The possible role of Ziziphus lotus as an ecosystem engineer in semiarid landscapes
Introduction
Interactions between individuals of different species regulate the spatial arrangement of plants in a community shaping its structure and dynamics (Tirado and Pugnaire, 2005; Padilla and Pugnaire, 2006). The net balance of positive and negative effects among individuals characterizes the interaction either as competition or facilitation (Callaway and Walker, 1997; Holmgren et al., 1997). Such interactions can be dynamic in space and time (Armas and Pugnaire, 2005). Competition or interference characterizes a community dominated by negative effects between neighboring plants, due to limited resources or allelopathy. On the other hand, when plants exercise a positive influence on their neighboring species, improving survival, reproduction, growth, or fitness, the interaction results in facilitation (Callaway, 2007).
The use of positive interactions between neighboring plants has received substantial attention during the past two decades (Maestre et al., 2001, 2002, 2003a, 2004; Padilla and Pugnaire, 2006; Valiente-Banuet et al., 2015; Losapio and Schöb, 2017). Positive interactions have been increasingly proposed as ubiquitous forces driving community structure and function, especially under harsh conditions such as thermal, water, or nutrient stress (Bertness and Callaway, 1994; Callaway, 1995; Stachowicz, 2001; Callaway et al., 2002). There are many examples of positive effects from the interaction among plants, starting from improving microclimatic conditions and soil properties (Bonanomi et al., 2011; Brooker et al., 2008; Maestre et al., 2010) to nurse-plant effects and enhanced growth as well as survival rates of seedlings and plants under trees and shrubs (Egerton et al., 2000; Tewksbury and Lloyd, 2001; Pugnaire et al., 1996a, 1996b; Holzapfel and Mahall, 1999).
However, indicating a positive effect of one species on another is a much clearer undertaking compared to demonstrating the ability of one species to act as an ecosystem engineer. Ecosystem engineers change their environment altering habitat suitability or community composition (Wright and Jones, 2006; Matsuzaki et al., 2009). Their influence is exerted by directly or indirectly modulating the availability of resources to other species, by causing physical state changes in biotic or abiotic materials, and by doing so modify, maintain, and create habitats. Many keystone species can exert such impacts and can be classified as ecosystem engineers based on six suggested criteria among which are: (a) the type and formation rate of the impacts, and their durability in the absence of the engineers; and (b) the number and types of resources that are directly or indirectly controlled, the ways these resources are controlled, and the number of other organisms that depend on these resources (Jones et al., 1994).
Ziziphus lotus (L.) is the keystone species of priority habitat ‘Arborescent matorral with Ziziphus’ (code *5220; Annex I; European Commission, 2013) occurring in Spain (south-eastern Iberian Peninsula), Greece, Sicily and Cyprus under a xerophytic thermo-Mediterranean bio-climate and corresponds to the mature phase or climax of climatophile and edapho-xero-psammophile vegetation (European Commission, 2013). Despite its importance the habitat is severely fragmented and of poor conservation status. In addition to Europe the habitat is found in semi-arid and arid zones of North Africa (Algeria, Morocco, Tunisia, and Libya; Pottier, 1981). Z. lotus is a facultative or partial phreatophyte with extreme anisohydric stomatal regulation able to obtain water from lower soil horizons and possibly from a free water table (Le Houérou, 1972; Drew, 1979; Evenari et al., 1982; Torres-Garcia et al., 2021). It maintains its vegetative growth throughout the summer and behaves as an arido-active species (Evenari et al., 1982; Gorai et al., 2010). It reaches 2–5 m in height, with mounds composed of wind-borne sediment that accumulate around it (Tengberg and Chen, 1998) and has a notable ability as a resprouter, with individual stands reaching up to 30 m diameter and living above 100 years (Rey et al., 2018). Z. lotus is indigenous to Cyprus, abundant mostly in the semi-arid areas of the central Mesaoria plain, and in the western part of the Island (Georgiou et al., 2008). However, due to intensive agriculture and grazing practices the species is restricted to isolated clusters, usually at the edges of cultivated fields (Delipetrou, 2005).
Cyprus is part of the East Mediterranean where areas particularly susceptible to desertification are likely to increase significantly due to climate change. The Island is mainly characterized by critical and fragile to desertification areas covering 42.9% and 44.6% of the total land, whereas potentially non-threatened areas to desertification cover only 3.9% and 0.8% of the land, respectively (CCRA, 2016). Therefore, drought resistant plant species capable of facilitative interactions with other plants may prove very useful in combating both desertification and mitigating climate change. Such interactions are broadly documented in many plant communities (Brooker et al., 2008; Maestre et al., 2009) and particularly in arid and semi-arid environments, where vegetation is often arranged in a two-phase mosaic composed of high plant cover patches in a low-cover matrix (Montaña, 1992; Aguiar and Sala, 1999). This clumped distribution pattern is often considered evidence for positive plant interactions (Cavieres et al., 2014; Losapio et al., 2018; Thomsen et al., 2018; Ellison, 2019).
