The Ficus whitefly, Singhiella simplex (Singh) (Hemiptera: Aleyrodidae), an Aleyrodidae species first described in India (Singh 1931), causes damage to Ficus spp. and was first reported in Turkey in 2016 on Ficus microcarpa L.f. (Moraceae) in Antalya (Yükselbaba et al. 2017). The Ficus whitefly is of Asia origin and has been detected in India, China, Myanmar, Puerto Rico, Jamaica, the Cayman Islands, Brazil, and Taiwan (Jesus et al. 2010; Vichiato et al. 2013; Ko et al. 2015; Ahmed et al. 2022). The Ficus whitefly was detected in Miami, Florida, USA, in 2007, Israel in 2011, Cyprus in 2014, and Italy in 2019 (Kondo & Evans 2012; Laudani et al. 2020). Adult and instar feed on leaves. Unlike many other whitefly species, instar stages appear on both sides of the leaf (Konda & Evans 2012; EPPO 2018). Adults are tiny, about 1 to 1.5 mm in length with a pale yellow body. Wings are white and waxy with 2 light gray bands, 1 in the middle and 1 like a stripe towards the top edge of the wing (Hodges 2007; Mannion 2010; Avery et al. 2011; Ahmed et al. 2022). A female can lay 46 eggs in its lifespan (Legaspi et al. 2011). Instar stages are usually flat, oval, and initially transparent. The pupa is oval, 1.3 mm in length and dark yellow to light green in color with red eyes (Hodges 2007; Mannion et al. 2010; Jesus et al. 2010). The adults fly very quickly when disturbed. While most of these flights are at close range, the wind can carry them to distant areas (Hodges 2007). Legaspi et al. (2011) reported that the total immature development time of S. simplex was 97.1 d at 15 °C and 25.2 d at 30 °C. According to Hodges (2007), S. simplex have at least 3 generations per yr like other Singhiella species in Florida.

As a result of the severe damage caused by the Ficus whitefly on the plant, yellowing and shedding of leaves and branch dieback usually occur before the death of the plant (Mannion 2010). Defoliation is the most obvious symptom of the S. simplex infestation (Mannion 2010; Avery et al. 2011; Ahmed et al. 2022). It was reported that severe infestations of Ficus trees by S. simplex caused intensive defoliation in Florida in Aug 2007 (Hodges 2007; Ahmed et al. 2017).

Various natural enemies have been observed in landscape areas that may play an important role in the long-term control of the Ficus whitefly (Ahmed et al. 2022). Awareness of these natural enemies is crucial in deciding on suitable pesticide applications which will not adversely affect them (Ahmed et al. 2022). Natural enemies of S. simplex have been reported from Florida, the US, and China (Hodges 2007; Mannion 2010; Ko et al. 2015; Lahey & Polaszek 2017; Ahmed et al. 2022).

The Ficus whitefly has been reported to cause serious damage to Ficus spp. in areas where the pest has dispersal (Ahmed et al. 2022), so it is necessary to monitor the geographical range of the pest and prevent its further dispersal. Ahmed et al. (2022) studied the behavior of the Ficus whitefly, the biology, and control measures in the US. Further studies on its biology, behavior, and control strategies are required to facilitate pest control in urban areas where the pest has dispersal. For the development of effective control strategies, it is important to have detailed information about the geographical distribution, damage potential, and biocontrol agents of the pest.

This study, therefore, sought to determine the geographical distribution and population status of S. simplex, as well as to determine the potential natural enemies that can be included in the IPM program in the Western Mediterranean Region of Turkey.

Material and Methods

DETERMINATION OF THE PARASITOIDS OF FICUS WHITEFLY, SINGHIELLA SIMPLEX

The collected branches were kept in parasitoid emergence boxes (similiar to that of Goolsby et al. 2002) for 15 d in order to identify potential parasitoids of the Ficus whitefly. Parasitoids emerging in the glass tubes of the parasitoid emergence boxes were collected and placed in 80% ethanol and stored at –20 °C for morphological identification studies. Slide mounting of parasitoids was carried out according to the method specified in Polaszek et al. (2014). Identification of the parasitoids was conducted using the morphological characters and identification keys specified in Huang and Polaszek (1998). At least 10 individual parasitoids were slide mounted and identified from each location.

Table 1.

Sampling locations for the determination of geographical distribution and natural enemies of Singhiella simplex.

