Oecologia https://doi.org/10.1007/s00442-018-4250-z PHYSIOLOGICAL ECOLOGY - ORIGINAL RESEARCH Tree growth and water‑use in hyper‑arid Acacia occurs during the hottest and driest season Gidon Winters1 · Dennis Otieno2 · Shabtai Cohen3 · Christina Bogner4 · Gideon Ragowloski1 · Indira Paudel5 · Tamir Klein5 Received: 10 April 2018 / Accepted: 13 August 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Drought-induced tree mortality has been recently increasing and is expected to increase further under warming climate. Conversely, tree species that survive under arid conditions might provide vital information on successful drought resistance strategies. Although Acacia (Vachellia) species dominate many of the globe’s deserts, little is known about their growth dynamics and water-use in situ. Stem diameter dynamics, leaf phenology, and sap fow were monitored during 3 consecutive years in fve Acacia raddiana trees and fve Acacia tortilis trees in the Arid Arava Valley, southern Israel (annual precipitation 20–70 mm, restricted to October–May). We hypothesized that stem growth and other tree activities are synchronized with, and limited to single rainfall or fashfood events. Unexpectedly, cambial growth of both Acacia species was arrested during the wet season, and occurred during most of the dry season, coinciding with maximum daily temperatures as high as 45 °C and vapor pressure defcit of up to 9 kPa. Summer growth was correlated with peak sap fow in June, with almost year-round activity and foliage cover. To the best of our knowledge, these are the harshest drought conditions ever documented permitting cambial growth. These fndings point to the possibility that summer cambial growth in Acacia under hyper-arid conditions relies on concurrent leaf gas exchange, which is in turn permitted by access to deep soil water. Soil water can support low- density tree populations despite heat and drought, as long as recharge is kept above a minimum threshold. Keywords Acacia raddiana · Acacia tortilis · Leaf phenology · Sap fow · Desert · Global warming · Tree drought resistance · Arava Introduction Drought-induced tree mortality has been increasing in recent Communicated by Louis Stephen Santiago. decades (Klein 2015; Anderegg et al. 2016), and is expected Electronic supplementary material The online version of this to increase further due to global warming and desertifcation, article (https​://doi.org/10.1007/s0044​2-018-4250-z) contains especially in already dry ecosystems (Steinkamp and Hickler supplementary material, which is available to authorized users. 2015). Conversely, tree species which already survive under * Tamir Klein arid conditions could provide vital information on success- [email protected] ful drought resistance strategies (Schwinning and Ehleringer 2001). Indeed, there is growing interest to elucidate some 1 The Dead Sea-Arava Science Center, Tamar Regional of these strategies, as demonstrated by recent studies on Council, 86910 Neve Zohar, Israel Tamarix and Populus in the Taklamakan desert (Gries et al. 2 Department of Biological Sciences, Jaramogi Oginga Odinga 2003; Lang et al. 2016) and Prosopis in the Atacama desert University of Science and Technology, Bondo, Kenya (Garrido et al. 2016). Water scarcity and high temperatures 3 Institute of Soil, Water, and Environmental Sciences, often interact to exacerbate drought stress on tree physiology Agricultural Research Organization, Rishon LeZion, Israel (Ruehr et al. 2016). Hence, resolving tree drought resistance 4 Ecological Modelling, BayCEER, University of Bayreuth, strategies, and specifcally in arid environments, is a major Bayreuth, Germany interest of scientists and stakeholders alike (Hartmann et al. 5 Department of Plant and Environmental Sciences, Weizmann 2015; Cobb et al. 2018). In deserts, trees such as Acacia, Institute of Science, Rehovot, Israel Vol.:(0123456789)1 3 Oecologia Tamarix, Populus, and Prosopis are often the only woody Eastern Desert of Egypt (North Africa), wood anatomy of species, and as such, they are considered keystone species A. raddiana was studied using 14C, due to the lack of annual (Ward and Rohner 1997). Successful desert trees are essen- tree-rings (Andersen and Krzywinski 2007). In the Arava tial locally for their associated ecosystems and important valley of Southern Israel, A. raddiana cambial activity was globally for their unique eco-physiology. studied in seedlings and in shoots of mature trees (Fahn et al. Among living tree species, Acacia raddiana and Acacia 1968; Arzee et al. 1970). Several other studies have tried to tortilis (the genus name changed to Vachellia1) inhabit some address the challenging task of identifying water source(s) of the hottest and driest places on Earth. These Acacia trees sustaining Acacia populations in the Arava. This topic has are major components of savannas and open woodlands in drawn particular attention, especially following mortality many arid regions of Africa and the