Tijdschrift voor Entomologie 161 (2018) 63–78
Aleurocanthus camelliae (Hemiptera: Aleyrodidae), a species possibly new for the European fauna of a genus in great need of revision Maurice Jansen & Francesco Porcelli
The genus Aleurocanthus Quaintance & Baker, 1914 comprises about 80 species worldwide, several of which are of economic importance for crops including Aleurocanthus woglumi and A. spiniferus. During import interceptions A. camelliae, a look-alike of the former species, has occasionally been found on imported Camellia bonsai, pot plants and shrubs in the Netherlands. Living populations of this species may be locally found on imported and traded plants in the EPPO region. In Europe all species of the genus Aleurocanthus are regulated, which makes early recognition necessary. A reliable identification is needed to take adequate measures that prevent the establishment and spread of newly intercepted species in Europe. A key is given to related genera and to developmental stages, together with an overview of field views of puparia and the main discriminating morphological and microscopic characters of both adult and pre-adult stages of three species. Since 2008, A. spiniferus is established in southern Italy and is spreading, both in Italy and in surrounding countries in the Mediterranean region, causing severe economic and ecological damage not only to the Citrus culture but because of its polyphagy to many other host plants as well. The early recognition of species newly introduced into Europe is complicated by the loss of taxonomical knowledge and the diminishing number of taxonomic workers. A revision of the genus should include the delimitation of the genus, separating it from related genera, the (re)description of the intraspecific variation of known species and the description of newly collected species by molecular techniques and morphological methods. Keywords: Hemiptera; Aleyrodidae; Aleurocanthus; Netherlands; import Maurice Jansen*, National Plant Protection Organization, NVWA, P.O. Box 9102, 6700 HC, Wageningen, the Netherlands. [email protected] Francesco Porcelli, Università degli Studi di Bari Aldo Moro, Di.S.S.P.A., Via Amendola 165/A, 70126 Bari, Italy. [email protected]
Introduction (Dubey & Ko 2012) and Australia (Martin 1999) The genus Aleurocanthus Quaintance & Baker, 1914 but no world key exists for the genus. The type ma- comprises about 80 species world-wide (Martin & terial may not always be traceable and part of the Mound 2007, Kanmiya et al. 2011, Gillespie 2012, species in collections all over the world is waiting Dubey & Ko 2012). The literature on this taxo- to be described. The morphological variety of these nomic group is scattered, there are keys to the spe- species and of the new species that may be collect- cies of countries or regions such as India (Dubey & ed in the field in the future may contribute to an Sundararaj 2004), Sri Lanka (David 1993), Taiwan amended genus concept. Sexual dimorphism, which
Tijdschrift voor Entomologie 161: 63–78, Tables 1–4, Figs 1–33. [ISSN 0040-7496]. brill.com/tve © Nederlandse Entomologische Vereniging. Published by Koninklijke Brill NV, Leiden. Published 2 April 2019. DOI 10.1163/22119434-00002075 *Corresponding author Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 1. Puparia of Aleurocanthus camelliae with exuviae of previous instars Photos: M. Jansen.
Fig. 2. Puparia of Aleurocanthus spiniferus on a leaf (left) and on a branch covered with sooty mold (right). Photos: F. Porcelli.
Fig. 3. Leaves infested by citrus blackfly, Aleurocanthus woglumi. Left photograph: Division of Plant Industry, Florida Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Bugwood.org. Right photograph: Natalie Hummel, Louisiana State University AgCenter, Bugwood.org.
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Fig. 7. Siphoninus phillyreae. Siphon-like setae. Photo: M. Jansen.
Fig. 4. Vasiform orifice of Siphoninus phillyreae with lingula (long arrow) and operculum (short arrow). Photo: M. Jansen.
Fig. 8. Siphoninus phillyreae. Not elevated vasiform ori- fice surrounded by flagellate (“normal”) setae (arrows) of S. phillyreae. Photo: M. Jansen.
