TY - JOUR
AU - Li, Dun-Song
AB - Abstract Secondary population outbreaks of Panonychus citri (McGregor) (Acari: Tetranychidae) are triggered by synthetic chemical applications (dose and method), which also elicited a change in mites’ behavioral responses. This study aimed to understand the dispersal pattern of P. citri and how changes in dispersal behavior may influence secondary pest outbreaks in the field with or without chemicals. We found positive density and time-dependent dispersal within the inoculated leaflet. Dispersion from inoculated leaflets to the last leaflet depends on initial density and time. A significant difference was observed in the composite dispersal index data and preferred midrib region. The minimum dispersal was observed by P. citri in no direct contact with treated surfaces, whereas attraction was observed on treated surfaces (right). All chemicals gave different dispersal and feed disruption responses depending on the treatment application pattern. The maximum number of mites dispersed and avoid surfaces treated with abamectin and vegetable oil, respectively. Vegetable and EnSpray 99 had a positive impact on toxicity, repellency, and irritancy. The fecundity rate of P. citri boosted with a high dose and direct exposure. Panonychus citri colonization as a single individual or gregarious distribution resulted in a rapid fecundity rate, which may explain why citrus orchards were severely damaged and how suddenly a whole citrus plantation can be highly infested. This study concluded that change in treatment application patterns leads to a change in the behavioral responses in P. citri. Dispersal behavior plays a vital role in the survival and population establishment of an organism, especially in the secondary population outbreak of phytophagous mites (Aliniazee and Cranham 1980, Iftner and Hall 1983, Zwick and Field 1987). Because of the nonviable environment, due to food shortage or pesticide application, the mite pests have to find better opportunities elsewhere and disperse (Azandeme-Hounmalon et al. 2014). Like Tetranychus urticae Koch and Panonychus citri (McGregor) (Acari: Tetranychidae) with strong reproductive ability, mite pests can infest the whole plant in a short time from one infested leaf or branch, depending on their dispersal behavior, which often leads to the population outbreak. For the secondary population outbreaks of mites in the field, the standard explanation suggests that reducing natural enemies population and resistance development mechanism of phytophagous mites by the board-spectrum insecticides (pyrethroids) would allow the mite population unchecked (Aliniazee and Cranham 1980, Zwick and Field 1987). Synthetic and natural chemicals exhibit repellent effects on phytophagous mites and impact their feeding and reproductive behaviors (Iftner and Hall 1983, Melo et al. 2014). The application of chemicals to protect fruit results in a secondary population outbreak due to restricted activity or destruction of natural enemies (Aliniazee and Cranham 1980, Zwick and Field 1987). However, Iftner and Hall (1983) suggested that the occurrence of a secondary outbreak in the absence of any other target pest and natural enemies also developed a relative outbreak of mites. Dispersal is a vital tool to understand the survivorship, distribution, and response to change, which is done in three different steps in all arthropods: emigration, displacement or a itinerant stage, and immigration (Ronce 2007). Dispersal may provide essential information for developing a well-adapted IPM strategy. Azandeme-Hounmalon et al. (2014) reported that Tetranychus evansi Baker & Pritchard exhibited greater positive density-dependent distribution and circadian migration, due to its gregarious behavior, disperse after lacking food and higher reproductive rate than T. urticae (Sabelis 1991, Bowler and Benton 2005). As a worldwide pest of citrus, P. citri has been focused on a considerable amount of research (Jamieson and Stevens 2009, Kasap 2009, Fadamiro et al. 2013, Faez et al. 2018, Karmakar 2019). In China, IPM strategies had been applied for the control of P. citri since the 1970s, including releasing and protecting predatory mites, bio-pesticides application, and beneficial weeds cultivation (Zhang et al. 2001, Zhang et al. 2002, Chen et al. 2009, Liu et al. 2019). However, most studies focus on the control effectiveness, pesticide resistance, and management (Marcic 2012, Liao et al. 2016, Zalucki and Furlong 2017), as the chemical applications are common tactics to control P. citri (Xiao et al. 2010). Chinese farmers aggressively overused more agricultural chemicals than the rest of the world due to small landholders (Wu et al. 2018). The sustainable agricultural management practices and latest technological