Acta agriculturae Slovenica, 120/1, 1–11, Ljubljana 2024 doi:10.14720/aas.2024.120.1.18050 Original research article / izvirni znanstveni članek Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organic citrus orchards under varying climatic conditions: A case study from north-west Algeria Abdelhaq MAHMOUDI 1, 2, 3 , Leila ALLAL BENFEKIH 2 , Matheus GOOSEN 4 Received January 24, 2024; accepted February 20, 2024. Delo je prispelo 24. januarja 2024, sprejeto 20. februarja 2024. 1 Department of Agronomy, Faculty of Life and Natural Sciences, Hassiba Benbouali University of Chlef, Chlef, Algeria 2 Laboratory of medicinal and aromatic plants, Department of biotechnologies, Faculty of Life and Natural Sciences, University of Blida, Blida, Algeria 3 Corresponding author, e-mail: a.mahmoudi@univ-chlef.dz 4 Office of Research & Graduate Studies, Alfaisal University, Riyadh, Saudi Arabia Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organ- ic citrus orchards under varying climatic conditions: A case study from north-west Algeria Abstract: The citrus pest, Dialeurodes citri (Ashmead, 1885), poses a significant threat to citrus crops, impacting growth. Various control methods, including biological mea- sures using natural predators like Clitostethus arcuatus (Rossi, 1794), Chrysoperla carnea (Stephens, 1836), and Semidalis aleyrodiformis (Stephens, 1836), were studied over a year in the Chlef region of northwest Algeria. Results indicated that a temperature range of 19.5 °C to 30.5 °C, with 65 % humid- ity and no precipitation, favored the emergence of D.  citri adults. Throughout the study, S. aleyrodiformis and C. arcuatus emerged as the predominant predators. A strong negative cor- relation (r = -0.91) was observed between D. citri abundance and C. arcuatus caught on traps. The correlation between nymphal infestation rates and monthly average temperatures was negative (r = -0.72), with temperatures ranging from 13 °C to 27 °C and humidity between 47 % and 73 %, conducive to D. citri nymphal infestation. Precipitation negatively impacted D. citri and its predators, causing a decline in adult numbers during the rainy season. The overarching goal is to establish an integrated biological control system, bolstering the economic viability of citrus cultivation in the region. Key words: D. citri, predators, citrus, climatic parameters, abundance, north-west Algeria Preučevanje nihanja napada agrumovega ščitkarja (Dialeu- rodes citri [Ashmead, 1885]) in njegovih plenilcev v ekološki pridelavi pri različnih podnebnih razmerah: vzorčna raziska- va iz severozahodne Alžirije Izvleček: Škodljivec agrumov Dialeurodes citri (Ashme- ad, 1885) predstavlja pomembno grožnjo pridelavi agrumov zaradi negativnega vpliva na rast. Različne metode njegovega zatiranja, vključno z biotičnimi, ki vključujejo plenilce, kot so vrste Clitosthutus arcuatus (Rossi, 1794), Chrysoperla carnea (Stephens, 1836) in Semidalis aleyrodiformis (Stephens, 1836), so bile preučevane v eni rastni dobi na območju Chlef v severo- zahodni Alžiriji. Rezultati so pokazali, da je temperatura v ob- močju od 19,5 do 30,5 °C, ob 65 % relativni zračni vlagi in brez padavin, pospeševala pojav odraslih osebkov škodljivca. Skozi celotno obdobje raziskave sta se vrsti S. aleyrodiformis in C. ar- cuatus pojavljali kot glavna plenilca. Ugotovljena je bila moč- na negativna korelacija (r = -0,91) med številčnostjo škodljiv- ca (D. citri) in plenilca C. arcuatus na pasteh. Korelacija med številčnostjo nimf in poprečno mesečno temperaturo je bila negativna (r = -0,72), s temperaturo od 13 do 27 °C in relativno zračno vlago med 47 in 73 %, kar je pospeševalo napad nimf škodljivca. Padavine so negativno vplivale na škodljivca in nje- gove plenilce, kar je povzročilo upad števila odraslih osebkov v deževnem obdobju. Glavni namen raziskave je vzpostaviti sistem integriranega varstva, kar bi pospešilo bolj gospodarno gojenje agrumov na območju raziskave. Ključne besede: D. citri, plenilci, citrus, podnebni para- metri, številčnost, severozahodna Alžirija Acta agriculturae Slovenica, 120/1 – 2024 2 A. MAHMOUDI et al. 1 INTRODUCTION Citrus is a major