Whitefly (Hemiptera: Aleyrodidae) Species Infesting Myrica rubra in China
To determine the species of whiteflies infesting Chinese bayberry, Myrica rubra Sieb. et Zucc. (Fagales: Myricaceae), in China, we collected samples from eight provinces (Zhejiang, Jiangsu, Shanghai, Anhui, Hubei, Fujian, Guizhou, and Yunnan) from 2014 through 2017. Six species representing six genera of the subfamily Aleyrodinae were identified, namely Aleurocanthus spiniferus (Quaintance), Aleurolobus szechwanensis Young, Aleuroplatus pectiniferus Quaintance & Baker, Cohicaleyrodes caerulescens (Singh), Dialeuropora brideliae (Takahashi), and Parabemisia myricae (Kuwana). Information on the pest status, illustrations, distribution worldwide, and hosts of each of these six species is provided.Abstract
Chinese bayberry, Myrica rubra Sieb. et Zucc. (Fagales: Myricaceae), is an economically important subtropical fruit crop native to southern China and other Asian countries (Chen et al. 2004). The fruit is popular for its appealing color, delicious taste, essential nutrients, and bioactive constituents such as antioxidants (Zhang et al. 2011) and antitumor properties (Sun et al. 2012). Chinese bayberry is widely planted not only as a fruit crop but also in forestry stands (Chen et al. 2004). Whiteflies are an economically important group of insects infesting a range of host plants (Mound and Halsey 1978). Four species, namely Aleuroplatus plumosus (Quaintance), Crenidorsum caerulescens (Singh), Parabemisia myricae (Kuwana), and Tetraleurodes ursorum (Cockerell), are recorded from Chinese bayberry (Evans 2008; Mound and Halsey 1978). We conducted a survey of whitefly species infesting Chinese bayberry in China from 2014 through 2017 in regions where Chinese bayberry is grown.
Materials and Methods
Specimens were collected in Chinese bayberry groves in eight provinces of China (Zhejiang, Jiangsu, Shanghai, Anhui, Hubei, Fujian, Guizhou, and Yunnan) by J.-R.W. Puparia were mounted using the method of Martin (1987) and Dubey and David (2012). All the specimens are deposited in the Insect Collection of Zhejiang Agriculture and Forestry University (ZAFU). Terminology used for morphological structures follows Bink-Moenen (1983), Martin (1985), and Gill (1990). The habitus images were taken using a LEICA M125 stereo-microscope (Leica, Wetzlar, Germany) equipped with a LEICA DFC290 (Leica) from the Insect Collection of ZAFU, Lin’an, China. Puparial measurements and microphotographs were taken using a Zeiss stereomicroscope (Carl Zeiss, Gottingen, Germany) at the ZAFU. Scanning electron microscope (SEM) images were taken using a Philips XL30-Environmental Scanning Electron Microscope (Philips, United Kingdom) at the Testing Center of Yangzhou University, Yangzhou, China at 20 kV/EHT and 80 Pa between 128× to 800× magnification. Adobe Photoshop software was used to make small adjustments and to assemble the plates.
Results
Six species representing six genera of the subfamily Aleyrodinae were identified from our collections. These were Aleurocanthus spiniferus (Quaintance), Aleurolobus szechwanensis Young, Aleuroplatus pectiniferus Quaintance and Baker, Cohicaleyrodes caerulescens (Singh), Parabemisia myricae (Kuwana), and Dialeuropora brideliae (Takahashi). Pest status, worldwide distribution, and host plants of each are listed. Illustrations also serve as an additional tool for the identification of the species.
Aleurocanthus spiniferus (Quaintance) (Fig.1)
-
Aleurodes spinifera: Quaintance, 1903: 63–64.
-
Aleurocanthus spiniferus: Quaintance and Baker, 1914: 102.
-
Material examined. 3 puparia, CHINA, Guiyang (26.64°N, 106.81°E), Guizhou Province, from Myrica rubra, 19.vi.2016, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China, Andaman Islands, Caroline Islands, Greece, Hawaii, India, Iran, Jamaica, Japan, Java, Kenya, Malaysia, Mauritius, New Caledonia, New Guinea, Nicobar Islands, Philippines, Sri Lanka, Sumatra, Tanzania, Thailand (Evans 2008), Italy (Porcelli 2008).
-
Host plants. Myrica rubra; see Evans (2008) for other hosts.
-
Comment. Aleurocanthus spiniferus, widely known as the citrus spiny whitefly, is native to Southeast Asia and has spread to Africa, Australia, Europe, and the Pacific Islands (Porcelli 2008). Citrus spp. are the main hosts of economic importance, but A. spiniferus is a polyphagous pest and has been recorded from more than 30 plant families. Cioffi et al. (2013) provided a comprehensive list of its host plants. Serious outbreaks of whiteflies infesting tea plants Camellia sinensis (L.) in China and Japan have been attributed to this species over the last 20 yr (Kanmiya et al. 2011). Kanmiya et al. (2011) compared the morphological, acoustic, and genomic features of tea-infesting versus citrus-infesting populations and proposed a new scientific name, Aleurocanthus camelliae Kanmiya and Kasai, and a new common name, camellia spiny whitefly for the tea-infesting population. We collected A. spiniferus on M. rubra in the Guizhou Province, but no major infestations were observed.



