Abstract
Background and aims
Olive trees are one of the most important crops in the Mediterranean, especially in Morocco, and they are vulnerable to various soil-borne pathogens that can cause significant yield losses and economic damage. This study aimed to investigate the diversity, abundance, and community composition of phytopathogenic nematodes in Moroccan olive agroecosystems, and to evaluate the impact of agroecological patterns on their abundance.
Methods
Soil and root samples were collected from 13 olive-growing localities across 7 Moroccan regions (43 nurseries/22 orchards), and nematodes were ecologically assessed through the calculation of several diversity indices (e.g., Shannon Index, Evenness, and Plant Parasitic Index). In addition, the main nematode genera were evaluated in terms of soil types, irrigation regimes, and landscape complexity.
Results
The obtained results revealed the presence of a diverse and complex community of phytopathogenic nematodes represented by 25 genera, including Meloidogyne, Pratylenchus, and Helicotylenchus among others. The abundance and diversity of nematodes varied significantly between the different regions and agroecological patterns, with higher densities observed in simple landscapes and higher irrigation regimes. Moreover, the community of dominant nematodes was influenced by soil types. Root-knot nematodes were the most prevalent in sandy soils, while root-lesion nematodes were significantly present in the clayish setting. The occurrence and severity of nematode damage were also correlated with the overall taxonomic richness shaped in different olive landscape modes.
Conclusion
This study provides updated information and prospects into nematode sustainable monitoring and management in North African olive agroecosystems.
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Introduction
Olive trees (Olea europaea L.) have a long and rich history in the Mediterranean region and have played an important role in the economy and culture of the area for centuries. Olives and their by-products are a crucial component of the Mediterranean diet, providing the primary source of dietary fats and vegetable oils (El and Karakaya 2009). In Morocco, olive trees have been cultivated for thousands of years, and today the country is one of the largest producers of olive oil in the world, with over 1.2 million hectares, making up to 65% of the total cultivated agricultural land with an annual production of over 1.9 Mt (FAOSTAT 2022). These trees are predominantly found in arid and semi-arid regions with inconsistent rainfall patterns (Breton et al. 2009).
However, the Moroccan production pattern of olives is facing numerous challenges caused by soil-borne pathogens including the infestation by phytopathogenic nematodes (PPNs). These microscopic pathogens cause extensive damage to crops worldwide estimated at 14.6% (157 billion US$/year) (Nicol et al. 2011). They can have negative effects on cultivated olive trees, reducing tree growth and causing yield losses of 5–10% (Koenning et al. 1999; Nico et al. 2002). Intensive cultivation systems and nurseries are more susceptible to the negative effects of nematode reproduction due to favorable irrigation conditions (Castillo et al. 2010). Research has discovered that olive trees, whether in orchards, nurseries, or even some wild areas, are hosts to 153 PPN species belonging to 56 genera (Ali et al. 2014). Several PPN genera have been reported in Moroccan olive nurseries and orchards (Ali et al. 2014, 2015, 2016; Hamza et al. 2017). For instance, root-knot nematodes (RKNs, Meloidogyne spp.), root lesion nematodes (RLNs, Pratylenchus spp.), and spiral nematodes (SNs, Helicotylenchus spp.) are the most dominant PPNs across olive-growing regions. The genus Meloidogyne has the largest economic importance in infesting olive areas as it occurs with four devastating species (Meloidogyne javanica, M. incognita, M. arenaria, and M. spartelensis) (Ali et al. 2015; Hamza et al. 2017, 2018). Furthermore, Pratylenchus genera are mainly represented by Pratylenchus neglectus, and P. pinguicaudatus (Ali et al. 2015; Hamza et al. 2017), and they are widely distributed with high densities. Helicotylenchus genera are also abundant with a large spectrum of species including Helicotylenchus vulgaris, H. dihystera, H. digonicus, and H. canadensis (Hamza et al. 2018). The impact of PPNs on olive trees can result in reduced growth, stunted plant development, and decreased fruit yield and quality. These effects can be compounded by agroecological factors, such as soil type, cropping system, water regime, and landscape complexity, which can all impact PPN distribution and biodiversity (Altaf et al. 2017).
