INSECT PESTS IN TUSCAN UNDER CLIMATE CHANGES Patrizia Sacchetti1, Bruno Bagnoli2, Marzia Cistiana Rosi1, Antonio Belcari1

1 Department of Agriculture, Food, Environment and Forestry, Florence University 2 Department for Innovation in Biological Agro-Food and Forest Systems (DIBAF), Tuscia University

This project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement nº 810176. This document reflects only the author’s view and the Commission is not responsible for any use that may be made of the information it contains. 1 Contents

Part 1 – Overview of abiotic factors influence on

Part 2 – Main pests in Tuscan vineyards

Part 3 – Case study: the

2 2 Overview of abiotic factors influence on insects

Main abiotic factors are:

Temperature Relative Humidity Rain Wind Soil

3 3 Part 1 – Overview of abiotic factors influence on insects

Effect of temperature on insects

Insects are poikilothermic

«Insect growth is faster as the temperature increases, up to the minimum, after which development slows for lethal temperature»

10 20 30 40 (From Wilson and Barnett, 1983) °C

4 4 Part 1 – Overview of abiotic factors influence on insects

Temperature-dependent growth is useful for modelling...

Thc = Thermal constant (thermal summation, °D) c = lower thermal threshold (developmental zero)

(T max + T min) °D = - c 2

5 5 Part 1 – Overview of abiotic factors influence on insects

Example: the olive fly, Bactrocera oleae

Thc = 379.015 °D

c = 8.99 °C

6 6 Part 1 – Overview of abiotic factors influence on insects

Maps of «dacic» risk 1956-1986

7 7 Part 1 – Overview of abiotic factors influence on insects

Maps of «dacic» risk 1970-2000

8 8 Part 1 – Overview of abiotic factors influence on insects

Maps of «dacic» risk 2010-2017

9 9 Part 1 – Overview of abiotic factors influence on insects

Grape in Spain

Changes in spring adult emergence and number of generations per year

(From Gutierrez et al., 2018)

1010 Part 2 – Main insect pests in Tuscan vineyards

2012 2016

150 insect pests of vineyards …in Italy about 50 insect pests, listed in the world…. although only a few species have economic importance 1111 Part 2 – Main insect pests in Tuscan vineyards

Leafhoppers (Hemiptera Cicadellidae)

Subfamily: Typhlocybinae:

1) Zygina rhamni Ferrari 2) Empoasca (Göthe) 3) Jacobiasca lybica (Bg. & Zanon) 2 Subfamily : Deltocephalinae 4) Scaphoideus titanus Ball

1

4 3 1212 Part 2 – Main insect pests in Tuscan vineyards

Jacobiasca lybica

African leafhopper density increased in Sicily, causing severe damage to Nero d’Avola variety (that is more susceptible). Due to climate warming, probable spread to Northern areas.

1313 Part 2 – Main insect pests in Tuscan vineyards

Mealybugs (Hemiptera Pseudococcidae)

Planococcus ficus (Signoret)

Multivoltine, non-diapausing, highly prolific species: it develops more generations in warmer climate, not hindered by cold periods (in winter below-ground populations survive). Pseudococcus comstocki From Marchesini et al., 2018 1414 Part 2 – Main insect pests in Tuscan vineyards

Mealybugs (Hemiptera Pseudococcidae)

 Species with temperature-dependent growth: they take advantage of local/global warming.  Anyway population dynamic depends also on natural enemies: unknown effects of climate change on predators and parasitoids

1515 Part 2 – Main insect pests in Tuscan vineyards

Main carpophagous feeding on grape in Tuscany

Tortricidae Lobesia botrana (Denis & Schiffermüller) ambiguella (Hübner) ljungiana (Thunberg)

Pyralidae Phycitinae Cryptoblabes gnidiella (Millière) Ephestia unicolorella woodiella Richards & Thomson

16 16 Part 2 – Main insect pests in Tuscan vineyards

Lobesia botrana European grapevine moth

Eupoecilia ambiguella Vine moth

Argyrotaenia ljungiana

17 17 Part 2 – Main insect pests in Tuscan vineyards

Cryptoblabes gnidiella Honeydew moth

Ephestia unicolorella woodiella

18 18 Part 2 – Main insect pests in Tuscan vineyards

Effects of climate change on the ratio and distribution of the two main moths

Temperature (°C) and R.H. (%) requirements for Lobesia botrana and Eupoecilia ambiguella adults (from Stellwaag, 1939)

Climatic parameters Lobesia botrana Eupoecilia ambiguella

Adult activity lower threshold from 13°C (90%) from 14° (90%) to 20° C (35%) to 25° (45%) Optimal temperature and RH range from 21°C (60%) from 19°C (100%) for adult activity and egg laying to 25°C (40-70%) to 25°C (75-100%)

Due to climate changes the vine moth nearly disappeared in South and Central Italy; in North Italy it was reduced and replaced by the European

grape moth 19 19 Part 2 – Main insect pests in Tuscan vineyards

Lobesia botrana spread in future scenarios

1980-2010 2041-2050

Applying simulation models (temperature, day-length and fruit stage), due to the expected climate warming, in Europe a wider distribution of the European grapevine moth, L. botrana, was predicted, with highest populations in warmer regions in a wide band along latitude 40°N. 20 (From Gutierrez et al., 2018) 20 Part 2 – Main insect pests in Tuscan vineyards

Lobesia botrana spread in future scenarios

In North Italy, Trento area, a dramatic increase in the number of generations was predicted using a phenological model with negative impact on crop , probably mitigated by the anticipated . (From Caffarra et al., 2012)

