Maryam MOSLEHI JOUYBARI, Asgahr BIJANI, Hossien PARVARESH,Ross SHACKLETON, Akram AHMADI

1 Research Division of Natural Resources, Hormozgan Agricultural and Natural Resources Research and Education Center,Agricultural Research, Education and Extension Organization (AREEO), Bandar Abbas 7915847669, Iran;

2 Department of Environmental Sciences, Bandar Abbas Branch, Islamic Azad University, Bandar Abbas 7915893144, Iran;

3 Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf 8903, Switzerland;

4 Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Stellenbosch 7602, South Africa;

5 Research Division of Natural Resources, Golestan Agricultural and Natural Resources Research and Education Center,Agricultural Research, Education and Extension Organization (AREEO), Gorgan 4915677555, Iran

Abstract: Biological invasions can alter soil properties within the range of their introduced, leading to impacts on ecosystem services, ecosystem functions, and biodiversity. To better understand the impacts of biological invasions on soil, we compared topsoil physiochemical properties at sites with invasive alien tree species (Prosopis juliflora), native tree species (Prosopis cineraria, Acacia tortilis, and Acacia ehrenbergiana), and mixed tree species in Hormozgan Province of Iran in May 2018. In this study, we collected 40 soil samples at a depth of 10 cm under single tree species, including P. juliflora, P. cineraria, A. tortilis, and A.ehrenbergiana, as well as under mixed tree species. The results showed that organic matter, moisture,potassium, calcium, nitrogen, and magnesium in topsoil at sites with A. tortilis and A. ehrenbergiana growing in combination with P. cineraria were higher than that at sites where P. juliflora was present (P＜0.05).Sodium at sites with A. tortilis and A. ehrenbergiana growing in combination with P. cineraria and P. juliflora was lower as compared to that at sites with just A. tortilis and A. ehrenbergiana. Electrical conductivity was lower at sites with A. tortilis and A. ehrenbergiana growing in combination with P. cineraria, and it was higher at sites with mixed Acacia and P. juliflora trees. Based on the generally more positive effect of native Acacia and P. cineraria on topsoil physiochemical properties as compared to the P. julifora, afforestation with native tree species is preferable for soil restoration. In addition, due to the negative effects of P. julifora on soil properties, P. julifora spread should be better managed.

Keywords: Prosopis juliflora; Prosopis cineraria; tree species; invasion; topsoil physiochemical properties; Iran

1 Introduction

Invasive alien species can negatively impact biodiversity, ecosystem services, and people's livelihoods and well-being (Hejda et al., 2009; Vilà et al., 2011; Shackleton et al., 2019). They can be predators, competitors, parasites, and disease transmitters, alter local biotic and abiotic environments, and become major ecosystem engineers in their new habitats (Reinhart and Callaway,2006; Blackburn et al., 2014), which can destabilize local environmental systems (Weidenhamer and Callaway, 2010; Gioria and Osborne, 2014).A key impact of invasive alien plant species on local soil is that they can alter soil chemistry and composition through mechanisms such as allelopathy, which in turn can alter native plant growth and development (Chou, 2010;Weidenhamer and Callaway, 2010). To better manage biological invasions, there needs to be sufficient scientific evidence of the impacts of introduced species on their recipient ecosystems to guide and justify decision-making.

Trees from the genusProsopishave been introduced to many regions around the world(Shackleton et al., 2014), and subsequent invasions have had significant effects on humans,biodiversity, and local environments (including soil).With regard to soil, it is known thatProsopis juliflorahas allelopathic effects and can impact adjacent plant communities (Inderjit et al., 2008; Kaur et al., 2012). Phenolic and other compounds such as tryptophan found in leaf and root extracts can induce these negative allelopathic effects. Allelopathic effects also influence cation exchange in soil (Shitanda et al., 2013; El-Shabasy, 2017).P. julifloracan also affect soil chemistry in other ways. In fact, one of the motivating factors for introducingP. juliflorais that it can increase soil carbon and nitrogen content (Moradi et al., 2013) as well as other nutrients such as potassium and organic matter. However,P. juliflorainvasions can also decrease calcium,magnesium, and sodium concentrations in soil (Shitanda et al., 2013). Furthermore,P. julifloracan alter soil microbial communities (Mosbah et al., 2018). These major changes in soil chemistry, properties, and biological communities may be one of the key factors influencing the prevalence ofP. julifloraand its spread in desert areas where it has been introduced (Al-Abdali et al., 2019).