The importance of soil type and irrigation on Phytopathogenic nematode communities in olive trees cannot be overstated. Soil characteristics and water availability are crucial factors influencing the distribution, abundance, and activity of nematodes in agricultural systems, including olive groves (Guesmi–Mzoughi et al. 2022; Barbera et al. 2013; Hamza et al. 2017; 2018; Laasli et al. 2023). Recent research studies have highlighted the influence of soil texture on the abundance and diversity of soil nematodes (Kekelis et al. 2022; Landi et al. 2022). These studies elucidated the significant affinity of these microorganisms in sandy and clayey soils. This affinity is strongly dependent on nematode genera. Specifically in olive groves, Guesmi–Mzoughi et al. (2022) demonstrated that sandy soils are more suitable for the multiplication of sedentary endoparasitic genera (e.g., Meloidogyne and Heterodera spp.), while the Pratylenchus genus was more prevalent in clay soils. These findings imply that soil is the most influential factor driving PPN communities when interacting with their respective host.
Irrigation practices significantly influence the population dynamics and distribution of olive PPNs (Guesmi–Mzoughi et al. 2022). The availability of water in the soil is a critical factor for the survival, movement, and infection process of these nematodes (Nicol et al. 2011; Mohawesh and Karajeh 2014). Nematode populations are sensitive and variable to changes in soil moisture, and the irrigation regime can be manipulated to reduce nematode infestation to recover the plant’s health and productivity (Reddy 2017). In that manner, studies conducted by Song et al. (2016) and Bristol et al. (2023) found that increased rainfall, simulated through irrigation, led to a rise in PPN populations, likely due to enhanced plant productivity. The effect of vegetation complexity on PPN communities is another area of growing interest. Complex vegetative cover can provide diverse habitats and resources for nematode populations, potentially influencing their abundance, diversity, and impact on different crops (Šalamún et al. 2017; Brustolin et al. 2018). In that sense, soil nematodes could be significantly impacted by landscape change (Porazinska et al. 2021).
Despite the recent progress made in understanding the effects of agroecological patterns on PPNs, there remain significant knowledge gaps in this area (especially in Morocco). One such gap is the influence of drip irrigation-based regimes (configured by evapotranspiration levels) and their subsequent effects on olive nematodes. In addition, vegetation patterns have not been studied yet on olive PPNs. These gaps constitute the main objectives of this study alongside further insights on soil type influence and nematode diversity in all potential olive areas in Morocco. The studied agroecological factors are hypothesized to have a significant effect on nematode entities, by creating distinct microenvironments that support specific nematode genera. This study will provide ecological insights into the dynamics of nematode communities in relation to their environment, which is crucial for their sustainable management.
Materials and methods
Survey description and sampling
An extensive survey was conducted in potential olive agroecosystems (nurseries and orchards) located in seven regions of Morocco (North: Rabat-Salé-Kenitra, Fes-Meknes, and Settat-Casablanca), (South: Draa-Tafilalet and Souss-Massa), (West: Marrakesh-Safi), and (East: Beni Mellal-Khenifra), divided in 13 localities (Fig. S1; Table 1). These regions are characterized by important olive production and were chosen based on their proximity to each other, their altitude range, and the presence of PPN damage signs. The climate in these regions ranged from arid to subhumid while the soil types are represented by all key components (sand, clay, and loam) (Table 1). Twenty-two olive orchards were surveyed, and 10 trees per orchard were considered for the sampling procedure. To collect soil and root samples, a zigzag pattern was followed in the top 25 cm layer of soil depth, covering approximately 100 m2 per orchard, using a 25 mm diameter auger. After collection, subsamples were combined to form a representative 2 kg sample, consisting of 20 soil and 15 root subsamples per olive orchard/nursery. In the case of nurseries, a total of 43 entities were prospected for PPN infestation, based on their geographic location, growth substrates, and cultivar diversity (Table 1). The majority of substrates used were loamy-cropped soils, and the five primary olive cultivars adopted were Picholine Marocaine (Morocco), Menara (Morocco), Haouzia (Morocco), Picholine Languedoc (France), and Arbequina (Spain). Following the same sampling procedure, we placed samples in polyethylene bags to prevent water loss and transported them immediately to the Nematology laboratory at INRA-Rabat for nematode extraction and processing.
