Laboratory evaluation of functional responses of predator Anthocoris nemoralis (Hemiptera: Anthocoridae) to Cacopsylla pyri (Hemiptera: Psyllidae), at two temperatures
Abstract
Biological control constitutes an effective approach for managing pest populations in horticulture, providing an alternative to chemical pesticide reliance. To ensure successful integration of predators into biological control programs, a precise assessment of their functional response to prey density variations under controlled laboratory conditions is essential. This study aimed to investigate the functional response of 5th stage nymph, male and female of Anthocoris nemoralis predator to pear psylla Cacopsylla pyri 4th and 5th nymphs on two temperatures (15 and 27 ºC). Logistic regression followed by nonlinear least squares regression were used to determine the type of functional response of predayor and to estimate the attack rate (a) and the handling time (Th). Our results exhibited a type II functional response for all experiments. There was a significant difference between attack rate of same stage of predator due to raising temperatures (a positive relationship), whereas no significant differences were observed for handling times (a negative relationship). 5th stage nymph showed the lowest attack rate and the highest handling time compared to other stages (0. 010, 0. 028 for a and 1. 846, 1. 658 for Th at 15 and 27 ºC, respectively), whereas females had the highest attack rate and the shortest handling time at all experiments (0. 035, 0. 086 for a and 1. 347, 1. 658 at 15 and 27 C, respectively), anyway there was no significant difference between parameters of 5th stage nymph and male. Female had the highest maximum theoritical attack rate (20. 924 and 30. 341 nymph/day) at 15 and 27 ºC, respectively. Our findings demonstrate that adult female of A. nemoralis can be used as optimal biological agents for controling C. pyri.
Full Text
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Introduction
The pear psylla, Cacopsylla pyri (Linne) (Hemiptera: Psyllidae), is one of the most serious economic pest of pear trees Pyrus communis Linnaeus, (Rosaceae) worldwide (Nin et al, 2012) [54] , which may cause heavy economical losses to most pear growing regions (Tešanović and Spasić, 2018) [75] . This pest can damage pear trees in two main ways classified as direct damages including weakening the plant by subtraction of nutrients; and indirect damages like production of large amounts of honeydew which stimulates the black sooty mold (Montanari et al., 2015) [47] , and the possible transmission of pear decline disease (Candidatus Phytoplasma pyri); which decreases pear vegetative and fruit growth eventually leading to the death of trees (Süle et al., 2007) [73] . For the beginning of laying egg by overwintered individuals a temperature over 10 °C for two successive days is required, as the first eggs are laid directly on wood, typically near of unopened bud bases (Nin et al., 2012) [54] , C. pyri develops 5-7 generations per year (Nin et al., 2012) [54] , and it has five development nymphal stages (Tešanović and Spasić, 2018) [75] . Throughout years and because of excessive use of chemical control, pear psylla has developed resistance to many commonly used insecticides (Emami, 2008; Civolani, 2012) [14,7] , consequently, there has been growing interest in adopting Integrated Pest Management (IPM) strategies of pear psylla, with particular emphasis on enhancing populations of natural enemy populations against this pest (Shaw et al., 2021) [69] . Several species of generalist predators commonly attack C. pyri like Coccinellidae, Chrysopidae, Aranae, Miridae and Anthocoridae (Daugherty et al., 2007) [8] . Anthocorid bugs (Anthocoridae) are among the most important predators of pear psylla, with Anthocoris nemoralis (Fabricius) (Hemiptera: Anthocoridae) being a particularly effective biological control agent of pear psylla, its natural range includes Europe and the Mediterranean region (Krndija et al., 2024) [39] . The adult overwinters beneath tree bark and other sheltered places, emerging when prey availability and weather conditions become favorable (Sigsgaard, 2010) [70] , then usually peaks during mid to late summer, helping to suppress C. pyri populations (Nagy et al., 2008) [51] . This predator has five nymphal instars, and both mature and immature stages feed on eggs as well as nymphs of pear psylla, and effectively reduce their numbers (Sigsgaard et al., 2006; Emami, 2010) [71,15] , an individual anthocorid predator can consume approximately 5,000 pear psylla eggs during its lifetime (Yanik and Ugur, 2004) [83] , showing equal feeding efficiency on both eggs and nymphs per unit biomass (Sigsgaard, 2010) [70] . In different ecological conditions, A. nemoralis might give three up to six generations/year being affected to temperature (Oudeh et al., 2013) [54] . Researches showed that anthocorids can be www.extensionjournal.com released artificially into orchards as a biological control agents, to suppress pear psylla populations effectively (Gajski and Pekár, 2021), adult anthocorids as well as nymphs are able to bring about 30-50% reductions or more in pear psylla numbers in pear orchards (Sigsgaard et al., 2006) [71] , also augmentative releases of the immature stage of A. nemoralis in olive orchards resulted in significant reductions in psylla densities (Gharbi, 2021) [20] . The functional response is the basic mechanism that reveals different aspects of prey-predator behavior, explains their coevolutionary interactions, and can determine the efficiency of a predator in regulating prey populations (Holling, 1965; Martinou et al., 2010) [30,44] . According to Solomon (1949) [72] and Holling (1959) [32] , the number of prey consumed per predator as a function of different prey densities is known as the functional response. The functional response of a predator is determined by two important parameters: attack rate ( a ) which conducts the ability to find a prey, and the handling (Th) which represents how fast a prey is consumed including discovering of a prey, killing, capturing, eating and digesting it (Holling, 1966) [31] . Three main functional response types are observed in predator-prey systems, a type I functional response shows a linear relationship between consumption rate and prey density, a type II functional response shows a hyperbolic relationship between consumption rate and prey density, that eventually reaches the predator's satiation level and remains constant at high densities and type III functional response which exhibits a sigmoid relationship between the number of prey consumed and the number of prey ofered, as at low prey densities the predator consumption increases slowly, then accelerates at intermediate densities, and finally plateaus at high densities (Holling, 1959) [32] . Various abiotic and biotic factors can affect the functional response type and its parameters: attack rate (a) and handling time (T h ), such as host plant type (Emami et al., 2014; Jafarian et al., 2022) [12,33] , prey type and size (Donnelly and Phillips, 2001 [11] ; Kalinoski and Delong, 2016 [37] ; Hassanzadeh-Avval et al. 2019) [24] , different life stages of predator or prey (Farhadi et al., 2010 [17] ; Shahpouri et al., 2019 [68] ; Hassanzadeh-Avval et al. 2019 [24] , Dehkordi et al., 2023) [9] , sex of predator (Emami et al., 2014 [12] ; Hassanzadeh-Avval et al. 2019 [24] ; Reeves et al., 2023) [57] , prey distribution (Feng et al., 2018) [18] , temperature (Gitonga et al., 2012; adbouni, 2017 [43] ; Hassanzadeh-Avval et al. 2019 [24] ; Hassanpour et al., 2020 [23] ; Reeves et al., 2023) [57] , spatial complexity (Alexander, 2012) [2] , presence of alternative prey (Murdoch, 1969; Wei and Walde, 1997) [50,82] , and arena size (Sabaghi et al., 2011 [61] ; Uiterwaal and Delong, 2018) [61] . Psylla mentioned as a key pest of pears in the climatic conditions of regions where spring and summer are dry and rainfall is rare, like The Middle East and near by. In Iran, Emami (2016) [13] mentioned Cacopsylla pyricola as an important pest of commercial pear in all pear-growing regions, also Esmaeily et al., (2022) [16] mentioned that Cacopsylla permixta and Cacopsylla bidens are major pests of pears, also Latifian, and Abdollahi (2025) [40] mentioned C. pyri as an important pest of pear oorchards In Syria, C. pyri recorded to infest pear orchards in north-west Damascus (Saour et al., 2010) [62] , also Almatni and Alabdulla (2003) [4] mentioned pear psylla C. bidens in as a main pest of pear in south of Syria (Alswaidaa), Oudeh et al., (2015) also mentioned pear psylla C. pyricola in pear orchards in the middle of Syria (Homs). In Turkey, Serce et al. (2006) [65] and Sertkaya et al. (2008) [66] mentioned C. pyri as a vector of pear decline diseases (PD) in the region of Turkey. In Iraq, despite projections that indicate sustained growth, with production expected to rise to 14,580 metric tons by 2026 for pear (a 12. 7% annual increase from 13,550 metric tons in 2025 (ReportLinker, 2025) [58] , highlighting pear's escalating economic significance production of pear reached 10613. 27 metric tons in 2023, with a yield of 7068. 4 kg/h harvested from 1502 hectares (FAOSTAT, 2023) [19] , research on pear insect pests particularly C. pyri still limited, underscoring the urgent need for focused studies on this damaging pest to support sustainable production of pear.