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Aleurolobus szechwanensis Young (Figs. 2–3)
-
Aleurolobus szechwanensis: Young, 1942: 99.
-
Material examined. 2 puparia, Wuyishan, (27.63°N, 118.01°E), Fujian Province, from Myrica rubra, 17. ix.2012, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China (Fujian, Sichuan, Chongqing, Shaanxi, Jiangxi, Yunnan).
-
Host plants. Myrica rubra, Citrus reticulate Blanco (Young 1942).
-
Comment. Earlier, Young (1942) described A. szechwanensis from citrus in China. In our study, a small infestation of this species was found on Chinese bayberry, which represents the first record of this species on this plant host. This species resembles Aleurolobus taonabae (Kuwana) and Aleurolobus rhododendri Takahashi but can be separated from the former by the different structure of the thoracic and caudal combs and from the latter by the shorter marginal teeth and the fewer basal marginal setae (Young 1942). Only one natural enemy, Encarsia fujianensis Huang and Polaszek (Hymenoptera: Aphelinidae), has been recorded from this species (Huang and Polaszek 1998).



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Aleuroplatus pectiniferus Quaintance and Baker (Figs. 4–5)
-
Aleuroplatus pectiniferus: Quaintance and Baker, 1917: 393.
-
Aleuroplatus ficusgibbosae: Corbett, 1926: 271. [Synonymized by Martin, 1999: 48]
-
Aleuroplatus buchananiae: Jesudasan and David, 1991: 282. [Synonymized by Martin, 1999: 48]
-
Aleuroplatus distinctus: Jesudasan and David, 1991: 283. [Synonymized by Martin, 1999: 48]
-
Aleuroplatus pectenserratus: Singh, 1945: 76. [Synonymized by Martin, 1999: 48]
-
Aleuroplatus walayarensis: Jesudasan and David, 1991: 285. [Synonymized by Martin, 1999: 48]
-
Material examined. 15 puparia, Lin’an, (30.25°N, 119.72°E), Zhejiang Province, from Myrica rubra, 12.iv.2016, Coll. J. R. Wang, deposited in ZAFU; 10 puparia, Thousand Island Lake, (29.59°N, 119.01°E), Zhejiang Province, from M. rubra, 14.v.2016, Coll. J. R. Wang, deposited in ZAFU; 5 puparia, Cixi, (30.16°N, 121.26°E), Zhejiang Province, from M. rubra, 9.vi.2016, Coll. J. R. Wang, deposited in ZAFU; six puparia, Zhoushan (29.98°N, 122.21°E), Zhejiang Province, from M. rubra, 6.viii.2016, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China, Australia, India, Iran, Java, Malaya, Malaysia, Pakistan, Sri Lanka, Sulawesi (Evans 2008).
-
Host plants. Myrica rubra; see Evans (2008) for other host plants.
-
Comment. Aleuroplatus pectiniferus has caused very serious damage to Chinese bayberry in most Chinese bayberry planting regions in recent years, particularly in the Zhejiang Province. It is often misidentified as Aleurotrachelus camelliae (Kuwana) in the agricultural production areas because the puparia are very similar in appearance, with the transparent gelatinous covering on the case and white waxy secretions arising from the end of thoracic and caudal tracheal pores. It can be distinguished from A. camelliae by its thoracic and caudal combs composed of four or five long, prominent teeth while, in A. camelliae, the teeth are as long as the marginal teeth, as a major diagnostic characteristic of this species, and by the presence of submedian depressions along the suture of each abdominal segment (Wang et al. 2017). Chemical control of A. pectiniferus has not been effective because of the transparent gelatinous covering on the case. It has a very wide plant host range. Its known natural enemies include Encarsia ishii (Silverstri), Encarsia lutea (Masi), Encarsia perplexa Huang and Polaszek, and Eretmocerus cadabae Viggiani (Hymenoptera: Aphelinidae) (Evans 2008), which may prove to be effective biological control agents.



