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. 2021 May 12;11(6):264. doi: 10.1007/s13205-021-02831-7

Occurrence of exotic whitefly, Paraleyrodes minei Iaccarino (Hemiptera: Aleyrodidae) and other whitefly species on fruit crops in Maharashtra, India

Chandrashekar Krishnappa 1, Anil Kumar Dubey 2, Abhishek Verma 1, Gagana Kumar Mahapatro 1,✉
PMCID: PMC8116409  PMID: 33996376

Abstract

Severe incidence of an exotic whitefly species Paraleyrodes minei Iaccarino (Homoptera: Aleyrodidae) was noticed in the Pune region of Maharashtra state, India, on the fruit trees guava (Psidium guajava L.), jamoon (Syzygium cumini L.), mango (Mangifera indica L.), chiku (Manilkara zapota L.), custard apple (Annona squamosa L.), citrus (Citrus spp.), banana (Musa spp.) and coconut (Cocos nucifera L.). Additional host plants of P. minei are neem (Azadirachta indica L.), Asoka (Saraca asoca (Roxb.) and temple tree (Plumeria alba L.). The identity of the pest was established based on sequences of the mitochondrial cytochrome oxidase 1 (mtCO-I) region amplified from genomic DNA of single whitefly. The incidence of P. minei was 100% on guava, jamoon, and custard apple; wherein under the surface of the infested leaves looks completely white with cottony wax. In the case of, coconut, guava, chiku, and banana, P. minei was co-colonising along with the rugose spiralling whitefly (Aleurodicus rugioperculatus Martin). Star gooseberry (Phyllanthus acidus L., new host record) plants were severely infested with less frequently collected whitefly, Bemisia bryniae (Singh). Pomegranate (Punica granatum L.) was infested by whitefly Siphoninus phillyreae (Haliday). The study highlights the need for continuous monitoring of invasive whitefly species population on important fruit crops for timely application of management practices to prevent losses of potential yield.

Keywords: Aleurodicus rugioperculatus, Bemisia breyniae, Fruit trees, Mitochondrial cytochrome oxidase 1

In recent years, a number of invasive pest species have been reported in India which includes several whitefly species in addition to prominent lepidopteran pests, the South American tomato pin worm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) (Shashank et al. 2015) and fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) (Sharanabasappa et al. 2018). Invasive whitefly (Hemiptera: Aleyrodidae) species reported from India are Solanum whitefly, Aleurothrixus trachoides (Back) (Dubey and Sundararaj 2015); the rugose spiralling whitefly, Aleurodicus rugioperculatus Martin (Shanas et al. 2016); the nesting whitefly Paraleyrodes minei Iaccarino (Sujithra et al. 2019); Bondar’s nesting whitefly Paraleyrodes bondari (Mohan et al. 2019; Vidya et al. 2019); the Neotropical whitefly, Aleurotrachelus atratus Hempel and woolly whitefly, Aleurothrixus floccosus (Maskell) (Selvaraj et al 2019; Sundararaj et al. 2020). Among the invasive whitefly species reported, only A. trachoides were established for transmitting plant viruses (Chandrashekar et al. 2020). Aleurodicus rugioperculatus invasion has already caused considerable loss to coconut production as well as quality due to retarded growth of nuts resulting from direct feeding of the nymphs and adults on leaves in large number, and secretion of honeydew leading to the growth of sooty moulds in important coconut growing states of the country, Andhra Pradesh, Karnataka and Kerala. A. rugioperculatus reportedly feeds on banana, Indian almond, palms and several ornamental plants. The pest infestation is up to 40–60% in coconut and 25–40% in banana, and it is continuously spreading to other coconut growing regions (Selvaraj et al. 2016). Similar damage may also be anticipated from other invasive whitefly P. minei which was first reported from Kerala, India in November 2018, infesting coconut gardens along the Western Ghat coasts of Kerala and Karnataka (Mohan et al. 2019; Sujithra et al. 2019). In India, P. minei is reported to feed on coconut, mango, guava, banana, banyan tree, Indian almond, Ixora sp., teak, etc. Further studies suggested on the bio-geographical distribution of the pest in India and its host plants to understand its pestiferous nature. Since it is a polyphagous pest, strict domestic quarantine recommended for preventing its spread to other coconut growing areas in the country. Paraleyrodes minei was also reported from the Andaman and Nicobar Islands of India feeding on Calophyllum inophyllum L., Morinda citrifolia L. and Psidium guajava (Dubey 2019). The status of the P. minei occurrence in Maharashtra state was unknown; Maharashtra stands second after Andhra Pradesh in the total production of fruits in the country (http://agricoop.nic.in). Severe incidence of the pest may cause a significant reduction in fruit production; hence, a field survey was carried out for the occurrence of the pest in the state.