fruit crop in many parts of the world (Ahmed & Azmat, 2019, Anjos et al., 2021) in- cluding Africa (Oke et al., 2020). Algeria, for example, is the fifth largest citrus producer in Africa with more than 1.478.053 tons generated from 71.470 ha (FAO, 2020). A major problem is that citrus products around the world have been affected by numerous insect pests (Uygun & Satar,2008), such as the citrus whitefly Dialeurodes citri (Wang et al., 2021, Butter & Dhawan, 2021), which can cause high yield losses due to sucking of plant sap by nymphs (Zhang & Li, 2012; Yuan et al., 2017; Boulahia- Kheder, 2021). Recently, Zhang et al. (2019) reported that D. citri can be an effective vector for virus CYVCV to citrus. It is also one of the most important citrus pests in the Mediterranean region (Bellows & Meisenbacher, 2007; Martin et al., 2000; Boulahia-Kheder, 2021) includ- ing Algeria (Boukhalfa & Bonafonte, 1979). Indeed, chemical treatment has been one of the best management strategies for controlling the citrus whitefly (Yuan et al., 2017). However, pesticides can have a nega- tive effect on natural enemies and sustainability of crop systems (Corallo et al., 2021).Several environmentally friendly approaches have been developed to control cit- rus pest (Wuryantini et al., 2021). In the biological con- trol of pests in citrus orchards, predatory insects can play a decisive role and can be a good alternative to chemical treatment (Rattanapun, 2017; Ahmed & Azmat, 2019; Oke et al., 2020; Smaili et al., 2020; Mansour et al., 2021). Their feeding habits are typically polyphagous, and thus help to prevent the buildup of populations of insects that feed on green plants. The identity and abundance of predatory insects has been studied in numerous cit- ruses producing areas around the world. Indeed, Jacas et al. (2010) reported that biological control has been very effective in managing whiteflies. The lacewings and Clitostethus arcuatus (Rossi, 1794), for instance, are the main predators of whiteflies (Sagar et al., 2020). The ladybird beetle, C. arcuatus, is one of the most effective predators of the whitefly since its feeds on all development stages of Aleyrodidae (Yazdani & Samih, 2012). A single beetle consumes more than 50 D. citri eggs per day (Onillon, 1975). Another predator is Chrys- operla carnea (Stephens, 1836), one of the species of common green lacewing insects in the Chrysopidae fam- ily. Although the adults feed on nectar, pollen and aphid honeydew, the larvae are active predators and feed on whiteflies and other small insects. This species has been used in the biological control of insect pests on crops (Villenave et al., 2005). The study of insect-pest biology is very important for developing effective biological control strategies (Umeh & Adeyemi, 2011). However, Benmessaoud-Boukhalfa & Chebrou (2014) reported that the study of the dynamics of whitefly populations is complicated because of their polyvoltinism (i.e., having several generations per year), and their intricate and variable interactions with climatic factors such as temperature, humidity, and precipitation, as well as their host plant. In the current investigation, the relationship be- tween the citrus whitefly pest D. citri and its predators C. arcuatus, C. carnea and S. aleyrodiformis (Stephens, 1836) was examined over a one-year period under vary- ing climatic conditions. Organic citrus orchards of the Chlef region in north-west Algeria was utilized as a case study. The long-term aim is to develop an integrated bio- logical control system to enhance the economics of citrus growth in the region. 2 MATERIALS AND METHODS 2.1 STUDY REGION AND EXPERIMENTAL SITES The current investigation was conducted in the cit- rus region of Chlef located in the north-west of Algeria close to the coast of the Mediterranean Sea. According to meteorological data provided by the Chlef meteoro- logical station for the period 2009-2017, the climate of the area is semi-arid, with hot summers and mild win- ters (Mahmoudi et al., 2018). The altitude varied from 83 to 156 m. Precipitation was irregular, and the wettest year was 2012 (525 mm) while the driest year was 2015 (256 mm).The mean annual temperature was 21 °C with an average maximum temperature of 30.8 °C in August. Furthermore, the selection of sampling sites was based on the choice of an orchard infested by citrus whitefly populations that had not been treated with pesticides. The experimental sites were in two localities, Boukadir Table 1: Description of orchards studied Study sites Study sites key Variety Age (years) Area (ha) Geographic coordinates Boukadir BOK Citrus sinensis ‘Thomson Navel’ 59 1.2 -36.04391 10.9496 Ouedfodda ODF Citrus sinensis ‘Valencia’ 38 3.2 -36.11569 13.4438 Acta agriculturae Slovenica, 120/1 – 2024 3 Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organic citrus orchards ... and Oued Fodda (Table 1). The Boukadir investigational site was located 39.6 km from the Oued Fodda citrus or- chard. 2.2 METEOROLOGICAL DATA AND INSECT SAMPLING Monthly maximum and minimum temperature, to- gether with monthly humidity, were recorded from the Chlef meteorological station. The sampling design allows for the collection of data on insect infestation, with a fo- cus on adult insects caught in sticky traps, along with the condition of leaves sampled from different trees. Sam- pling of insects was made under field conditions approxi- mately every month during the winter periods and fort- nightly during the entire season of insect activity (Soto, 1999; Rodrigues & Cassino, 2012) from the first week of July 2015 to the last week of June 2016. For the same sam- pling periods, the first emerged adults were reported by visual observations on infested young shoots. For each sampling visit, the experiment is replicated and each rep- lication involves selecting 10 trees randomly from each orchard. From each selected tree, 5 leaves are chosen for sampling chosen from different orientations around the tree: North, South, East, West, and the center. With 10 trees sampled and 5 leaves per tree, a total of 50 leaves are sampled per replication and were placed separately in plastic bags to be observed on the laboratory under a binocular microscope. Living nymphs were counted on the leaves to estimate infestation rate of D. citri larvae. Nymphal infestation rate and adult abundance in each grove were correlated with climatic parameters. Larval infestation rate equals (number of live larvae/total of lar- vae)/100. However, adult abundance refers to the mean number of adults for each sampling. D. citri adults and their predators were caught by suspending randomly three yellow sticky traps (25 x 10 cm) at a height of 1.5 m on the outside of the tree canopy (Calabuig et al., 2015; Eserkaya & Karaca, 2016; Hernán- dez-Landa et al., 2018).The yellow sticky traps were placed diagonally, and spaced 50 meters apart from each other, and replaced at every visit and the insects captured were counted under a binocular microscope (x20, ×40, and ×80) (Ekbom & Rumei, 1990). This study employed a total of 120 yellow sticky traps. 2.3 INSECT IDENTIFICATION Butter and Dhawan (2021) reported that the taxon- omists use the characteristic features of the fourth instar pupa of whitefly for species identification. Insect identification relying solely on external mor- phology indeed has its limitations, particularly when dealing with species that exhibit morphological varia- tions. In such cases, genetic analysis through DNA bar- coding can provide more accurate species identification, with complement morphological observations (Tahir et al., 2018). Collaborating with taxonomic experts can aid in accurate species identification. In our case, Mr. Streito (INRA Montpellier) and Mr. Reynaud (ANSES Plant Health Laboratory) were actively involved in the identifi- cation of whitefly specie as well as their predators. W e utilized identification keys based not only on ex- ternal morphological criteria but also on internal organs within insect bodies, such as the cement gland of D. citri female adult’s. By incorporating both external and inter- nal characteristics, we were able to enhance the accuracy and reliability of our identification methods. This com- prehensive approach allowed us to effectively distinguish between different species. Indeed, the fourth pupal stages of D. citri were col- lected from infested leaves and prepared for microscopic observation according to the method established by Mar- tin et al. (2000) and Hodges and Evans (2005). Female adults were removed from sticky traps, their cement glands were extracted and observed under optical micro- scope to confirm the identification of the pupa (Guima- rães, 1996). Martin (1987) reported that the identifica- tion of adult whiteflies based on external morphology is difficult when the populations of adults captured through the sticky traps are heterogeneous with more than one species. In the current study, only the D.citri were reg- istered without other whiteflies species. The adults were 1.2–1.4 mm long, with body and wings covered with white wax powder (Alford, 2012). Identification of adult predators captured was based on external morphology, C. carnea adult’s body was green and slender (i.e., 15- 20 mm long) with golden eyes (Dreistadt, 2012). How- ever, the C. arcuatus body was yellow to reddish brown, with an arc-shaped design on the dorsal side (1.2-1.5 mm long) (Klausnitzer, 2011). Although often confused with whiteflies because their bodies and wings are covered with whitish waxy secretion (Lee et al., 2010), S. aley- rodiformis is larger and has four wings with front wings larger than the hind ones (Mcewen et al., 2001). 2.4 STATISTICAL ANALYSIS The statistical analysis of the data involved the uti- lization of Past program version 3.24. This software was chosen for its capability to handle the specific analyses required for our study. In particular, Pearson correlation Acta agriculturae Slovenica, 120/1 – 2024 4 A. MAHMOUDI et al. tests were employed to assess the relationship between insect abundance and various meteorological param- eters. This choice of statistical tool was based on its suit- ability for examining the linear association between two continuous variables, which aligns with the nature of our research objectives. Furthermore, significance levels were established at p < 0.05, adhering to conventional standards in statisti- cal analysis to denote a statistically significant result. This threshold ensures that observed correlations are unlikely to have arisen by chance alone, thus lending credibility to our findings. In interpreting the strength of correlations, we fol- lowed the guidelines outlined by Schober et al. (2018). According to their classification, correlations with an r-values ranging from 1.0 to 0.9 were considered very strong, indicating a robust and almost perfect linear rela- tionship between variables. Correlations falling between 0.7 and 0.89 were deemed strong, suggesting a substan- tial linear association. Those ranging from 0.4 to 0.69 were classified as moderate, indicating a moderate degree of linear relationship. Finally, correlations between 0.10 and 0.39 were categorized as weak, signifying a minimal linear association. By adhering to these established criteria and em- ploying rigorous statistical methods, we aimed to ensure the reliability and validity of our data analysis, thereby enhancing the credibility of the results obtained. 3 RESULTS AND DISCUSSION 3.1 PERIODS OF D. citri EMERGENCE Table 2 shows that the adults of the first generation were recorded in the autumnal period (2015) generally from the end of August to the beginning of September, coinciding with the citrus autumn growth flush, when the mean maximum daily temperature exceeded 37 °C with a mean minimum daily temperature of 24 °C. The mean daily humidity was estimated at 63 % with an ab- sence of precipitation. Furthermore, the second emer- gence period was recorded in the spring period in mid- April (2016). In the spring citrus growth flush when the mean maximum daily temperature exceeded 26 °C with a mean minimum daily temperature of 13 °C. The mean daily humidity was estimated at 65 % without precipita- tion (Table 2). 3.2 NUMBER OF ADULTS OF D. citri AND ITS PREDATORS DETECTED IN THE CASE STUDY ORCHARDS The D. citri adults were measured in the Oued fodda (ODF) and Boukadir (BOK) groves. The number of cit- rus whitefly D. citri adult pests was found to be the largest in the BOK orchard compared to the ODF grove. In con- trast C. carnea adult predators were captured in just very small numbers in each orchard with only some adults be- ing trapped from January through June 2016 (Table 3). For example, for the ODF grove the C. carnea predator count was only 0.3 ±0.39 from January to July 2016, while the D. citri adult pest count was 309.6 ± 421.75. The C. ar- cuatus and S. aleyrodiformis adults were more abundant than C. carnea. In the ODF grove S. aleyrodiformis adults were more abundant from July through December 2015 (19.9 ± 19.70) but their number was small from January through June 2016 (7.5 ± 9.43) (Table 3). The relationship in seasonal abundance between D. citri pests and its predator C. arcuatus was analyzed from July 2015 to June 2016 (Figure 1). The number of D. citri adults and C. arcuatus caught on yellow sticky traps were the largest from July through December 2015 then grad- ually decreased from January through June 2016 (Figure 1). A moderate positive correlation (r= -0.42) in ODF grove was noted and a very strong positive correlation (r= -0.91) in the BOK grove between mean abundance of the D .citri and its predator C. arcuatus adults caught on sticky traps. Table 2: Dates of first emergence of D. citri adults during the sampling period (July 2015-June 2016) Generation Citrus grove Approximate emergence period of earliest adults Citrus growth flush T Max (°C) T Min (°C) H (%) P (mm) 1 st Oued fodda 2015 28 August Autumn growth flush 37 24 63 0 Boukadir 1 September 2 nd Oued fodda 2016 20 April Spring growth flush 26 13 65 0 Boukadir 23 April T Max (°C): mean maximum daily temperature during emergence period of D. citri T Min (° C): mean minimum daily temperature during emergence period of D. citri H (%): mean daily humidity during emergence period of D. citri P (mm): daily precipitation amounts during emergence period of D. citri Acta agriculturae Slovenica, 120/1 – 2024 5 Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organic citrus orchards ... 3.3 RELATIONSHIP BETWEEN TEMPERATURE, HUMIDITY, PRECIPITATION AND NUMBER OF D. citri ADULTS In the two citrus groves, the mean number of D. citri adults caught on sticky traps was the highest during Sep- tember and October (2015) and during April and May (2016), when monthly average temperatures varied from 18 to 30 °C, monthly average humidity varied from 46 to 69 % and with a low precipitation (0 to 27 mm). No D. citri adults were trapped in ODF and BOK citrus grove from December 2015 to March 2016 when monthly av- erage temperatures did not exceed 13 °C and with a high precipitation (59 to 130 mm), and a high relative humid- ity (72 to 77 %)(Figure 2). In ODF and BOK orchards, the number of adults of D. citri was correlated positively with monthly average Table 3: Composition and mean abundance of the D. citri and their predators C. arcuatus, C. carnea and S. aleyrodiformis caught on sticky traps in citrus orchards (July 2015-June 2016) Orders Family Species Sampling period Citrus groves ODF BOK Hemiptera Aleyrodidae Dialeurodes citri (Ashmead, 1885) July-Dec 2015 598.4 ± 527.95 1135.3 ± 1652.13 Jan-June 2016 309.6 ± 421.75 421.4 ± 612.01 Coleoptera Coccinellidae Clitostethus arcuatus (Rossi,1794) July-Dec 2015 19.4 ± 13.19 6.2 ± 7.05 Jan-June 2016 16.5 ± 16.81 1.7 ± 2.14 Neuroptera Chrysopidae Chrysoperla carnea (Stephens, 1836) July-Dec 2015 1.9 ± 4.20 0.9 ± 0.81 Jan-June 2016 0.3 ± 0.39 0.4 ± 0.66 Coniopterygidae Semidalis aleyrodiformis (Stephens, 1836) July-Dec 2015 19.9 ± 19.70 17.42 ± 17.40 Jan-June 2016 7.5 ± 9.43 1.06 ± 2.42 Figure 1: Relationship between the D. citri pests and its preda- tor C. arcuatus caught on yellow sticky traps in the semi-arid citrus region of Chlef from July 2015 to June 2016. a, Sampling conducted from July through December; b, Sampling con- ducted from January through June Table 4: Correlation between mean adult abundance and climatic parameters Climatic parameters ODF citrus grove BOK citrus grove Mean adult abundance r-Value p-Value r-Value p-Value Monthly average temperature (°C) 0.5219 0.0208* 0.4397 0.0116* Monthly average humidity (%) -0.4491 0.0936 -0.4549 0.0463* Monthly precipitation (mm) -0.5659 0.0903 -0.4378 0.0366* p < 0.05 (significant) * Acta agriculturae Slovenica, 120/1 – 2024 6 A. MAHMOUDI et al. temperatures (r (ODF) = 0.52, p (ODF) = 0.021, r = 0.43) (Table 4). Whereas the correlation was moderate and negative between monthly data of average humidity, rainfall and mean number of D. citri adults (r (BOK) = -0.45 &r (BOK) = -0.43) in BOK citrus grove. 3.4 RELATIONSHIP BETWEEN TEMPERATURE, HUMIDITY, PRECIPITATION, AND D. citri NYMPHAL INFESTATION RATES The population dynamics of D. citri nymphs from July 2015 to June 2016 in the ODF citrus grove showed three infestation peaks appearing respectively in Sep- tember 2015 (37 %), January 2016 (49 %) and April 2016 (48 %) corresponding to periods of high activity of nym- phal populations(Figure 3). Indeed, in the BOK citrus grove, three infestation peaks were recorded in August 2015 (29 %), January (25 %) and April 2016 (26 %) (Fig- ure 3). Additionally, during peaks of the nymphal infesta- tion, the monthly average temperatures varied between 13 and 27 °C, where average monthly humidity data var- ied between 47 % and 73 % and average monthly rainfall ranged from 3 to 30 mm. In ODF orchards a significant strong negative cor- relation (r= -0,72) was noted between monthly average temperatures and nymphal infestation rates of D. citri. However, a significant moderate positive correlation(r= 0,62)was recorded between nymphal infestation rate and monthly average humidity. Results were not significant for nymphal infestation rate in BOK orchard, probably due to a low nymphal infestation rate (Table 5). The re- lationship between climatic parameters and nymphal infestation rates in the semi-arid citrus region of Chlef from July 2015 to June 2016 are shown in Figure3. Figure 2: Evolution of D. citri captured in relation to monthly average temperatures (T °C), relative humidity (H %) and rainfall (P mm), during the one-year period of study Table 5: Correlation between nymphal infestation rate and climatic parameters Climatic parameters ODF citrus grove BOK citrus grove Nymphal infestation rate r-Value p-Value r-Value p-Value Monthly average temperature (°c) -0.7221 0.0080* -0.2682 0.3992 Monthly average humidity (%) 0.6209 0.0312* 0.2485 0.4362 Monthly precipitation (mm) 0.4444 0.1477 0.1810 0.5734 p < 0.05 (significant) * Acta agriculturae Slovenica, 120/1 – 2024 7 Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organic citrus orchards ... 3.5 ANALYSIS OF OCCURRENCE OF POLYVOL- TINISM & DIAPAUSE FOR D. citri PESTS IN CASE STUDY ORCHARDS The current findings showed two egg laying periods for D. citri leading to the appearance of two homoge- neous peaks of population clearly separated from each other by a diapause period of 5 to 6 months from Novem- ber to March. This period of suspended or arrested de- velopment, diapause, is usually caused by environmental changes such fluctuations in daylight, temperature, or humidity. These were observed with the current investi- gation and were like those reported by Saini et al. (2016) in India. Benmessaoud-Boukhalfa & Chebrou (2014) de- scribed that the dynamics of whitefly populations is com- plex because of their polyvoltinism (i.e., having several broods per year), and their interactions with climatic fac- tors such as temperature, humidity, and precipitation, as well as their host plant. Similarly, polyvoltinism was seen by Onillon (1976); Lloréns (1994); Bellows & Meisen- bacher (2007),who counted two annual generations of D.citri in France, in California and in Spain while three generations per year were found in Japan (Kaneko, 2017). However, unlike in Japan in the sub-humid citrus region in Mitidja plain (north of Algeria), Benmessaoud-Bouk- halfa (1987) estimated that the D. citri’s diapause period has a duration of 4 to 5 months which would make it un- likely for the pest to have more than two broods a year. Figure 3: Relationships between climatic parameters and nymphal infestation rate in the semi-arid citrus region of Chlef from July 2015 to June 2016. The principal x-axis illustrates the values of climatic parameters (T (°C), H (%) and P (mm)) It has been found from the current investigation of the orchards in the Chlef region, that the daily average temperature of 19.5 °C and 30.5 °C in the spring and au- tumn period, respectively, with a daily average humid- ity of 65 % with no rainfall, were favorable for the early emergence of the D. citri adults. Boukhalfa & Bonafonte (1979) also noted that the beginning of emergence start- ed from mid-April in the sub-humid citrus region of Mitidja. However, in France and Spain, the earliest adults were observed in May (Onillon, 1975, Soto 1999), while Ohgushi & Ohkubo (2005) reported that the first adult emergence appeared in early May to mid-June in Japan. The earliest adults of D. citri were found during citrus flushing cycles over April-August and September (2015- 2016). It was observed, that the females of D. citri lays eggs on young shoots of citrus flush growth. Singh et al. (2021) reported that exclusively during the flush period, D. citri population was very active. All of this suggests that colder temperatures increase the diapause phase by suppressing emergence. 3.6 EFFECTIVENESS OF PREDATORS Chrysoperla carnea, Clitostethus arcuatus AND Semidalis aley- rodiformis IN REDUCING POPULATIONS OF CITRUS WHITEFLY PESTS The authors reported three species of predators: Acta agriculturae Slovenica, 120/1 – 2024 8 A. MAHMOUDI et al. Chrysoperla carnea, Clitostethus arcuatus and Semidalis aleyrodiformis. Khan et al. (2020) reported that several insect species belonging to Neuroptera order are a nat- ural enemy of great numbers of pests. C. carnea adults however were rarely observed, and their activity was lim- ited as light reduction in the number of adults and eggs of D. citri. It can be argued that the effect of the predator C. carnea is not significant in decreasing the populations of the citrus whitefly pest. This conclusion is supported by the results of the current study as shown in Table 3. In contrast, large captures of C. arcuatus and S. aleyrodi- formis adults were observed in the citrus orchards in the present investigation (Table 3). Benmessaoud-Boukhal- fa (1987) reported that C. arcuatus is the most efficient predator of D. citri in Algeria. The ladybird beetle Cli- tostethus arcuatus is one of the most effective predators of the whitefly. This ladybird feeds on all development stages of Aleyrodidae (Yazdani and Samih, 2012). A sin- gle beetle consumes more than 50 D. citri eggs per day (Onillon, 1975). In Egypt, C. arcuatus is considered as the most im- portant predator of D. citri with more of 41.9 % of the total number of predators (El-Husseini et al., 2018). A positive correlation was found between the D. citri count and the predator C. arcuatus adults, which means that this predatory coccinellids feeds on white- fly but without significantly reducing their abundance. Thus, it can be reasoned that C. arcuatus can be efficient against D. citri but only when this whitefly lays few num- bers of eggs (EPPO, 2004). In addition, the influence of predators on D. citri populations decreased with increas- ing temperature (Bale et al., 2002, Thomson et al., 2010). Increased precipitation also greatly reduces their abil- ity to move and search for prey (Thomson et al., 2010). However, Thöming & Knudsen (2021) reported that the diversity of beneficial insects was dependent on vegeta- tion diversity. 3.7 DYNAMICS OF EFFECT OF TEMPERATURE, PRECIPITATION & HUMIDITY ON INSECT INFESTATION RATES Dreistadt (2012) reported that the honeydew secret- ed by D. citri nymphs attracts ants, which can disrupt the activity of whitefly predators. According to Byrne (1991), whitefly population dynamics depends on different cli- matic factors and natural enemies. Climatic parameters such as temperature, rainfall and relative humidity are known to impact the population dynamic of D. citri (Kumar, 2001; Rashid et al., 2003; Saini et al., 2016). The present study revealed that temperature may influence the dynamics of D. citri nymphal population because a strong negative correlation was found between nymphal infestation rate and monthly average temperatures. This correlation revealed that the D. citri nymphal infestation peaks occurred in winter and autumn which were cold to mild periods with monthly average temperatures varying between 13 and 27 °C. The same results were obtained by Saini et al. (2016) who reported a negative correlation between nymphal population of D. citri and the mean minimum and maximum temperature. From the correlation results, a decrease in monthly average temperature resulted in an increase in the D. citri nymphal infestation rate (Figure 3). Similarly, Bernardo et al. (2006) also signaled the strong effect of temperature on the development rate of insects. However, a moderate positive correlation was found between D. citri nymphal infestation rate and monthly average humidity. Unlike the temperature, increased monthly average humidity re- sulted in an increase of D. citri nymphal infestation rate with values varying between 47 % and 73 % during the D. citri nymphal infestation peaks (Figure 3). These results were consistent with a study by Kumar (2001) that dem- onstrated that humidity varying between 60-75 % was favorable for development of D. citri. Likewise, several investigations have also focused on the impact of relative humidity on populations of D. citri (Mansour et al., 2021; Zeb et al., 2011; Saini et al., 2016). The correlation analysis between weather param- eters and mean adult abundance of D. citri revealed that the monthly average temperatures exhibited a significant moderate positive influence. Two peaks of abundance were recorded in spring and autumn period, seasons which are characterized by higher monthly average tem- peratures (18 to 30 °C) with less rainfall. In particular, an increase in monthly average temperature resulted in an increase of D. citri adult abundance. While monthly average humidity and monthly precipitation had a sig- nificant moderate negative correlation with the number of D. citri adults caught on sticky traps, this indicated that a decreased monthly average humidity and month- ly precipitation resulted in an increase of D. citri adult abundance. In addition, the absence of D. citri adults on the sticky traps was observed in the winter period when monthly precipitation exceeds 130 mm and monthly av- erage humidity varies between 72 to 77 %. In closing, with the present study a decrease in D. citri adult count was noted during rainy periods and an increase was seen during dry periods. This was like that cited by Rashid et al.(2003) who reported that precipita- tion and humidity affect the abundance of whitefly popu- lations. Insects can be affected in their development by environmental factors (Bale et al., 2002). Indeed, global warming causes critical changes in population abun- dance of insects (Sharma, 2014). Finally, there is a need Acta agriculturae Slovenica, 120/1 – 2024 9 Investigation of fluctuation in infestation of citrus whitefly Dialeurodes citri (Ashmead, 1885) and its predators in organic citrus orchards ... to set up an integrated control system against insect pests (Saini et al., 2016). This must be coordinated with studies of their population dynamics. 4 CONCLUSIONS This article may facilitate the implementation of an integrated pest management program in Chlef citrus region by understanding the tri-trophic interaction be- tween host plants, D. citri populations and theirs preda- tors under the impact of the particular climatic condi- tions of the region. 4.1 ACKNOWLEDGEMENTS We are grateful to Mr. Jean-Claude Streito (INRA, UMR CBGP , Montpellier, France) and Dr. Philippe Rey- naud (ANSES Plant Health Laboratory, Montpellier, France) for their valuable contributions on insect iden- tifications. 4.2 LIST OF ABBREVIATIONS BOK: Boukadir; ODF: Oued fodda; FAO: Food and Agriculture Organisation; D. citri: Dialeurodes citri; C. arcuatus: Clitostethus arcuatus; S. aleyrodiformis: Semida- lis aleyrodiformis; C. carnea: Chrysoperla carnea; T Max: maximal temperature; T Min: minimal temperature; H (%): humidity; P (mm): precipitation. 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