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Cohicaleyrodes caerulescens (Singh) (Figs. 6–7)
-
Aleurotrachelus caerulescens: Singh, 1931. 12: 59.
-
Crenidorsum caerulescens: David et al., 2006. 13: 25.
-
Cohicaleyrodes caerulescens: Dubey and Ko, 2010. 2685: 12–13.
-
Material examined. 1 puparia, Tianmu Mountain (30.31°N, 119.45°E), Zhejiang Province, from M. rubra, 6.vii.2017, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China, India.
-
Host plants. Myrica rubra, see Evans (2008) for other hosts.
-
Comment. Cohicaleyrodes caerulescens was recorded on M. rubra in Taiwan (Takahashi 1932). Dubey and Ko (2010) discussed the taxonomic status of this species in detail and placed this species in the genus Cohicaleyrodes. We collected C. caerulescens on M. rubra in Tianmu Mountain, but no serious damage to plants was observed.



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Dialeuropora brideliae (Takahashi) (Figs. 8–9)
-
Dialeurodes (Dialeuropora) brideliae: Takahashi, 1932: 15.
-
Dialeurodes (Dialeuropora) brideliae: Takahashi, 1934: 46.
-
Material examined. 2 puparia, Thousand Island Lake (29.59°N, 119.01°E), Zhejiang Province, from M. rubra, 14.v.2016, Coll. J. R. Wang, deposited in ZAFU; 1 puparia, Zhoushan (29.98°N, 122.21°E), Zhejiang Province, from M. rubra, 6.viii.2016, Coll. J. R. Wang, deposited in ZAFU; 8 puparia, Gutian Mountain National Nature Reserve (29.25°N, 118.15°E), Zhejiang Province, from Myrica rubra, 24.viii.2017, Coll. J. R. Wang, deposited in ZAFU; 10 puparia, Kunming, (30.16°N, 121.26°E), Yunnan Province, from M. rubra, 16.x.2016, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China, Japan.
-
Host plants. Bridelia ovate, Machilus sp., Myrica rubra, Stauntonia sp. (Evans 2008).
-
Comment. This represents the first record of this species on Chinese bayberry; it was collected in the Zhejiang and Yunnan Provinces. This species resembles Dialeurodes decempuncta (Quaintance & Baker) in having relatively small submarginal pores for the genus, lacking submarginal spines, and in possessing papillae. It is also resembles Dialeurodes holboelliae Young in shape but differs in the structure of the narrow marginal area, and D. holboelliae has numerous small papillae while D. brideliae is without small papillae.



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Parabemisia myricae (Kuwana) (Figs. 10–11)
-
Bemisia myricae: Kuwana, 1927: 249.
-
Parabemisia myricae: Takahashi, 1952: 24.
-
Material examined. 6 puparia, Thousand Island Lake (29.59°N, 119.01°E), Zhejiang Province, from M. rubra, 14.v.2016, Coll. J. R. Wang, deposited in ZAFU; 8 puparia, Cixi (30.16°N, 121.26°E), Zhejiang Province, from M. rubra, 9.vi.2016, Coll. J. R. Wang, deposited in ZAFU; 9 puparia, Zhoushan (29.98°N, 122.21°E), Zhejiang Province, from M. rubra, 6.viii.2016, Coll. J. R. Wang, deposited in ZAFU.
-
Distribution. China, Egypt, India, Iran, Israel, Italy, Japan, Morocco, Spain, Turkey, United States, Venezuela (Evans 2008), Croatia (Šimala et al. 2016).
-
Host plants. Myrica rubra; refer to Evans (2008) for other hosts.
-
Comment. Parabemisia myricae is commonly known as the “bayberry whitefly” due to its frequent and heavy infestations on bayberry worldwide. It is a polyphagous species recorded on 14 families of woody, broad-leaved angiosperm hosts (Mound and Halsey 1978), including many other economic plants such as tea plants and mulberry trees, which are very common in China (Luo and Zhou 1997; Wang et al. 2014). Kuwana (1927) described this species from Japan in 1927 and it has since become an invasive pest, particularly on citrus crops and avocados in several parts of the world (Benfatto 2015; Martin 1999; Šimala et al. 2016; Uygun et al. 1990). New host plant associations are common for some species of whiteflies, indicating their high potential to adapt and expand their geographic and plant host range effectively and cause problems on many plants (Martin 1996; Martin et al. 2000). Therefore, measures should be taken to prevent its further expansion in the region accompanied with effective control methods. This whitefly species is sometimes responsible for serious crop damage when it first arrives in a new geographical area, but usually soon falls below economic injury levels as natural enemies become established (Hernández-Suárez et al. 2012). Numerous parasitoid and predatory species are known to be associated with P. myricae (Evans 2008).



