Abstract
Persian walnut (Juglans regia L.), which is native to Central Asia, has been widely cultivated throughout Europe over millennia as a multipurpose tree. However, only recently the naturalization process outside cultivation has been studied, mostly in temperate Europe, with no information regarding the Mediterranean region. Here we provide the first field investigations about the natural regeneration of walnut in two traditional Mediterranean agroecosystems: an irrigated mixed orchard in suburban areas and a non-irrigated prickly pear (Opuntia ficus-indica [L.] Mill.) orchard. The natural regeneration densities were statistically different in the two agroecosystems, ranging from 75 individuals per hectare in the prickly pear orchard to 200 individuals per hectare in the mixed orchard. Crows were frequently observed actively carrying walnuts in both environments. The irrigation practices and the shade provided by larger trees in the mixed orchard, and the potential benefits provided by prickly pear individuals, seemed to be crucial for seedling establishment and development in the two orchards, respectively. On the other hand, climate does not seem to represent a constraint for walnut recruitment, even if the mean annual temperature at the mixed orchard is slightly above the optimal temperature for walnut. Other biotic and abiotic factors that may trigger or hamper the naturalization process are also discussed in this paper, which explores the research needs for better understanding the naturalization potential of the Persian walnut in Mediterranean agroecosystems, as well as the effects of different land uses and future climate change on this process.
INTRODUCTION
One of the major issues facing the study of the invasion process by alien species is high unpredictability, either concerning which plant taxa will become invasive, or the time needed to reach an invasive status (Williamson 2006). This is also true for plant taxa which have been cultivated since ancient times and are seldom studied in their naturalization process (Verloove 2006). The duration of the lag-phases can be highly variable from species to species, so that plants that have never shown any tendency to naturalization can suddenly spread even centuries after their introduction (Aikio et al. 2010). Several biotic and abiotic factors may trigger the naturalization process. For example, biotic interactions with the organisms necessary for pollination and seed dispersal, or the availability of water resources and nutrients, may be crucial (Glyphis et al. 1981; Badalamenti et al. 2014), in addition to the relationships with primary biotic soil components, such as arbuscular mycorrhizal fungi (Badalamenti et al. 2015; Carvalho et al. 2018).
The Persian walnut (Juglans regia L., Juglandaceae) is one of the most intensively cultivated nut tree species worldwide due to the high nutritional value of the fruits and good timber quality (Bottema 1980; Barone et al. 1997; de Rigo et al. 2016; Pelleri et al. 2020). Probably native to a large area of the mountain ranges of Central Asia, Persian walnut has been cultivated for a long time throughout Europe, including the Mediterranean and temperate areas (Pini et al. 1999; Pollegioni et al. 2017). Walnut cultivation in Italy has very old traditions and probably dates back to the pre-Roman period (Barone et al. 1990). Originally, trees for orchards were often produced from seed, a still-common practice in some Italian regions (Barone et al. 1997). Currently, walnut is propagated by grafting (patch budding, T-budding, or whip grafting) or micropropagated, whereas seeds are mainly used to obtain seedling rootstocks (Grauke and Thompson 2003) or for timber production in forest plantations and agroforestry systems (Dupraz et al. 1999; Eichhorn et al. 2006; Paris et al. 2019). In these cases, large seeds are preferred for planting, because seedling size is generally correlated to kernel weight of the seed (Lagerstedt 1979). The seeds of Juglans species are included among recalcitrant and/or short-lived seeds (Hartmann et al. 2002), having a low genetic potential to tolerate storage. Saline habitats and water stress may severely and negatively affect walnut germination (Vahdati et al. 2009). Furthermore, germination may be delayed or prevented due to the mechanical barrier offered by seed-enclosing structures (shells), which may play a significant role on the release from embryo dormancy. As a whole, such biological traits, together with the attractiveness of nuts for a number of predators, reduce the likelihood of naturalization.
Nevertheless, natural seed dispersal of Juglans spp. largely relies on birds (primarily corvids) and some rodents through a mechanism known as “sinzoochory” (Vander Wall 2001; Beck and Vander Wall 2010). In particular, this biotic interaction occurs when the potential animal vector caches the nuts in the soil for later consumption, especially during periods of low resource availability (e.g., winter). Since not all of the buried nuts are then rescued, the condition for germination and subsequent seedling recruitment is determined by disperser behavior.
Despite its history of cultivation, J. regia seemed to face many constraints to becoming naturalized in areas far from its origin. Nevertheless, in previous decades, naturalization events have been increasingly reported in several temperate regions of Europe, including Germany (Keil and Loos 2005), Belgium (Verloove 2011), Poland (Lenda et al. 2012), Slovakia (Uhliarová et al. 2012), and Ukraine (Baranovski et al. 2016). The remarkable increase in the frequency of naturalized individuals observed in Poland, also within forest habitats, has been attributed to the increased activity of seed dispersers, accompanied by the progressive abandonment of traditional agricultural activities (Lenda et al. 2012, 2018).