Fig. 5. Aleurocanthus spiniferus. Legs of puparium ori- the EPPO-list: Aleurocanthus spiniferus and A. wo- entated towards median. glumi. Measures are obligatory if these are detected Photo: M. Jansen. on Citrus, Fortunella, Poncirus and their hybrids (Anonymous 2017a, b).
Diagnostic protocols Since 1998, the European and Mediterranean Plant Protection Organization (EPPO) has estab- lished a work programme in its region to harmonize diagnostic procedures. This programme was initi- ated to develop diagnostic protocols for the recogni- tion of all insect species listed on the EPPO A1 and A2 lists (Petter et al. 2011, Žlof et al. 2000). The practical implications for the use and compilation of these protocols are not always well understood. Ac- Fig. 6. Aleurocanthus spiniferus. Shape of spines. cording to Petter et al. (2011) protocols contain all Photo: M. Jansen. information necessary for an identification. Because Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 10. Spines and elevated vasiform orifice ofAleuro - canthus spiniferus. Fig. 9. Aleurocanthus woglumi. Shape of spines. Photo: M. Jansen. Photo: M. Jansen.
Fig. 11. Aleurocanthus woglumi. Microphotograph of Fig. 12. Aleurocanthus spiniferus. Microphotograph of the puparial margin. the puparial margin. Photo: F. Porcelli. Photo: F. Porcelli. not all detailed information may be included which Methods is needed for a reliable identification, diagnostic The taxonomy of Aleyrodidae is based on the struc- protocols are considered to be a guidance (Anony- tures of the fourth nymphal instar, which is usually mous 2017c). Experience is a prerequisite for reli- called a puparium or pupal case when empty. Table 1 able identifications and diagnostic protocols are summarizes the characteristics of pre-adult stages. no replacement. The identification process is not Puparia have many more definitive morphological necessarily linear in time, decisions are a result of structures than the adult stage, making it easier to interpretations and morphological characters are separate the genera and species. Distinctive micro- subject to interpretations which take into account scopic characteristics were studied by means of mi- the known intraspecific variation. As a consequence croscopic examination. Puparia were treated with this knowledge-driven work cannot be standardized cold 10% KOH for several days to bleach the black or harmonized. Besides, the decrease of the num- cuticle and the bleaching process was stopped when ber of experienced taxonomic workers hampers the the specimen turned light brown. It was then rinsed progress of taxonomic knowledge of this economic in ethanol 70% for several minutes for cleaning, important group of insects. Although the premises placed in glacial acetic acid for several minutes, trans- are that diagnostic protocols do not contain origi- ported to clove oil for at least 15 minutes and finally nal work, their compilation may require additional mounted in Canada balsam. Prepared slide-mounted taxonomic work, which in the case of Aleurocanthus, specimens were observed and identified by using an is presented here. interference contrast compound light microscope Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 13. Field view of a heavy infestation of Aleurocan- Fig. 14. Field view of adults of Aleurocanthus thus spiniferus. spiniferus. Photo: F. Porcelli. Photo: F. Porcelli.
Table 1. Characteristics of pre-adult stages of specimens of the genus Aleurocanthus (Anonymous 2010; Dubey, in litt. 2012). Stage Antennae Legs First (crawler) Two-segmented with the apical segment Well developed three-segmented legs elongated Second One-segmented Triangular conical shaped; usually orientated antero-lateral of rostrum Third One-segmented Orientated towards body margin (Fig. 20). Triangular, conical-shaped, bigger in size than those from second stage. Fourth (puparium) One-segmented (Fig. 19) Oriented down or towards median (Figs 5, 19).
