 284-294.
| Crossref | Google Scholar |
Tesky R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment 38, 1699-1712.
| Crossref | Google Scholar |
Timbal B, Arblaster JM, Power S (2006) Attribution of the late-twentieth-century rainfall decline in southwest Australia. Journal of Climate 19, 2046-2062.
| Crossref | Google Scholar |
Titze JF, Palzer CR (1969) Host list of Phytophthora cinnamomi Rands with special reference to Western Australia. Forestry and Timber Bureau, Department of National Development. Technical. Note No. 1.
| Google Scholar |
Tsao PH (1990) Why many phytophthora root rots and crown rots of tree and horticultural crops remain undetected. EPPO Bulletin 20, 11-17.
| Crossref | Google Scholar |
Wentzel JJ, Craig MD, Barber PA, Hardy GESJ, Fleming PA (2018) Tuart (Eucalyptus gomphocephala) decline is not associated with other vegetation structure and composition changes. Australasian Plant Pathology 47, 521-530.
| Crossref | Google Scholar |
Wills RT (1993) The ecological impact of Phytophthora cinnamomi in the Stirling Range National Park, Western Australia. Australian Journal of Ecology 18, 145-159.
| Crossref | Google Scholar |
Wilson BA, Zdunic K, Kinloch J, Behn G (2012) Use of remote sensing to map occurrence and spread of Phytophthora cinnamomi in Banksia woodlands on the Gnangara Groundwater System, Western Australia. Australian Journal of Botany 60, 495-505.
| Crossref | Google Scholar |
Withers PC (2000) Overview of granite outcrops in Western Australia. Journal of the Royal Society of Western Australia 83, 103-108.
| Google Scholar |