In addition to the impacts on soil,Prosopisinvasions produce dense and impenetrable stands,affecting native biodiversity (El-Keblawy and Al-Rawai, 2007; Shackleton et al., 2015). TheProsopisinvasions also drastically reduce the growth of palatable forage species, which have negative implications for pastoralists' livelihoods (Pasiecznik et al., 2004; Linders et al., 2020).P.juliflorainvasions can also impact numerous other ecosystem services, such as water supply(Dzikiti et al., 2013; Shiferaw et al.,2019).

P. juliflorawas introduced to Iran and other parts of the Middle East, where it has become invasive and co-exists with the nativeProsopis cinerariaand other local tree species (Nascimento et al., 2020; Sharifian et al., 2022). In Iran,P. juliflorawas introduced to mitigate desertification and serve as a wood resource, despite its ecological role and some positive effects, it is now considered as a threatening invasive tree in many ecosystems in the country (Nahali, 2000;Sharifian et al., 2022). Despite the well-known negative effects ofP. juliflora,the treeis still recommended for land restoration programs in Asia (Edrisi et al., 2020), and more evidence of the effects of this tree on local desert systems is needed to guide decision-making.

The Sahara-Sindian forests of Iran are a highly fragile ecosystem, and undesired changes can drastically alter the succession paths of vegetation after disturbances, with implications for local pastoralists. In particular, the introduction, utilization, and dissemination ofP. juliflorapose a major threat to local arid forest systems. However, there is limited scientific evidence on the effects ofP. juliflorainvasions in Iran, and further information is needed to guide robust decision-making regarding the use and management of invasive trees and the selection of tree species for restoration in arid landscapes. Therefore, the aim of this study was to better understand the impacts ofP. juliflorainvasions on soil properties. To this end, we compared topsoil physiochemical properties at sites with invasive alien tree species (P. juliflora), native tree species (P. cineraria, Acacia tortilis,andAcacia ehrenbergiana), and mixed tree species in Hormozgan Province of Iran.

2 Materials and methods

2.1 Study area

The study was located in an arid riparian forest (26°31?34?N, 57°06?13?E), which is 75 km southeast of Minab City, Hormozgan Province of Iran. It covers 980 hm2and ranges between 0 to 100 m a.s.l. The annual average temperature is 28°C and the average annual precipitation is 226 mm. The study area has a sandy soil texture and extremely light soil. The flora of the study area is categorized as Sahara-Sindi, and common tree species includeA. tortilisandP. cineraria, withAcacia oerfota,Ziziphus spina-christi,A. ehrenbergianabeing less common. Annual and perennial grasses, such asCymbopogon olivieri,Chrysopogon aucheri,Cenchrus ciliaris,Pennisetum divisum, andTavernierasp., are dominant in the lower stratum. The increasingly invasiveP. juliflorais also becoming common in the area (Bijani et al., 2020).

2.2 Site selection

After scoping the area in May 2018, we selected a 5-hm2site that included all focal tree species for the study, includingP. juliflora,P. cineraria,A. tortilis, andA. ehrenbergiana. Specifically, we chose five sites with a canopy diameter greater than 2 m for each of the four target tree species(with no other tree species nearby). In addition, sites with the combinations ofP. cinerariaandA.tortilis,P. cinerariaandA. ehrenbergiana,P. julifloraandA. tortilis,andP. julifloraandA.ehrenbergiana(canopy diameter greater than 2 m) were also selected. The distance between sampling sites is 14 to 59 m.

2.3 Soil sampling

At the five sites, for each of the four individual tree species (P. juliflora,P. cineraria,A. tortilis,andA. ehrenbergiana), we collected four soil samples at a depth of 10 cm in four directions under the tree canopy, including north, east, south, and west (Fig. 1). The four samples were then mixed so that one composite soil sample was obtained from each individual site. A total of 20 samples were obtained from the sites with single tree species (Fig. 1a). For the sites with mixed tree species (i.e.,P. cinerariagrowing in combination withA. tortilis,P. cinerariagrowing in combination withA. ehrenbergiana,P. julifloragrowing in combination withA. tortilis, andP.julifloragrowing in combination withA. ehrenbergiana), five sites were randomly selected for each pair (El-Keblawy and Abdelfatah, 2014), and samples were obtained at a depth of 10 cm in four directions (north, east, south, and west) where the two tree canopies were overlapped (Fig.1b). The four samples were mixed to obtain one composite soil sample for each sample site. A total of 20 samples were obtained from the sites with mixed tree species (Fig. 1b). Finally, 40 soil samples were used for analysis.