Middle East (Maslin events due to consecutive drought years in the 1980s (Peled et al. 2003). Within the arid Arava valley, along the Syr- 1988; Shrestha et al. 2003). Based on the dynamics of A. ian–African transform (Great Rift valley) in southern Israel raddiana shoot water potential across sites and seasons, it and Jordan, A. raddiana and A. tortilis are the two most was suggested that surface foods are the major water source abundant and, in many places, the only tree species present for populations in the Arava (Shrestha et al. 2003). Such a (Danin 1983). In these arid habitats, Acacia trees are found strategy is typical of pulse-driven arid ecosystems (Schwin- mostly growing in the channels of ephemeral river beds ning and Ehleringer 2001). Studying the water source for (“wadis”, a term from Arabic; Ward et al. 1993; Munzber- Acacia trees in situ has been done by exposing their root sys- gova and Ward 2002). Here, both A. raddiana and A. tortilis tems (Peled 1988), comparing the 18O/16O isotopic ratios in are considered keystone species that support the majority of water samples extracted from Acacia twigs and from nearby the biodiversity surrounding them and locally improve soil water sources (Sher et al. 2010), and using Electrical Resis- conditions for other plant species (Milton and Dean 1995; tivity Tomography (ERT; Winters et al. 2015). Yet, none of Ward and Rohner 1997; Munzbergova and Ward 2002). these studies monitored in situ Acacia growth and water-use Although Acacia species dominate many of Earth’s hot- in stems and leaves to observe their temporal dynamics and test and driest deserts, little is known about their growth relationships to local meteorological conditions. dynamics in situ. Some knowledge of related eco-physiolog- Here, we aimed to decipher the eco-physiological dynam- ical parameters does exist but not for Acacia trees growing ics of both A. raddiana and A. tortilis, the dominant tree spe- in situ and in arid environments. Water relations were studied cies in the hyper-arid regions of North Africa and the Middle extensively for A. tortilis, but not in hyper-arid conditions; East, as a case of tree growth at the hot and dry extreme. for example, Do et al. (2008) studied water-use of A. tortilis We hypothesized that stem growth and other tree activities in the northern Sahel, where annual rainfall ranged between are synchronized with rainfall or fashfood events. We took 146 and 367 mm. Ludwig et al. (2003) studied hydraulic advantage of state-of-the-art monitoring technologies, and lift in A. tortilis trees on an East African savanna where used a high-resolution, long-term, and continuous obser- the climate is tropical seasonal (650 ± 272 mm year−1). vation approach. Electronic dendrometers, sap fow sen- Studies by Otieno et al. (2003, 2005a) were based on seeds sors, and phenology cameras were connected to individual that were collected in Kenya but brought back to Germany trees, to produce an accurate and detailed representation of where they were germinated and grown under controlled Acacia survival and growth in one of Earth’s most hostile conditions. Both Otieno et al. (2005b) and Do et al. (2008) environments. showed the high drought resistance of this species, including physiological and morphological adaptations, in semi-arid environments, which do not represent the real extreme envi- Materials and methods ronments that some Acacias can tolerate. In the more arid Site and climate 1 The genus (Acacia) was recently split (Kyalangalilwa et al. 2013) Our study was conducted in Wadi Sheizaf, a dry sandy stre- into two diferent genera, Vachellia and Acacia. While the origi- ambed at the northern edge of the Arid Arava Valley, south- nal name (Acacia = "thorn" in latin) was reserved for the Australian ern Israel (Fig S1; 30°44′N, 35°14′E; elevation 137 below Acacia Vachellia (thornless) trees, the new name, , was reserved for sea level). Meteorological data were obtained from the the Acacias from the rest of the world, with thorns. Searching the web science for scientifc papers published from 2015 to June 2016 Israeli Meteorological Service for station 340528 in Hatzeva, showed that only 2.6% from the 346 Acacia papers published dur- located 7 km north of Wadi Sheizaf. The climate here is hot ing this periord chose to use the new name. A short survey among and dry: 30-year average minimum, mean, and maximum Israel’s botanists also demsonstrates that it is preferable to continue temperature of the hottest month were 26.2 °C, 33.2 °C, to use the genera name Acacia (see for example Winters et al. 2015; Nothers et al. 2017; Rodger et al. 2018). For these reasons, we chose and 40.2 °C, respectively; average minimum, mean, and to use the genera Acacia. maximum temperature of the coolest month was recorded 1 3 Oecologia Fig. 1 Meteorological condi- 50 16 Temperature VPD (-kPa) diurnal rain (mm) ) tions at Hatzeva, 7 km north 45 of Wadi Sheizaf (Arava valley, 14 C) Israel; Fig. S1) in 2014–2016.