innovations are less effective for small landholder farmers due to higher input costs (Foster and Rosenzweig 2017). The efficacy of pesticides depends on their direct application rate (lethal or sublethal or overdose) (Haynes 1988). Chemicals gave a chance of dispersal (irritancy or repellency) to pests before causing required mortality which resulted in undesirable consequences (Grieco et al. 2007). Hence, the description of lethal or sublethal effects of chemicals gained importance due to impact on physiology or behavioral changes of pest and its natural enemies during management programs as well as overdosing is an important factor need to be addressed (Perveen and Miyata 2000, Desneux et al. 2004, Desneux et al. 2007, Wu et al. 2018). Research on dispersal behavior related to pest outbreaks was seldom concerned (Iftner and Hall 1983). This study aimed to explore the dispersal pattern of P. citri and how changes in dispersal behavior may influence pest outbreaks in the field. Research on the distribution of P. citri within leaves and plants, and the effect of SYP-9625, abamectin, vegetable oil, and EnSpray 99 on the dispersal behavioral responses (irritancy and repellency) and oviposition of P. citri were investigated. We tested whether the sublethal (LC30) and lethal (LC50 and LC90 [for overdosing/overuse]) of these acaricides/insecticides influenced P. citri responsive behavior and oviposition. Materials and Methods Mite culture Citrus red mites, P. citri, used in this study were collected from an orange orchard of Huizhou city, Guangdong province, China (N23, 11′ 43.9833″, E114, 15′ 17.1387″). The mites’ population was regularly maintained for >75 generations in the Biological Control Section, PPRI (Plant Protection/Plant Protection Research Institute), GAAS (Guangdong Academy of Agricultural Sciences), China. All the mites’ mass rearing was done under control laboratory conditions (26 ± 1°C, 16:8 [L:D] h) on lemon leaves by placing on a water-saturated sponge. We used 1-d older adult female mites for experiments. Citrus Plantation Small, 1- to 2-mo Citrus reticulata (Rutaceae) plants were shifted from the citrus nursery of GAAS to PPRI greenhouse. Plants were kept on pots watering them daily and spreading compost (Shanghai Worth Garden Co., Ltd, China) as needed for 7 mo before experimentation. All plants used for experiments were washed with water three-time for 3 d to be sure not having any life stages mites under a hand lens and a dissecting microscope during January 2020. Chemicals Commonly used insecticides (SYP-9625 and abamectin) were compared with vegetable oil and EnSpray 99, including control treatment. The lethal and sublethal concentrations of the above chemicals were calculated using probit analysis from concentrations (2, 1, 0.5, and 0.25%) after 24 h with 10–90% corrected mortality as shown in Table 1. We used LC30, LC50, and LC90 doses as the concept of sublethal, lethal, and farmers/recommended field application rate (approximately), respectively. All the treatments were diluted with water and 1% tween (20(1):80(1)) and all dose units in % in 100 ml. Previously, chemical application pattern layout and treatments were presented in Supp Table 3 and Fig. 1 (online only), using a fine misted hand sprayer to cover the treated leaf surfaces carefully with no exposure to other leaflet surfaces or leaves. Table 1. Lethal and sublethal concentration (%) of chemicals and oils against susceptible strain population of P. citri Lethal conc. . SYP-9625 (30%) . Abamectin (5%) . Vegetable oil (99%) . Mineral oil (99%) . . Shenyang Kechuang Chemicals Co. Ltd . North China Pharmaceutical Group Ainuo Co. Ltd . Institute of Zoology, Guangdong Academy of Sciences . Korea oil energy Ltd . LC30 0.065 0.049 0.024 0.08 (0.038–0.098) (0.031–0.068) (0.017–0.032) (0.004–0.012) LC50 0.196 0.110 0.018 0.024 (0.133–0.306) (0.081–0.150) (0.011–0.025) (0.016–0.037) LC90 2.836 0.812 0.347 0.368 (1.321–10.774) (0.509–1.657) (0.181–0.965) (0.166–1.541) Lethal conc. . SYP-9625 (30%) . Abamectin (5%) . Vegetable oil (99%) . Mineral oil (99%) . . Shenyang Kechuang Chemicals Co. Ltd . North China Pharmaceutical Group Ainuo Co. Ltd . Institute of Zoology, Guangdong Academy of Sciences . Korea oil energy Ltd . LC30 0.065 0.049 0.024 0.08 (0.038–0.098) (0.031–0.068) (0.017–0.032) (0.004–0.012) LC50 0.196 0.110 0.018 0.024 (0.133–0.306) (0.081–0.150) (0.011–0.025) (0.016–0.037) LC90 2.836 0.812 0.347 0.368 (1.321–10.774) (0.509–1.657) (0.181–0.965) (0.166–1.541) Note: Lethal concentrations were calculated by using four concentrations (2, 1, 0.5, and 0.25%) bioassay result after 24 h of posttreatment. The data were replicated three times, and regression probit analysis was used (IBM SPSS statistical software). Open in new tab Table 1. Lethal