(Olympus BX 50). Measurements were made with 3. Puparia with acute spines-like gland duct tips a micrometer eyepiece and a micrometric slide for (Figs 6, 9); posterior edge of vasiform orifice comparison. elevated (Fig. 10), operculum always cover- ing lingula; margin regularly toothed (Figs 11, Taxonomy 12), double-toothed or deflexed; cuticle colo ration very variable, may be black (Figs 1, 2), Key to the puparia of genera morphologically related dark brown, pale or dusky ��������� Aleurocanthus to Aleurocanthus Quaintance & Baker, 1917 (modi- – Puparia with siphon-like gland duct with fied after Bink-Moenen 1983, Martin 1999, Martin blunt or expanded apices (Fig. 7) ����������������� 4 et al. 2000). 4. Puparial margin smooth and not deflexed; va- 1. With subdorsal compound pores (Fig. 22), siform orifice not elevated Fig.( 8), operculum each of which may bear a central process; lin- often not covering lingula (Fig. 4) ��Siphoninus gula (Fig. 4) large, with four stout setae; each – Puparial margin toothed; dorsum with only leg with an apical claw (Fig. 23) ��������������������� four pairs of blunt siphon-like setae; vasiform �������������������������������������������������Aleurodicinae orifice slightly elevated, operculum fully occu- – Without subdorsal compound pores; lingula pying the orifice and obscuring lingual ���������� smaller, with two setae or none visible; legs ������������������������������������������������������Aleurotuba (Fig. 5) without claws ������������ (Aleyrodinae) 2 2. Dorsum of puparia with many long acute Key to some closely related black Aleurocanthus spe- spines or siphon-like setae (Fig. 10) ������������� 3 cies. Puparia may be very similar in appearance to – Dorsum of puparia without long acute spines related species including A. camelliae. Kanmiya et al. or siphon-like setae but stout normal setae (2011) summarize all morphological differences in (Fig. 8) may be present on dorsal disc or sub- puparial and adult stages between A. camelliae and margin ���������������� other genera of Aleyrodidae A. spiniferus. Future studies may reveal additional Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Material examined: (All data concern puparia and pre- adult stages.) The Netherlands: Bergsenhoek, 8.xii.2005, Camellia sinensis, pot plant, import China; leg. W. den Hartog NVWA3084246 [4 slides and additional dry ma- terial]; Bleiswijk, 30.i.2006, Camellia sp., pot plant, im- port China, leg. Willemsen, NVWA3086030; Harmelen, 5.iv.2006, Camellia sp., pot plant, import China, leg. K. Maasbach, NVWA3083366; Bergsenhoek, 24.i.2006, Camellia sinensis, pot plant, import China, leg. W. den Hartog, NVWA3084692 [additional dry material]; De Kwakel, 23.vii.2009, Camellia sp., shrub, import China, leg. W. Zijlstra, NVWA4856316; De Kwakel, 23.xi.2011, Camellia japonica, import South China, leg. A. de Wit, NVWA4869264 [2 slides, additional dry material]; De Kwakel, 23.v.2013; Camellia sp,; import China; leg. W. Zi- Fig. 16. Aleurocanthus woglumi. Female genitalia. jlstra, NVWA4165031 [3 slides, additional dry material]; Photo: M. Jansen. Harmelen, 25.ii.2016, Camellia japonica, shrub, import China, leg. W. Zijlstra, NVWA6740351 [dry material]; Bleiswijk, 24.ii.2016, Camellia sp., shrub, import China, leg. M. Koning, NVWA6508796 [dry material]; Harmel- en, 2.ii.2017, Camellia japonica, import China, leg. W. Zijlstra, NVWA33223691 [dry material]; De Kwakel, 25.i.2018, Camellia sasanqua bonsai, import China, leg. W. Zijlstra, NVWA32940461 [dry material]; Harmelen, 23.i.2018, Camellia sp., bonsai, import China, leg. M. Koning, NVWA6090529 [dry material]; De Kwakel, 6.ii.2018, Camellia sasanqua, bonsai, import China, leg. W. Zijlstra, NVWA33372484 [1 slide]; De Kwakel, 19.ii.2018, Camellia sasanqua, bonsai, import China, leg. W. Zijlstra, NVWA4311279 [9 slides].