Despite the naturalization of the walnut already being reported for Mediterranean-type climate regions (Casasayas 1990; Knops et al. 1995), there is limited information concerning the causes and the extent of this process. In the present work, in order to clarify some of these aspects, we studied the regeneration of walnut in two traditional Mediterranean orchards of western Sicily (Italy): a mixed, tree-dominated orchard, and a prickly pear (Opuntia ficus-indica [L.] Mill.) orchard. The aim of this study was to determine whether the different agroecological conditions of the two study sites could affect walnut naturalization and eventually reveal the major factors involved in this process.
MATERIALS AND METHODS
The field surveys were carried out in Sicily in a 100 ha mixed suburban orchard (“Fondo Micciulla”— 38°06′20.74″ N, 13°19′25.38″ E, 90 m above sea level; hereafter “Palermo”) and in a 1 ha prickly pear orchard (37°48′52.39″ N, 13°39′26.34″ E, 455 m above sea level, hereafter “Roccapalumba”) located inland in a rural area about 70 km south-east of the first site (Figure 1). Following the Köppen climatic classification, both sites fall within the warm-temperate climate, with dry and hot summers (code Csa: Beck et al. 2006). The “Palermo” orchard is a traditional orchard irrigated through water channels, a traditional gravitational system inherited from Arabs with a “forest-like” structure, located at about 90 m above sea level in the Conca d’Oro plain. This area surrounding the city of Palermo has been characterized over the centuries by the presence of many natural environments of great ecological and faunal importance, in a context characterized by minimal and sustainable urban development and large agriculture areas, dedicated to the development of fruit tree crops (Sparacio et al. 2017). The dominant tree species in the surveyed area are Citrus spp., Eriobotrya japonica (Thunb.) Lindl., Celtis australis L., and Laurus nobilis L. (La Mantia 2006, 2007). Mean annual precipitation in this area is 747 mm; mean annual temperature is 18.8 °C; and the soils are Typic rhodoxeralfs (Fierotti 1988; SIAS [Accessed 2019]). Weed control in the “Palermo” orchard until the 1970s was made through soil tillage. Year after year, this cultural practice has been gradually substituted by the use of herbicides applied repeatedly during the growing season. More recently, during the last decade, these practices were progressively abandoned in favor of mechanical weed control. Eleven mature walnut trees, with scattered distribution, are interspersed with other trees in the orchard (Figure 1).
Location of the two study areas in Sicily (Italy): (A) “Palermo” orchard with white circles showing the position of the mature walnut trees, and the white polygon delimiting the study area; (B) “Roccapalumba,” with the white circles showing the position of the mature walnut trees, and the black polygon delimiting the prickly pear orchard (images from Google Earth®).
The “Roccapalumba” orchard is located in an inner hilly area at about 500 m above sea level, dominated by cultivated lands, especially wheat fields, olive groves, and prickly pear orchards. Mean annual precipitation in this area is 561 mm; mean annual temperature is 15.7 °C; and the soils are Typic pelloxererts (Fierotti 1988; SIAS [Accessed 2019]). Only two mature walnut trees are present, 80 and 120 m apart from the prickly pear orchard edge, respectively (Figure 1). The inter-rows are regularly mowed and tilled, whilst the soil strips along the rows are not managed, neither mechanically nor chemically.
The walnut natural regeneration was assessed in ten 50 × 2 m transects randomly distributed at “Palermo” orchard (total sample size of 1,000 m2) and in one hundred 3 × 2 m plots within prickly pear rows at “Roccapalumba” (total sample area of 600 m2). All self-sown walnut individuals higher than 10 cm were recorded. In both sites, in order to detect eventual seed dispersers, periodic observations in the proximity of the fruiting walnut trees were performed during the fruiting season. To assess the possible influence of climate (rainfall and temperature), we analyzed the most recent data (from 2002 to 2018), coming from the thermo-pluviometric stations closest to the two study sites (Palermo and Alia, for “Palermo” and “Roccapalumba,” respectively)(SIAS [Accessed 2019]). Specific information about the environmental conditions and the avifauna of the two experimental sites can be found in La Mantia (1982) and Cairone (1982). The summary of the main characteristics of the study sites is provided in Table 1.
Main characteristics of the sampled areas in the study sites.