To date experiments of studying functional response for mature and immature srages of predator A. nemoralis at multiple temperatures, still scarce, so the present research was designed to observe the type of functional response of 5 th stage nymphs, male and female predator A. nemoralis at two different temperatures (15 and 27 °C), The temperature 15 °C was selected as it is close to the thermal threshold for oviposition initiation in C. pyri, and 27°C represents an optimal developmental temperature for both pest and predator populations.
Materials and Methods
Collection and rearing of predator and prey
The experiment was conducted in 2023, different nymphal instars and adults of pear psylla and Anthocorid were collected from pear orchards in Babel governoriate, pear psylla nymphs were hand-collected carefully using a finehaired brush, to prevent injury to vulnerable nymph stage. For adult sampling, A. nemoralis and C. pyri individuals were captured via beat tray methodology: a foam-covered stick was used to sharply tap pear tree branches, while a white collection tray (230 × 450 mm) positioned beneath intercepted dislodged insects, besides collecting infested plant material (shoots with psyllids), and place them in ventilated cages, and harvest emerging predators, Adult C. pyri were maintained in transparent aerated plastic containers (10 cm diameter, 18 cm height) with 4 pear shoots (9 cm in length) damped with a wet cotton wool to prevent dehydration. Individuals were kept in an environmentally controlled growth chamber at 23 °C and 65% RH. Adult and nymphal stages of C. pyri were morphologically identified using the standardized psyllid key (Agroscience, 2022) [1] . Anthocorid individuals were maintained in an aerated plastic pots, and fed on C. pyri nymphs daily. The collected bugs were identifed using the taxonomic keys of Linnavuori and Hosseini (2000) [42] and Hasanzadeh and Modarres (2010) [22] and adults were allowed to mate as they were kept in one container at 23 °C in the controlled chamber. Sex determination of anthocorids was conducted via light microscopic examination of genitalia. Individuals with inconclusive morphology were subsequently dissected to detect male-specific parameres (Hassanzadeh-Avval et al. 2020), or female copulatory tubes (Bu, 2007) [6] . www.extensionjournal.com
Functional Response Experiments
Trials were conducted in a 10 cm petri dish, the petri dish lid fitted with a ventilation hole covered with fine gauze. fresh pear leaf discs (30 mm) were placed abaxial side up on a moistened filter paper to preserve leaf discs (Montserrat et al., 2000) [48] . Different densities of 4 th and 5 th C. pyri nymphs (5, 10, 20, 40 and 80)/petri dish were used, as prey densities were established based on preliminary doseresponse assays conducted prior to the main experiment, besides preys were depleted during all trials. An adult predator (3 days old) or newly emerged 5 th stage nymph was transferred to each petri dish after a 24-hours starvation period, finally the petri dishes were secured using a paraffin film to avoid escaping of C. pyri nymphs (Emami et al., 2014) [12] After 24 hours, the predators were removed from the petri dishes and the numbers of consumed nymphs were recorded. The trials were performed at 15 and 27 ºC, 65% RH, and a photoperiod of 16:8 h (L: D) in an environmentally controlled chamber. Ten replicates were used for 5th stage nymph, male and female of predator for each prey density at two tested temperatures, with 300 total observations. To check the natural survival rate of nymph stage psylla, ten replicates were conducted at each density in the absence of predator. In our current study we reffered to different stages and sexes of A. nemoralis predator as stages.