DETERMINATION OF THE NATURAL PARASITISM RATES

The parasitism rate was determined by counting the parasitized instar stages of S. simplex on the branches. Under the above-referenced stereomicroscope, parasitoid larvae and pupae in the instars also were counted separately. When using the parasitoid emergence box to determine the parasitism rate, the number of parasitoids and whiteflies obtained differed from the numbers on the branches. Therefore, the parasitism rate was determined by counting the parasitized and non-parasitized instars of the Ficus whitefly on the branches. Parasitism rate (%) was calculated according to Telli and Yiğit (2012) with the formula:

DETERMINATION OF THE PREDATORS OF SINGHIELLA SIMPLEX

To determine the predators of the Ficus whitefly, the trees infected with S. simplex were examined first by the visual inspection method after waiting for a few minutes around the trees. Predators that were observed to be feeding on the Ficus whitefly stages were collected, after which they were separated and kept in Petri dishes. Petri dishes with predators were checked under the above-referenced stereomicroscope to confirm that the predator was feeding on the Ficus whitefly stages. Density of predators, both adults and larvae, were determined by recording them visually. Species identification of the predators were done by their experts. Species diversity of the predators of S. simplex in the Western Mediterranean Region were estimated for each yr by the Shannon-Weiner index of Diversity (H') (Shannon 1948) and Equitability divided by evenness (E') (Pielou 1966). The higher the value of H', the higher the diversity of species. The lower the value of H', the lower the diversity. The E' index value ranges from 0 to l, with a value of 1 being the maximum possible evenness (Shannon 1948; Pielou 1966).

Table 2.

Standard evaluation procedure by presence in branches.

H′ = Pi lnpi

i=1

S = Total number of species

Pi = proportion of individuals of ith species in total sample

E′ = H′/lnS:

Equitability or evenness

H: Shanon's index

S = Total number of species

Results

GEOGRAPHICAL DISTRIBUTION OF FICUS WHITEFLY, SINGHIELLA SIMPLEX

In this study, the geographical distribution, population density, and natural enemies of S. simplex which have been recorded newly in Turkey were investigated in the Western Mediterranean Region. For this purpose, the samplings were carried out in Antalya Center, Alanya, Serik, Gazipaşa, Manavgat, Kumluca, Finike, Demre, and Kaş districts where the pest and its hosts were more intense in the mo of Aug, Sep, and Oct of 2018 and 2019 (Yükselbaba et al. 2018). From Tables 3 and 4, it is shown that S. simplex dispersed to all the districts within the Antalya province.

Table 3.

Results of Singhiella simplex and parasitoid samplings and parasitisim rate in 2018.

From Table 3, it is shown that the number of whiteflies per shoot was found to be lower in Aug compared to the other 2 mo in all the districts. In Kumluca, Manavgat, Gazipaşa, and Serik districts, the highest Ficus whitefly number per shoot was shown to be in Sep. In Antalya Center, Alanya, Demre, Finike, and Kaş districts, the highest Ficus whitefly number per shoot was shown to be in Oct.

According to the grade indicated in Table 2, a very high prevalence was detected in each district. In 10 of the branches collected from Demre and Kumluca districts, no immature stage of S. simplex was observed.

The highest number of whiteflies per shoot was recorded in Central Antalya, Finike, and Gazipaşa districts in Sep of 2019 (Table 4). In Serik and Manavgat districts, the highest number of whiteflies were detected in Aug, whereas it was detected in Oct in Kaş and Demre districts (Table 4). In 2019, the number of pests increased in all the districts and mo compared to the previous yr.

In addition, similar to the previous yr, it was determined that the pest had a very high prevalence in 2019 in the sampling areas. In 10 of the branches collected in Demre and Kumluca districts in 2019, no immature of S. simplex was observed.

PARASITOIDS OF FICUS WHITEFLY, SINGHIELLA SIMPLEX, AND NATURAL PARASITISM RATE

The result of the morphological analysis of the parasitoid samples showed Encarsia protransvena Viggiani (Hymenoptera: Aphelinidae) as the only parasitoid species of the pest. The numbers of E. protransvena larvae and pupae detected in shoot counts and natural parasitism rates are given in Tables 3 and 4.

Table 4.

Results of Singhiella simplex and parasitoid samplings and parasitisim rate in 2019.

From Table 3, it is shown that the lowest number of parasitoids was detected in Aug, whereas the highest number was observed in Oct in 2018. While natural parasitism rates ranged from 0% to 16.07% in Aug, the highest natural parasitism rate was found in Oct. The natural parasitism rate was detected between 12.81% and 32.88% in Oct. The result from Table 4 showed that natural parasitism rates were between 0% and 13.20% in Aug. In Sep, the natural parasitism rates were found to be between 0.4% and 20.23%. Similar to the previous yr, the highest rates of natural parasitism were observed in Oct, except in the Finike district. In Oct, the lowest parasitism rate was observed in Manavgat with 11.01%, and the highest in Serik with 21.66% (Table 4).