Nematode extraction and diagnosis
The soil and root samples were processed for nematode isolation within 48 h of collection using the modified Baermann method as described by Hooper (1986). Nematodes were extracted from 100 cm3 of soil and 20 g of root samples over a 72-hour incubation period. The nematode suspension was then examined under a stereomicroscope (Olympus CH-2, Japan) to measure the abundance of each genus. To preserve the samples, the nematodes were killed and fixed with hot formaldehyde (4%) and then transferred to a solution consisting of formaldehyde (4%) and glycerin (99/1; v/v). The nematodes were placed on a square watch glass with a diameter of 7 cm in a desiccator containing approximately 1/10 ethanol volume. The following day, the nematodes were removed from the desiccator and incubated at 37 °C. Within 3 h, a solution consisting of ethanol (96%) and glycerin (95/5; v/v) was added in triplicate to a watch glass partially covered with a glass slide to promote evaporation. Finally, a solution of ethanol (96%) and pure glycerol (50/50; v/v) was added, and the watch glass was placed in an incubator at 37 °C overnight according to De Grisse’s method (De Grisse 1969).
The nematodes were identified based on their morphological characteristics, such as body size, shape, and stylet features using diagnostic keys (Mai and Lyon 1975; Mai and Mullin 1996). The glycerin-ethanol method was used for species identification using specific keys (Ryss 1988; Siddiqi 2000; Castillo 2007; Brzeski 1991; Andrássy 2005; Geraert 2008, 2010, 2011) under a light microscope (Nikon Eclipse E200, Tokyo, Japan). For Meloidogyne species, perineal samples were used for identification, and five samples were prepared and placed in glycerin for microscopy according to Taylor and Netscher (1974). Heterodera species (CNs) were extracted using the flotation method according to Hooper et al. (2005), and vulval cones were used for identification as described by Handoo (2002).
Nematode assessment
Following the evaluation of PPN densities (per 100 cm³ and 20 g of soil and root matrices, respectively), a taxonomic assessment of PPNs was established by calculating different ecological indices based on the total number of nematodes (Ntotal), generic richness (G) stating the number of genera per each community. These indices include Plant Parasitic Index (PPI = \(\sum \left(\text{v}\text{i}\right)\times \left(\text{f}\text{i}\right)\)), where vi involves the p-p (plant-parasitic) values of nematode genus i, and fi is the relative frequency of genus i occurring in a sample (Bongers 1990). Shannon–Weaver diversity index \(\text{H}^{\prime}=-\sum\nolimits_{\text{i}-1}^\text{s}\text{pi ln pi}\), where s depicts the richness of nematode genera, pi is the genera proportion, and the Evenness \(\text{E}=\text{H}/\text{Hmax},\text{Hmax}={\text{log}}_2s\) (Krebs 1985). In addition, specific indices of nematode species were calculated considering their feeding level: ectoparasites (Iecto), migratory endoparasites (Iendo_mig), and sedentary endoparasites (Iendo_sed). Each index highlights specifically the extent of the corresponding nematode species in their ecological niche (Guesmi-Mzoughi et al. 2022).
Agro-ecological relationships to phytopathogenic infestations of nematodes
To investigate the relationships between PPN infestation in olive areas (orchards and nurseries) and agro-ecological patterns, three main nematode genera (Meloidogyne spp., Pratylenchus spp., and Helicotylenchus spp.) were assessed for their abundance according to progressive levels of soil substrates, irrigation regime, and landscape complexity.
Nematode genera abundance was assessed in four soil types i.e., sandy, sandy-clay-loam, medium loam, and clay. For irrigation regime (IR), these genera were evaluated in olive nurseries at three levels according to the evapotranspiration percentage (ETP) (Low = 25%, Moderate = 50%, and High = 75%) in a drip irrigation setting (Fig. 1). Five olive varieties were considered including Picholine Marocaine (Pm), Picholine Languedoc (PL), Arbequina (Arb), Menara (Mn), and Haouzia (Hz). The experiment was conducted in a fully randomized block design (FRBD) and repeated 3 times (n = 3) for data validation. A negative control (C) plot was considered for all varieties with a regular IR and no nematode infection.
In olive orchards, main PPN feeding types (e.g., sedentary endoparasites, migratory endoparasites, and ectoparasites) were further assessed as a function of the associated landscape complexity (LC). This parameter highlights the amount of vegetation presented within olive cultivation and it ranged from low to complex (Fig. S2). Intercropping events were observed in intermediate and complex landscape levels.