Data Analysis
Due to the unbalanced sampling design (10 units in “Palermo” and 100 units in “Roccapalumba”), we first pooled “Roccapalumba” data by combining the number of individuals of 10 consecutive sampling plots, following the order they appear (1 through 10, 11 through 20, and so forth) to standardize the number of sampling units. Then, we obtained the walnut density for both sites based on the specific sampled area of each sampling unit (100 m2 and 60 m2 for “Palermo” and “Roccapalumba,” respectively). Once density data fit a normal distribution (Shapiro-Wilk, W = 0.91, P = 0.07) and had equal variance (Levene’s index = 0.06, P = 0.8), we ran a t-test to check for differences in the density of naturalized walnuts between “Palermo” and “Roccapalumba.” Once climatic data did not follow a normal distribution, we compared the data (monthly values) between the two orchards using the nonparametric Kruskall-Wallis test.
RESULTS
The density of naturalized walnut individuals was higher in “Palermo” (200 ha−1) than in “Roccapalumba” (75 ha−1), with statistically significant differences (t = −2.62, P = 0.02). In “Palermo,” the individuals were found scattered over the transects, whereas in “Roccapalumba,” all individuals were found beneath prickly pear plants. We found self-sown seedlings up to 50 cm high from the last fruiting season, thus being less than 1 year old (Figure 2). In “Palermo,” we also observed the tallest individuals, 3.8 m and 4.8 m high, aged 3 and 4 years, respectively, as assessed by the counting of the annual rings. In “Roccapalumba,” the tallest individual was 2.8 m high, with an estimated age of 2 to 3 years (Figure 3). There were significant differences in all climatic variables between the two sites, with all values higher in “Palermo” (Table 2). Direct observations carried out on the mature walnut trees existing in “Palermo” allowed us to repeatedly notice, during the whole period of fruit ripening, hooded crow individuals (Corvus cornix L.) visiting the walnut canopies carrying nuts in their beaks (Figure 4). Interestingly, crows dropping the nuts on the ground in an attempt to crack out the shell were also observed. In “Roccapalumba,” we observed Corvus cornix and Pica pica L. (magpie) using prickly pear cladodes as perches, although no direct interaction with walnuts was recorded. In both areas, walnuts were found to be preyed upon by rats (personal observation).
The natural regeneration of walnut in “Palermo” orchard, which includes: (A) two-year-old juveniles which resprouted after cutting; (B) one-year-old self-sown seedling, still bearing at the base the original nut (you can see the detail on the left); (C) a young individual 4.8 m high.
A naturalized walnut individual growing within a prickly pear plant.
Comparison of the climatic variables between the two study sites from 2002 to 2018. Minimum (min), maximum (max), mean, and standard deviation (SD) refer to the monthly values, which were obtained from the average of daily values. Tmax = average of maximum temperatures; Tm = average of mean temperatures; Tmin = average of minimum temperatures.
Corvus cornix carrying a walnut in its beak within “Palermo.”
DISCUSSION
Environmental Constraints for Naturalization
As far as the naturalization process of Juglans regia in Europe is concerned, we report a summary of the current state of knowledge (Table 3). It can be seen that, despite the increasing trend of the walnut naturalization reports in the last few years in more than 10 European countries, very rarely do these reports include detailed information because data are primarily inferred from presence/absence check-lists. The only exception is represented in the works by Lenda et al. (2012, 2018), which are focused on walnut naturalization and its main driving factors, and where all these aspects are interestingly and thoroughly discussed. Juglans regia grows well in mild and warm-mild climates, with mean annual temperatures of 10 °C to 17 °C, and on fresh, fertile, and deep soils, with a pH ranging from 6.5 to 7.5 (Bosco et al. 1997; Fernandez-Lopez et al. 2002). The main climatic constraints for its natural regeneration are the vulnerability of seedlings to both early and late frost (Loacker et al. 2007) and the relatively high water requirements. Most walnut varieties require approximately 800 hours of temperatures below 7.2 °C (winter chilling requirement for a regular bud dormancy completion)(Barone and Zappia 1993), and the annual precipitation should be at least of 700 to 800 mm (Lestrade et al. 2013). Indeed, J. regia is very sensitive to water stress, which can negatively affect seed germination and root development (Vahdati et al. 2009), as well as competitive ability against other plants (de Rigo et al. 2016). Concerning the first limiting factor, neither of the two sites experienced frost events in the considered time frame (2002 to 2018), with minimum temperatures never falling below 1.9 °C, and in such a case, only for a short period. Moreover, no decreasing or increasing trends in the minimum temperatures have been detected, suggesting that frosts or winter chilling have not represented a limiting factor for walnut regeneration. The water supply, crucial for seedling survival and growth (Janku et al. 2017), should not represent a constraint in the tested conditions due to the irrigation practices carried out in “Palermo.” Nevertheless, in abandoned orchards where irrigation has been given up, walnut seedlings must face serious survival risks (personal observation). We observed a fast growth in the early life stages of walnut seedlings in the “Palermo” orchard, as previously detailed. Then, most of the juvenile individuals were destroyed during the mechanical control of weeds, although some of them were able to resprout (Figure 2A), whereas only a few individuals were left to grow deliberately (Figure 2C). However, this fast growth under irrigation may be not enough, as young walnuts are usually outcompeted by faster-growing woody species present in the orchard, such as Celtis australis and Laurus nobilis. Thus, competition also has to be considered as a serious factor impeding walnut establishment and naturalization in abandoned orchards.