and sublethal concentration (%) of chemicals and oils against susceptible strain population of P. citri Lethal conc. . SYP-9625 (30%) . Abamectin (5%) . Vegetable oil (99%) . Mineral oil (99%) . . Shenyang Kechuang Chemicals Co. Ltd . North China Pharmaceutical Group Ainuo Co. Ltd . Institute of Zoology, Guangdong Academy of Sciences . Korea oil energy Ltd . LC30 0.065 0.049 0.024 0.08 (0.038–0.098) (0.031–0.068) (0.017–0.032) (0.004–0.012) LC50 0.196 0.110 0.018 0.024 (0.133–0.306) (0.081–0.150) (0.011–0.025) (0.016–0.037) LC90 2.836 0.812 0.347 0.368 (1.321–10.774) (0.509–1.657) (0.181–0.965) (0.166–1.541) Lethal conc. . SYP-9625 (30%) . Abamectin (5%) . Vegetable oil (99%) . Mineral oil (99%) . . Shenyang Kechuang Chemicals Co. Ltd . North China Pharmaceutical Group Ainuo Co. Ltd . Institute of Zoology, Guangdong Academy of Sciences . Korea oil energy Ltd . LC30 0.065 0.049 0.024 0.08 (0.038–0.098) (0.031–0.068) (0.017–0.032) (0.004–0.012) LC50 0.196 0.110 0.018 0.024 (0.133–0.306) (0.081–0.150) (0.011–0.025) (0.016–0.037) LC90 2.836 0.812 0.347 0.368 (1.321–10.774) (0.509–1.657) (0.181–0.965) (0.166–1.541) Note: Lethal concentrations were calculated by using four concentrations (2, 1, 0.5, and 0.25%) bioassay result after 24 h of posttreatment. The data were replicated three times, and regression probit analysis was used (IBM SPSS statistical software). Open in new tab Dispersal Behavior of P. citri Panonychus citri dispersal behavior was assessed within leaf parameters, leave surfaces, and plant distribution. The leaf parameters assessment was done by dividing the leaf into six different portions; base, apex, margin, midrib, veins, and petiole. This division was further assessed on the lower (abaxial surface) and upper (adaxial surface) sides of leaves. All the leaves were numbered from top to bottom, and vaseline applied 2.5 cm below the last leaflet. Plant pots were placed in a water-filled tray with 2.5–3 feet distance between plants to avoid mites dispersal from one plant to another. Panonychus citri were maintained in a laboratory on the lemon leaves with the water-saturated sponge. With a camel brush, 30 adult females were released on the ADR (adaxial right) in each replication. The experiment was replicated three times simultaneously, and dispersal data were recorded every 12 h for 11 d after release, estimating the mites distribution, fecundity rate, and leaf damage index (scale from 0 [no damage] to 5 [shriveling of the leaf]). Toxicity and Behavioral Assays The lethal and sublethal concentrations for each chemical were calculated from the preliminary chemical bioassay test under laboratory conditions. The toxicity of LC30, LC50, and LC90 that used chemicals produced (Table 1) were tested on the adult females from the P. citri population (laboratory-reared) in greenhouse conditions. Citrus reticulata were covered each with double side sticky plastic tape to record the escaped mites. Each plant leaflet had designated either right or left or upper (adaxial) and lower (abaxial) leaf surfaces. All leaf surfaces were designated with letters: ADR, ABR, ADL, and ABL, used for adaxial right, abaxial right, adaxial left, and abaxial left, respectively. In this study, we used nine different treatments (Trt.'s) by changing the chemical application sites as shown in Supp Table 3 and Fig. 1 (online only). We used three concentrations (LC30, LC50, and LC90). Each treatment was replicated three times by releasing the 30 adult females of P. citri on the right adaxial surface of the upper, middle, and lower leaves (90 in total). The number of dead or alive mites was recorded from three leaves from the upper, lower, and middle parts of each plant (each replicated) using a hand lens 24 h after treatment. The number of dead mites (due to toxicity of treatments) dropped onto white paper placed at ground level was also counted. Leaves were examined under a dissecting microscope immediately to recode the number of eggs per female and number of mites more precisely without changing the plat architecture. Three major behavioral factors (contact irritancy, repellency, and oviposition) were evaluated (Sarfraz et al. 2005, Wu and Appel 2018). Panonychus citri dispersal consists of moving away from the treated to the untreated surface after physical contact (when released on the treated surface). Repellency consists of mites’ dispersal away from the treated surface without physical contact with the surface. Irritancy and repellency of mites were recorded by releasing mites on treated and untreated right adaxial surfaces, respectively, from the experimental layout (Supp Table 3 and Supp Fig. 1 [online only]). A fully treated application treatment was not included in this study. The experiment was replicated six times by considered two surfaces