Patterns in Tree Cavities (Hollows) in Euphrates Poplar (Populus euphratica, Salicaceae) along the Tarim River in NW China

Tree stems connect the roots and crown and have major transporting and supporting functions [1,2]. Cavities or hollows in the trunk of a tree reduce its mechanical stability [3]. The distribution of cavities or hollows in living trees varies among forest types and under different site conditions within any given forest stand [4,5,6,7,8,9]. A tree is classified as hollow- or cavity-bearing if it contains at least one hollow in its trunk or branches [6]. Furthermore, studies have shown that there are significantly more or fewer decay hollows in tree trunks in certain specific environments (humidity, diseases, drought, etc.), and that the formation and development of hollow decay in tree trunks are greatly affected by the specific site conditions [10,11,12]. Therefore, understanding the relationship between hollow formation or cavity occurrence in living trees and site conditions is necessary to inform forest conservation and sustainable management.

As the main body of the natural riparian vegetation in the inland river basins of Northwestern China, Euphrates poplar (Populus euphratica, Salicaceae) stands constitute an ecological corridor that constitutes the regional biodiversity hotspot and has the highest bioproductivity in the region [13,14]. These forests play a key role in maintaining the structure and function of riparian ecosystems in arid areas, acting as natural barriers to protect oasis agriculture and livestock production from the adverse impacts of desertification. However, in the particularly arid region of Tarim River Basin, owing to the excessive utilization of water and soil resources and anthropogenic disturbances such as deforestation over the past 50 years, natural vegetation habitats dominated by P. euphratica have been continuously lost. Specifically, in this region, natural oases have been shrinking, lakes have been drying up or disappearing, and desertification has increased. The natural P. euphratica desert forest ecosystems distributed on both banks of the lower reaches of the Tarim River have experienced dry flow for nearly 30 years, which has caused serious damage to the ecosystem [15,16].

As an indicator species of regional environmental change, P. euphratica riparian forests adapt their growth and development in response to biotic and abiotic stresses in different ways, including certain unique strategies that developed over evolutionary time to respond to extreme environments [17]. For example, P. euphratica trees grow a well-developed horizontal root system and heteromorphic leaves in response to drought stress [18]; additionally, the species responds to salt stress through selective absorption and the storage of salt ions in the body [19]. In disconnected rivers and areas with a low soil moisture content, self-renewal occurs through clonal reproduction by root suckering [20]. Moreover, P. euphratica exhibits a phenomenon that is easily overlooked, namely cavity or hollow formation in tree trunks.

Study have shown that, as the age of trees increases, the probability of hollow formation in the trunk also increases [21]. In addition, the degree or rate of tree hollowness is allegedly affected by its specific environment; thus, trees have a defense system against internal decay in the trunk [22]. Further, tree growth is affected by changes in site conditions, resulting in different extents of tree cavity formation [23]. Therefore, from the perspective of site conditions, researching the characteristics of hollow-bearing tree trunks would facilitate an understanding of the reasons for hollow formation and provide scientific evidence to support developing protective measures for existing natural P. euphratica forest resources. To date, studies in this field remain scarce, and the reasons for hollow formation and their influencing factors remain unclear [24,25]. In particular, in extremely arid habitats with strong wind erosion, P. euphratica forests are exposed to strong winds, rendering hollow-bearing trees susceptible to breakage and collapse [26]. A clearer understanding of the patterns of tree cavities/hollow in P. euphratica forests can provide basic data for urgently needed protection measures. In this study, we investigated the quantitative characteristics and distribution patterns of cavities in P. euphratica trees and attempted to answer the following scientific questions: What is the relationship between hollows and tree architectural characteristics? What is the influence of groundwater depth on the formation of cavities in P. euphratica trees? Our findings provide a useful update on the ecology of hollow P. euphratica and a scientific reference for maintaining and managing desert riparian forest ecosystems in arid regions.

