Effects of jujube witches'broom stress and grass cover management on arthropod community structure and functional group proportions in northern jujube orchard

【Objective】Jujube witches' broom (JWB), caused by Candidatus Phytoplasma ziziphi, is a destructive systemic disease known as the“cancer of jujube trees”, which has severely threatened the sustainable development of the jujube industry in northern China. In recent years, JWB has continued to spread in major jujube-producing regions such as Hebei and Shandong provinces, leading to extensive orchard abandonment and devastating economic losses. Although leafhoppers are recognized as the primary known vectors of JWB, field investigations have found that their population density in JWB-hit areas is extremely low, which contradicts the worsening epidemic trend of the disease. This discrepancy suggests the potential existence of alternative transmission vectors that have not yet been identified. Ad-ditionally, orchard management practices (e.g., natural grass cover vs clean tillage) and geographical environmental differences may modulate the structure and function of arthropod communities, thereby affecting the occurrence and spread of JWB. To address these knowledge gaps, this study aimed to systematically explore the regulatory mechanisms of JWB stress on arthropod community structure and functional group dynamics in jujube orchards and provide scientific support for the development of region-specific green control strategies against JWB.【Methods】Field investigations were conducted in four major jujube- producing regions, including Zanhuang County and Xingtang County (Hebei Province), as well as Feicheng City and Ningyang County (Shandong Province), during the 2024 growing season. Two complementary sampling methods were employed to ensure comprehensive collection of arthropods: sweep netting was carried out from April to September to collect arthropods on jujube canopies and surrounding vegetation, with three 10×20 m sampling plots set in each orchard (healthy vs JWB-infected), and 5 target trees selected per plot for 50 cumulative sweeps per sample. Malaise traps were deployed in healthy orchards under two management regimes (natural grass cover with 60%-80% coverage vs clean tillage with ＜5% coverage) from June to September, with one trap per orchard placed in the central area to avoid edge effects, and samples collected monthly. Collected specimens were identified to the family level and categorized into five functional groups: predatory natural enemies (e.g., Coccinellidae and Araneae), parasitic natural enemies (e.g., Ichneumonidae and Braconidae), phytophagous insects (e.g., Cicadellidae and Miridae), pollinators (e.g., Apidae), and neutral insects (e. g., Muscidae and Culicidae). Prior to statistical analysis, the Shapiro-Wilk test and Levene test were performed to assess normality and homogeneity of variance, respectively. One-way Analysis of Variance (One-way ANOVA) was used for data meeting both assumptions, while the Mann-Whitney U nonparametric test was applied for non-normal data, with a significance level set at α = 0.05. Diversity indices, including the Shannon-Wiener index (H'), Pielou evenness index (J), Simpson dominance index (D), and Margalef richness index (dM), were calculated to characterize community structure differences. 【Results】In Zanhuang County, JWB-infected orchards (JMG) exhibited significant changes in arthropod functional group composition compared with healthy orchards (HJG): the number of phytophagous insects (e.g., Pentatomidae and Cicadellidae) increased by 67.4% (308 vs 184 individuals), predatory natural enemies (e.g., Coccinellidae and Araneae) increased by 64.0% (82 vs 50 individuals), while pollinators (mainly Apidae) decreased by 65.0% (7 vs 20 individuals) and neutral insects decreased by 15.4% (154 vs 182 individuals). A critical finding was that Cicadellidae, the known primary vector, accounted for less than 1% of the total phytophagous insects in JWB-infected orchards. In contrast, piercing-sucking insects, particularly Miridae (10.18%) and Lygaeidae (12.55%), underwent explosive outbreaks in JMG, and their ecological niches (piercing-sucking phloem sap and active foraging behavior) are highly congruent with the transmission requirements of phytoplasma, suggesting they may serve as potential alternative vectors. JWB exerted distinct region-specific effects on arthropod communities. In Feicheng, Lygaeidae dominated JWB- infected orchards with a proportion of 58.73% , which was 22 times higher than that in healthy orchards; in Xingtang, the proportion of Coccinellidae in JMG rose to 34.41% , representing a 129.4% increase compared with HJG; in Zanhuang, the dominant species in JMG shifted to a dual-dominance pattern of Scolytidae and Cecidomyiidae (21.43% each) with the disappearance of Coccidae, which was the dominant group in HJG; in Ningyang, JMG formed a compound dominant community of Lygaeidae (37.25% ) and Crambidae (9.80% ). The response of natural enemies also showed regional differentiation: the proportion of predatory natural enemies increased to 34.4% and 19.6% in JMG of Xingtang and Ningyang, respectively, while it was only 6.4% in Feicheng’sJMG, possibly inhibited by the explosive outbreak of Lygaeidae. Statistical analysis revealed significant differences in the number of Coccinellidae between HJG and JMG in Xingtang (P=0.037), and significant differences in phytophagous Pentatomidae and Lygaeidae between HJG and JMG in Zanhuang and Feicheng (P=0.000 3 and P=0.035, respectively), while no significant regional differences were observed in neutral insects and pollinators. For healthy orchards in Zanhuang, natural grass cover management significantly enhanced ecological pest suppression capacity compared with clean tillage. A total of 854 individuals belonging to 22 families were collected in natural grass cover orchards (NG), while 1133 individuals belonging to 18 families were collected in clean tillage orchards (CT). The combined proportion of predatory and parasitic natural enemies in NG reached 19.90%, which was 1.87 times that of CT (10.61%). Parasitic natural enemies, especially Ichneumonidae (5.97% vs 0.62%) and Braconidae (3.16% vs 0.71% ), were prominently dominant in NG. Community diversity analysis showed that NG had higher values of the Shannon-Wiener index (H' =2.08 vs 1.84), Margalef richness index (3.11 vs 2.42), and Pielou evenness index (0.58 vs 0.51), while the Simpson dominance index was lower (0.19 vs 0.32) compared with CT. Statistical tests confirmed significant differences in the composition of natural enemy groups (Araneae, Ichneumonidae and Braconidae) and some phytophagous insects (Scolytidae and Pieridae) between NG and CT (P＜0.01 or P＜0.05).【Conclusion】JWB drives specific restructuring of arthropod communities in jujube orchards by altering jujube tree metabolic characteristics, leading to significant differentiation of functional groups: the population sizes of phytophagous insects and predatory natural enemies increase significantly, while pollinators and neutral insects decline. Notably, Miridae and Lygaeidae, which exhibit explosive outbreaks in JWB-infected orchards and have ecological niches matching phytoplasma transmission requirements, are proposed as potential alternative vectors requiring targeted attention and subsequent transmission experiments for verification. The interaction between geographical environments (e.g., climate and local vegetation) and JWB induces distinct regional differentiation in community responses, with different JWB-infected regions forming unique dominant group combinations, which provides direct scientific basis for formulating region- specific control strategies. Natural grass cover management, as an effective ecological regulation measure, optimizes the microhabitat of jujube orchards, enhances the diversity and functional proportion of natural enemy communities, and thereby strengthens ecological pest control capacity, enriching the theoretical and practical approaches for the sustainable ecological management of jujube orchards. Overall, this study clarifies the patterns of JWB-mediated arthropod community restructuring, the mechanisms of regional differentiation, and the ecological regulatory effects of natural grass cover management, providing key scientific support for the development of differentiated green control strategies against JWB and the targeted monitoring of potential vector insects.