e.g., for Trt. no. 1; ADR (three replicates) +ADL (three replicates) = six replications. All the treatments remained the same, as mentioned above. The role of oviposition is a significant factor of the secondary population outbreak mechanism of tetranychid mites (Adesanya et al. 2019), so it is essential to record the impact of behavioral changes on the oviposition of a female. We compared the irritated and nonirritated as well as repelled and nonrepelled P. citri oviposition rate of a female (alive on the surface) at LC30, LC50, and LC90 doses of each chemical, including control (1% (1:1) tween20: tween80). The oviposition assay was similar to the above methodologies. The number of eggs laid by mites was recorded after 24 h under a dissecting microscope. Statistical Analysis For the dispersal index, we used the composite dispersal index (CDI) formula for summarizing the mite location among the leaf parameters and surfaces mentioned by (Azandeme-Hounmalon et al. 2014). The formula used for CDI calculation as below: CDI=(1×NbL1+2×NbL2+3×NbL3+4×NbL4+5×NbL5+5×NbL6+6×NbL7)╱n where Nb.Lx is number of mites noted on the xth leaflet and n is the total number of mites (30 mites). As mentioned above, we assigned index letters, values 1, 2, 3, 4, and 6 to mites noted on the first, second, third, fourth, and seventh leaflets, respectively, while value 5 to mites present on the fifth and sixth leaflets. The same index value designated to leaflets <5 cm closer to each other and originated from the next node. ANOVA test was used to calculate the dispersal responses of P. citri (within leaf parameters, leaf surfaces, and plants) and effectiveness of acaricides (dose, treatments (Trt’.s) and their interaction (dose* Trt’.s)) on the mortality, irritancy, and repellency percentage including the number of eggs per female within each treatment. The mean comparison was made by using Tukey’s HSD post-hoc test at α = 0.05. The acaricidal effect on the dispersal rate of Panonychus citri was calculated by using residual Chi-square (χ 2). For better understanding, the interaction between the treatment and behavioral responses (irritancy and repellency) and correlation analysis (Pearson’s product–moment) was used by comparing toxicity, irritancy, and repellency within each treatment used for P. citri. All statistical analyses were performed using the Jamovi 1.2 version (Jamovi 2020) and the R language program 3.6.2 version (RCore-Development-Team 2019). Results and Discussions Panonychus citri Distribution Within the Inoculated Leaflet The adult female movement in a new place is called the ‘Trivial movement’ (Southwood 1962) for suitable feeding and oviposition site, may or may not depend on the initial population density of phytophagous mites. After releasing of P. citri on the inoculated leaflet, results showed an exceedingly decreasing distribution due to density-dependent response (from 40 ± 0.00 to 3.33 ± 3.33 mites; Fig. 2A) and quick movement to other leaflets as Wanibuchi and Saitô (1983) and Azandeme-Hounmalon et al. (2014) observed. The average composite dispersal index (CDI) differences between adaxial and abaxial surfaces were significantly different (Fig. 1B) by preferring adaxial surfaces (Childers and Fasulo 2009) similar to Brevipalpus obovatus Donnadieu, 1875 (Sudo and Osakabe 2011), but most of the tetranychids (Jhonson and Lyon 1991, Park and Lee 2002). From CDI of P. citri, midrib was the most favorable site for feeding and oviposition indicating a close and significant relationship between phytophagous mites and the architecture of leaves (leaf domatia) (Sudo and Osakabe 2011, Debnath and Karmakar 2013). Fig. 1. Open in new tabDownload slide The number of (%) Panonychus citri on inoculated leaflet surfaces (adaxial and abaxial) (A) and CDI mites distribution with surfaces (adaxial and abaxial) of leaflets. CDI summarized the position of mites on the leaf relative to its density. The SE bars are used here (α = 0.05). (ns = not significant, ***significant) Fig. 1. Open in new tabDownload slide The number of (%) Panonychus citri on inoculated leaflet surfaces (adaxial and abaxial) (A) and CDI mites distribution with surfaces (adaxial and abaxial) of leaflets. CDI summarized the position of mites on the leaf relative to its density. The SE bars are used here (α = 0.05). (ns = not significant, ***significant) Fig. 2. Open in new tabDownload slide Dispersal pattern of Panonychus citri (mean ± SE) and the number of eggs laid (mean ± SE) by a female per leaflet on different observational time. ANOVA resulted that comparison between number of mites versus eggs laid/female versus leaflets found significantly different (α = 0.05) except after 8 h (interaction = mites vs eggs per female vs leaflets), 16 h (interaction), 64 h (interaction), and 