Discussion

In this study, the geographical distribution, abundance, and natural enemies of Ficus whitefly have been determined. The result of the study showed that S. simplex is common in all the locations within Antalya province and its districts in the Western Mediterranean Region. While the lowest population of S. simplex was determined as 90% in the Demre and Kumluca districts, it was found to be 100% in other districts and Central Antalya. In the Kumluca and Demre districts, it was observed that the branches in which S. simplex was not detected were the branches collected from the Ficus trees found on the main road edges. The reason for this may be that the whiteflies were affected by the exhaust fumes of vehicles. Another reason may be distance, as reported by Ahmed et al. (2022). They observed that an infestation started on one side of the road and moved on the same side along the hedge for over a yr. Ahmed et al. (2022) stated that the Ficus whitefly is unable to fly long distances, and its dispersal can be interrupted when there is a sufficient distance between trees. It was observed that there was an increase in Ficus whitefly population in the second yr of sampling. The increase in Ficus whitefly population in 2019 caused intense defoliation of Ficus trees. Due to the increasing damage by S. simplex, especially in the Kumluca and Demre districts, chemical management and pruning of Ficus trees were applied to control the pest by local municipalities (personal communication). However, despite the management, an increase in the Ficus whitefly abundance per shoot was observed in these 2 districts and others (Table 4). While the lowest population was determined in Aug in all districts, the highest Ficus whitefly population was recorded in Sep and Oct (Tables 3 and 4). Similar to our study, Mannion (2010) reported in a study on the population fluctuation of S. simplex that the whitefly population increased in Aug, reached the highest number in Sep and Oct. Mannion (2010) stated that the first leaf shedding started in the last d of Aug and increased in other mo. In a similar development, Yükselbaba et al. (2018) also determined the population dynamics of the pest with yellow sticky trap in Antalya between 2017 to 2018. In their study, they reported the first appearance of S. simplex adults on sticky traps in early Apr and reached the highest numbers of 1,035 and 643 in Aug and Sep, respectively. Parallel with our findings, Ahmed et al. (2022) found that the S. simplex population started to increase in Apr, remained high until Oct, and then decreased.

Table 5.

Density of the predators of Singhiella simplex in 2018.

Table 6.

Density of the predators of Singhiella simplex in 2019.

To determine the parasitoids of the Ficus whitefly, morphological characters were examined, and it was observed that all parasitoids collected from the central area and districts of Antalya had the same diagnostic characters. Encarsia protransvena was determined as the only parasitoid species of the S. simplex in the Western Mediterranean Region. Hodges (2007) has reported the S. simplex for the first time in Florida and Encarsia tricolor Förster (Hymenoptera: Aphelinidae) as the parasitoid of the Ficus whitefly. Avery et al. (2011) speculated that the parasitoid detected in S. simplex larvae was E. protransvena. Myartseva et al. (2014) indicated that E. protransvena and Encarsia hispida De Santis (Hymenoptera: Aphelinidae) are parasitoids of S. simplex in Mexico. Ko et al. (2015) stated that there may be a possible native parasitoid species that would be a good candidate in the classical biological control of S. simplex, and this could be Encarsia singhiellae Shih & Polaszek (Hymenoptera: Aphelinidae), which they identified as a new species in their study. Ahmed et al. (2017) reported 3 parasitoid species of S. simplex in their research conducted between 2014 to 2016 in Florida, namely Amitus bennetti Viggiani & Evans (Hymenoptera: Platygasteridae), Baeoentedon balios Wang, Huang & Polaszek (Hymenoptera: Eulophidae), and E. protransvena. Lahey and Polaszek (2017) reported S. simplex as the second confirmed host for parasitoid B. balios. When the literature above is examined, 5 parasitoids of S. simplex have been reported from different parts of the world. In our study, E. protransvena was detected as the only parasitoid of Ficus whitefly in the Western Mediterranean Region. Ulusoy and Ülgentürk (2003) reported E. protransvena as the parasitoid of Dialeurodes citri Ashmead (Hemiptera: Aleyrodidae) and Tetraleurodes neemani Bink-Moenen in Bink-Moenen & Gerling (Hemiptera: Aleyrodidae) in Turkey. Huang and Polaszek (1998) reported the distribution of E. protransvena in various parts of the world that include Guangzhou, Taiwan, Puerto Rico, Spain, and the US (Florida, Georgia, and Hawaii). They reported Bemisia tabaci (Gennadius), D. citri, Dialeurodes citrifolii (Morgan), Dialeurodes kirkaldyi (Kotinsky), and Trialeurodes packardi Morrill (all Hemiptera: Aleyrodidae) from the Aleyrodidae family as hosts of E. protransvena.

In the present study C. mutata, S. aleyrodiformis, C. psociformis, and Conwentzia sp. in the order Neuroptera, and O. conglobata and S. parcesetosum in the order Coleptera were determined to be the predators of S. simplex. The generally observed natural enemies are Harmonia axyridis (Pallas), Olla-v-nigrum (Mulsant), Exochomus childreni Mulsant, Chilocorus nigritus (Fabricius), Curinus coeruleus (Mulsant) (all Coleoptera: Coccinellidae), and Neuroptera Chrysopa spp. (Mannion 2010). Avery et al. (2011) observed adult ladybird beetles C. coeruleus, H. axyridis, eggs and larvae of the green lacewing, Chrysopa spp., as predators of S. simplex. Ahmed et al. (2022) reported Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), C. nigritus, C. coeruleus, H. axyridis, O. v-nigrum, Brachiacantha dentipes (Fabricius), Coelophora inaequalis (Fabricius), Delphastus pallidus (LeConte), Egius platycephalus Mulsant, E. childreni Mulsant (all Coleoptera: Coccinellidae) species as predators of S. simplex. In this study, predator abundance was observed at its highest in Oct among the mo studied. According to the results of the H' and E' values, the diversity index of predators was considered low in the Western Mediterranean Region for both yr of the study period. The fact that the abundance of natural enemies is low and it differs among the districts may be the reason for the relatively low H' and E' values. The low density of natural enemies may be because natural enemies already are adapting to different hosts. The observed predator density was lower than that of parasitoid E. protransvena. Telli and Yiğit (2012) reported Clitostethus arcuatus Risso, Cryptoleamus montrouzieri Mulsant, Chilocorus bipustulatus L., S. parcesetosum (all Coleoptera: Coccinellidae), Conwentzia sp., and C. carnea as the predators of Aleurothrixus floccosus (Maskell) (Hemiptera: Aleyrodidae) in Turkey. In the same study, they indicated Cunaxa potchensis Den Heyer (Acari: Cunaxidae), C. arcuatus, C. bipustulatus, Conwentzia sp., and C. carnea as the predators of Paraleyrodes minei Iaccarino (Hemiptera: Aleyrodidae).

In this study, the highest natural parasitism rates recorded in Oct of 2018 and 2019 were 32.88% and 21.65%, respectively, across the sampling mo. In 2019, compared to the previous yr, a decrease was observed in natural parasitism rates, especially in Oct in all the districts. One of the principal reasons for the proportional decrease in the natural parasitism rate was due to the increase in the Ficus whitefly populations. The second reason could be due to chemical control of S. simplex and mosquitoes that indirectly might have affected the parasitoid population. Supporting our judgment, Ahmed et al. (2022) reported that foliar application of contact insecticides may affect the resident natural enemies of S. simplex. They also stated that applying systemic insecticide by soil drenching could minimize the chemical impact on resident natural enemies of S. simplex. The third reason may be due to routine pruning in the landscaped areas. Municipalities usually do the pruning in the early summer mo (personal communication) and there is a possibility of the adult Ficus whitefly flying away to lay their eggs on other leaves and reproduce there. The possibility of the parasitoid finding the whitefly instar decreases and, therefore, the parasitoid population may be more affected. Avery et al. (2011) reported in their study that 10% death was caused by parasitization of Encarsia species, and 90% death was due to natural causes such as entomopathogenic fungi and predators, but they stated that these findings should be confirmed with a more comprehensive study. Telli and Yiğit (2012) determined the natural parasitism rates of A. floccosus and P. Minei in a study conducted in Hatay (Turkey) between 2005 to 2006. The result of their study showed that A. floccosus was suppressed by the species specific parasitoid, Cales noacki Howard (Hymenoptera: Aphelinidae), and the natural parasitism rate was found to be 88.71% in Erzin and 70.27% in Samandag in Oct. In the same study, they reported the natural parasitism rate of P. minei by E. hispida to be 25.60% in Oct and the highest of 38.73% in Jun.

In the light of these data, it has been observed that the dispersal ability of S. simplex is high. It was observed that the population of Ficus whitefly increased as of the end of Aug and the population of natural enemies increased in parallel. Improving the effectiveness of its natural enemies, especially parasitoids, and taking protective measures such as partial pruning, using selective insecticides will make a serious contribution to the management of the Ficus whitefly. Studies to determine the seasonal relationship between the Ficus whitefly and parasitoid, the biology and the parasitism capacity of the parasitoid on S. simplex will contribute to the development of more effective control methods in urban environments for control of S. simplex. In addition, applications of entomopathogenic fungi and continued research in this direction will be useful.