The host plants reported for P. minei, were surveyed in and around Pune (IARI- Research Farm, Aundh, Directorate of Floriculture Research Farm, Hadapsar, Kusgaon, Punawale and Agricultural College, Shivajinagar, Maharashtra) for the occurrence of the pest. The adult whiteflies were directly collected into micro-centrifuge tubes from host plants viz., guava (Psidium guajava), jamoon (Syzygium cumini), mango (Mangifera indica), chiku (Manilkara zapota), pomegranate (Punica granatum), custard apple (Annona squamosa), citrus (Citrus species), banana (Musa spp), coconut (Cocos nucifera), star gooseberry (Phyllanthus acidus), neem (Azadirachta indica), Ashoka (Saraca asoca) and temple tree (Plumeria alba). Live insect samples were quickly freezed at − 80 °C for a few minutes and used for DNA extraction from individual whiteflies using DNAeasy Blood and Tissue Kit (Qiagen, Amph, Germany) as per the reported method (Chandrashekar et al. 2020). The identity of the pest was established using sequences of the mitochondrial cytochrome oxidase 1 (mtCO-I) amplified using universal primers LCO1490-F and HCO2198-R (Folmer et al. 1994) from the total DNA extracted from individual whitefly as per the set PCR conditions of our laboratory (initial denaturation: 94 °C/5 min; denaturation: 94 °C/1 min; annealing: 55 °C/1 min; extension: 72 °C/1 min and final extension: 72 °C/10 min; 35 cycles) (Chandrashekar et al. 2020). DNA extraction, PCR, and sequencing were done in biological duplicates for each host plant. Whitefly from star gooseberry was additionally also identified using morphological characters. Consensus sequences were derived for the sequences of samples of each host plant using MEGA X software. The sequences were submitted to NCBI, and GenBank Accession numbers are given in Tables 1 and 2. BLASTn search performed with default settings for consensus sequences in the NCBI databases (http://www.ncbi.nlm.nih.gov/). Paraleyrodes minei sequences compared with reported P. minei sequences from the states of Karnataka and Kerala.

Table 1.

Bio-informatic analysis of Paraleyrodes minei sequences for the samples collected from different host plants

S. No GenBank accession Number Host Similarity (%) with P. minei sequences reported from India
Kerala Karnataka
MK776865 MK421974 MT422350 MT472560
1 MW586870 Banana (Musa sp.) 100 100 100 99.52
2 MW587270 Citrus sp. 100 100 100 99.69
3 MW587324 Guava (Psidium guajava) 100 100 100 99.69
4 MW587331 Jamoon (Syzygium cumini) 100 100 100 99.69
5 MW587332 Mango (Mangife indica) 100 100 100 99.69
6 MW741558 Chiku (Manilkara zapota L.) 99.84 99.84 99.84 99.51
7 MW741557 Custard apple (Annona squamosa L.) 100 100 100 99.68%
8 MW750441 Coconut (Cocos nucifera L.) 97.69 97.68 97.70 97.36
9 MW595955 Ashok tree (Saraca asoca) 100 100 100 99.70
10 MW595953 Neem Azadirachta indica 100 100 100 99.54
11 MW595921 Temple tree Plumeria sp. 100 100 100 99.54
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Table 2.

Bio-informatic analysis of Bemisia breyniae, Aleurodicus rugioperculatus and Siphoninus phillyreae sequences for the samples collected from different host plants

Host plant Whitefly species GenBank accession number Matching sequences Similarity (%)
Star gooseberry Bemisia breyniae MW595996 GQ867716 (B. breyniae isolate ws12, Taiwan.) 100
KJ190499 (B. breyniae isolate Bbre_TWKH1, Taiwan) 100
Pomegranate Siphoninus phillyreae MW595922 LR739219 (S. phillyreae from Israel) 100
JQ340199 (S. phillyreae isolate SL, China) 100
Banana Aleurodicus rugioperculatus MW750563 KY574535.1 and MW041900.1 (A. rugioperculatus) 100
Coconut A. rugioperculatus MW750575 KY574535.1 and MW041900.1 (A. rugioperculatus) 100
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The incidence of P. minei was severe on the tree hosts guava (Psidium guajava), jamoon (Syzygium cumini), mango (Mangifera indica), chiku (Manilkara zapota), pomegranate (Punica granatum), custard Apple (Annona squamosa), citrus (Citrus species), Banana (Musa spp), coconut (Cocos nucifera), neem (Azadirachta indica), Ashoka (Saraca asoca) and temple tree (Plumeria alba) (Fig. 1). The incidence was 100% on guava, jamoon, and custard apple trees. Undersides of the infested leaves look completely covered with white cottony wax. The sequences obtained for whiteflies collected from host plants guava, jamoon, mango, custard apple, banana, citrus, neem, Ashoka and temple tree showed (99.5–100%) sequence similarity with P. minei sequences from NCBI: GenBank Accession: MK776865 and MK421974 from Kerala and MT422350 and MT472560 from Karnataka, while the sequences for coconut whitefly samples showed 97% similarity (Table. 1). Paraleyrodes minei was co-colonising along with the rugose spiralling whitefly, Aleurodicus rugioperculatus Martin on banana and coconut, where A. rugioperculatus infestation was more severe (Figs. 1 and 2). In the coconut plantation of Kayamkulam, Kerala, P. minei occurs on coconut leaflets previously infested by A. rugioperculatus along with Paraleyrodes bondari (Mohan et al. 2019).