256 h (mites vs eggs and interaction). Fig. 2. Open in new tabDownload slide Dispersal pattern of Panonychus citri (mean ± SE) and the number of eggs laid (mean ± SE) by a female per leaflet on different observational time. ANOVA resulted that comparison between number of mites versus eggs laid/female versus leaflets found significantly different (α = 0.05) except after 8 h (interaction = mites vs eggs per female vs leaflets), 16 h (interaction), 64 h (interaction), and 256 h (mites vs eggs and interaction). Panonychus citri Distribution, Fecundity, and Damage Within Plant The distribution of P. citri from inoculated leaflets to others by minimal settlement on the central leaflets (Fig. 2). The mites distribution were observed to be unidirectional, but this may change to a multidirectional (Tashiro 1966). This distribution on the last leaflet was observed similar to the inoculated leaflet but in the opposite trend (Fig. 2). This change in density-dependent to independent behavior was also observed in other tetranychids (Bowler and Benton 2005, Fellous et al. 2012, Azandeme-Hounmalon et al. 2014), a phenomenon that may be at a specific density level (Yasuda 1978). This nondependent density behavior may be due to the positive relationship between leaf domatia and age (Agrawal 1997, English-Loeb et al. 2002, Antipolis and Parolin 2011, Situngu and Barker 2017). The distributed number of mites and time spend on the feeding site (leaflet) significantly affected the mite oviposition rate and damage index. The fecundity rate found significantly different within leaves (F = 9.44; df = 6, 125; P = 0.000) and observational time (F = 2.05; df = 5, 125; P = 0.077) at α = 0.05 (Fig. 2). The number of eggs between adaxial and abaxial surfaces, and within adaxial was observed significantly different (Supp Table 2 [online only]). Damage index varies within leaflets from low (at fifth leaflet between 1 [≤20%] and 2 [≤40%]), to severe (at seventh leaflet between 3 [≤60%] and 5 [≤100%]) after 256 h (Fig. 3). As reproduction and damage of P. citri were observed as moderate (overall) to higher with the gregarious distribution of mites on the Citrus reticulata, it confirms previous findings of tetranychids species. This dispersal behavior of P. citri indicates that stress-bearing within-population may vary. We concluded that P. citri could start colonization with a single individual and dispersed due to a shortage of food depending on genetic variation and communication behavior within the population (Osakabe et al. 2005, Yuan et al. 2010a, b, Yuan et al. 2011). Fig. 3. Open in new tabDownload slide The mean leaf damage index of P. citri at top released. ANOVA resulted the significant different of leaf damage per leaflet and per unit observational time (F = 22.72; df = 6,125; P = 0.000 and F = 87.61; df = 5,125; P = 0.000 respectively) and no difference observed in the interaction between time and leaflets (α = 0.05). Fig. 3. Open in new tabDownload slide The mean leaf damage index of P. citri at top released. ANOVA resulted the significant different of leaf damage per leaflet and per unit observational time (F = 22.72; df = 6,125; P = 0.000 and F = 87.61; df = 5,125; P = 0.000 respectively) and no difference observed in the interaction between time and leaflets (α = 0.05). Effect of Chemicals on Dispersal Behavior of Panonychus citri Using the Iftner and Hall (1983) methodology, dispersal rate, toxicity, irritancy, and repellency of chemicals were checked against P. citri. Here, we used the chemicals’ and oils’ treatment as environmental stress or repellent factor based on lethal (LC50 and LC90) and sublethal (LC30) concentrations, as shown in Table 1. Dispersal Rate of Chemicals After releasing mites on the leaf’s adaxial surface (right), the movement starts immediately for a suitable feeding site. This searching behavior takes few minutes to an hour until found a better feeding site (Iftner and Hall 1983). Location of P. citri after 24 h of application of spray for each treatment representing χ 2 values (dispersal rate value) as given in Supp Table 3 [online only]. The lowest dispersal rate was observed in Trt. no. 7 and Trt. no. 1 at LC30, and Trt. no. 2 at LC90, where nonirritated P. citri were not on a fully treated surface with minimum movement. Maximum dispersal with a higher dispersal rate difference was observed in Trt. no. 1, 5, and 6 at LC90, LC50, and LC30 of all chemicals (Supp Fig. 1 and Supp Table 3 [online only]). The dispersal of mites away from treated surfaces was observed in Trt. no. 7, where dispersal increased from 1.86 to 3 folded by increasing dose from LC30 to LC50 within half treated surfaces. Vegetable oil and SYP-9625 responded almost similarly, while abamectin and EnSpray 99 had the same response. Even P. citri reported