Thymbra capitata [(L.) Cav.] is a very drought resistant plant found in the thermo-Mediterranean vegetation belt of the Mediterranean, typical of garrigue or phrygana vegetation, and is abundant within the *5220 habitat type in Cyprus. Because of such properties, it can also be considered as a candidate plant for combating desertification. Although, T. capitata grows within the habitats of Z. lotus in Cyprus, the possible facilitation between these two species has never been investigated and could be used to elucidate the potential role of Z. lotus as ecosystem engineer. There has been limited evidence that Ziziphus can influence the distribution of other plants (Tirado and Pugnaire, 2003; as well as support numerous pollinators; González‐Robles et al., 2020). For example, Asparagus albus has been found to produce a significant trend towards spatial aggregation in the presence of Z. lotus, but this has never been assessed with respect to Thymbra capitata.
Hence, it seems that Z. lotus is as a keystone species with a wide distribution range around the Mediterranean capable of maintaining the presence of its stands for centuries as the climax vegetation in arid and semiarid conditions with some known facilitating properties. Further investigation of the facilitation potential of Z. lotus could play a prominent role in restoring the dynamics of plant communities in degraded arid and semiarid ecosystems, while helping to halt desertification.
This paper aims to assess the potential role of Z. lotus in combating desertification and identify whether it behaves as an eco-engineer at the habitat level by testing for the first time: (i) the impact it may exert on the population dynamics of T. capitata, and the durability of such impacts in the absence of the Z. lotus, (ii) whether moisture availability is one of the key resources that is directly or indirectly controlled by the potential eco-engineer within the habitat. To address these goals, we explored whether the (i) density and the (ii) moisture content of T. capitata increases based on its proximity to Z. lotus, and whether this occurs (iii) against expected moisture gradients shaped by topography.
Section snippets
Study area
The study was conducted in Cyprus, in a lowland semi-arid arborescent matorral with Ziziphus lotus (L.) (priority habitat type *5220) within the National Forest Park of Rizoelia (34ο56′10.28″ N, 33ο34′23.57″ E; Fig. 1). The selected total study area within the park was 9692 m2, divided into three subareas (classes) based on topographic aspect, namely East, Ridge and South. The soil within the sampling area is sandy with poor organic content at the top 10 cm and is of gypsiric formation
Results
Volumetric Water Content (VWC) in topsoil was the highest in the East-facing slope (Table 1) and statistically significant compared to the South-facing slope (distribution not normal; medians for VWC 2.4% for East, 2.2% for Ridge, 1.6% for South) at p = 0.006 (p = 0.019 when adjusted by the Bonferroni correction; Dunn-Bonferroni post hoc test following a significant Kruskal-Wallis test at p = 0.024). It confirmed that thymes on the South-facing slope experience reduced soil moisture
Impact on T. capitata population dynamics
The classification of a species as an ecosystem engineer requires significant evidence of its impacts on community structure and functions, with the impacts diminishing in its absence (Jones et al., 1994). Our findings indicate that the population density of T. capitata can significantly increase c. 2.5 times when located up to 5 m away from Z. lotus (Fig. 3) compared to thymes growing 10–15m away, where the impact of Z. lotus roots and canopy is not expected to exert any strong influence. The
Conclusions
Z. lotus seems to exert a significant positive impact on the investigated community of habitat type *5220, and can modify population densities, together with limiting resources or constraining variables in the system i.e. moisture availability, improving habitat suitability. It thus appears to possess key properties of an ecosystem engineer, as it has been reported for other shrub species (Cushman et al., 2010). However, the mechanisms with which Ziziphus improves the moisture availability of
CRediT authorship contribution statement
Elena Constantinou: Data curation, Writing – original draft, preparation, Visualization, Investigation. Dimitrios Sarris: Conceptualization, Methodology, Writing – review & editing. Ioannis N. Vogiatzakis: Supervision, Writing – review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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Alhagi sparsifolia: An ideal phreatophyte for combating desertification and land degradation
2022, Science of the Total EnvironmentCitation Excerpt :Its anisohydric stomatal regulation enables it to obtain water from lower soil horizons and from groundwater table (Torres-Garcia et al., 2021). It is considered as an ecosystem engineer that plays a crucial role in improving semi-arid ecosystem productivity by mitigating desertification under global climate change, but despite its importance the habitat of Z. lotus is severely fragmented, and the conservation status is poor (Constantinou et al., 2021). Another example, Tamarix ramosissima is a drought-tolerant typical phreatophyte and is widely distributed native species in Asia (Gries et al., 2005).
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