A. camelliae, a cryptic species morphologically near to A. spiniferus, has recently been described Fig. 17. Field view of the aphid Cerataphis brasiliensis. from Japan (Kanmiya et al. 2011). Samples with Photo: J.-F. Germain. Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 18. Field view of the scale insect Parlatoria ziziphi. Photo: F. Porcelli.
Fig. 20. Aleurocanthus spiniferus, Arrows indicate the legs of the third-instar nymph, orientated towards the body margin. Photo: M. Jansen.
Fig. 19. Aleurocanthus spiniferus. Antenna (arrows) of Fig. 21. Part of female puparium of Aleurocanthus. puparium. woglumi with the third posterior-most submarginal Photo: M. Jansen. spine (arrows) which is doubled; males have a single spine in this position . Specimen on Citrus, Trinidad, Aleurocanthus puparia were intercepted in consign- 28.vii.2005, leg. P. Ram. Photo: M. Jansen. ments with Camellia originating from China since 8.xii.2005. Once, in 2017, the species was found on an unidentified Camellia plant species in the Neth- on imported Camellia plants in other European erlands on a direct import from Japan. Later on this countries. Nevertheless, it is possible that small species was found on Camellia japonica, C. sasan- populations survive on single pot plants or it may be qua and C. sinensis on pot plants in four different introduced in the rare places with Camellia exhibi- localities in the Netherlands: De Kwakel, Harmelen, tions or tea production with a fertile acid soil, suffi- Bleiswijk and Bergschenhoek. The identification was cient rainfall and a mild climate. In the northwestern confirmed by Prof. Kanmiya (personal communica- part of Turkey, a large amount of tea is produced in tion, 2 February 2018). The species had never been the Rize province. recorded elsewhere in Europe and as far we know Aleurocanthus camelliae is probably native to Tai- Aleurocanthus specimens have never been intercepted wan or China and introduced into Japan where it has Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 25. Aleurocanthus camelliae. Eye region (arrow) clearly defined, close to 3rd spine. Photo: M. Jansen.
Fig. 22. Part of the puparium of Aleurodicus dispersus with two rows of abdominal compound pores (arrow). Photo: M. Jansen.
Fig. 23. Part of puparium of Aleurodicinae: legs with a claw (arrow). Photo: M. Jansen.
Fig. 26. Aleurocanthus spiniferus. Submedian abdomi- nal spines: sockets of 2nd to 5th not in line, 2nd and 4th (right arrows) placed distal and 3rd and 5th proxi- mal (left arrows). Photo: M. Jansen.
Fig. 24. Aleurocanthus spiniferus. Eye (arrow), weakly 2011), C. japonica L. (Kanmiya et al. 2011), Eurya defined, less close to 3rd spine Photo: M. Jansen. japonica Thunb. (Kanmiya et al. 2011) and Cleyera japonica Thunb. (Kanmiya et al. 2011); Illiciaceae: Illicium anisatum L. (Yamashita et al. 2016); Ruta- been spreading throughout tea plantations ever since ceae: Zanthoxylum piperitum (L.) DC. (Yamashita 2004 (Kanmiya et al. 2011, Saito et al. 2012). et al. 2016). The present host plants are of East Asian This species is recorded from three plant families: origin and not very commonly traded, nor widely used Theaceae: Camellia sinensis (L.) Kuntze (Kanmiya as amenity trees in the public green. Local populations et al. 2011), C. sasanqua Thunb. (Kanmiya et al. on single or groups of plants are likely to survive the Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Fig. 29. Aleurocanthus camelliae. Three to five micro- scopic papillae lined outside submarginal spines. Photo: M. Jansen.
Fig. 27. Aleurocanthus camelliae. Submedian abdomi- nal spines lined up roughly linearly. Photo: M. Jansen. Fig. 30. Aleurocanthus woglumi. Three to five micro- scopic papillae (thin arrows below) lined outside each two submarginal spines (thick arrows above). Photo: M. Jansen.