resistance against abamectin (Hu et al. 2010, Ouyang et al. 2012, Pan et al. 2020), maximum mites dispersed away from abamectin-treated surfaces except for Trt no. 5 (SYP-9625 gave maximum dispersal). The maximum number of mites avoid vegetable oil-treated surfaces by releasing on untreated surfaces followed by EnSpray 99, SYP-9625=abamectin, and control (Supp Fig. 1 and Supp Table 3 [online only]). There is no evidence of uniform application of chemicals in the field, even using the most efficient chemical application techniques that resulted in many small patches of unsprayed areas within the tree. A change in dispersal behavior response or colonization patterns were observed (Vonesh and Kraus 2009), depending on treatment by diving into different groups. With break up into smaller groups by chemicals applications to not only avoid community formation on the treated surfaces (Guedes et al. 2016) but also provide a chance to build new responsive colonies (Vonesh and Kraus 2009). This phenomenon, gave maximum survival and population growth, which result in an outbreak. The variation in mites population responses was observed depending on the chemical application pattern, dose, nature/mode of action, and acaricidal, while environmental conditions (temperature, wind speed, and relative humidity), foliage thickness, spraying equipment, and spraying reachability are additional factor in the field (Iftner and Hall 1983, Marcic 2012). The ability to build a strong colony either as a single individual or with a group is also an important factor for a secondary outbreak in the field. Toxicity, Irritancy, and Repellency of Chemicals The management of the P. citri population is commonly done by using chemicals that impact behavioral responses (Maltby 1999, Desneux et al. 2007, Misra et al. 2011). As incomplete spray coverage of chemicals and resistance issues are counted as a major cause of secondary population outbreak and decrease their efficacy (Martini et al. 2012, Adesanya et al. 2019). Usually, the mites’ susceptibility is directly linked with contact toxicity and irritancy/repellency of acaricides (Adesanya et al. 2019), as an outbreak of T. urticae in hop farms was reported due to acaricidal control in Washington State (Wu et al. 2019). This outbreak raises many questions regarding the chemical dose and sprays’ coverage in the cropping system (Wu et al. 2019). Hence, further evaluations of insecticides (SYP-9625 and abamectin) and oils’ (vegetable oil and EnSpray 99) efficacy need to check behavioral responses, including acute toxicity and spray coverage (Piraneo et al. 2015, Zalucki and Furlong 2017). The acute toxicity, irritancy, and repellency and their impact on the oviposition rate of P. citri were evaluated. The degree of chemicals toxicity (mortality) to adult P. citri varied significantly within different treatments (α = 0.05) depending on change in treatment and dose. The overall toxicity of oils (vegetable and EnSpray 99) was significantly lower than SYP-9625 and abamectin with a similar trend. SYP-9625 gave higher toxicity followed by ABA in Trt. no. 9 (the whole plant treated) across the doses (Fig. 4). Fig. 4. Open in new tabDownload slide Toxicity (% mortality) of four chemicals (SYP-9625 [SYP], abamectin [ABA], vegetable oil [VO], and EnSpray 99 [MO]) on Panonychus citri within different treatments (Trt’.s). Toxicity of Insecticides depended on Trt.'s (df = 8, 54; P = <.001, for SYP: F = 74.82; for ABA: F = 35.74), dose (df = 2,54; P = <.001, for SYP: F = 12.03; for ABA: F = 80.45), and interaction (Trt.'s*dose; df = 16,54, for SYP: nonsignificant; for ABA: F = 2.35; P = 0.010), whereas toxicity of oils depended Trt.'s (df = 8,54; P = < 0.001; for VO: F = 33.59; For MO: F = 22.28), dose (df = 2,54; P = <.001, For VO: F = 38.23; For MO: F = 45.26) and interaction (df = 16,54, For VO: F = 2.54; P = 0.0056, For MO: F = 2.70; P = 0.0033). Bars represent percentage of dead mites. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). The control treatment gave zero mortality which is not presented here. Fig. 4. Open in new tabDownload slide Toxicity (% mortality) of four chemicals (SYP-9625 [SYP], abamectin [ABA], vegetable oil [VO], and EnSpray 99 [MO]) on Panonychus citri within different treatments (Trt’.s). Toxicity of Insecticides depended on Trt.'s (df = 8, 54; P = <.001, for SYP: F = 74.82; for ABA: F = 35.74), dose (df = 2,54; P = <.001, for SYP: F = 12.03; for ABA: F = 80.45), and interaction (Trt.'s*dose; df = 16,54, for SYP: nonsignificant; for ABA: F = 2.35; P = 0.010), whereas toxicity of oils depended Trt.'s (df = 8,54; P = < 0.001; for VO: F = 33.59; For MO: F = 22.28), dose (df = 2,54; P = <.001, For VO: F = 38.23; For MO: F = 45.26) and interaction (df = 16,54, For VO: F = 2.54; P = 0.0056, For MO: F = 2.70; P = 0.0033). Bars represent percentage of dead mites. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). The control treatment gave zero mortality which is not presented here. The irritancy and repellency of mites were observed in which mites released on the treated (Trt. no. 1, 3, 5, and 7) and untreated surfaces (Trt. no. 2, 4, 6, and 8). Abamectin gave a higher irritancy percentage as compare to SYP-9625 and was not significantly different for LC50 and LC90 concentrations, but different from LC30 in both insecticides (SYP-9625 and abamectin) (Fig. 5). Maximum irritancy (%) was obtained with a higher concentration in oils. A significant difference in irritancy (%) was observed between doses of SYP-9625 and Abamectin (Trt. no. 1 and 7), vegetable oil (Trt. no. 7), and EnSpray 99 (Trt. no. 1) within treatments. The chemical dose, treatments, and interaction did not affect the repellency of mites (Fig. 6) as LC90 SYP-9625 and abamectin on P. citri (female adults) gave with less repellency than LC50 or control (Trt. no. 2 and Trt. no. 4). The repellent effect of vegetable oil responded differently within the treatments with higher repellency at lowest dose (LC90 lowest among all) and maximum dose (Trt. no. 8) than others. The effect of EnSpray 99 LC50 was lowest among all treatments (Fig. 6). As a result of our study, abamectin gave less toxicity, repellency and irritancy as compared with SYP-9625 (Ouyang et al. 2018) due to resistance development against tetranychids including P. citri (Hu et al. 2010, Zhu et al. 2010). The vegetable oil and EnSpray 99 gave similar results to SYP-9625 and abamectin (Irulandi et al. 2008, Zanardi et al. 2015) with a positive impact on the toxicity, repellency, and irritancy (Kord-Firozjaee and Damavandian 2018, Topuz et al. 2018, Downing 2019). The toxicity of oils increased with the increase of the number of carbon atoms and their chemical bonding (Parry and Rose 1983, Xue 2007, Sims et al. 2014, Oliveira et al. 2017). The maximum concentration of vegetable oil also gave attraction behavior that also depends on fatty acids like palmitic acid (Nilsson and Bengtsson 2004). Fig. 5. Open in new tabDownload slide Irritancy of four chemicals (SYP-9625 [SYP], abamectin [ABA], vegetable oil [VO], and EnSpray 99 [MO]) on P. citri within different treatments (Trt’.s). The percentage of P. citri irritated by all chemicals observed nonsignificantly different within treatments (except for VO: F = 3.16, df = 3,80; P = 0.0293) and interaction (Trt.'s*dose). The irritancy across the doses found significantly different in all chemicals (df = 3,80; for SYP: F = 3.27, P = 0.0254; for ABA: F = 4.99, P = 0.0032 and for MO: F = 3.24, P = 0.0264) except vegetable oil. Bars represent percentage of irritated. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). Fig. 5. Open in new tabDownload slide Irritancy of four chemicals (SYP-9625 [SYP], abamectin [ABA], vegetable oil [VO], and EnSpray 99 [MO]) on P. citri within different treatments (Trt’.s). The percentage of P. citri irritated by all chemicals observed nonsignificantly different within treatments (except for VO: F = 3.16, df = 3,80; P = 0.0293) and interaction (Trt.'s*dose). The irritancy across the doses found significantly different in all chemicals (df = 3,80; for SYP: F = 3.27, P = 0.0254; for ABA: F = 4.99, P = 0.0032 and for MO: F = 3.24, P = 0.0264) except vegetable oil. Bars represent percentage of irritated. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). Fig. 6. Open in new tabDownload slide Repellency of four chemicals (SYP-9625, abamectin, vegetable oil and EnSpray 99) on Panonychus citri within different treatments (Trt’.s). The mites’ repellency was not dependent on dose, Trt.'s and Trt.'s*dose and nor across the doses in a treatment. Bars represent the percentage of mites repelled. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). Fig. 6. Open in new tabDownload slide Repellency of four chemicals (SYP-9625, abamectin, vegetable oil and EnSpray 99) on Panonychus citri within different treatments (Trt’.s). The mites’ repellency was not dependent on dose, Trt.'s and Trt.'s*dose and nor across the doses in a treatment. Bars represent the percentage of mites repelled. Similar letters above bars indicate nonsignificant differences in mite mortality (α = 0.05). A Pearson’s correlation analysis was executed within each applied treatment for each used chemicals to better understand between toxicity, irritancy, and repellency. No correlation is observed between two factors when one factor is zero. The positive and negative correlations were observed by comparing two different factors (irritancy and repellency) within treatment combinations (Supp Tables 4–8 [online only]). Interestingly, there was an equal chance to adopt