Fig. 1 The schematic images of the soil sampling method at the sites with single tree species (a) and the sites with mixed tree species (b). N, north; E, east; S, south; W, west.

2.4 Measurement of soil physiochemical properties

The collected soil samples were sieved through a 2-mm mesh and transferred to the laboratory for the measurement of soil physiochemical properties. Soil acidity, soil organic matter, electrical conductivity (EC), exchangeable cations (sodium, potassium, calcium, nitrogen, and magnesium),and soil moisture were analyzed. Soil acidity was determined by using potentiometric method.The soil solutions were prepared with soil and distilled water at a ratio of 1:20, and soil pH was measured 24 h later with a pH meter (HM30V, TOA Electronics Ltd., Tokyo, Japan) (Smith and Doran, 1996). Soil organic matter content was determined using dry oxidation after burning the soil samples at 430°C. EC was determined on a saturation paste extract (Black, 1965).Exchangeable cations were calculated by ammonium acetate extraction method and quantified by an atomic absorption spectrophotometer (UNICAM 919, Unicam Ltd., Cambridge, UK) (Thomas,1982). Soil moisture was calculated by measuring the difference between wet weight and dry weight (placed in an oven at 105°C for 24 h) (Fadoul and Mohamed, 2016).

2.5 Data analysis

The data were analyzed using SPSS 24.0 statistical software. One-way analysis of variance(P＜0.05) was used to evaluate the difference in topsoil physicochemical properties among individual tree species, includingP.cineraria,P. juliflora,A. tortilis, andA. ehrenbergiana, and mixed tree species with the combinations of these tree species. Duncan's multiple range test was used to compare group means (P＜0.05). The normality of the data distribution and homogeneity of variance were evaluated by Shapiro-Wilk test and Levon's test, respectively.

3 Results

3.1 Effects of Prosopis cineraria, Prosopis juliflora, and Acacia tortilis as well as the combinations of these tree species on topsoil physiochemical properties

Soil organic matter, soil moisture, soil acidity, and EC differed significantly among sites with single tree species and also those withP. julifloragrowing in combination withA. tortilis(Table 1). Soil organic matter was higher at sites with onlyA. tortilis(1.36%) andP. cineraria(1.27%)and those withP. cinerariagrowing in combination withA. tortilis(1.46%), as compared to those with onlyP. juliflora(1.07%)andP. julifloragrowing in combination withA. tortilis(1.03%). Similar to soil organic matter, soil moisture was the highest at sites withP. cinerariagrowing in combination withA. tortillas(14.97%), followed by sites with singleP. cinerariaandA. tortilis;and it was lower at sites with singleP. julifloraandP. julifloragrowing in combination withA. tortilis(6.50%). Similarly, sites with singleP. juliflorahad lower soil acidity than those with native tree species. EC showed a different trend from other soil physiochemical properties. It was the highest at sites with onlyP. juliflora(2.23 S/cm), as opposed to sites with native tree species.

Table 1 Comparison of the effects of Prosopis cineraria, Prosopis juliflora, and Acacia tortilis as well as the combinations of these tree species on topsoil physiochemical properties

Exchangeable cations (sodium, potassium, calcium, and magnesium) at sites withA. tortilis,P.cineraria, andP. juliflorawere different from those at sites with mixed tree species (Fig. 2). Sodium(172.7 mg/L) and calcium (209.6 mg/L) concentrations were significantly higher at sites with onlyP. julifloraas compared to sites with mixed tree species (Fig. 2a and c). Calcium was significantly lower at sites withP. julifloragrowing in combination withA. tortilis(144.2 mg/L), which was similar for potassium (211.7 mg/L) and magnesium (45.22 mg/L). Magnesium was the highest at sites with onlyA. tortilis(86.96 mg/L) as well as at sites withA. tortilisgrowing in combination withP. cineraria(88.34 mg/L) (Fig 2d). Nitrogen at sites with only invasiveP. juliflorawas significantly lower than that at sites with the native tree species (Fig 2e). Sites withA. tortilisgrowing in combination withP. cinerariahad the highest nitrogen(0.71 g/kg).