Summary of the naturalization reports of Juglans regia in Europe and in other Mediterranean-climate areas, listed in chronological order.
In “Roccapalumba,” the lower regeneration density we observed seemed to be primarily caused by the low water availability. Such water shortage may be the combined result of a lower precipitation regime, the lack of irrigation, and the presence of hard clay soils, all factors determining less suitable ecological conditions for walnut growth and performance (Fernandez-Lopez et al. 2002). In this context, the role played by single prickly pear plants (Figure 3) in creating a suitable microhabitat for walnut regeneration appeared to be crucial.
In a scenario of ongoing climate change, contrasting patterns may arise. In the inner Alpine valleys of Tyrol (Austria), milder winters and higher annual temperatures have been identified as key factors in favoring the recent spread of walnut (Loacker et al. 2007). Such findings support the hypothesis of a progressive northward shift in the European distribution of the species (Hemery et al. 2010) as well as that of other woody species (Walther 2003). At the same time, this would suggest a concurrent decrease of the naturalization potential in a scenario of a hotter and drier Mediterranean climate, although the recent data we assessed (the last 16 years) seem not to show any increasing temperature or decreasing precipitation trends. In a potential similar climatic environment like California, walnut has been reported as naturalized for more than 20 years (Knops et al. 1995), yet only occasional natural regeneration has been reported to date (Whittemore 2012).
Our observations suggest that in environmental Mediterranean conditions not affected by frost events, irrigated agroecosystems may offer favorable conditions for the naturalization of walnut once the water stress is avoided. Seedling emergence and survival, at least in the early developmental tree stages, may also considerably benefit from plant canopies acting as a shelter against the excessive heat in summer, thus improving microclimatic and edaphic conditions as observed in “Roccapalumba.”
Dispersal Mechanisms
The transport of viable propagules towards suitable microsites is one necessary step for the naturalization process of a plant. Seed dispersal in walnut species is generally performed by animals through sinzoochory, in which predation is the main goal, but dispersal may arise as a beneficial outcome (Vander Wall 2001). Firstly, animals have to open the hard nut shell to reach its nutritious contents. For instance, the ability of corvids to feed on walnuts using different strategies to open their fruits has long been reported (Foerstel 1993; Cristol 2005). In suburban areas, crows may surprisingly take advantage of cars and other vehicles to crack nuts (Mainardi 2006). Within the “Villa Borghese” urban park in Rome, carrion crows have carried the Juglans nigra L. nuts in their beaks and dropped them on the asphalt, as recently reported (Fraticelli 2000). Additionally, rooks (Corvus frugilegus L.) and jays (Garrulus glandarius L.) have been reported to play a major role for the invasion of walnut from commercial plantations to rural fields and forest habitats in Poland (Lenda et al. 2018). Interestingly, the recent arrival of jays in the “Palermo” orchard has triggered the natural regeneration and spread of the holm oak (Quercus ilex L.)(La Mantia and Bueno 2016). Hence, we hypothesize that similar outcomes may arise following the fluctuations of seed disperser populations.
Important plant-animal interactions have been already described for other walnut species. For instance, the role of the carrion crows for the dispersal of Juglans nigra has been recognized, as well as for the dispersal of pecan nuts (Carya illinoensis [Wangenh.] K. Koch) and Juglans regia (Termine et al. 2013). Walnuts are also avidly preyed upon by rats (Rattus norvegicus Berkenhout and black rat Rattus rattus L.)(Bueno and La Mantia, personal observations), which are able to move the nuts above the trees and on the main branches, thus potentially contributing to walnut spread in relatively small scales.
CONCLUSIONS
Juglans regia has been widely cultivated outside its native range for a long time. Despite some reports of its naturalization in Europe dating back to 1950, just recently this process was confirmed by specific investigations in some temperate areas, with no information for the Mediterranean region. We provide the first field surveys about the walnut naturalization process within two different Mediterranean agroecosystems, characterized by distinct agroecological features. This preliminary survey highlights the need for further studies to better understand the diffusion of this phenomenon and to better identify the main environmental and biotic drivers, including climate and land use changes as well as the role of animal dispersers.
ACKNOWLEDGMENTS
This work was financially supported by the MIUR-PRIN project “Climate change mitigation strategies in tree crops and forestry in Italy” (CARBOTREES) under Grant 20085FL4E4, national coordinator: R. Valentini. The paper was prepared with the support of the “RUDN University program 5-100.”
Footnotes
Conflicts of Interest:
The authors reported no conflicts of interest.
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