Data Analyses Functional Response Experiments
This experiment involved two main steps: model Selection and parameters estimation. The type of the functional response for each stage and temperature was determined using a logistic regression analyse (Juliano 2001) [35] . Data were fitted to (Eq. 1) that describes the relationship between the proportion of consumed prey N a /N 0 as a function of initial prey density N 0 .
where N a is the number of consumed prey, N 0 is the initial number of preys, P0 is the intercept, P1 is the linear parameter, P2 is the quadratic parameter, and P3 is the cubic parameter. The parameters were calculated, using the method of maximum likelihood (PROC CATMOD, SAS Institute, 2004) [64] . If the linear term does not differ from 0, it indicates a type I functional response that is densityindependent. Suppose the linear parameter is significantly negative (P 1 < 0), in that case, the proportion of prey consumed by the predator declines monotonically as the initial prey density increases, indicating a type II functional response. In contrast, a significant positive linear parameter (P 1 > 0) with a negative quadratic parameter (P 2 < 0) demonstrates a type III functional response (Juliano, 2001) [35] . In the second step of the analysis, because the experiments allowed prey depletion (nymphs were not replaced when consumed), we used Rogers random equation (Eq. 2) (Rogers, 1972) [60] for functional response Type II and the integral Hassell equation (Eq. 3) (Hassell, 1978) [26] for functional response type III to fit data, using a nonlinear least squares regression (PROC NLIN; SAS Institute Inc.
2004) [64] as theses equations are applicable to nonreplacement experiments.
N a is the consumed number of prey (pear psylla nymphs) by predator individual, N 0 is the initial prey density, a is the attack rate, T h is the handling time and T is the total time in hours for the experiment (24 h).
(Eq. 3) where b, c, and d are constants from the function that relates the attack coefficient (a) and N 0 in the type III functional response. The attack coefficient (Eq 4) (Hassell 1978) [26] .
Functional response models (Types II and Type III) were statistically compared using Okuyama's (2013) [53] AICbased framework (Eq. 5), with optimal model selection determined by minimum AIC values AIC = n log (MSE) + 2q (Eq. 5)
n is the sample size, MSE is mean square error and q is number of parameters
To compare predator functional response parameters (attack eate and handling time) for A. nemoralis stages on two temperatures, we fitted the data to Juliano (2001) [35] equation (Eq. 6).
Na= N 0 {1 -exp[a+D a (j)(T h +D Th (j)Ne -T)]} (Eq. 6)
Where, j, is an indicator variable takes value 0 for data set 1 and value 1 for data set 2. The parameters, D a and, D Th , estimate the differences between the two data sets being compared for the parameters a and, T h values, respectively. In other words, a and T h are the estimates of the parameters for data set 1, and a + D a and,, T h + D Th , are the estimates of the parameters for dataset 2. We can assess the significant difference in parameters for the two sets as 95% confidence intervals included 0 (the difference was non-significant) or not (the difference was significant) (Juliano, 2001) [35] , nonlinear least square regressions were again used to obtain parameter estimates.
For each prey density we calculated total handling time (Eq. 7), search time (Eq. 8), attack rate (Eq. 9), and search efficiency (Eq. 10) (Hassell, 2000; Rocha and Redaelli, 2004) [27,59] .
Th total = T h x Na (Eq. 7)
T s =T -Th total (Eq. 8) a = N a / (N 0 x T s ) (Eq. 9) E = N a /N 0 (Eq. 10) www.extensionjournal.com
Statistical analysis was performed using SAS software, the difference between numbers of prey consumed depending on initial density at the two tested temperatures was tested using a KruskalWallis test, as data were non-normally distributed. The curves of the number of consumed prey by A. nemoralis different stages to different densities of C. pyri nymphs were plotted by Excel software.