nonirritated or nonrepelled behavior by acaricides (negative correlation between toxicity vs irritancy and repellency) without or less contact toxicity except at LC30 and LC90 in all chemicals (Trt. no. 7 except vegetable oil), and at LC50 (Trt. no. 7 (for SYP-9625 and EnSpray 99), Trt. no. 5 (for abamectin), and Trt. no. 1 [for vegetable oil]). This behavior was also observed even in the resistant population (T. uricae;Adesanya et al. 2019). Though our research did not evaluate the resistance mechanism and chemosensory activities of P. citri, it resulted in variation in correlations between toxicity versus repellency and toxicity versus irritancy across different treatments for the change in behavioral response. These variations also depend on the chemosensory gene (gustatory receptor gene; Ngoc et al. 2016) and genetic diversity within the population (Osakabe et al. 2005, Yuan et al. 2010a, b, Yuan et al. 2011). Due to the above factors, we got mixed and complex effects between toxicity and irritancy behavioral response of P. citri. Active ingredients of acaricides are major contributor to synergize mites’ toxicity (Axelrad et al. 2002, Fanning et al. 2018), but nonactive ingredients also play a role in behavioral changes of P. citri due to sensory organs interaction. Future more deep studies are needed to check all ingredients’ behavioral effects in chemicals to get more accurate results (Zalucki and Furlong 2017). Oviposition Rate of P. citri With Chemical Contact Irritancy and Repellency The acaricidal effect’s impact is mostly evaluated by life-history traits, especially the fecundity rate for secondary population outbreak mechanisms (James and Price 2002). Hence, it is important to understand the fecundity rate of irritated and repelled mites. In all treatments, the number of eggs per female P. citri were nonsignificant differences between irritated or repelled and nonirritated or nonrepelled in control. Female mites irritated by abamectin and EnSpray 99 application at LC90, laid a significant higher number of eggs per female. While vegetable oil (except non-irritated in Trt. no. 1) and SYP-9625 at LC50, laid maximum number of eggs (Supp Figs. 2–5 [online only]). Mites repelled by LC90 gave a higher number of eggs per female for SYP-9625 (except Trt. no. 2 and 6), abamectin (except Trt. no. 2 and 6), vegetable oil (except Trt. no. 2), and EnSpray 99 (except Trt. no. 2 and 8) (Supp Figs. 6–9). Different treatments evaluate that some chemical doses induced fecundity rate at LC30 in all treatments as colupulone for T. urticae (Jones et al. 1996). While mites with direct exposure to chemicals boosted the fecundity rate of P. citri as resulted by James and Price (2002) and Adesanya et al. (2019) against T. urticae due to fecundity stimulation by different chemicals like imidacloprid (James and Price 2002) instead of hormoligosis (Cutler 2013, Guedes and Cutler 2014). Some individuals gave more irritancy, repellency, and fecundity rate on the untreated leaf surfaces after contact with the treated surface. This suggests that P. citri may have a negative or positive effect, which may or may not depend on the treated surfaces. Furthermore, assessing the resistance mechanism of P. citri to synthetic and natural chemicals provides additional information for better control strategies. In this study, we showed the dispersal behavior of P. citri for a better understanding of secondary outbreaks in the future. Citrus red mites movement from apex to base leaves for better habitat and food. This dispersal behavior of mites found time-dependent and mature leaves lovers. Within leaflets, the maximum number of mites was recorded on the adaxial surface along the midrib. Furthermore, our result demonstrates that change in treatments leads to a change in the behavioral responses. This study covers the problems of ineffective chemical application in the field for the management of P. citri. It addresses the secondary outbreak mechanism of pests by the impact of repellency and irritancy on its dispersal. Future studies need to check long-term dispersal behaviors, life-history traits (as tetranychids elicit sensory responses), and physiological alteration. Acknowledgments All aurthors acknowledged the support of Guangdong provincial government, China and Guangdong Academy of Agricultural Sciences for their support and facilities. 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TI - Dispersal Mechanism Assessment for Panonychus citri (Acari: Tetranychidae) Secondary Outbreaks
JF - Annals of the Entomological Society of America
DO - 10.1093/aesa/saab008
DA - 2021-04-12
UR - https://www.deepdyve.com/lp/oxford-university-press/dispersal-mechanism-assessment-for-panonychus-citri-acari-30icd4lPiw
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -