Parasitisation of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), by Encarsia spp. (Hymenoptera: Aphelinidae) in relation to hostplant and weather factors

Parasitisation of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), by Encarsia spp. (Hymenoptera: Aphelinidae) in relation to hostplant and weather factors | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Parasitisation of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), by Encarsia spp. (Hymenoptera: Aphelinidae) in relation to hostplant and weather factors Caroline Oyindamola Filani, Olufemi Richard Pitan This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-6498232/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 22 Dec, 2025 Read the published version in International Journal of Tropical Insect Science → Version 1 posted 5 You are reading this latest preprint version Abstract In Nigeria, the spiralling whitefly (SWF), Aleurodicus dispersus , is a highly polyphagous and serious pest of horticultural crops. Although its parasitoid, Encasia sp., has been accidentally introduced, information on its suitability in the ecosystem is still scanty. The study therefore investigated factors influencing whitefly parasitisation by Encasia sp, from 2014 to 2019 on Citrus sinensis (sweet orange), Acalypha wilkensiana (red acalypha), Ficus polita (fig) and Psidium guajava (guava) at two sites in Ibadan, Nigeria. SWF abundance and mummification, and weather factors were monitored monthly and correlated. Total rainfall and mean temperature were significantly associated (P < 0.05) with both SWF density and parasitisation, while Encarsia sp., the only natural enemy found during the study, improved the regulation of SWF on all the hostplants at both sites. Number of parasitoids was highly correlated and synchronized (P < 0.05) with that of SWF throughout the sampling period although the spatial patterns of parasitism distribution in relation to SWF population density were not totally directly density dependent. Local extinction of SWF was observed on Citrus, Acalypha and Ficus spp., whereas whitefly regulation with reduced and stabilized numbers and stable percentage parasitism was evident on Psidium. While there was no significant difference (P > 0.05) between parasitism indices either within or between sites on Psidium , the cumulative numbers of SWF were significantly higher (P < 0.05) than other hostplants. The continued presence of the regulated SWF number on Psidium and its extinction on Citrus, Acalypha and Ficus suggested a combination of hostplant quality and Encarsia sp. as major factors in SWF regulation. Population dynamics Aleurodicus dispersus Encarsia spp. efficacy hostplant Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction The spiralling whitefly, A. dispersus , is a highly polyphagous and serious pest of guava, pawpaw, banana / plantain, cassava, many vegetables and ornamentals (Ajuonu et al ., 2011). The pest, which is a native of the Caribbean region and Central America (Russell, 1965) was first noticed as a pest in Hawaii in 1978 (Kumashiro et al. 1983) and has since spread across the pacific and southeast Asia (Srinivasa, 2000). It was first reported from Africa in the early 1992 in Ibadan and Lagos, Nigeria (Akinlosotu et al . 1993) and thereafter, in Benin, Togo, Ghana and Congo (Neuenschwander 1994; Ajuonu et al. 2011) where it occurred in large numbers on at least 32 different plant families. In Nigeria, Pitan et al. (2008) recorded the pest on at least 66 species of beneficial plants in 32 different plant families including fruit crops, ornamentals, tuber crops and shade trees. The most important hosts were guava ( Psidium guajava) , almond tree ( Terminalia catappa ), fig Ficus spp.), acalypha ( Acalypha spp.), oranges ( Citrus spp.) and cassava Manihot esculenta) . A. dispersus sucks sap from leaves and secretes honeydew which encourages the growth of sooty mould on the foliage. The mould inhibits photosynthesis and causes leaf drop leading to a marked reduction in fruit production (Pitan, 2003). Infestations pose a serious threat to subsistent farmers in areas where fruit crops and vegetables are often the most freely available food providing energy and vitamins in the diet and where ornamentals are planted for shade and aesthetic beauty (Zakkum et al . 2024). Some of the pest control measures adopted by growers in Nigeria, which only gave short-lived control, include pruning and outright felling and burning of the infested plants; and application of insecticides (Boopathi et al. 2017). Although, Sampiano et al . (2024) suggested certain natural oils for control, Akinlosotu et al. (1993) proposed the use of natural enemies as a reliable and ecologically sound control option for mitigating the spiralling whitefly menace in Nigeria due to its exotic and polyphagous nature. Due to the importance of the spiralling whitefly to horticulture in Nigeria, a nation-wide biological control of the spiralling whitefly project was initiated in 1993 with the initial task of determining the status of the A. dispersus infestation in Nigeria. Remarkably, in all areas surveyed in Nigeria, Encasia dispersa Dozier (Hymenoptera: Encyrtidae), a natural enemy of A. dispersus was found together with the whitefly (Akinlosotu et al. 1993; Pitan et al . 2008). Encasia dispersa is a primary parasitoid of the spiralling whitefly. It has been used effectively either singly or in combination with other natural enemies in previous attempts at the biological control of A. dispersus in Hawaii, Pacific countries such as Palau and Pohnpei and in the Maldives with varying degrees of successes (Neuenschwander, 1994; Chand et al . 2018)). Since there was no record of any formal release of the parasitoid anywhere in Nigeria, the wasp must have arrived by accident, presumably together with A. dispersus . It is therefore, necessary to determine the suitability of the introduced natural enemy in order to determine whether further importations of other natural enemies would be necessary. In practice, evaluation of the efficacy of biological control agents is very important in any biological control programme and has been recognized as the key to the development of biological control as a science (Chand et al . 2018). Long-term population dynamics studies are no doubt the backbone of such evaluations and will clearly provide the most important demonstration of impact. Therefore, this study was designed to determine the temporal patterns of the distribution of the spiralling whitefly on 4 different host plants and to highlight major factors in whitefly population fluctuations with emphasis on the evaluation of Encasia sp. as an efficient biological control agent. Materials and methods Study Area The study was carried out between January, 2014 and December, 2019 in Ibadan, southwest of Nigeria (guinea savannah zone) (7 o 30’N, 3 o 54’E, 210 m above sea level) at two of the sites where growers reported heavy infestation of A. dispersus in 2010. Generally, in southern Nigeria, the rainfall pattern is bimodal, with a long rainy season lasting from March to July followed by a dry spell. The short rainy season lasts from September until November. Until February-March the weather is dry, with frequent periods of 'harmattan', a dry, dusty wind originating in the Sahara Desert. The first site was in Bashorun area in the north eastern part of Ibadan and contained the following hosts: 6 stands of Citrus sinensis , 2 of Ficus polita , 4 of Psidum guajava , 28 of Acalypha wikensiana , 2 of Mangifera indica (mango), 11 of Carica papaya ( pawpaw) and 18 of Musa paradisiaca (plantain). At the second site which was at Jericho Reservation Area, south of Ibadan, had 4 stands of Citrus sinensis , 2 of Ficus polita , 2 of Psidium guajava and 101 of Acalypha wilkensiana . A preliminary visual examination was made of all the plants in the study areas to determine the severity of infestation. One severely infested plant was selected from only four hosts for sampling in this study - Citrus sinensis, Ficus polita , Psidium guajava and Acalypha wilkensiana because they were common to the two sites, making a total of 4 plants per site (i.e. 8 plants in all). Monitoring of the spiralling whitefly and its parasitoid For monitoring of A. dispersus population densities on the four host plants, the sampling procedure was as follows: 20 leaves per host tree were randomly selected for examination once a month from the bottom, middle and top parts of the host plants. Counts of adults, nymphs and parasitised A. dispersus (mummies) were made in situ and were recorded separately. After removing live insects, others were kept in the laboratory for 3–4 weeks until emergence of primary parasitoids was completed. In order to allow comparisons to be made between the different host plants with leaf sizes greatly varied, the total number of the spiralling whitefly (adults, nymphs and mummies) was calculated on a leaf surface area basis. To do this, leaf surface areas of 5 randomly selected leaves out of the 20 leaves sampled from each host plant were measured and the mean (x) was multiplied by the number of leaves sampled (s) to give the total leaf area sampled (sx). The number of A. dispersus and Encasia spp. per square centimeter (w/cm 2 ) was then determined by dividing the total number of whiteflies found per sample per host plant (t) by the calculated leaf area (w/cm 2 = t/sx) (Tingle and Copland, 1987). Differences in the population densities of A. dispersus and Encasia per square centimeter of the leaf areas on different host plants were detected using student’s t-tests (P < 0.05) after such data were arcsine-transformed. Temperature and rainfall data collection Average monthly temperature and rainfall data collected to determine a possible influence of rainfall and temperature on A. dispersus densities. The data covered the rainfall of the month preceding each sampling time. Correlation and regression analyses (Draper and Smith 1981) were carried out to determine the relative importance of different ecological factors examined. Density dependence of Encasia sp. Parasitism index was computed and was transformed into the arcsine of its square root and plotted against log (x + 1) – transformed whitefly densities. The significance of the slopes was judged with a t-test at P ≤ 0.05 (Boavida and Neuenschwander 2010; Ajuonu et al. 2011). Results Rainfall and temperature pattern, population fluctuation of the spiralling whitefly and its parasitoid, Encasia sp., on each of the 4 host plants at the 2 sites are presented in Figs. 1 – 3 . Between 2014 and 2019, there was a sharp, consistent and irredeemable decline in the population densities of the whitefly to zero from 2016 on Citrus , Acalypha and Ficus spp. at the two experimental sites. The data from the first sample and those taken between January and May, 2014 at the two sites showed significant differences in the densities of A. dispersus on the different host plants (P < 0.05). But marked reduction in the numbers of A. dispersus was noticed from the 6th month (June, 2014) (Figs. 2 & 3 ); the reduction became significant (P < 0.05) on Citrus, Acalypha and Fig at the end of the second year (2015); and at the end of the third year for Psidium . Largely, on the four hosts, following the detection of Encasia sp. peaks of A. dispersus infestations, estimated from the numbers of adult whiteflies became lower each year. In 2015, peaks reached only about 20% of those of 2014. The total number of parasitized pupae increased from one year to the next (Figs. 2 and 3 ), indicating that parasitism rates generally increased from 1993 to 1996. On Psidium at the two sites, whitefly numbers decreased and remained relatively constant at a low level while percent parasitism was stable. Although initial whitefly densities varied significantly between trees, fluctuation trends were similar on each of the host plants. At each site, there was a significantly higher number of A. dispersus than on other host plants in which in themselves were not significantly different (P < 0.05). There was no difference between the densities of A. dispersus on Psidium at the two sites but significant differences occurred between the population densities of A. dispersus on Psidium and other host plants both within and between sites (Table 1 ). On the other hand, percent parasitism did not differ significantly on plants within or between the sites even though it varied significantly at the first sampling in January, 2014 and was observed to be highest on Acalypha (Fig. 4 ). The abundance of the parasitoid followed the same pattern as that of the host on the 4 host plants, which illustrates the ability of the parasitoid population to track down the spiralling whitefly population densities. The parasitoid population varied greatly with plant species but generally peaks of percentage parasitism occurred at the same periods of the year on the different plant species (Figs. 2 and 3 ). This suggests that plant species have an important role to play on the level of parasitism observed. There was no significant correlation between percent parasitism and mean temperature during the sampling period on any of the host plants studied (Table 2 ). The contributions of various biotic and abiotic factors to the size of whitefly populations on the four hostplants were quantified in a multiple regression analysis (Tables 3 ). On the basis of infested trees, three independent factors influenced A. dispersus populations. Parasitism played a very important role in the occurrence of A. dispersus , with the highest values found on Citrus , Acalypha and Ficus spp. relative to Psidium at the two experimental sites. The second most important influence was temperature while rainfall was clearly not a major factor. However, the relatedness of whitefly parasitism and temperature as well as rainfall was low though significant. Slope (b) which represents the rate of change, and in this case rate of population collapse was significant and higher with parasitism than those of other factors at the two sites. In addition, parasitism was found to be density-dependent on Acalypha, Citrus and Ficus judged by the significance of the regression coefficients but on Psidium , it was a density-independent relationship (Table 4 ). The similarity in the trends of the results from the two sites justified the pooling of data to determine the functional relationship between A. dispersus and its parasitoid which was found to be polynomial in all cases with a 6th degree on Psidium , 5th degree on Ficus , 3rd on both Citrus and Acalypha spp. (Fig. 4 ). Discussion Results showed that the degree of pest regulation achieved was not uniform but depended on host plants; there was also a general marked decline in the population of the whitefly from 2014 to 2019 on all the host plants at the two sites. The positive correlation between A. dispersus population and rainfall on the one hand and temperature on the other suggests that both factors influenced the population of the spiralling whitefly. The direct influence of the rain could be the washing-off of whiteflies from host leaves while the indirect is mediated through the physiological condition of the host plants could be responsible (Mani and Krishnamoorthy 2002; Mani et al . 2004). But because of the low correlation between whitefly population and each of temperature and rainfall on the four host plants, the sudden decline of A. dispersus population following the peaks and the reduction in A. dispersus population density which also occurred in both the raining and dry season, the impact of rainfall and temperature on A. dispersus , though important, was considered minor. Although temperature may not be the factor inducing whitefly outbreaks (on Psidium ) as stated earlier, the significant correlation between temperature and percent parasitism on the host plants at the two sites indicated that temperature influenced parasitism and is important probably in determining parasitoid efficiency. Similar reports on the influence of temperature have been reported on the searching, oviposition and developmental rates of Leptomastidae abnormis Girault and Leptomastix dactylopii Howard and consequently on the control of Planococcus citri Risso by the parasitoids (Tingle and Copeland 1987). These features of parasitoids that are affected by temperature are those that contribute to success of the natural enemy in terms of number of hosts parasitized at a given time. The decline in the population of the whitefly observed on the 4 host plants might be a result of the temporal synchrony of the numbers of Encasia sp. with that of the hosts, and which resulted in the highly significant correlation that existed between the two populations on each of the host plants. Rate of decline was very high on the indicating steepest slope was obtained with parasitism on the four hosts, though higher on Acalypha, Citrus and Ficus than Psidium. Only a natural enemy, in this case Encasia sp. appeared to be capable of causing that type of variation in the host’s population. Though positive density dependence has rarely been found in natural host–parasitoid interactions despite their apparent stability (Mani et al . 2004), Encasia sp. appeared to show this type of dependence on the population of A. dispersus in the first two years of sampling on the four host plants. Some of the attributes of the parasitoid that could enable such a response include high fecundity and shorter generation time compared with that of its host (Tanga et al . 2013). The extinction of A. dispersus on Citrus, Ficus and Acalypha at different times during the study agrees with modern reasoning that biological control is compatible with local pest extinctions (Tanga et al . 2013). Similarly, the marked reduction in the population density of the whiteflies on Psidium and lack of pest outbreaks subsequently indicated that a stable relationship had been established between the parasitoid and its host. It also implies that the Encasia sp. is adequately regulating the number of A. dispersus though it appears it may not be able to singly cause the extinction of A. dispersus on Psidium . Such differences in pest numbers on different host plants have also been reported for some aphids (Wellings and Dixon 1987) and the level of control achieved by the aphelinid parasitoid, Encasia formosa Gahan on Trialeurodes vaporarium . This was attributed to a combination of the effect of the host plant on pest fecundity, lifespan and developmental rate and on the searching efficiency by the parasitoid (Ajuonu et al. 2011). Several plant features such as leaf surface topography and toxic secondary substances have also been reported to affect parasitoids’ efficacy (Campbell and Duffey 1979). This suggests that plant susceptibility to insects may result from the detrimental effects of plant antibiotics on the biological control agents of insect pests in question. Though there was no enough evidence from the present study to suggest that the fecundity and lifespan of A. dispersus were more stimulated on Psidium than other host plants, significantly higher population of A. dispersus observed on Psidium is an agreement with earlier report that total developmental time for A. dispersus is shorter on Psidium than on Citrus, Acalypha and Ficus in that order (Pitan and Odebiyi 2002; Han et al. 2009). The shorter developmental time on Psidium suggests that more whiteflies would be found on the plant, while an impressive control (and in fact extinction) of the whitefly would be more likely on Citrus, Acalypha and Ficus where replacement of parasitized A. dispersus is much slower due to more prolonged developmental time compared to Psidium . The 6th degree polynomial relationship recorded on Acalypha also suggest that more factors regulate the population density of A. dispersus on the plant compared to the other hosts trialed and therefore, will be take more time to achieve whitefly extinction than on Citrus, Acalypha and Ficus spp. Both sets of data from the two orchards demonstrate a decline in A. dispersus populations with increasing time of parasitoid presence. Since other factors remained mostly unchanged, the decline is attributed to this exotic parasitoid. It is concluded that differences in pest regulation observed on Psidium, Citrus, Acalypha and Ficus are entirely due to an effect on the parasitoid. The significant correlation between parasitism and temperature and not whitefly population density and temperature indicate that the effect of temperature is likely to on the parasitoid rather than the whitefly. Similarly, the significance of the relationship between rainfall and whitefly population density and not parasitism means the effect of rainfall is on the whiteflies. However, the fact that Psidium still harbours whitefly numbers suggest that rainfall and temperature are minor factors, and hostplant and parasitism major factors. Therefore, although rainfall and temperature are important factors too, they are considered minor in this study, while Encasia sp. and host plant qualities were major factors affecting the population of A. dispersus and are important in its regulation. Declarations The authors declare that this manuscript has not been considered elsewhere for publication. Acknowledgements The supports of those whose premises were used at Bashorun and Onireke, Ibadan, Nigeria for the study are appreciated. Author’s contribution statements : Dr. FILANI, OYINDAMOLA CAROLINE carried out the research work and wrote up the paper. Prof. PITAN, OLUFEMI RICHARD conceived the experiment and review the paper write-up. Funding This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Data availability Not applicable in the study. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest regarding the publication of this paper. Ethics approval This study does not involve human participants and so ethics approval is not applicable. Consent No consent was required for the study. Code availability Not applicable in the study. Competing Interests: Authors did not have any financial support either directly or indirectly as regards this work submitted for publication. References Ajuonu O, Neuenschwander P, Korie S (2011) Niche separation between Encarsia dispersa and Encarsia guadeloupae , two biological control agents of the spiraling whitefly Aleurodicus dispersus , in Benin, West Africa BioControl 56: 277–282 doi:10.1007/s10526-010-9331-9 Akinlosotu TA, Jackai LEN. Ntonifor NN, Hassan AT, Agyakwa CW, Odebiyi JA, Akingbohungbe AE, Rossell HW (1993) Aleurodicus dispersus in Nigeria, FAO Plant Protection Bulletin 41: 127–129. Boavida C, Neuenschwander P (2010) Population dynamics and life tables of the mango mealybug, Rastrococcus invadens Williams, and its introduced natural enemy, Gyranusoidea tebygi Noyes in Benin. Biocontrol Science and Technology 5: 489–508. Boopathi T, Sankari K, Meena M, Ravi Thirunavukarasu K (2017) Impact of insecticides on spiralling whitefly, Aleurodicus dispersus (Hemiptera: Aleyrodidae) and its natural enemy complex in cassava under open field conditions. Crop Protection 94: 137–143 Campbell BC, Duffey SS (1979) Tomatine and parasitic wasps’ potential incompatibility of plant antibiosis with biological control. Science 205: 700–702. Chand R, Jokhan A, Kelera, R (2018) Spiralling whitefly and its management practices in the South Pacific. A review. Advances in Horticultural Science , 33 (1), 123–131. https://doi.org/10.13128/ahs-22952 Draper NR, Smith H (1981) Applied Regression Analysis, 2nd Edition, John Wiley, New York. Han DY, Liu Kui, Zhang Fang-Ping, Huang Wu-Ren, Zhang Jing-Bao, Jin Qi-An, Fu Yue-Guan (2009) Biological characteristics of the Spiralling whitefly, Aleurodicus dispersus Russell (Homoptera:Aleyrodidae. Acta Entomologica Sinica 3:445–454 Kumashiro BR, Lai PY, Funasaki GY, Teramoto KK (1983) Efficacy of Nephaspis amnicola and Encasia ?haitiensis in controlling Aleurodicus dispersus in Hawaii. Proceedings of Hawaiian Entomological Society 24 (2 &3): 261–269 Mani M, Krishnamoorthy A (2002) Classical Biological Control of the Spiralling whitefly, Aleurodicus dispersus Russell—An Appraisal. Journal of Tropical Insect Science 22: 263–273 Mani M, Krishnamoorthy A, Venugopalan R (2004) Role of the aphelinid parasitoid Encarsia guadeloupae in the suppression of the exotic spiralling whitefly Aleurodicus dispersus on banana in India Biocontrol Science and Technology 14: 619–622 Neuenschwander P (1994) Spiralling whitefly, Aleurodicus dispersus: a recent invader and a new cassava pest. African Crop Science Journal 2 & 4: 419–421. Pitan OOR, Odebiyi JA (2002). Aspects of biology and variation in the developmental time on different hosts of the spiralling whitefly. Nigerian Journal of Entomology 20:23–27 Pitan OOR (2003) The response of two growth stages of pepper to different population densities of the spiralling whitefly ( Aleurodicus dispersus Russell) Insect Science and Its Application 23: 115–120. Pitan OOR, Fajinmi AA, Akinyemi SOS, Ayodele EA (2008) Status of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), infestation in Nigeria. Nigerian Journal of Plant Protection 24: 21–26 Russell LM (1965) New species of Aleurodicus Douglas and two close relatives (Homoptera: Aleyrodidae). Florida Entomologist 48: 47–55. Sampiano KFS, Sibongga LMA, Ramos FRA, Aceres LV (2024) Sustainable Management for Spiralling Whitefly, Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae) Infesting Guava and Its Effects on the Natural Enemies. Mindanao Journal of Science and Technology 21: 165–185 Srinivasa MV (2000). Host plants of the spiraling whitefly, Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae). Pest Management in Horticultural Ecosystems 6: 79–105 Tanga CM, Ekesi S, Govender P, Mohamed SA (2013). Effect of Six Host Plant Species on the Life History and Population Growth Parameters of Rastrococcus iceryoides (Hemiptera: Pseudococcidae). Florida Entomologist 96: 1030–1041 URL: https://doi.org/10.1653/024.096.034 Tingle CCD; Copland MJW (1987) Predicting development of the mealybug parasitoids, Anagyrus pseudococci, Leptomastix dactylopii and Leptomastidae abnormis under glasshouse conditions. Entomologia Experimentalis et Applicata 45: 56–65 Wellings PW, Dixon AFG (1987) Sycamore aphid numbers and population density III. The role of aphids – induced changes in plant quality. Journal of Animal Ecology 56: 161 − 170. Zakkum GB, Madhavi M, Guru SS (2024) Interplay between natural compounds of Mundulea sericea Bark Extract in combating Aleurodicus dispersus, spiralling whitefly an invasive pest of Telangana. Int. J. Curr. Microbiol. App. Sci. 13(6): 260–268. doi: https://doi.org/10.20546/ijcmas.2024.1306.028 Tables Tables 1 to 4 are available in the Supplementary Files section. Supplementary Files UploadedparasitisationTables.docx Cite Share Download PDF Status: Published Journal Publication published 22 Dec, 2025 Read the published version in International Journal of Tropical Insect Science → Version 1 posted Editorial decision: Major revisions 27 Jul, 2025 Reviewers agreed at journal 18 Jun, 2025 Reviewers invited by journal 13 Jun, 2025 Editor assigned by journal 01 May, 2025 First submitted to journal 28 Apr, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-6498232","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":470836721,"identity":"245783a6-911b-470e-ac55-0775dd0f4b1e","order_by":0,"name":"Caroline Oyindamola Filani","email":"","orcid":"","institution":"Federal University of Agriculture, Abeokuta, Ogun State.","correspondingAuthor":false,"prefix":"","firstName":"Caroline","middleName":"Oyindamola","lastName":"Filani","suffix":""},{"id":470836722,"identity":"b71a4f87-75ff-40c4-a4fc-075b3c1013ea","order_by":1,"name":"Olufemi Richard Pitan","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA6UlEQVRIiWNgGAWjYDACZgglx94AJBlBxAGCWiB6jHkOEK0Fak1iD9FazNn5D34uqLiX3iORe/DDzx0Mcnw3EtgefsGjxbKZmVl6xpni3B6JvGTJ3jMMxpI3EtiNZfBoMTjMzCDN25aQu18ix0CCt40hcQPQFmkJ/FqYfwO1pPNI5Bj//NvGUE+MFjaQLQlALWZABkOCAVCL5Af8fjGz5jmTYNjD88bMWvaMhOHMMw/bpPHoYDDnP/j4Nk9FgjwPe47xzbc7bOT5jicfk/yBz2FofJAnGBuYeUjQAgGM+GwZBaNgFIyCEQcAk/lG4PY4hm0AAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0001-6465-8168","institution":"Federal University of Agriculture, Abeokuta, Ogun State.","correspondingAuthor":true,"prefix":"","firstName":"Olufemi","middleName":"Richard","lastName":"Pitan","suffix":""}],"badges":[],"createdAt":"2025-04-21 18:44:15","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-6498232/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-6498232/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s42690-025-01709-y","type":"published","date":"2025-12-22T15:57:57+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":84777799,"identity":"00390c89-014a-4474-9599-5acd710f850c","added_by":"auto","created_at":"2025-06-17 09:09:33","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":14081,"visible":true,"origin":"","legend":"\u003cp\u003eDaily rainfall (a) and average monthly temperature (b) between 2014 and 2019 in Ibadan, a typical guinea savanna zone.\u003c/p\u003e\n\u003cp\u003eSource: The National Horticultural Research Institute, Ibadan, Nigeria.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/42b84d5fcebaa331a9500d99.png"},{"id":84778508,"identity":"df0ccbdb-b237-4d31-9341-2c7aa8f91232","added_by":"auto","created_at":"2025-06-17 09:17:33","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":17827,"visible":true,"origin":"","legend":"\u003cp\u003ePopulation fluctuations of \u003cem\u003eAleurodicus dispersus\u003c/em\u003e and its parasitoid, \u003cem\u003eEncasia \u003c/em\u003esp. between January 2014 and December 2019 on different host plants in the first site.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/49ad1091ce54832c883f801e.png"},{"id":84781195,"identity":"d742b859-42a4-4cc7-829c-1dac0ab06ee5","added_by":"auto","created_at":"2025-06-17 09:33:33","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":13633,"visible":true,"origin":"","legend":"\u003cp\u003ePopulation fluctuations of \u003cem\u003eAleurodicus dispersus\u003c/em\u003e and its parasitoid, \u003cem\u003eEncasia\u003c/em\u003e sp. between January 2014 and December 2019 on different host plants in the second site.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/aae034a218ceb09846a64ecd.png"},{"id":84777826,"identity":"57ada57f-23b1-4fee-868f-582bc398cf45","added_by":"auto","created_at":"2025-06-17 09:09:34","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":18126,"visible":true,"origin":"","legend":"\u003cp\u003eThe functional relationship between parasitoid activity (parasitism index) and whitefly population density on (a) \u003cem\u003ePsidium\u003c/em\u003e, (b) \u003cem\u003eCitrus\u003c/em\u003e, (c) \u003cem\u003eAcalypha\u003c/em\u003e, (d) \u003cem\u003eFicus\u003c/em\u003e spp.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/21792957fab1c71940e98019.png"},{"id":99172745,"identity":"1c81585e-7920-4190-a0c5-7d9cc73645aa","added_by":"auto","created_at":"2025-12-29 16:11:19","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":596650,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/b6f1dee7-8aca-4350-a206-6ae6e99b75ae.pdf"},{"id":84777802,"identity":"f487ad7a-806b-4b97-994f-ac7b66710f51","added_by":"auto","created_at":"2025-06-17 09:09:33","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":26065,"visible":true,"origin":"","legend":"","description":"","filename":"UploadedparasitisationTables.docx","url":"https://assets-eu.researchsquare.com/files/rs-6498232/v1/476ae6c099b3e220a2e3d960.docx"}],"financialInterests":"","formattedTitle":"Parasitisation of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), by Encarsia spp. (Hymenoptera: Aphelinidae) in relation to hostplant and weather factors","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe spiralling whitefly, \u003cem\u003eA. dispersus\u003c/em\u003e, is a highly polyphagous and serious pest of guava, pawpaw, banana / plantain, cassava, many vegetables and ornamentals (Ajuonu \u003cem\u003eet al\u003c/em\u003e., 2011). The pest, which is a native of the Caribbean region and Central America (Russell, 1965) was first noticed as a pest in Hawaii in 1978 (Kumashiro \u003cem\u003eet al.\u003c/em\u003e 1983) and has since spread across the pacific and southeast Asia (Srinivasa, 2000). It was first reported from Africa in the early 1992 in Ibadan and Lagos, Nigeria (Akinlosotu \u003cem\u003eet al\u003c/em\u003e. 1993) and thereafter, in Benin, Togo, Ghana and Congo (Neuenschwander 1994; Ajuonu \u003cem\u003eet al.\u003c/em\u003e 2011) where it occurred in large numbers on at least 32 different plant families. In Nigeria, Pitan \u003cem\u003eet al.\u003c/em\u003e (2008) recorded the pest on at least 66 species of beneficial plants in 32 different plant families including fruit crops, ornamentals, tuber crops and shade trees. The most important hosts were guava (\u003cem\u003ePsidium guajava)\u003c/em\u003e, almond tree (\u003cem\u003eTerminalia catappa\u003c/em\u003e), fig \u003cem\u003eFicus\u003c/em\u003e spp.), acalypha (\u003cem\u003eAcalypha\u003c/em\u003e spp.), oranges (\u003cem\u003eCitrus\u003c/em\u003e spp.) and cassava \u003cem\u003eManihot esculenta)\u003c/em\u003e.\u003c/p\u003e \u003cp\u003e \u003cem\u003eA. dispersus\u003c/em\u003e sucks sap from leaves and secretes honeydew which encourages the growth of sooty mould on the foliage. The mould inhibits photosynthesis and causes leaf drop leading to a marked reduction in fruit production (Pitan, 2003). Infestations pose a serious threat to subsistent farmers in areas where fruit crops and vegetables are often the most freely available food providing energy and vitamins in the diet and where ornamentals are planted for shade and aesthetic beauty (Zakkum \u003cem\u003eet al\u003c/em\u003e. 2024). Some of the pest control measures adopted by growers in Nigeria, which only gave short-lived control, include pruning and outright felling and burning of the infested plants; and application of insecticides (Boopathi \u003cem\u003eet al.\u003c/em\u003e 2017). Although, Sampiano \u003cem\u003eet al\u003c/em\u003e. (2024) suggested certain natural oils for control, Akinlosotu \u003cem\u003eet al.\u003c/em\u003e (1993) proposed the use of natural enemies as a reliable and ecologically sound control option for mitigating the spiralling whitefly menace in Nigeria due to its exotic and polyphagous nature.\u003c/p\u003e \u003cp\u003eDue to the importance of the spiralling whitefly to horticulture in Nigeria, a nation-wide biological control of the spiralling whitefly project was initiated in 1993 with the initial task of determining the status of the \u003cem\u003eA. dispersus\u003c/em\u003e infestation in Nigeria. Remarkably, in all areas surveyed in Nigeria, \u003cem\u003eEncasia dispersa\u003c/em\u003e Dozier (Hymenoptera: Encyrtidae), a natural enemy of \u003cem\u003eA. dispersus\u003c/em\u003e was found together with the whitefly (Akinlosotu \u003cem\u003eet al.\u003c/em\u003e 1993; Pitan \u003cem\u003eet al\u003c/em\u003e. 2008). \u003cem\u003eEncasia dispersa\u003c/em\u003e is a primary parasitoid of the spiralling whitefly. It has been used effectively either singly or in combination with other natural enemies in previous attempts at the biological control of \u003cem\u003eA. dispersus\u003c/em\u003e in Hawaii, Pacific countries such as Palau and Pohnpei and in the Maldives with varying degrees of successes (Neuenschwander, 1994; Chand \u003cem\u003eet al\u003c/em\u003e. 2018)). Since there was no record of any formal release of the parasitoid anywhere in Nigeria, the wasp must have arrived by accident, presumably together with \u003cem\u003eA. dispersus\u003c/em\u003e. It is therefore, necessary to determine the suitability of the introduced natural enemy in order to determine whether further importations of other natural enemies would be necessary. In practice, evaluation of the efficacy of biological control agents is very important in any biological control programme and has been recognized as the key to the development of biological control as a science (Chand \u003cem\u003eet al\u003c/em\u003e. 2018). Long-term population dynamics studies are no doubt the backbone of such evaluations and will clearly provide the most important demonstration of impact. Therefore, this study was designed to determine the temporal patterns of the distribution of the spiralling whitefly on 4 different host plants and to highlight major factors in whitefly population fluctuations with emphasis on the evaluation of \u003cem\u003eEncasia\u003c/em\u003e sp. as an efficient biological control agent.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy Area\u003c/h2\u003e \u003cp\u003eThe study was carried out between January, 2014 and December, 2019 in Ibadan, southwest of Nigeria (guinea savannah zone) (7\u003csup\u003eo\u003c/sup\u003e30\u0026rsquo;N, 3\u003csup\u003eo\u003c/sup\u003e54\u0026rsquo;E, 210 m above sea level) at two of the sites where growers reported heavy infestation of \u003cem\u003eA. dispersus\u003c/em\u003e in 2010. Generally, in southern Nigeria, the rainfall pattern is bimodal, with a long rainy season lasting from March to July followed by a dry spell. The short rainy season lasts from September until November. Until February-March the weather is dry, with frequent periods of 'harmattan', a dry, dusty wind originating in the Sahara Desert.\u003c/p\u003e \u003cp\u003eThe first site was in Bashorun area in the north eastern part of Ibadan and contained the following hosts: 6 stands of \u003cem\u003eCitrus sinensis\u003c/em\u003e, 2 of \u003cem\u003eFicus polita\u003c/em\u003e, 4 of \u003cem\u003ePsidum guajava\u003c/em\u003e, 28 of \u003cem\u003eAcalypha wikensiana\u003c/em\u003e, 2 of \u003cem\u003eMangifera indica\u003c/em\u003e (mango), 11 of \u003cem\u003eCarica papaya (\u003c/em\u003epawpaw) and 18 of \u003cem\u003eMusa paradisiaca\u003c/em\u003e (plantain). At the second site which was at Jericho Reservation Area, south of Ibadan, had 4 stands of \u003cem\u003eCitrus sinensis\u003c/em\u003e, 2 of \u003cem\u003eFicus polita\u003c/em\u003e, 2 of \u003cem\u003ePsidium guajava\u003c/em\u003e and 101 of \u003cem\u003eAcalypha wilkensiana\u003c/em\u003e. A preliminary visual examination was made of all the plants in the study areas to determine the severity of infestation. One severely infested plant was selected from only four hosts for sampling in this study - \u003cem\u003eCitrus sinensis, Ficus polita\u003c/em\u003e, \u003cem\u003ePsidium guajava\u003c/em\u003e and \u003cem\u003eAcalypha wilkensiana\u003c/em\u003e because they were common to the two sites, making a total of 4 plants per site (i.e. 8 plants in all).\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eMonitoring of the spiralling whitefly and its parasitoid\u003c/h3\u003e\n\u003cp\u003eFor monitoring of \u003cem\u003eA. dispersus\u003c/em\u003e population densities on the four host plants, the sampling procedure was as follows: 20 leaves per host tree were randomly selected for examination once a month from the bottom, middle and top parts of the host plants. Counts of adults, nymphs and parasitised \u003cem\u003eA. dispersus\u003c/em\u003e (mummies) were made \u003cem\u003ein situ\u003c/em\u003e and were recorded separately. After removing live insects, others were kept in the laboratory for 3\u0026ndash;4 weeks until emergence of primary parasitoids was completed. In order to allow comparisons to be made between the different host plants with leaf sizes greatly varied, the total number of the spiralling whitefly (adults, nymphs and mummies) was calculated on a leaf surface area basis. To do this, leaf surface areas of 5 randomly selected leaves out of the 20 leaves sampled from each host plant were measured and the mean (x) was multiplied by the number of leaves sampled (s) to give the total leaf area sampled (sx). The number of \u003cem\u003eA. dispersus\u003c/em\u003e and \u003cem\u003eEncasia\u003c/em\u003e spp. per square centimeter (w/cm\u003csup\u003e2\u003c/sup\u003e) was then determined by dividing the total number of whiteflies found per sample per host plant (t) by the calculated leaf area (w/cm\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;t/sx) (Tingle and Copland, 1987). Differences in the population densities of \u003cem\u003eA. dispersus\u003c/em\u003e and \u003cem\u003eEncasia\u003c/em\u003e per square centimeter of the leaf areas on different host plants were detected using student\u0026rsquo;s t-tests (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) after such data were arcsine-transformed.\u003c/p\u003e \u003cp\u003eTemperature and rainfall data collection\u003c/p\u003e \u003cp\u003eAverage monthly temperature and rainfall data collected to determine a possible influence of rainfall and temperature on \u003cem\u003eA. dispersus\u003c/em\u003e densities. The data covered the rainfall of the month preceding each sampling time. Correlation and regression analyses (Draper and Smith 1981) were carried out to determine the relative importance of different ecological factors examined.\u003c/p\u003e \u003cp\u003e \u003cb\u003eDensity dependence of\u003c/b\u003e \u003cb\u003eEncasia\u003c/b\u003e \u003cb\u003esp.\u003c/b\u003e\u003c/p\u003e \u003cp\u003eParasitism index was computed and was transformed into the arcsine of its square root and plotted against log (x\u0026thinsp;+\u0026thinsp;1) \u0026ndash; transformed whitefly densities. The significance of the slopes was judged with a t-test at P\u0026thinsp;\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e\u0026le;\u003c/span\u003e\u0026thinsp;0.05 (Boavida and Neuenschwander 2010; Ajuonu \u003cem\u003eet al.\u003c/em\u003e 2011).\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eRainfall and temperature pattern, population fluctuation of the spiralling whitefly and its parasitoid, \u003cem\u003eEncasia\u003c/em\u003e sp., on each of the 4 host plants at the 2 sites are presented in Figs. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e\u0026ndash;\u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e. Between 2014 and 2019, there was a sharp, consistent and irredeemable decline in the population densities of the whitefly to zero from 2016 on \u003cem\u003eCitrus\u003c/em\u003e, \u003cem\u003eAcalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e spp. at the two experimental sites. The data from the first sample and those taken between January and May, 2014 at the two sites showed significant differences in the densities of \u003cem\u003eA. dispersus\u003c/em\u003e on the different host plants (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05). But marked reduction in the numbers of \u003cem\u003eA. dispersus\u003c/em\u003e was noticed from the 6th month (June, 2014) (Figs. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e \u0026amp; \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e); the reduction became significant (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFig\u003c/em\u003e at the end of the second year (2015); and at the end of the third year for \u003cem\u003ePsidium\u003c/em\u003e. Largely, on the four hosts, following the detection of \u003cem\u003eEncasia\u003c/em\u003e sp. peaks of \u003cem\u003eA. dispersus\u003c/em\u003e infestations, estimated from the numbers of adult whiteflies became lower each year. In 2015, peaks reached only about 20% of those of 2014. The total number of parasitized pupae increased from one year to the next (Figs. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e and \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e), indicating that parasitism rates generally increased from 1993 to 1996. On \u003cem\u003ePsidium\u003c/em\u003e at the two sites, whitefly numbers decreased and remained relatively constant at a low level while percent parasitism was stable. Although initial whitefly densities varied significantly between trees, fluctuation trends were similar on each of the host plants. At each site, there was a significantly higher number of \u003cem\u003eA. dispersus\u003c/em\u003e than on other host plants in which in themselves were not significantly different (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05). There was no difference between the densities of \u003cem\u003eA. dispersus\u003c/em\u003e on \u003cem\u003ePsidium\u003c/em\u003e at the two sites but significant differences occurred between the population densities of \u003cem\u003eA. dispersus on Psidium\u003c/em\u003e and other host plants both within and between sites (Table \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003eOn the other hand, percent parasitism did not differ significantly on plants within or between the sites even though it varied significantly at the first sampling in January, 2014 and was observed to be highest on \u003cem\u003eAcalypha\u003c/em\u003e (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003e). The abundance of the parasitoid followed the same pattern as that of the host on the 4 host plants, which illustrates the ability of the parasitoid population to track down the spiralling whitefly population densities. The parasitoid population varied greatly with plant species but generally peaks of percentage parasitism occurred at the same periods of the year on the different plant species (Figs. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e and \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e). This suggests that plant species have an important role to play on the level of parasitism observed. There was no significant correlation between percent parasitism and mean temperature during the sampling period on any of the host plants studied (Table \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e). The contributions of various biotic and abiotic factors to the size of whitefly populations on the four hostplants were quantified in a multiple regression analysis (Tables \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e). On the basis of infested trees, three independent factors influenced \u003cem\u003eA. dispersus\u003c/em\u003e populations. Parasitism played a very important role in the occurrence of \u003cem\u003eA. dispersus\u003c/em\u003e, with the highest values found on \u003cem\u003eCitrus\u003c/em\u003e, \u003cem\u003eAcalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e spp. relative to \u003cem\u003ePsidium\u003c/em\u003e at the two experimental sites. The second most important influence was temperature while rainfall was clearly not a major factor. However, the relatedness of whitefly parasitism and temperature as well as rainfall was low though significant. Slope (b) which represents the rate of change, and in this case rate of population collapse was significant and higher with parasitism than those of other factors at the two sites. In addition, parasitism was found to be density-dependent on \u003cem\u003eAcalypha, Citrus\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e judged by the significance of the regression coefficients but on \u003cem\u003ePsidium\u003c/em\u003e, it was a density-independent relationship (Table \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003e). The similarity in the trends of the results from the two sites justified the pooling of data to determine the functional relationship between \u003cem\u003eA. dispersus\u003c/em\u003e and its parasitoid which was found to be polynomial in all cases with a 6th degree on \u003cem\u003ePsidium\u003c/em\u003e, 5th degree on \u003cem\u003eFicus\u003c/em\u003e, 3rd on both \u003cem\u003eCitrus\u003c/em\u003e and \u003cem\u003eAcalypha\u003c/em\u003e spp. (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eResults showed that the degree of pest regulation achieved was not uniform but depended on host plants; there was also a general marked decline in the population of the whitefly from 2014 to 2019 on all the host plants at the two sites. The positive correlation between \u003cem\u003eA. dispersus\u003c/em\u003e population and rainfall on the one hand and temperature on the other suggests that both factors influenced the population of the spiralling whitefly. The direct influence of the rain could be the washing-off of whiteflies from host leaves while the indirect is mediated through the physiological condition of the host plants could be responsible (Mani and Krishnamoorthy 2002; Mani \u003cem\u003eet al\u003c/em\u003e. 2004). But because of the low correlation between whitefly population and each of temperature and rainfall on the four host plants, the sudden decline of \u003cem\u003eA. dispersus\u003c/em\u003e population following the peaks and the reduction in \u003cem\u003eA. dispersus\u003c/em\u003e population density which also occurred in both the raining and dry season, the impact of rainfall and temperature on \u003cem\u003eA. dispersus\u003c/em\u003e, though important, was considered minor.\u003c/p\u003e \u003cp\u003eAlthough temperature may not be the factor inducing whitefly outbreaks (on \u003cem\u003ePsidium\u003c/em\u003e) as stated earlier, the significant correlation between temperature and percent parasitism on the host plants at the two sites indicated that temperature influenced parasitism and is important probably in determining parasitoid efficiency. Similar reports on the influence of temperature have been reported on the searching, oviposition and developmental rates of \u003cem\u003eLeptomastidae abnormis\u003c/em\u003e Girault and \u003cem\u003eLeptomastix dactylopii\u003c/em\u003e Howard and consequently on the control of \u003cem\u003ePlanococcus citri\u003c/em\u003e Risso by the parasitoids (Tingle and Copeland 1987). These features of parasitoids that are affected by temperature are those that contribute to success of the natural enemy in terms of number of hosts parasitized at a given time.\u003c/p\u003e \u003cp\u003eThe decline in the population of the whitefly observed on the 4 host plants might be a result of the temporal synchrony of the numbers of \u003cem\u003eEncasia\u003c/em\u003e sp. with that of the hosts, and which resulted in the highly significant correlation that existed between the two populations on each of the host plants. Rate of decline was very high on the indicating steepest slope was obtained with parasitism on the four hosts, though higher on \u003cem\u003eAcalypha, Citrus\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e than \u003cem\u003ePsidium.\u003c/em\u003e Only a natural enemy, in this case \u003cem\u003eEncasia\u003c/em\u003e sp. appeared to be capable of causing that type of variation in the host\u0026rsquo;s population. Though positive density dependence has rarely been found in natural host\u0026ndash;parasitoid interactions despite their apparent stability (Mani \u003cem\u003eet al\u003c/em\u003e. 2004), \u003cem\u003eEncasia\u003c/em\u003e sp. appeared to show this type of dependence on the population of \u003cem\u003eA. dispersus\u003c/em\u003e in the first two years of sampling on the four host plants. Some of the attributes of the parasitoid that could enable such a response include high fecundity and shorter generation time compared with that of its host (Tanga \u003cem\u003eet al\u003c/em\u003e. 2013).\u003c/p\u003e \u003cp\u003eThe extinction of \u003cem\u003eA. dispersus\u003c/em\u003e on \u003cem\u003eCitrus, Ficus\u003c/em\u003e and \u003cem\u003eAcalypha\u003c/em\u003e at different times during the study agrees with modern reasoning that biological control is compatible with local pest extinctions (Tanga \u003cem\u003eet al\u003c/em\u003e. 2013). Similarly, the marked reduction in the population density of the whiteflies on \u003cem\u003ePsidium\u003c/em\u003e and lack of pest outbreaks subsequently indicated that a stable relationship had been established between the parasitoid and its host. It also implies that the \u003cem\u003eEncasia\u003c/em\u003e sp. is adequately regulating the number of \u003cem\u003eA. dispersus\u003c/em\u003e though it appears it may not be able to singly cause the extinction of \u003cem\u003eA. dispersus\u003c/em\u003e on \u003cem\u003ePsidium\u003c/em\u003e. Such differences in pest numbers on different host plants have also been reported for some aphids (Wellings and Dixon 1987) and the level of control achieved by the aphelinid parasitoid, \u003cem\u003eEncasia formosa\u003c/em\u003e Gahan on \u003cem\u003eTrialeurodes vaporarium\u003c/em\u003e. This was attributed to a combination of the effect of the host plant on pest fecundity, lifespan and developmental rate and on the searching efficiency by the parasitoid (Ajuonu \u003cem\u003eet al.\u003c/em\u003e 2011). Several plant features such as leaf surface topography and toxic secondary substances have also been reported to affect parasitoids\u0026rsquo; efficacy (Campbell and Duffey 1979). This suggests that plant susceptibility to insects may result from the detrimental effects of plant antibiotics on the biological control agents of insect pests in question.\u003c/p\u003e \u003cp\u003eThough there was no enough evidence from the present study to suggest that the fecundity and lifespan of \u003cem\u003eA. dispersus\u003c/em\u003e were more stimulated on \u003cem\u003ePsidium\u003c/em\u003e than other host plants, significantly higher population of \u003cem\u003eA. dispersus\u003c/em\u003e observed on \u003cem\u003ePsidium\u003c/em\u003e is an agreement with earlier report that total developmental time for \u003cem\u003eA. dispersus\u003c/em\u003e is shorter on \u003cem\u003ePsidium\u003c/em\u003e than on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e in that order (Pitan and Odebiyi 2002; Han \u003cem\u003eet al.\u003c/em\u003e 2009). The shorter developmental time on \u003cem\u003ePsidium\u003c/em\u003e suggests that more whiteflies would be found on the plant, while an impressive control (and in fact extinction) of the whitefly would be more likely on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e where replacement of parasitized \u003cem\u003eA. dispersus\u003c/em\u003e is much slower due to more prolonged developmental time compared to \u003cem\u003ePsidium\u003c/em\u003e. The 6th degree polynomial relationship recorded on \u003cem\u003eAcalypha\u003c/em\u003e also suggest that more factors regulate the population density of \u003cem\u003eA. dispersus\u003c/em\u003e on the plant compared to the other hosts trialed and therefore, will be take more time to achieve whitefly extinction than on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e spp. Both sets of data from the two orchards demonstrate a decline in \u003cem\u003eA. dispersus\u003c/em\u003e populations with increasing time of parasitoid presence. Since other factors remained mostly unchanged, the decline is attributed to this exotic parasitoid.\u003c/p\u003e \u003cp\u003eIt is concluded that differences in pest regulation observed on \u003cem\u003ePsidium, Citrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e are entirely due to an effect on the parasitoid. The significant correlation between parasitism and temperature and not whitefly population density and temperature indicate that the effect of temperature is likely to on the parasitoid rather than the whitefly. Similarly, the significance of the relationship between rainfall and whitefly population density and not parasitism means the effect of rainfall is on the whiteflies. However, the fact that \u003cem\u003ePsidium\u003c/em\u003e still harbours whitefly numbers suggest that rainfall and temperature are minor factors, and hostplant and parasitism major factors. Therefore, although rainfall and temperature are important factors too, they are considered minor in this study, while \u003cem\u003eEncasia\u003c/em\u003e sp. and host plant qualities were major factors affecting the population of \u003cem\u003eA. dispersus\u003c/em\u003e and are important in its regulation.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003eThe authors declare that this manuscript has not been considered elsewhere for publication.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe supports of those whose premises were used at Bashorun and Onireke, Ibadan, Nigeria for the study are appreciated.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor\u0026rsquo;s contribution statements\u003c/strong\u003e: Dr. FILANI, OYINDAMOLA CAROLINE carried out the research work and wrote up the paper.\u003c/p\u003e\n\u003cp\u003eProf. PITAN, OLUFEMI RICHARD conceived the experiment and review the paper write-up.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u0026nbsp;\u003c/strong\u003eThis study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability\u003c/strong\u003e Not applicable in the study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompliance with ethical standards\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u0026nbsp;\u003c/strong\u003eThe authors declare that they have no conflict of interest regarding the publication of this paper.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e This study does not involve human participants and so ethics approval is not applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent\u003c/strong\u003e No consent was required for the study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCode availability\u003c/strong\u003e Not applicable in the study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests:\u003c/strong\u003e Authors did not have any \u0026nbsp;financial support either directly or indirectly as regards this work submitted for publication.\u0026nbsp;\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAjuonu O, Neuenschwander P, Korie S (2011) Niche separation between \u003cem\u003eEncarsia dispersa\u003c/em\u003e and \u003cem\u003eEncarsia guadeloupae\u003c/em\u003e, two biological control agents of the spiraling whitefly \u003cem\u003eAleurodicus dispersus\u003c/em\u003e, in Benin, West Africa \u003cem\u003eBioControl\u003c/em\u003e 56: 277\u0026ndash;282 doi:10.1007/s10526-010-9331-9\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAkinlosotu TA, Jackai LEN. Ntonifor NN, Hassan AT, Agyakwa CW, Odebiyi JA, Akingbohungbe AE, Rossell HW (1993) Aleurodicus dispersus in Nigeria, FAO Plant Protection Bulletin 41: 127\u0026ndash;129.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBoavida C, Neuenschwander P (2010) Population dynamics and life tables of the mango mealybug, Rastrococcus invadens Williams, and its introduced natural enemy, Gyranusoidea tebygi Noyes in Benin. Biocontrol Science and Technology 5: 489\u0026ndash;508.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBoopathi T, Sankari K, Meena M, Ravi Thirunavukarasu K (2017) Impact of insecticides on spiralling whitefly, Aleurodicus dispersus (Hemiptera: Aleyrodidae) and its natural enemy complex in cassava under open field conditions. Crop Protection 94: 137\u0026ndash;143\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCampbell BC, Duffey SS (1979) Tomatine and parasitic wasps\u0026rsquo; potential incompatibility of plant antibiosis with biological control. \u003cem\u003eScience\u003c/em\u003e 205: 700\u0026ndash;702.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChand R, Jokhan A, Kelera, R (2018) Spiralling whitefly and its management practices in the South Pacific. A review. \u003cem\u003eAdvances in Horticultural Science\u003c/em\u003e, \u003cem\u003e33\u003c/em\u003e(1), 123\u0026ndash;131. https://doi.org/10.13128/ahs-22952\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDraper NR, Smith H (1981) Applied Regression Analysis, 2nd Edition, John Wiley, New York.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHan DY, Liu Kui, Zhang Fang-Ping, Huang Wu-Ren, Zhang Jing-Bao, Jin Qi-An, Fu Yue-Guan (2009) Biological characteristics of the Spiralling whitefly, \u003cem\u003eAleurodicus dispersus\u003c/em\u003e Russell (Homoptera:Aleyrodidae. \u003cem\u003eActa Entomologica Sinica\u003c/em\u003e 3:445\u0026ndash;454\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKumashiro BR, Lai PY, Funasaki GY, Teramoto KK (1983) Efficacy of Nephaspis amnicola and Encasia ?haitiensis in controlling Aleurodicus dispersus in Hawaii. Proceedings of Hawaiian Entomological Society 24 (2 \u0026amp;3): 261\u0026ndash;269\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMani M, Krishnamoorthy A (2002) Classical Biological Control of the Spiralling whitefly, Aleurodicus dispersus Russell\u0026mdash;An Appraisal. Journal of Tropical Insect Science 22: 263\u0026ndash;273\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMani M, Krishnamoorthy A, Venugopalan R (2004) Role of the aphelinid parasitoid \u003cem\u003eEncarsia guadeloupae\u003c/em\u003e in the suppression of the exotic spiralling whitefly \u003cem\u003eAleurodicus dispersus\u003c/em\u003e on banana in India \u003cem\u003eBiocontrol Science and Technology\u003c/em\u003e 14: 619\u0026ndash;622\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNeuenschwander P (1994) Spiralling whitefly, Aleurodicus dispersus: a recent invader and a new cassava pest. African Crop Science Journal 2 \u0026amp; 4: 419\u0026ndash;421.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePitan OOR, Odebiyi JA (2002). Aspects of biology and variation in the developmental time on different hosts of the spiralling whitefly. \u003cem\u003eNigerian Journal of Entomology\u003c/em\u003e 20:23\u0026ndash;27\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePitan OOR (2003) The response of two growth stages of pepper to different population densities of the spiralling whitefly (\u003cem\u003eAleurodicus dispersus\u003c/em\u003e Russell) \u003cem\u003eInsect Science and Its Application\u003c/em\u003e 23: 115\u0026ndash;120.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePitan OOR, Fajinmi AA, Akinyemi SOS, Ayodele EA (2008) Status of the spiralling whitefly, \u003cem\u003eAleurodicus dispersus\u003c/em\u003e Russell (Homoptera: Aleyrodidae), infestation in Nigeria. \u003cem\u003eNigerian Journal of Plant Protection\u003c/em\u003e 24: 21\u0026ndash;26\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRussell LM (1965) New species of \u003cem\u003eAleurodicus\u003c/em\u003e Douglas and two close relatives (Homoptera: Aleyrodidae). \u003cem\u003eFlorida Entomologist\u003c/em\u003e 48: 47\u0026ndash;55.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSampiano KFS, Sibongga LMA, Ramos FRA, Aceres LV (2024) Sustainable Management for Spiralling Whitefly, Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae) Infesting Guava and Its Effects on the Natural Enemies. Mindanao Journal of Science and Technology 21: 165\u0026ndash;185\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSrinivasa MV (2000). Host plants of the spiraling whitefly, \u003cem\u003eAleurodicus dispersus\u003c/em\u003e Russell (Hemiptera: Aleyrodidae). \u003cem\u003ePest Management in Horticultural Ecosystems\u003c/em\u003e 6: 79\u0026ndash;105\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTanga CM, Ekesi S, Govender P, Mohamed SA (2013). Effect of Six Host Plant Species on the Life History and Population Growth Parameters of Rastrococcus iceryoides (Hemiptera: Pseudococcidae). Florida Entomologist 96: 1030\u0026ndash;1041 URL: https://doi.org/10.1653/024.096.034\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTingle CCD; Copland MJW (1987) Predicting development of the mealybug parasitoids, Anagyrus pseudococci, Leptomastix dactylopii and Leptomastidae abnormis under glasshouse conditions. Entomologia Experimentalis et Applicata 45: 56\u0026ndash;65\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWellings PW, Dixon AFG (1987) Sycamore aphid numbers and population density III. The role of aphids \u0026ndash; induced changes in plant quality. \u003cem\u003eJournal of Animal Ecology\u003c/em\u003e 56: 161 \u0026minus;\u0026thinsp;170.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eZakkum GB, Madhavi M, Guru SS (2024) Interplay between natural compounds of Mundulea sericea Bark Extract in combating Aleurodicus dispersus, spiralling whitefly an invasive pest of Telangana. Int. J. Curr. Microbiol. App. Sci. 13(6): 260\u0026ndash;268. doi: https://doi.org/10.20546/ijcmas.2024.1306.028\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 to 4 are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":true,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"international-journal-of-tropical-insect-science","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"jtis","sideBox":"Learn more about [International Journal of Tropical Insect Science](http://link.springer.com/journal/42690)","snPcode":"42690","submissionUrl":"https://www.editorialmanager.com/jtis/default2.aspx","title":"International Journal of Tropical Insect Science","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Population dynamics, Aleurodicus dispersus, Encarsia spp., efficacy, hostplant","lastPublishedDoi":"10.21203/rs.3.rs-6498232/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-6498232/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eIn Nigeria, the spiralling whitefly (SWF), \u003cem\u003eAleurodicus dispersus\u003c/em\u003e, is a highly polyphagous and serious pest of horticultural crops. Although its parasitoid, \u003cem\u003eEncasia\u003c/em\u003e sp., has been accidentally introduced, information on its suitability in the ecosystem is still scanty. The study therefore investigated factors influencing whitefly parasitisation by \u003cem\u003eEncasia\u003c/em\u003e sp, from 2014 to 2019 on \u003cem\u003eCitrus sinensis\u003c/em\u003e (sweet orange), \u003cem\u003eAcalypha wilkensiana\u003c/em\u003e (red acalypha), \u003cem\u003eFicus polita\u003c/em\u003e (fig) and \u003cem\u003ePsidium guajava\u003c/em\u003e (guava) at two sites in Ibadan, Nigeria. SWF abundance and mummification, and weather factors were monitored monthly and correlated. Total rainfall and mean temperature were significantly associated (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) with both SWF density and parasitisation, while \u003cem\u003eEncarsia\u003c/em\u003e sp., the only natural enemy found during the study, improved the regulation of SWF on all the hostplants at both sites. Number of parasitoids was highly correlated and synchronized (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) with that of SWF throughout the sampling period although the spatial patterns of parasitism distribution in relation to SWF population density were not totally directly density dependent. Local extinction of SWF was observed on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e spp., whereas whitefly regulation with reduced and stabilized numbers and stable percentage parasitism was evident on Psidium. While there was no significant difference (P\u0026thinsp;\u0026gt;\u0026thinsp;0.05) between parasitism indices either within or between sites on \u003cem\u003ePsidium\u003c/em\u003e, the cumulative numbers of SWF were significantly higher (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) than other hostplants. The continued presence of the regulated SWF number on Psidium and its extinction on \u003cem\u003eCitrus, Acalypha\u003c/em\u003e and \u003cem\u003eFicus\u003c/em\u003e suggested a combination of hostplant quality and \u003cem\u003eEncarsia\u003c/em\u003e sp. as major factors in SWF regulation.\u003c/p\u003e","manuscriptTitle":"Parasitisation of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae), by Encarsia spp. (Hymenoptera: Aphelinidae) in relation to hostplant and weather factors","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-06-17 09:09:28","doi":"10.21203/rs.3.rs-6498232/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Major revisions","date":"2025-07-27T17:58:00+00:00","index":"","fulltext":""},{"type":"reviewerAgreed","content":"","date":"2025-06-18T04:14:28+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-06-13T10:00:30+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-05-01T06:50:02+00:00","index":"","fulltext":""},{"type":"submitted","content":"International Journal of Tropical Insect Science","date":"2025-04-28T06:32:06+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"international-journal-of-tropical-insect-science","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"jtis","sideBox":"Learn more about [International Journal of Tropical Insect Science](http://link.springer.com/journal/42690)","snPcode":"42690","submissionUrl":"https://www.editorialmanager.com/jtis/default2.aspx","title":"International Journal of Tropical Insect Science","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"8c1a4737-0d63-4377-9d9d-bbe375015aac","owner":[],"postedDate":"June 17th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-12-29T16:08:21+00:00","versionOfRecord":{"articleIdentity":"rs-6498232","link":"https://doi.org/10.1007/s42690-025-01709-y","journal":{"identity":"international-journal-of-tropical-insect-science","isVorOnly":false,"title":"International Journal of Tropical Insect Science"},"publishedOn":"2025-12-22 15:57:57","publishedOnDateReadable":"December 22nd, 2025"},"versionCreatedAt":"2025-06-17 09:09:28","video":"","vorDoi":"10.1007/s42690-025-01709-y","vorDoiUrl":"https://doi.org/10.1007/s42690-025-01709-y","workflowStages":[]},"version":"v1","identity":"rs-6498232","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-6498232","identity":"rs-6498232","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}