Statistical data analytics
In the surveyed areas, the dominance parameter was determined for each nematode genera, and their frequencies were recorded. To analyze the abundance variables, a distribution diagram of nematode communities was generated after transforming the values to log10 (X + 1). To examine the distribution of PPN communities in different olive agroecosystems, Principal Component Analysis (PCA) was carried out using sklearn.decomposition.PCA module implemented in Python. The datasets involving nematode abundances for each factor were first normalized using the Anderson-Darling normality test (Stephens 1974), and the PPN variables associated with the PCA were analyzed using a one-way ANOVA with the XLSTAT 2016.02.28451 software (Addinsoft, New York, NY, USA). To determine the significant differences among the variables at P < 0.05, Fisher’s protected least significant difference (LSD), Tukey, and Duncan tests were employed. Score plots were performed to visualize and assess the homogeneity of the prospected olive sites in terms of PPN distribution patterns. Furthermore, a correlation matrix (Pearson type) was generated to highlight the relationship strengths between different nematode genera using the package corrplot (ver. 0.92) in R (ver. 4.0.5) software (Wei et al. 2017).
For agroecological patterns, a Violin plot was generated using seaborn.violinplot module in Python to compare different nematode abundance values between IR levels. In addition, exponential regression analysis was produced to predict the linkage between nematode taxonomic richness (G), the total number of genera, and land complexity levels that occurred within olive orchards.
Results
Nematode community composition and ecological distribution in moroccan olive agroecosystems
The collected soil and root samples from the olive orchards contained a total of 25 different genera of phytopathogenic nematodes. The most common species found were Meloidogyne spp., Pratylenchus spp., and Helicotylenchus spp. (Table 2). The diversity of nematode communities varied between nurseries/orchards, with some localities showing high levels of diversity and others showing low levels (Fig. S3). The highest PPN density rates were recorded in MK, FS, OU, and CH. In terms of feeding behavior, sedentary endoparasites (Meloidogyne and Heterodera spp.) were significantly dominant in CH, FS, MK, OU, SM, and TA (up to 895 nematodes per 100 cm³ of soil and 20 g of roots) (Findex = 150.6; df = 12; P < 0.05) (Fig. S3). Migratory endoparasites (e.g., Pratylenchus spp.) were significantly present in CH, FS, and MK (up to 720 nematodes), while ES, SK, SM, and TA recorded lower values (down to 256 nematodes) (Findex = 124.3; df = 12; P < 0.05). Furthermore, significant densities of ectoparasites were also recorded in ES, MA, MK, OU, and TF (up to 149 nematodes) (Findex = 81.5; df = 12; P < 0.05) (Fig. S3).
At the genus level, the RKN (Meloidogyne spp.) had the highest average density in the olive root matrix (750.4 nematodes) (Findex = 102.9; df = 24; P < 0.05) followed by the Pratylenchus spp. (560.9 nematodes) and Tylenchorhynchus spp. (285.6 nematodes) (Fig. S4). On the other hand, Pratylenchus genera were significantly found in soil matrices at the highest rates (721.6 nematodes) (Findex = 111.2; df = 24; P < 0.05) followed by Meloidogyne spp. and Helicotylenchus spp. (566.2 and 480.1 nematodes, respectively). The lowest rates were recorded by 11 nematode genera in both matrices including Aphelenchus, Aphelenchoides, Coslenchus, Criconema, Criconemoides, Ditylenchus, Filenchus, and Zygotylenchus spp. (down to 9.4 nematodes) (Fig. S4).
The abundance and frequency of nematodes in each surveyed region were calculated. A total of 25 genera were identified, with Meloidogyne, Pratylenchus, and Helicotylenchus being the dominant and frequent ones. Ten genera were frequent but with lower abundance in the surveyed areas, namely Aphelenchoides, Hoplolaimus, Rotylenchus, Ditylenchus, Heterodera, Paratylenchus, and Zygotylenchus. Additionally, there were some occasional genera observed, including Aphelenchus, Pratylenchoides, Longidorus, and Xiphinema. However, 7 genera were rarely found, such as Rotylenchulus, Filenchus, Trichodorus, Trophorus, Telotylenchus, Criconema, and Criconemoides (Fig. 2).
At the species level, three distinct species of Meloidogyne spp. were identified according to the perineal patterns including Meloidogyne incognita (high presence), M. javanica, and M. arenaria. Pratylenchus spp. were represented in two species including Pratylenchus thornei, and P. neglectus (high presence) (Table S1). Similarly, Helicotylenchus vulgaris and H. dihystera were the two species recorded for Helicotylenchus genus. The stem nematode (Ditylenchus spp.) was represented by D. dipsaci, while the citrus nematode (Rotylenchulus semipenetrans) was also detected.