Fig. 2 Effects of Prosopis cineraria, Prosopis juliflora, and Acacia tortilis as well as the combinations of these tree species on topsoil exchangeable cations. (a), sodium; (b), potassium; (c), calcium; (d), magnesium; (e),nitrogen. Different lowercase letters indicate significant differences among tree species (P＜0.05). Bars are standard deviations.

3.2 Effects of P. cineraria, P. juliflora, and Acacia ehrenbergiana as well as the combinations of these tree species on topsoil physiochemical properties

There was no significant difference in soil organic matter among sites with different tree species(Table 2). Soil moisture was significantly higher at sites with onlyP. cineraria(13.52%)and at sites withP. cinerariagrowing in combination withA. ehenbergiana(13.66%) as compared to sites with onlyP. juliflora(8.26%) andP. julifloragrowing in combination withA. ehenbergiana(8.03%). The highest soil acidity was observed at sites with onlyA. ehrenbergiana(7.60), which was significantly higher than that at sites with onlyP. juliflora(Table 2). The highest EC was observed at sites with onlyP. juliflora(2.23), which was significantly higher than that at sites with native tree species.

Table 2 Comparison of the effects of P. cineraria, P. juliflora, and Acacia ehrenbergiana as well as the combinations of these tree species on topsoil physiochemical properties

Exchangeable cations (sodium, potassium, calcium, and magnesium) were significantly different between sites with invasiveP.julifloraand native tree species (Fig. 3). Sodium (172.7 mg/L) and calcium (209.6 mg/L) were significantly higher at sites with onlyP. julifloracompared to sites with native tree species (Fig. 3a and c). In contrast, magnesium was significantly lower at sites withP. julifloraas compared to sites with single native tree species (Fig. 3 d). Potassium was the highest at sites withP. cinerariagrowing in combination withA. ehrenbergiana, and that was the lowest at sites with onlyP. julifloraand onlyA. ehrenbergiana(Fig. 3b). Nitrogen was the highest at sites with onlyP. cineraria(0.61 g/kg) and at sites withP. cinerariagrowing in combination withA. ehrenbergiana(0.63 g/kg), and was lower at sites with onlyP. juliflora(Fig.3e).

Fig. 3 Effects of P. cineraria, P. juliflora, and Acacia ehrenbergiana as well as the combinations of these tree species on topsoil exchangeable cations. (a), sodium; (b), potassium; (c), calcium; (d), magnesium; (e), nitrogen.Different lowercase letters indicate significant differences among tree species (P＜0.05). Bars mean standard deviation.

4 Discussion

P. juliflorais a notorious global invader with multiple negative effects (Shackleton et al., 2014),and despite this, the planting of this tree species is still promoted in many arid lands for improving the soils and restoring degraded ecosystems (Edrisi et al., 2020), including in Iran. To provide evidence to guide better decision-making, we assessed the effects ofP. julifloraon topsoil physiochemical properties in comparison to native tree species in Iran. The results showed that generally native tree species had similar or even better effects on topsoil physiochemical properties as compared toP. juliflora,suggesting that promoting native tree species for soil restoration in arid lands of Iran might be better than the use of non-native tree species. This is in line with the findings and suggestions of Sharifian et al. (2022).

More specifically, we found that soil organic matter at sites with single native tree species (A.tortilisandP. cineraria) and the combinations of native tree species (P. cinerariagrowing in combination withA. tortilis) was higher than that at sites with onlyP. julifloraorP. juliflorain the combination with native tree species. These results are consistent with the findings of Goel et al. (1989), Kahi et al. (2009), and Kaur et al.(2012), who also found the differences in soil organic matter betweenP. julifloraand native tree species. Annual fall of litter from trees constitutes the most important source of organic matter in soil, but this is also affected by some additional factors, such as decomposition under the influence of microbial activity,mineralization, the release of exchangeable cations, and soil moisture and oxygen (Kahi et al.,2009; El-Shabasy, 2017). These factors might explain the differences found in this study.