Fig. 1.

Fig. 1

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Incidence of Paraleyrodes minei on different host plants. a Banana, b Chiku, c Citrus sp., d, e Custard apple, f, g Guava, h Jamoon, i Mango, j Neem, k Temple tree

Fig. 2.

Fig. 2

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Coconut showing mixed incidence of Paraleyrodes minei (a) and Aleurodicus rugioperculatus (b) and their enlarged images

Sequences obtained for whitefly samples collected from pomegranate showed sequence similarity with Siphoninus phillyreae (Haliday) (NCBI, GenBank Accession: JQ340199 isolate from China and LR739219 from Israel) (Table 2). Severe incidence of S. phillyreae on pomegranate reported from Karnataka, India (Balikai et al 1999; Mani and Krishnamoorthy 1995a), but the population was suppressed by parasitism of E. inaron (Walker) and Encarsia sp. Star gooseberry showed severe infestation as almost all the leaves were infested with B. breyniae in large numbers (Fig. 3). Sequences obtained for these whitefly samples showed 100% sequence similarity with B. breyniae sequences from Taiwan (NCBI, GenBank Accession No.: KJ190499 and GQ867716) (Table 2). Bemisia breyniae was described by Singh (Singh 1931) from India, it is closely related to Bemisia vernoniae (David and Thenmozhi), but distinguishable in having a triangular lingula and in lacking the first abdominal setae. Dubey et al. (2009) considered Bemisia leguminicola Takahashi, 1942 as a synonym of B. breyniae (Singh), and host plants are Breynia vitis-idaea (Burm, F.) (= B. rhamnoides), B. officinalis Hemsl. and Indigofera cassioides DC. The incidence of B. breyniae on gooseberry is reported here as a new host record. Phyllanthus acidus suffers severe infestation of whitefly Bemisia euphorbiae (David and Subramaniam 1976) (Mani and Krishnamoorthy 1995b), and Phyllanthus emblica L. (= E. officinalis Gaertn) by whitefly species Dialeurodes citri (Ashmead) and Dialeuropora decempuncta (Quaintance and Baker) (Dubey and Ko 2008).

Fig. 3.

Fig. 3

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Star gooseberry showing severe incidence of Bemisia breyniae (left) and its close-up view (right)

Previous reports of P. minei suggested studies on bio-geographic distribution of the pest in India and its host plants to understand its pestiferous nature. Since it is a polyphagous pest, strict domestic quarantine is recommended for preventing its spread to other coconut growing areas in the county. Pest whitefly is reported to multiply throughout the year and egg to adult development requires only 20 days in summers months (Bellows et al. 1998). On coconut in India, pest reported to complete nymphal development period in 13 to 16 days with 42.67% survival rate (Sujithra et al. 2019). Extensive occurrence of this pest in Pune indicated the spread of this pest to Maharashtra. Since Maharashtra is the second after Andhra Pradesh in the total production of fruits (117.28 Lakh Tonnes per year) (http://agricoop.nic.in). Severe incidence of this pest species could be a challenge for fruit production and management. Hence, continuous monitoring is necessary for all the important fruit crops for the occurrence of invasive whitefly species and their population that will enable the timely application of management practices to minimise potential losses of crop yield.

Acknowledgements

KC, AV and GKM are thankful to the Director, ICAR-Indian Agricultural Research Institute for the facilities. AKD is thankful to the Director, ZSI, Kolkata for the infrastructure facility and MoEF and CC for financial support.

Author contributions

KC: conceptualization, survey, and sample collection: AV: performed molecular work and data analysis: AKD: morphological identification of whitefly samples: GKM: survey, funds and facility. All authors contributed to manuscript writing and approved it.

Conflict of interests

The authors report no competing interests.

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