Results
Functional Response Experiments
Functional response curves of 5 th stage nymph, male and female of A. nemoralis to the various densities of C. Pyri nymphs are presented in (Figs. 1 and2). The female curve was the highest which indicate that female was more voracious than other stages. The number of consumed nymphs by the predator increased with increasing prey density and temperature (Figs. 1 and2). The proportion of the prey killed by 5 th stage nymph, male and female of A. nemoralis declined with increasing prey density for the two tested temperatures (Fig. 3 and4). Parameter estimates form the logistic regressions equation (Eq. 1) showed a significantly negative linear coefficients (P1) for all tested stages (5 th stage nymph, male and female) (Table 1) on the two tested temperatures, which all suggested a Type II functional response. No mortality was observed during the experiments in the control. 3). Our results demonstrated that attack rate had a positive relationship with temperature as it increased for all predator stages by temperature increasing. On the other hand, handling time had a negative relationship with temperature for all predator stages (Table 3). Female had the highest maximum theoritical predation rate to pear psylla nymphs (T/T h ) 20. 924 and 30. 341 at 15 and 27 ºC, respectively, whereas 5 th stage nymph had the minimum theoretical preparation rate, 13. 001 and 14. 475 nymph/day at 15 and 27 ºC, respectively. The predatory efficiency of A. nemoralis can be accurately objectived by the functional response ratio (FRR = a/T h ) (Wang et al., 2023) [41] , according to our results female showed the highest FRR, which had a positive relationship with temperature increasing (0. 030, 0. 108 for 15 and 27 ºC, respectively), while 5 th srage nymph showed the lowest FRR at all temperatures (0. 005 and 0. 016 at 15 and 27 ºC, respectively). The 95% confidence intervals, estimated by (Eq. 5), for D a and D Th comparisons between 5 th stage nymph and male included 0 in all experiments (Table 4), which indicated that no significant differences of attack rate and handling time was found between these two stages (the 95% confidence intervals for a and T h overlapped between 5 th stage nymph and male in all experiments). Whereas the 95% confidence intervals for D a and D Th comparisions between female and other stages (5 th stage nymph and male) in all experiments didn't include 0, (Table 4), which indicated a significant differences in attack rate and handling time between female and other stages (the 95% confidence intervals for a and T h didn't overlap between female and other stages; 5 th stage nymph and male; in all experiments). www.extensionjournal.com Raising in temperature had a significant impact on attack rate (a) of the same stage or sex of A. nemoralis as the 95% confidence intervals didn't contain 0, on the other hand it didn't have any significant effect on handling time T h of the same stage or sex of A. nemoralis as the 95% confidence intervals contained 0 (table 5). The results showed a significant difference between the number of prey consumed on different prey densities on all predator stages in all experiments, (Kruskal Wallis: χ 2 =186. 562, df=4, p<0. 001). With an average of 3. 7±1. 14, 12. 46±2. 72 nymphs consumed over 24 h at the lowest (5) and highest (80) densities, respectively. However, no significant differences were observed between the three densities 20, 40 and 80 for 5 th stage nymph and male, also no significant differences were observed between the two densities 40 and 80 for suggesting that the satiation point for prey consumption had been reached (Reeves et al., 2023) [57] .
There was a significant difference in number of nymphs consumed depending on predator stage (Kruskal Wallis: χ 2 =43. 094, df=2, p<0. 001), with an average of 9. 3±2. 34 nymphs consumed by 5th stage nymph, an average of 10. 25±3. 52 consumed by males and an average of 17. 85±2. 46 nymphs consumed by females at the highest density (80).
Also, the number of nymphs consumed depending on temperature differed significantly for 5th stage nymph (Kruskal Wallis: χ 2 =14. 041, df=1, p<0. 001), males (Kruskal Wallis: χ 2 =16. 951, df=1, p<0. 001), and females (Kruskal Wallis: χ 2 =19. 258, df=1, p<0. 001) with an average of 9. 3±0. 34 nymphs killed at 15 ºC and 15. 63±1. 14 nymphs at 27 ºC, for the highest prey densities (80). The total handling time (T h ) for 5 th stage nymph, male and females of A. nemoralis increased with increasing prey densities and temperature increasing, but was the least for female at all densities. However, the total searching time (T s ), the attack rates (a) and searching efficiency (E) for 5 th stage nymph, male and females of A. nemoralis showed an inverse relationship with both prey densities and temperature, with highest values for female at all densities (table 6).
Discussion
Functional Response of predator A. nemoralis to C. pyri According to the results of our research, all tested stages of A. nemoralis (5 th stage nymph, male and female) showed an increasing predation rate with increasing prey density, and a declining proportion of prey consumed by increasing prey density, which indicated a type II functional response (Holling, 1959) [32] for all temperature experiments when feeding on 4 th and 5 th stage nymphs of C. pyri. Several authors reported a type II functional response for some species of anthocorids including Xylocoris flavipes to three store insect pests (Rahman et al., 2009) [56] , Orius sauteri on Thrips palmi (Hemerik and Yano, 2010) [28] , Orius aalbidipenni on barely aphid Sipha maydis (Moghaddam et al., 2012) [46] , A. nemoralis on C. pyri; (Reeves et al., 2023) [57] , adult predator A. minki to 4 th stage nymph of prey Psyllopsis repens (Hassanzadeh-Avval et al. 2019) [24] , A. nemoralis on C. pyricola (Emami et al., 2014) [12] , A. minki pistaciae on Agonoscena pistaciae (Kheradmand et al., 2017) [38] and Orius vicinus on Bactericera cockerelli (Tran et al. 2012) [76] , so we can say that A. nemoralis has potential in suppressing C. pyri populations in pear orchards, as predators that show type II functional response can be used in inundative biological control programs that aim at direct pest suppression (Van Lenteren, 2012) [79] . In contrast, Anthocorid predators have occasionally exhibited type III functional responses in some cases like adult predator of A. minki to 2 nd stage nymphs of prey P. repens (Hassanzadeh-Avval et al., 2019) [24] and adult female of predator Hyperaspis popoli to the 1 st instar of Phenacoccus solenopsis (Seyfollahi et al., 2019) [67] , and this typically occur when feeding on cryptic, relatively small and immobile prey (Hassell, 1978) [26] as predation rate accelerates at intermediate pre densities due to learning or switching behavior.
Type II functional responses may lead to instability in predator-prey systems, as high predation pressure at low prey densities may lead prey population to collapse. In contrast, Type III functional responses typically stabilize predator-prey systems through two mechanisms: providing a prey refuge at low densities (due to low predator search efficiency), and density-dependent switching to alternative prey, coupled with improved foraging efficiency at high prey densities (Varshney et al., 2018) [78] . Thus, Type II functional response predators like A. nemoralis are often more effective at controlling low-density pest populations, idealizing them for augmentative biological control, particularly at high predator-prey ratios. Theoretical maximum predation rate (T/T h ) is the upper asymptote of the functional response curve and represents the high potential of a predator to eat its prey during a period of 24 h (Jafari et al., 2012) [34] , and in our findings female showed the highest T/T h along with the highest temperature (27 ºC) which indicated that it was more voracious than other stages, and more efficient at high temperature, this is likely due to nutritional requirements for reproduction (li et al., 2024), that was in agreement with Hassanpour et al. (2020) [23] who found that the highest maximum predation rate (T/T h ) showed by females followed by males of Orius laevigatus feeding on A. gossypii happened at 30 ºC compared to lower temperatures tested. The estimation of FRR (a/T h ) can be useful for determining the possibility of the optimal ratio between predator and target pest for inoculative release (Wang et al., 2019) [81] , and according to our results the estimated a/T h showed that female of A. nemoralis had an effective predatory potential for the control of C. pyri ah high temperature, and 5 th stage nymph had the least efficiency for the control of C. pyri at all temperatures, which indicate thar FRR influenced by temperature, stage and sex predator. Functional Response and stage of A. nemoralis Attack rate and handling time are important indicators to the voracity of stages of A. nemoralis predator. Our results showed significant differences in the estimated attack (a) rates across the mature and immature stages of A. nemoralis, finding that female had the highest attack eate, which indicated that attack rate was affected by predator stage and sex. The larger body size of females and their metabolic costs associated with producing eggs makes a high foraging requirement of females consequently a higher prey attack and consuming compared than to other stages (Hodek and Honek 1996) [29] . The attack rate determines how steeply the functional response curve rises with increasing prey density (Dehkordi et al., 2023) [9] . Thus, according to our findings, the steepness changed among different developmental stages of A. nemoralis, while female had the highest capacity to respond to prey densities, the 5 th stage nymph and male had almost similar capacities. The handling time (T h ) is a good indicator of the predation rate since it exhibits the total accumulative time spent in catching, subduing, killing, and digesting the prey (Veeravel and Baskaran, 1997) [80] , our results indicated that the 5 th stage nymph of A. nemoralis spent more time handling and consuming C. pyri nymphs than adult males and females, while the handling time of female was the shortest among other stages, in other word, the handling time decreased as the predator age increased, but with no significant differences between 5 th stage nymph and male.