Diversity Trends of moroccan olive PPNs
The PCA showed a diverse pattern of PPN genera distributed differently in the sampling sites (Fig. S5). The first two PCA axes (PC1 and PC2) accounted for 39.8% and 23.1%, respectively of the total variance (Fig. S5A). The score plots (Fig. S5B) showed that the prospected sites are well separated and classified by PPN diversity. For instance, the TA region was distinctively separated from MA, ES, CH, and HZ by the absence or presence of the Rotylenchus, Heterodera, and Merlinius genera. The same goes for all localities.
Figure 3 showcased the attribution trends of the PPN ecological indices calculated for olive-growing locations. The first two PCA axes accounted for 52.3% and 39.8%, respectively of the total variance (Fig. 3A). The PCA plot showed that some diversity indicators (e.g., G, PPI, and E) were more important in the localities of FS, CH, TA, SM, HZ, and MK. The H’, and Hmax were of high weight in MK, ES, and HZ. In addition, specific indices of nematode species (Iecto, Iendo_mig, and Iendo_sed) were highly indicated in the MK region (Fig. 3B).
The relationship patterns between PPNs identified in Moroccan olive agroecosystems were established through a correlation analysis (Fig. S6). Significant positive correlations were detected including those between Aphelenchus and Zygotylenchus (r = 0.72), Criconema and Paratylenchus (r = 0.83), and Rotylenchulus and Tylenchorhynchus (r = 0.86). Furthermore, Hoplolaimus was moderately associated with Paratylenchus (r = 0.54) while Trichodorus was similarly linked with Tylenchorhynchus (r = 0.46). On the other hand, Ahelenchus had a significant negative correlation with Tel (r = − 0.87). The same was recorded with Xiphinema and Rotylenchulus (r = − 0.76), and Telotylenchus and Xiphinema (r = − 0.69) (Fig. S6). In other cases, many nematode genera didn’t have any association with each other.
Impact of agroecological factors (soil type, irrigation regime, and landscape complexity) on olive PPNs
The abundance of dominant PPN genera detected in Moroccan olive orchards (Meloidogyne, Pratylenchus, and Helicotylenchus spp.) was assessed in terms of four soil types (sandy, clay, medium loam, and sandy-clay-loam). Meloidogyne was significantly abundant in sandy, sandy-clay-loam, and medium loam types (60–70%) (Findex = 72.9; df = 3; P < 0.05). Oppositely, Pratylenchus significantly prevailed in clay and medium loam soils compared to the others (Findex = 87.5; df = 3; P < 0.05). No significant differences were obtained between soil types in terms of Helicotylenchus abundance (Findex = 56.1; df = 3; P > 0.05) (Fig. 4A).
The dominant nematode genera in olive nurseries were also assessed as a function of three irrigation regimes (IRs) levels according to the evapotranspiration percentages (ETP) performed in drip irrigation mode. Meloidogyne genera were significantly abundant starting from the moderate regime to the higher one (Findex = 71.2; df = 2; P < 0.05) (Fig. 4B). Furthermore, Pratylenchus genera showed to be in significant abundance in the higher IRs (especially in 75% ETP regime) (Findex = 76.5; df = 2; P < 0.05). Furthermore, Helicotylenchus genera were relatively less abundant in the three IRs compared to the other genera. In addition, these nematodes are seemingly unaffected by the higher IRs (Findex = 56.8; df = 2; P < 0.05) (Fig. 4B).
Throughout the experiment, plant parameters such as plant height and root length were assessed to see the impact of PPNs functioning within progressive IR levels (Fig. 5). In terms of irrigation regimes, plant height was significantly reduced in the low and high IRs (25 and 75% ETP), while the moderate IR showed high values (Findex = 103.5; df = 2; P < 0.05). However, the values were significantly lower than the negative control (C) (Findex = 123.4; df = 3; P < 0.05) (Fig. 5A). The same trend was more or less observed with the root length (Findex = 96.1; df = 3; P < 0.05) (Fig. 5B). As for nematode genera factor, Meloidogyne and Pratylenchus seem to have a significant impact on plant height (Findex = 120.6; df = 2; P < 0.05) and root length (Findex = 104.3; df = 2; P < 0.05). Noticeably, all olive varieties were negatively and prominently affected by Meloidogyne compared to Pratylenchus and Helicotylenchus (Fig. 5).