Populus euphratica forests are likely to contain a high proportion of trees with hollows, with a hollow-bearing-tree density of 159 tree/ha, which is much higher than those of tropical seasonal rain forests (87 trees/ha), tropical mountain evergreen broad-leaved forests (approx. 86 trees/ha), subtropical humid evergreen broad-leaved forests (94.3 trees/ha), and even desert riparian forest in the middle reaches of the Tarim River (78 trees/ha) in China [25,29,30,31]. Populus. euphratica forests in this area are primeval, and most are over-matured [14] and contain numerous trees with hollows. External factors, such as sandstorms, strong winds, and long-term river desiccation, may cause hollows to form more easily in P. euphratica forests, resulting in different densities of hollow-bearing trees in different locations. Further, factors such as water conditions (mainly groundwater depth), desertification, and human interference also significantly influence the growth and distribution pattern of natural vegetation in the Tarim River Basin [13,14]. Therefore, water availability is likely the key environmental factor affecting the formation of tree cavities. In this study, the presence of cavities in P. euphratica increased significantly with increasing DBH and decreased significantly with increasing TH. Owing to the extremely arid conditions in the lower Tarim River, the vertical growth of most P. euphratica forests is limited by water; thus, lateral growth is dominant [14]. Therefore, taller trees are likely to be distributed in areas with favorable water conditions, as well as be less exposed to water stress and maintain normal growth. Temperature is the main limiting factor in tropical rainforests, and the specific orientation of tree hollows is related to thermal conditions (such as the angle of the sun) [32]. In this study, 82 (23.4%) of the hollow-bearing trees sampled exhibited clear signs of broken stems or branches. In desert riparian forests, factors such as water availability and strong winds may lead to differences in the distribution patterns of tree cavities. Hollow-bearing trees provide critical microhabitat resources for forest fauna and play an important role in maintaining biodiversity [33,34]. Of the 352 tree holes sampled, only 3 (0.85%) exhibited signs of animal use; hence, almost no tree holes were used as animal habitats. Compared with other forest types, P. euphratica desert riparian forests are characterized by a simple community structure and relatively poor biodiversity. Therefore, the relationship between P. euphratica tree cavities and biodiversity was not quantified or further analyzed in the present study.

In the study area, most of the hollows were observed on P. euphratica trunks that had been blown down by wind or had broken branches. The formation of tree hollows may also be an indicator of P. euphratica senescence. In addition, we observed that P. euphratica stored large amounts of water in the trunk; it can be assumed that this storage would make the middle of the trunk susceptible to porosity and eventually lead to cavity formation. The more severe drought conditions become, the more likely a P. euphratica trunk will develop empty spaces by storing water. Therefore, the formation of tree holes in the trunk may also be a strategy of P. euphratica to adapt to extreme drought conditions. In addition, our study reveals that the height and width of P. euphratica cavities are significantly correlated with the distance from the river. As groundwater depth increased, the proportion of hollow-bearing trees in P. euphratica stands increased from 26.2% to 100%. P. euphratica trees, as phreatophytes (i.e., plant species that have evolved the capacity to access groundwater), mainly depend on groundwater to survive [14]. As shallow soil water sources are gradually depleted with increasing distance from the river, the depth and proportion of water uptake by phreatophytes from groundwater typically increases [35,36,37]. Therefore, phreatophytes develop deeper roots to track the capillary fringe and/or saturated zone of aquifers. Thus, groundwater depth is considered a key limiting factor that regulates stand structure and function in desert riparian forests. The habitat conditions of the lower Tarim River are more challenging than those of the upper and middle reaches, with frequent river-flow disconnections and deeper groundwater tables; all together, these conditions cause continuous water stress and also cause P. euphratica forests to develop an association between increasing tree age, declining tree function, and greater hollowing. Therefore, habitat quality, particularly with respect to water availability, is an important factor in the hollowing of P. euphratica forests.

The formation of hollow trees is a slow and complex process that is influenced by a combination of factors, including the habitat conditions of the forest and the characteristics of the trees themselves. Hollowing is the end result of decay in living trees, with some trees forming hollows gradually from the inside out and exhibiting large external holes that are visible to the naked eye, and others starting directly from the outside, with various decay fungi invading the sapwood exterior. This study identified several issues that need to be investigated and addressed in future research. For example, drilling samples of heartwood and sapwood revealed that some of the trunks were extensively decayed internally and that the heartwood was decayed or in a crumbly state. Consequently, quantitative studies of internal decay in living trees are needed, and characteristics such as the decay ratio, decayed area, volume, and decay orientation need to be quantified using high-precision non-destructive instrumentation, such as Arbotom stress-wave detection and TreeRadar [2,38,39,40]. In addition, this study was mainly concerned with the physical parameters of the trees and thus can be improved by the addition of chemical (biochemical) parameters at a later stage. Therefore, it is expected that this aspect will be thoroughly investigated in depth in future studies.