Dendrometric measurements reveal stages leading to tree mortality in a semiarid pine forest Fyodor Tatarinov, Yakir Preisler, Tamir Klein, Eyal Rotenberg, and Dan Yakir Weizmann Institute of Science  234 Herzl St. PO Box 26 Rehovot 7610001 Israel

Resilience, survival and tree water saving strategies Night: No transpiration, sap flow may continue, phloem refilling Daytime: Transpiration (may exceed sap flow), water movement from phloem to xylem, phloem shrinkage Processes driving stem diameter variations Stem expansion (growth, forming xylem) Non-permanent stem variation (Cambium, phloem) Water related stem size variations (elastic tissues) Example of diurnal stem diameter variations in a semiarid pine forest Seasons Consequently, diameter maximum is usually observed in the morning and minimum in the evening

Yatir forest experimental site Located in the Northern edge of the Israeli Negev desert, about 650m a.s.l., 3,000 ha Dominated by Aleppo pine (Pinus halepensis) planted in the mid-1960s Mean current stand density of 300 trees ha-1. Summer drought period is from May to October ( 25°C in July) Winter period has low precipitation (280 mm on average) and moderate temperature (10°C in January) Monthly median air temperature and precipitation totals (2000-2016)

Yatir measurements Eddy covariance – since 2000. Sap flow – since 2009 by heat dissipation probes (HDP, Granier 1987). Dendrometers – since 2012 (by electric band dendrometers). 5 trees were measured since 2012 and 36 trees since August 2015) Branch and soil chambers – since 2016.

Chronology of tree mortality event in Yatir experimental site In August 2015 an intensive 24-hours campaign of leaf-scale measurements accompanied with shoot sampling was conducted in Yatir on 5 sample trees, what could be a trigger of beetle attack. In spring 2016 mortality was observed among sample trees. This was accompanied by bark-beetle attack, and with visual drying of needles starting in April 2016. Totally 7 of 31 trees with sap flow (SF) and dendrometry measurements died (including all trees applied in 24-h campaign) and 24 survived (mean DBH 18.4 and 20.6 cm, respectively). Decrease of diameter of dying trees was first observed around November 2015. Sap flow decline relatively to survived trees was observed first at the start of new wet season around January 2016.

Stem circumference changes of living and dying trees Stem circumference (CBH) variation of dying and living trees since the start of the period (medians±st.dev) Dry season Shoots sampling Start of visible needles drying Typical annual CBH course includes intensive growth in wet season (December-April) and a plateau with small shrinkage in the dry season In late September and October 2015 all dying and living trees showed certain plateau. Since mid November all dying trees showed decrease of CBH, whereas living trees remained stable. Since a strong rain around Jan 1, 2016 all living trees started to grow, whereas CBH of dying trees remained stable and then restarted to decrease since March

Time of daily max CBH, 7-days moving averages Medians (among trees) and standard deviations All living trees showed decreasing trend of time of DBH maximum (shifting earlier) in November – April from 9-13 h to 6-9 h At the same time dying trees showed stable or slightly shifting later trend since late November (from 9-12 h to 12-14 h)

Maximum daily shrinkage (MDS, max-min of CBH , 30-days moving averages) CBH daily range of all living trees increased during wet season from 0.05-0.1 to 0.2-0.5 mm At the same time CBH daily range of dying trees remained stable since early September (0.05-0.15 mm)

Diurnal CBH curves in November 2015 of living and dying trees (Y-axis is in mm of CBH change since 22.02.2015) In mid November all dying trees showed small or negligible diurnal oscillations However in early October most of dying trees still showed diurnal CBH variations similar to living trees

Start of visible needles drying Medians of daily sap flow density totals (cm3cm-2day-1) of dying and living trees Dry season Start of visible needles drying Shoots sampling Generally dying trees showed higher median flux until autumn 2015, which can be occasional result of sample trees combination Since the start of the new wet season dying trees showed considerably lower sap flow

Diurnal of monthly sap flow averages (L h-1) No expressed difference until April 2015 Generally similar courses until October 2015 with max in dying trees shifting later Since November 2015 the big difference occurs: whereas in living trees expressed diurnal curve with midday max started, dying trees show noise apparently related with sun shining.

New bark beetle attack – spring 2017 Bark beetle attack was observed around March 1, 2017 in two trees with similar DBH: 55 (18.1 cm) and 45 (17.7 cm) Tree 55 had enough resin and showed good larvae's wholes closing Consequently it showed a normal restart of growth the new wet season Tree 45 had not enough resin and it showed continued CBH decrease in the new wet season

Bark beetle attack in spring 2017 However both trees showed high SF until tree 45 was cut at the end of March Mean diurnal branch-level water fluxes in affected trees in 2017 At the branch level results of beetle attack (as the difference in water fluxes between survived and dying trees) started to be visible approximately since March

Conclusions Chronology of tree mortality was typically observed by a clear cascade of gradual decline of the following parameters 7-8 months prior to visual mortality- Bark Beatle attack (probably…) damaging the phloem and bark tissue Decline in diurnal shrinkage of tree stem as observed by dendrometers data - expressing radial water movement from phloem to xylem 4-5 months prior to visual mortality- Total stem shrinkage as observed by dendrometers data - expressing water loss and biomass degradation 2-3 months prior to visual mortality- Decrease in SF values expressing a decrease in the axial water flow, from soil to canopy  via stem  This chronology nicely demonstrates the importance and the sensitivity of the radial water flow, being first to decline after the tree weakened and imitating the process of unrepairable damage to the hydraulic system We thus conclude that the first signal of tree decline will be observed in its internal phloem transport ability on transferring water radially from the living tissues to the xylem transport. Which can be used in the early diagnostic of tree mortality