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81



Citation: Journal of Entomological Science 54, 3; 10.18474/JES18-81
Discussion
Few publications have dealt with whitefly species that infest specific economic crops. Quaintance (1907) published a list of a number of economic plants and the whiteflies then known to colonize them (Martin 1987). Quaintance and Baker (1916) recorded 16 species including 3 new species of whiteflies feeding on Citrus. Twenty species of whiteflies belonging to seven genera have been recorded from Citrus in China (Lin 1960a, 1960b; Luo and Zhou 2000, 2001; Tang 1956; Young 1942). Patti and Rapisarda (1981) provided a discussion on the morphology and biology of whiteflies injurious to economic plants. Martin (1987) presented a key to aid in the identification of puparia (pupal cases) of 46 species of whitefly often found infesting economic plants worldwide. Worldwide, there are 24 species of whiteflies known to infest mulberry trees, Morus alba L. (Rosales: Moraceae) (David and Ragupathy 2004, Wang et al. 2014, 2016). In China, 10 species of whiteflies infest tea plants C. sinensis (Luo and Zhou 1997; Meng et al. 2017; Wang et al. 2016,). David (2012) presented details of the distribution and host plants and their influence on the morphological features of puparial cases, damage potential, and management practices of many economically important species of whiteflies which cause substantial damage to agricultural, horticultural, ornamental, and forest crops in India.
Large infestations of whiteflies may adversely affect their plant hosts by their direct feeding and loss of plant sap and by the formation of sooty mold on honeydew produced by the whiteflies, as well as by interfering with photosynthesis (Martin et al. 2000). Much work remains to be done on the whitefly pests that infest other economic crops.

Microscopic photographs of slide-mounted puparium of Aleurocanthus spiniferus. (A) Puparium, dorsal view; (B) lateral margin and the spines; (C) vasiform orifice.

Live images of Aleurolobus szechwanensis, puparium, dorsal view.

Microscopic photographs of slide-mounted puparium of A. szechwanensis. (A) Puparium, dorsal view; (B) lateral margin and the tracheal combs; (C) vasiform orifice and caudal furrow.

Live images of Aleuroplatus pectiniferus puparium. Aleuroplatus pectiniferus infesting the leaves of Myrica rubra (left); Puparium dorsal view (right), showing the transparent gelatinous wax around the case and the waxy secretion arising from the end of thoracic and caudal tracheal pores.

Microscopic photographs of slide-mounted puparium of Aleuroplatus pectiniferus. (A) Puparium, dorsal view; (B) lateral margin and the tracheal combs; (C) vasiform orifice.

Live images of Cohicaleyrodes caerulescens, puparium, dorsal view.

Microscopic photographs of slide-mounted puparium of Cohicaleyrodes caerulescens. (A) Puparium, dorsal view; (B) lateral margin; (C) vasiform orifice.

Live images of Dialeuropora brideliae, puparium, dorsal view.

Microscopic photographs of slide-mounted puparium of Dialeuropora brideliae. (A) Puparium, dorsal view; (B) lateral margin and the submarginal pores; (C) vasiform orifice.

Live images of Parabemisia myricae. (A) Puparium, dorsal view; (B) empty pupal case.

Microscopic photographs of slide-mounted puparium of P. myricae. (A) Habitus, dorsal view (parasitoid emerged); (B) lateral margin and the submarginal setae; (C) vasiform orifice and caudal furrow.
Contributor Notes