Tracing the role of human civilization in the globalization of plant pathogens. Alberto Santini

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1 Tracing the role of human civilization in the globalization of plant pathogens Alberto Santini Andrew Liebhold, Duccio Migliorini and Steve Woodward

2 Co-evolution between plants and parasites generated much of earth s biodiversity

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5 Exponential increase in establishment of forest pathogens updated from Santini et al., 2013 New Phytologist, 197:

6 Mid-Holocene Elm and Hemlock Decline Clark and Edwards, J Quat Sci 19: Ellison et al Ecology 67:

7 Evidence offered in support of fungal diseases and/or insect infestations being contributory factors in the mid-holocene declines of hemlock (Tsuga) and elm (Ulmus) pollen. 1. The apparent synchronicity of the events across broad geographical regions. 2. The rapidity of the declines in Tsuga and Ulmus pollen values, as recorded at sites where high-precision dating evidence is available 3. The long-term impact on the abundance of hemlock and elm. However, it should be noted that the late Holocene abundance of elm in Europe is likely to have been heavily influenced by human activity. 4. Fossil evidence for the contemporaneous presence of phytophagous insects. 5. Modern outbreaks of virulent strains of fungal pathogens (e.g. Chestnut blight, Dutch elm disease) have produced pollen stratigraphic signatures comparable to the mid-holocene declines. 6. The continued abundance of elm at a site in western Ireland through into the late-holocene, despite evidence of localized disturbance due to human activity in the mid-holocene. The pathogen, vector or the tree was less susceptible near to the margins of the range of elm. Waller, 2013 J Quat Sci. 28:

8 Archeophytes vs. Neophytes Cristoforo Colombo 1492 Discovery of America by Europeans

9 Before 7000 B.C B.C B.C B.C B.C. Santini et al., 2018, mod. from Cavalli-Sforza and Feldman, Nat Gen 33: modified from Zohary and Hopf, 1993

10 Ulmus procera Salisb. English?????? elm

11 Stevens et al., The Holocene 26:

12 Stukenbrock et al., Mol. Ecol. 15: Phaeosphaeria nodorum

13 Origin of the most important crops Khoury et al Proc Biol Sci 283(1832):

14 Main Famines in the last 200 years Country Year Name Pathogen Host Ireland Late potato blight Phytophthora infestans Potato France Powdery and Downy mildew Erysiphe necator, Plasmopara viticola Grape Ceylon 1870s Coffee rust Hemileia vastatrix Coffee Central America early 1900s Fusarium wilts of cotton and flax Fusarium oxysporum Cotton and Flax Central America early 1900s Southern bacterial wilt of tobacco Ralstonia solanacearum Tobacco Central America Sigatoka leaf spot Mycosphaerella musicola Banana Central America Panama disease of banana Fusarium oxysporum Banana Bengal Brown spot of rice Bipolaris oryzae Rice Rwanda-Burundi Ruzagayura famine P. infestans, Rhizoctonia solani Potatoes, Cassava and Sweet potatoes USA 1916, 1935, Black stem rust of wheat Puccinia graminis Wheat USA 1970 Southern corn leaf blight Bipolaris maydis Corn Africa 1975 Groundnut rosette virus Groundnut rosette virus (GRV) Groundnut (peanut) Santini et al., 2018, ISME journal 12:

15 Main drivers of the increase in arrivals of alien pests and pathogens 1819 First steamboat crossed Atlantic Ocean SS. Savannah

16 The world's first purpose-built containership, the Clifford J. Rogers. Photo credits Canadian shipper online Porttechnology.org

17 Santini et al., 2018, ISME journal 12:

18 Main drivers of the increase in arrivals of alien pests and pathogens 1945 End of WWII and rise in trade between North America, Europe, and Asia Yalta Conference, February 4-11, 1945

19 Main drivers of the increase in arrivals of alien pests and pathogens 1989 Fall of Berlin wall and onset of globalisation era

20 Temporal changes in origin of forest pathogens established in Europe Africa Asia Australasia Europe South America Temp N America Trop N America Hybrid Seiridium cardinale; Ceratocystis platani; Heterobasidion irregulare updated from Santini et al., 2013 New Phytologist, 197:

21 Costa Rica Oceania Australia South Africa Santini et al., 2018, ISME journal 12: EU Kenya New Zealand Israel USA China

22 Eschen et al., 2017 Biol Invasions DOI /s origin diversity of genera

23 Regulations of trade: International Convention on Measures against Phylloxera vastatrix; USA Quarantine act; USA Quarantine General Agreement on Tariffs and Trade; GATT promoted Agreement on Application of Sanitary and Phytosanitary Measures (SPS Agreement); International Plant Protection Convention (IPPC)

24 Take Home Messages Scientific: - we need more integration among invasion biology, history and sociology to understand the phenomenon and to make long-term and large-scale forecasts What we understood so far is that the solution doesn't lie in Politics: halting the trend of globalization, which is neither realistic nor -desirable, we need because more integration there are also between positive scientists aspects and in policy it, but makers, to better capitalize in order scientific to give birth knowledge. to a "scientific knowledge based policy" which allow globalization to proceed while, simultaneously, minimize the spread of plant pathogens, thus preventing further economic and ecological disasters.