Phytopathogenic nematodes, grouped into main feeding aspects were thoroughly assessed in different olive landscape complexity (LCs) levels (simple, intermediate, and complex). Sedentary (Endo_sed) and migratory (Endo_mig) endoparasites were significantly abundant in simple and intermediate landscapes (Findex = 88.9; df = 2; P < 0.05), while lower values were observed in complex structured orchards (Fig. 6). Similarly, ectoparasites (Ecto) showed a significant abundance (70%) in simple landscapes compared to the diversified ones (Findex = 71.2.9; df = 2; P < 0.05). Interestingly, the Pratylenchus genus was more dominant than Meloidogyne in all landscape settings except for the intermediate one, while genera including Xiphinema, Longidorus, and Trichodorus were less redundant in the complex landscapes (Fig. 6).
By going deep into the landscape complexity mechanics in the distribution of olive PPNs, the relationship between taxonomic richness (G) and the total number of species (Ntotal) was elaborated using exponential regression analysis (Fig. S7). Overall, a strong association was obtained between the two parameters (R² = 0.74) that highlighted PPN distribution patterns based on different LCs. For instance, the studied parameters were significantly increased in complex landscapes followed by intermediate, and then came the samples orchards (Fig. S7).
Discussion
Diversity of phytopathogenic nematodes in moroccan olive agroecosystems
The biodiversity of phytopathogenic nematodes in olive nurseries and orchards has extensive trends worldwide. These pathogens represent a prominent threat to both agronomic and socioeconomic sectors of olive-producing areas (Pandey and Mukerji 2006; Fernández-Escobar et al. 2013; Laasli et al. 2023). In most cases, PPN damages cause significant yield loss, especially for susceptible olive varieties which require immediate interventions targeting sustainable PPN management (Nico et al. 2003; Abbas and Mohammad 2005; Palomares–Rius et al. 2019). This study provides insights and updated information on the biodiversity of PPN communities in Moroccan olive nurseries/orchards and their linkage to agroecological patterns.
Across 43 prospected olive nurseries and orchards, twenty-five PPN genera were detected and identified. Meloidogyne spp., Pratylenchus spp., and Helicotylenchus spp. were abundant and frequent in all olive-growing areas. In the same manner, Hamza et al. (2018) discussed the diversity of phytopathogenic nematode communities found in Moroccan olive nurseries and the potential impacts of these communities on the environment. They found that the nematode communities in the olive nurseries were diverse, with a mix of native and introduced species. Thirteen nematode families were shown to be linked with olives including Telotylenchidae, Pratylenchidae, Longidoridae, and Hoplolaimidae. The latter had the highest number of species identified. In our study, Pratylenchus spp., Helicotylenchus spp., and Meloidogyne spp. had the highest infestation frequencies. The same findings were obtained in Tunisia (Guesmi–Mzoughi et al. 2022), Algeria (Chafaa et al. 2014; Belahmar et al. 2015), Libya (Buarousha et al. 2020), and Egypt (Ibrahim et al. 2010; Abdel–Baset et al. 2022).
Meloidogyne genera are significant pathogens of olive trees, causing damage in many olive nurseries around the world (Martelli et al. 2000). In our study, three species were encountered including Meloidogyne javanica, M. incognita, and M. arenaria. Several studies highlighted the occurrence of the same species across multiple olive agroecosystems worldwide (Nico et al. 2002; Wesemael et al. 2011; Archidona-Yuste et al. 2018; Keshari and Mallikarjun 2022). Pratylenchus genera are migratory endoparasites that are widely distributed and capable of infecting a diverse range of plant species (Vovlas et al. 2000). Among the species identified in our study, Pratylenchus neglectus, and P. thornei were the most prevalent. Other studies have highlighted the diversity of the same RLN species alongside the presence of others including P. zeae, P. mediterraneus, P. crenatus, and P. vulnus (Lamberti and Vovlas 1993; Cilbircioğlu 2007). As for Helicotylenchus spp., it has been well-established in most Moroccan olive nurseries and orchards surveyed. Two distinct species (H. vulgaris, and H. dihystera) have shown a prominent presence. However, A total of 11 species have been found previously in Morocco including H. crassatus, H. digonicus, and H. varicaudatus which were the most dominant (Hamza et al. 2018). Helicotylenchus digonicus is a dominant spiral nematode species in many olive orchards, with high prevalence in many regions (Archidona-Yuste et al. 2020), while other species (e.g., H. oleae) were found across Mediterranean countries (Inserra et al. 1979).
Impact of soil type on olive PPN distribution patterns
Soil type can have a significant impact on the distribution and abundance of nematodes (Nisa et al. 2021). Understanding the relationship between soil type and nematode populations can help farmers and researchers develop effective management strategies to reduce crop damage and increase yields (Neher 2001). In our study, Meloidogyne, Pratylenchus, and Helicotylenchus are the main genera of PPNs that have been extensively studied with four soil types (sandy, sandy-clay-loam, medium loam, and clay) due to their representative dominance throughout all localities. Meloidogyne was abundant in sandy soils while Pratylenchus was highly present in clayish and loam settings. Similarly, previous studies have shown that the distribution of Meloidogyne and Pratylenchus was significantly influenced by soil texture (Griffin 1996; Trinh et al. 2009; Hamza et al. 2018; Mokrini et al. 2019). In Tunisia, Guesmi–Mzoughi et al. (2022) found that Meloidogyne genera were more abundant in sandy soils, while Pratylenchus were more abundant in clay soils within olive orchards. Another study conducted in Benin found that the abundance of Helicotylenchus dihystera was positively linked to the soil’s organic properties and negatively affiliated with soil granulometry (Baimey et al. 2009).
Meloidogyne species prefer sandy soils due to their larger particle sizes, which result in high permeability and rapid drainage. Sandy soils have low water-holding capacity, limited nutrient availability, and reduced competition from other soil organisms, all of which favor survival and reproduction. These nematodes can easily migrate through sandy soil particles, access plant roots, and cause root damage (Perry et al. 2009; Nyczepir and Thomas 2009; Nicol et al. 2011). Conversely, Pratylenchus species prefer clayish and loam soils due to their smaller pore spaces and higher water-holding capacities. These soils allow nematodes to move more freely and provide a suitable environment for their life cycle (Luc et al. 2005). Clayish and loam soils also retain organic matter, promoting microbial communities that support nematode populations. The compact structure of these soils facilitates the nematodes’ feeding processes and leads to root damage and plant decline (Sundararaju and Jeyabaskaran 2003; Nicol et al. 2011).
Irrigation regime influence on olive PPN abundance and plant interactions
The effect of irrigation regimes on PPNs has been studied extensively, and the results have shown that different nematode species respond differently to different IRs based on ETP percentages. For instance, Meloidogyne and Pratylenchus genera were significantly abundant in high IR levels. In that manner, Meloidogyne spp. is known to prefer moist soil conditions for their survival and reproduction (Evans and Perry 2009). Hence, continuous and heavy irrigation regimes promote their growth and reproduction (Porazinska et al. 1998; Majić et al. 2021). Studies have shown that increasing levels of drip irrigation, which provides water directly to the plant roots, increase PPN populations in the soil compared to traditional flood irrigation (Okasha et al. 2020; Choudhary and Bhambri 2013; 2021). In addition, some Pratylenchus species are known to prefer drier soil conditions for their survival and reproduction without relying on a rhizospheric biota (Castillo and Vovlas 2010). Studies have shown that reduced irrigation regimes can help in reducing the populations of Pratylenchus in the soil (Kuchta et al. 2021; Phani et al. 2021). For instance, a study conducted on cotton crops in Brazil showed that the reduction in irrigation from 60 to 30% of the crop’s water requirement resulted in a significant reduction in RLN populations in the soil (Ribeiro et al. 2012). On the other hand, Helicotylenchus spp. has shown mixed responses to different IRs. Studies have shown that under water-stressed conditions, their populations decrease, while under excessive irrigation, their populations increase (Ko et al. 1997; Eissa et al. 2003; Majić et al. 2021). For instance, a study conducted on tomato crops in Egypt showed that Helicotylenchus populations increased with increasing irrigation levels (Taha 2020). Therefore, these abundance trends are dependently affiliated with plant growth parameters as they affect the tendencies of plant height and root length values (Cadet et al. 2004; Da Silva et al. 2017). These values are essentially dependent on the Plant × Nematode interaction (Wilschut and Geisen 2021).
Varied effects of landscape complexity on olive PPN
Understanding how landscape complexity affects these nematodes is crucial in developing effective management strategies to minimize their impact (Brustolin et al. 2018). Our findings revealed that nematode abundance was significantly decreased going from simple landscapes to complex ones. In simple landscapes, such as monoculture fields or urban areas, the nematode populations may be higher due to the lack of natural predators and other factors that could limit their growth (Jackson et al. 2019; Porazinska et al. 2021). In contrast, complex landscapes with more diverse plant communities and varied topography can provide a habitat for natural enemies of nematodes, such as predatory mites and fungi (Porazinska et al. 2021). Therefore, nematode populations may be lower in complex landscapes. For instance, a study conducted in a complex landscape in France found that the nematode community could have some diversity limitations in areas characterized by high land complexity. These limitations are attributed to the homogeneity of vegetation in the landscape rather than the presence of multiple plant genera within (Duyck et al. 2012).
Moreover, a study by Flores et al. (2014) found that increasing landscape complexity (i.e., increasing the number of landscape elements such as hedgerows, woodlands, and ponds) decreased the abundance of Meloidogyne spp., in agricultural soils. Similarly, a study by Tarno et al. (2021) found that increasing landscape complexity reduced the abundance of Pratylenchus spp., in agricultural soils. However, the effects of landscape complexity on PPNs can be complex and may depend on the specific nematode species and the surrounding landscape (Flores et al. 2014). For instance, a study conducted by Cavigelli et al. (2005) found that landscape complexity did not affect the abundance of the dagger nematode, Xiphinema spp., in maize-based soils. This may be because these nematodes have a specific host range and are less affected by the diversity of vegetation types in the surrounding landscape (Cavigelli et al. 2005).
Future research implications
The study of phytopathogenic nematode communities infesting Moroccan olive agroecosystems and the impact of agroecological patterns presents significant implications for future research. A comprehensive understanding of these communities and their influence on olive crop productivity is essential for developing effective, sustainable management strategies (Ali et al. 2014). Recent studies have started to uncover the complex interactions between nematode communities, agroecosystem characteristics, and environmental factors in Moroccan olive orchards (Laasli et al. 2023). However, more extensive research is needed to fully grasp the ecological processes shaping these communities and the potential consequences of agroecological patterns on crop health and disease management. Future studies should consider expanding the geographic scope and incorporating advanced molecular techniques to characterize nematode diversity and their functional roles within the agroecosystem. Additionally, research should focus on understanding the effects of land use change, agricultural practices, and climate change on nematode community dynamics to help inform policy and decision-making in the context of sustainable agriculture.
Conclusion
This study provides updated information and insights on the incidence of phytopathogenic nematode communities in Moroccan olive agroecosystems. Twenty-five PPN genera were detected, with Meloidogyne, Pratylenchus, and Helicotylenchus being the most prominent. Their positive/negative interaction with soil, irrigation, and landscape complexity was revealed, offering opportunities for sustainable management. Future research should focus on the dynamics of all soil nematode communities, employing metagenomics, transcriptomics, and proteomics for deeper insights into their functional dynamics and interactions. Additionally, a comprehensive soil health mapping of olive-growing regions is recommended to develop sustainable agricultural practices for effective nematode population management and disease control.
Data availability
The data that supports the findings of this study are available on request from the corresponding author.
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The authors are grateful to the farmers and stakeholders for assisting by giving the required information during field surveys.
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This work was funded by SIRAM (Sustainable Innovations for Regenerative Agriculture in the Mediterranean Area) Project affiliated with PRIMA.
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Conceptualization: SEL, FM, AAD and RL; Methodology: SEL, RL and FM; Formal analysis and investigation: SEL, FM, and RL; Writing - original draft preparation: SEL; Writing - review and editing: SEL, FM, DI, MS, SA, AAD, TP, KK, and RL; Funding acquisition: RL; Resources: SA, and RL; Supervision: FM, AAD and RL.
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Laasli, SE., Mokrini, F., Iraqi, D. et al. Phytopathogenic nematode communities infesting Moroccan olive agroecosystems: impact of agroecological patterns. Plant Soil 501, 39–55 (2024). https://doi.org/10.1007/s11104-023-06190-5
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DOI: https://doi.org/10.1007/s11104-023-06190-5