Soil moisture at sites withA. tortilis,A. ehrenbergiana, andP. cinerariawas higher than that at sites withP. juliflora. These results are consistent with those found by Guevara et al. (2010).P.juliflorahas extensive horizontal and vertical root systems that can absorb more moisture around itself (limiting the topsoil moisture available to other plants), which is less common in other tree species. Furthermore,P. juliflorais known to have a higher density of rhizobia and associated arbuscular mycorrhizal fungi thanA. tortilisandA. ehrenbergiana(Guevara et al., 2010), which allowsP. juliflorato obtain more water and thus leads to drier soil. InvasiveProsopis glandulosain South Africaalso has higher ground-water uptake (due to its larger root network and higher density) than native tree species, which may lead to the increased mortality of native trees where they co-exist withP. glandulosa(Schachtschneider and February, 2013; Dzikiti et al., 2017). This alteration to local soil moisture byP. julifloracompounded with climate change may lead to greater impacts on water availability in this region in the future (Sintayehu et al., 2020).

Similarly, we found that sites withP. juliflorahad lower soil acidity than those with native tree species,which is consistent with the findings of Goel and Behl (1999), Garg and Singh (2003),Bavaraja et al. (2007), and Shitanda et al. (2013). Soil acidity is an important factor in plant nutrient utilization, which increases the solubility of soil nutrients and the surface uptake of elements. A decrease in soil acidity can therefore be considered as a major ecological and ecosystem impact (Inderjit et al., 2008). It is likely thatP. juliflorahas inhibitory compounds in its litter and secretes organic acids from its roots (Goel and Behl, 1999; Shitanda et al., 2013),which can affect soil acidity. Most of the compounds in the topsoil are phenolic compounds,which are the result of allelopathy caused byP. juliflora. These compounds lead to the decrease in soil acidity at sites withA. tortilisandA. ehrenbergianain combination withP. juliflora(Bavaraja et al., 2007; Inderjit et al., 2008). In Sahara-Sindi forests, species prefer alkaline soil, so the reduction of soil acidity byP. julifloramay lead to a decrease in native plant species growth. This could have significant impacts on native plant communities and biodiversity in this region over the long-term (Bijani, 2020).

We found that EC in the topsoil at sites withP. juliflorawas higher than those withP.cineraria,A. tortilis,andA. ehrenbergiana, which is similar to the findings of Abbasi et al. (2011)and Moradi et al.(2013). Humus plays an important role in enhancing EC and is one of the reasons for its increase under tree canopies (Garg and Singh, 2003). Organic matter acts as a sponge, increasing the secretion of soil micro-organism gels and soil moisture retention potential(Kazemi et al., 2015). The higher soil moisture produced by soil organic material makes the soil more active. These factors can cause the release of inorganic ions, increasing the solute concentration and consequently lead to an increase in the EC of soil. Trees also influence the amount of EC by absorbing solutes from their roots and bringing them to the surface (Moradi et al., 2013). It is therefore likely that the strong rooting system ofP. julifloracan lead to an increase in soil EC as compared toA. tortilisandA. ehrenbergiana(Kahi, 2009).

Sodium and calcium concentrations were generally higher in soil under the canopy of invasiveP. juliflora.Conversely, magnesium, nitrogen, and potassium were generally lower at sites withP.julifloraas compared to sites with just nativeAcaciaandProsopis. This is similar to the findings of Garg and Singh (2003), Bavaraja et al. (2007), and Kahi (2009), who also found differences in topsoil exchangeable cations at sites with invasiveP. juliflora.It should be noted that the combination of cations and metal ions in the soil accelerates the inhibitory effect of allelopathy(Zhang et al., 2015). This might be the main reason for the generally lower levels of calcium,potassium, and magnesium at sites withA. tortilisandA. ehrenbergianain combination withP.julifloraas opposed to sites with onlyAcaciaspecies.

5 Conclusions

Our results highlighted thatP. juliflorainvasions can alter topsoil physiochemical properties which may have knock-on negative effects on native plant communities.The results showed that soil organic matter, soil moisture, and exchangeable cations (potassium, calcium, nitrogen, and magnesium) were generally higher at sites with the native tree species (A. tortilis,A.ehrenbergiana, andP. cineraria) as compared to sites withP. juliflora. In addition, we also found that sites withP. julifloraled to an increase in EC and a decrease in soil acidity, which could affect the growth of native plants and the stability of local ecosystems in the long-run. This suggests that caution is needed when promoting and using known invasive trees such asP.juliflorafor restoration initiatives, and that the use of native tree species may be more suitable for building resilient ecosystems in the long-term. More research is needed on which native tree species are most suitable for restoration programs in arid areas.

Acknowledgements

The authors appreciate the Bandar Abbas Branch, Islamic Azad University and Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization(AREEO), Iran.