21 21 Part 2 – Main insect pests in Tuscan vineyards

Lobesia botrana: climate warming is not always favourable… EGVM embryos and neoformed larvae collapsed within the egg chorion, due to the high temperatures of August 2017

22 22 Part 2 – Main insect pests in Tuscan vineyards

Climate affects also natural enemies… European grapevine moth has a very rich natural enemies complex: several predators and more than 100 parasitoids, mainly polyphagous

It is very difficult to evaluate climate direct effects and interactions Campoplex capitator Aubert among all the biotic and (Ichneumonidae Campopleginae) abiotic factors. Future Monophagous parasitoid on L. botrana scenario projections might be different. 23 23 Part 2 – Main insect pests in Tuscan vineyards

Cryptoblabes gnidiella case

In several Italian coastal areas, a more significant infestation and damage by the honeydew moth was observed. Possible main reasons: effects of global warming and wider mating disruption application for the control of L. botrana. The spread of some varieties such as Sangiovese, Montepulciano d’Abruzzo and Aglianico, with late ripening, may have contributed to increase the harmfulness of the species. 24 24 Part 3 – Case study: the grape phylloxera

Leaf galling infestation on Sangiovese

Holocycle on American grapevines 2525 Part 3 – Case study: the grape phylloxera

Changes on grape phylloxera life cycle on European grapevine

More than one century after its introduction, much knowledge is still lacking:

 Distribution (soil population distribution)  Relationship between soil and leaf populations  Possible damage to grape production by leaf populations  Genetic variability  Beginners of spring infestation  Possible role of sexuparae  Practical aftermaths

26 26 Part 3 – Case study: the grape phylloxera

Genetic studies

In USA: biotype A and B (Granett, 1987) In Europe: many biotypes evidenced by Forneck and colleagues In Australia: a huge number of biotypes

Different groups of grape phylloxera biotypes by screening 103 European populations and 6 American ones

Great genetic variation From Forneck et al., 2000 27 27 Part 3 – Case study: the grape phylloxera

Is grape phylloxera threatening grapevine health in Europe?

According to current regulations (nurseries), there is no risk to spread the species

28 28 Part 3 – Case study: the grape phylloxera

Grape phylloxera has a temperature-dependent growth c = 8.7 °C Thc = 281.5 °D

From Raspi et al., 1987 Thermal parameters can be used for growth simulation models 2929 Part 3 – Case study: the grape phylloxera

Investigations on soil populations

Sampled 3 cultivars in different vineyards

3 1,4

2,5 1,2

1 2

0,8 1,5

0,6

1 nodosità / cm di nodosità radici nodosità / cm di nodosità radici 0,4

0,5 0,2

0 0 La Spinetta Fichino Palaia Campigiana Piano Bellavista Podere Forte Podere Forte 2 3 4 vitigno Vermentino Sangiovese Sangiovese Sangiovese Sangiovese Sangiovese Greco di Tufo Sangiovese 420A Kober 5BB 779 Paulsen portainnesto 1103 Paulsen 420 A 779 Paulsen Kober 5BB 420 A 420 A 161-49 161-49

resistenza 4 2 4 3 2 2 3 3

All the roostocks were infested by grape phylloxera, without evident differences or damage symptoms 30 30 Part 3 – Case study: the grape phylloxera

Assessment of leaf galling infestation

Farm 1

Farm 2

South North center end end

West end

3131 Part 3 – Case study: the grape phylloxera

Assessment of leaf galling infestation

Leaf galling infestation level in the three zones of the two farms

Farm 1 Farm 2

In the farm 1 the infestation started from a corner and spread through the , while in the farm 2 the infestation level was high throughout the whole vineyard In August 2017, high temperatures killed most of the leaf galling populations

32 32 Part 3 – Case study: the grape phylloxera

Damage assessment: gas exchange evaluation

Ciras-3

In collaboration with Mattii, G., Cataldo E., Salvi L.

3333 Part 3 – Case study: the grape phylloxera

Damage assessment: Net Photosynthesis

Highly infested grapevines show reduced photosynthesis

3434 Part 3 – Case study: the grape phylloxera

Damage assessment: Grape quality

Sugar content decreases as the level of the Sugar content leaf galling infestation increases

Anthocyanins Highly infested grapevines show reduced content anthocyanins content Total polyphenols Highly infested grapevines show reduced total polyphenols content (similar results for content extractable polyphenols)

Technological and phenolic analyses of highlighted a reduction of the grape quality due to phylloxera infestation: grapes from heavy infested vines showed reduced sugar and polyphenol contents with significant differences between extreme levels 3535 Part 3 – Case study: the grape phylloxera

Grape phylloxera leaf galling infestation: distribution based on regional monitoring network

2016 2017

grape phylloxera grape phylloxera rare spread rare other vineyards spread other vineyards

3636 Part 3 – Case study: the grape phylloxera

Possible cause of 2017 decrease of leaf galling infestation

8.7 °C grape phylloxera

lower thermal threshold

C

° Temperature Temperature

Castiglione d' Orcia (Siena) 3737 Effects of climate change on insects pests: A complex and difficult assessment

Climate change ()

Insect pests

38 38 Conclusions  Insect pests of vineyards are affected by climate changes, however climate influences the whole vineyard system as well as the natural enemies complex, with unpredictable effects  Moreover, frequent rains, due to climate changes, reduce pesticide persistence (pesticide wash off)  Mild winters followed by rainy and warm summers (2007, 2014 and 2016) favoured economically important species such as olive fruit fly, D. suzukii and European grapevine moth  On the contrary, hot and dry summers (2017) significantly reduced population density of vineyard insect pests, despite high theorical number of generations  Grape phylloxera is no exception and can represent a valuable model to study the effects of climate changes 39 39 Thanks!

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