According to our results we can suggest that female was the most effective stage of predator A. nemoralis to C. pyri nymph, as natural enemies with high attack rate (a) and low handling time (T h ) are considered to be the most effective biocontrol agents (Bayoumy, 2011; Tazerouni et al., 2016) [5, 74] . Also we can say that adult male of A. nemoralis was more favourable as a biocontrol agent compared to 5 th nymph stage, as it had a slightly higher attack rate and shorter handling time.
Our results was in agreement with Reeves et al. (2023) [57] who found that female of A. nemoralis predator had a significantly higher attack rate and a significantly lower handling time compared to male at three different temperatures (18,21 and 23 ºC) when feeding on C. pyri. Also our results was similar to Hassanzadeh-Avval et al.
(2019) [24] who mentioned that attack rates of nymph and adult of A. minki predators were significantly different but no differences on handling times were observed when feeding on P. repenis. Rocha and Redaelli (2004) [59] found that handling time of Cosmoclopius nigroannolatus on Spartocera dentiventris was higher in males than females; also Bayoumy (2011) [5] found that the functional response of 4 [29,3] . Functional response and temperature Our results showed that all temperature experiments exhibited a type II functional response. For all tested stages attack rate had increased significantly as temperature increased, indicating that temperature clearly influenced the magnitude of predator response to prey, this may be attributed to temperature-related changes in the metabolism and activity of predator and prey (McCoull et al. 1998) [45] . Reeves et al., 2023 [57] revealed that no significant difference was noticed in attack rate of male and female A. nemoralis due to temperature, and demonstrated that this non significant difference might be due to small intervals among tested temperatures (i. e 18, 21 and 23 ºC), while our result was in agreement with other authers who studied temperature effect on functional response with clear intervals between tested temperatures like Hassanzadeh-Avval et al. (2019) [24] who found a signifcant diferences in attack rate between the 15 and 30 ºC treatments used with the anthocorid A. mink, Hassanpour et al. (2020) [23] who studied the functional responses of Orius laevigatus at 20, 25 and 30 ºC and found that attack rate raised significantly of female anthocorids as temperature raised from 30 ºC to 20 ºC and DingXu et al. (2007) who find that temperature had a significant effects on the predation and functional response of the predator Scolothrips takahashii when fed on Tetranychus viennensis, On the others hand, handling time had decreased as temperature increased, which suggested that predator across developmental stages exhibited prolonged non-searching behavior at reduced temperatures like resting, while elevated temperatures triggered more intensive searching and feeding activities, indicating that high temperature had a positive effect on the foraging behavior of predator. Our findings was in agreement with Hassanzadeh-Avval et al.
(2019) [24] who revealed that temperature rising had an adverse effect to handling time, while it had a positive effect on attack rate. The negative relationship between temperature and handling time might be due to the increasing rate of metabolism which led to a reducing in digestion time (Sentis et al., 2013; Robertson and Hammill 2021).
Conclusions
This study provides valuable insights into the functional response of A. nemoralis predator to pear psylla C. pyri, contributing to the understanding of more effective pest management strategies in pear-growing regions. With Pear Psylla posing an escalating threat to pear orchards, these findings are critical for mitigating its impact on pear production in Iraq and beyond. To build upon these findings, we propose conducting field studies on the predator's functional response towards the target prey. This will yield more comprehensive results reflecting the influence of local climatic conditions on predator-prey dynamics. Furthermore, studying numerical responce and life tables for A. nemoralis on this specific prey and for C. pyri itself is recommended. Crucially, linking the pest's life table parameters with locally cultivated pear cultivars would help identify varieties exhibiting heightened susceptibility to infestation, as indicated by elevated values in key life table parameters. This integrated approach will significantly enhance the practical application of biological control measures against C. pyri in Iraq.
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