A. camelliae). Whitefly damages tea production by reducing tree vigour as a result of sap loss and sooty mold and negatively affects harvest productivity by degrading tea-leaf quality (Uesugi et al. 2016, Ya- mashita et al. 2016). Farmers suffer discomfort from inhaling the adults through the mouth and nose during harvesting operations and other work in the field (Kasai et al. 2012). Yamashita et al. (2016) re- corded densities of A. camelliae adults of up to sev- eral hundred individuals on the lower surface of a Fig. 28. Aleurocanthus spiniferus. Microscopic papillae (arrow) situated between submarginal spines. leaf. In the Shizuoka prefecture, Japan, the highest Photo: M. Jansen. population densities were 123 nymphs per leaf in September. In some sites of this region the rate of parasitism by the hymenopterous parasite Encarsia Mediterranean climate. In Japan A. camelliae is sup- smithi (Silvestri, 1926) tended to remain at low lev- posed to have 2–5 generations per year (Kasai et al. els or declined with increasing population density of 2012). A. camelliae (Uesugi et al. 2016) whereas Ozawa & In China several outbreaks in tea regions have Uchiyama (2013) recorded 1.5% to 97.0% parasit- been recorded from Hainan Province, Southern ism in investigated tea fields. Differences may have China, and the middle and lower reaches of the to do with the moment of introduction of the white- Yangtze River, and outbreaks were reported all over fly: “The fields in which no parasitism was detected the tea growing areas in China in 1989 (Han & are the fields where the pest was first identified in Cui 2003 as A. spiniferus, Yamashita et al. 2016 as 2012, whereas the fieldsDownloaded where from the Brill.com09/29/2021 pest was earlier 09:03:18PM via free access
Aleurocanthus spiniferus (Quaintance, 1903) or orange spiny whitefly (OSW) Figs 2, 5, 6, 10, 12–14, 19, 20, 24, 26, 28, 32, 33
The widespread tropical species A. spiniferus is native to South and East Asia. At present it is widely dis- tributed: Asia: Bangladesh (Alam et al. 1965), Bhu tan, Brunei Darussalam (Jeffers 2009), Cambodia (Takahashi 1942), China, Democratic People’s Re Fig. 31. Aleurocanthus camelliae. Submedian abdomi- public of Korea (Jeffers 2009), India (Singh 1931), nal spines, 2nd placed distal (left arrow) and 4th placed Indonesia (Fletcher 1919; Sumatra: Weems 1974), proximal (right arrow). Iran (Jeffers 2009), Japan (Moutia 1955), Repub Photo: M. Jansen. lic of Korea, Laos (Jeffers 2009), Malaysia (Gater 1924), Marianas Islands, Mauritius (Moutia 1955), Pakistan (Gentry 1965), Philippines (Peter- son 1955), Sri Lanka (Takahashi 1956), Thailand (Takahashi 1942), Taiwan, Vietnam (Jeffers 2009); Oceania: Caroline Islands, Federated States of Micronesia (Takahashi 1956), Guam, Palau, Pa pua New Guinea (Jeffers 2009); Australia (Carver & Reid 1996); Africa: Kenya, Mauritius, Nigeria, South Africa (Van den Berg et al. 1990), Swaziland (Van de Berg & De Beer 1997), Tanzania, Uganda (Jeffers 2009); North-America: Hawaii (Anony- mous 1974). It is established and spreading in Italy (Puglia) and thus recorded from the EPPO region (Porcelli 2008, Cioffi et al. 2013, El Kenawy et al. 2016). It is a highly polyphagous insect that is threatening Euro- pean Citrus culture and also infests the wild flora. The species is known to feed on plants of at least 38 plant families. After its introduction in Italy it was reported from several new hosts (Cioffi et al. Fig. 32. Aleurocanthus spiniferus. Female puparium 2013, El Kenawy et al. 2016): Araliaceae: Hedera with 11 submarginal spines on each side. helix L., Fatsia sp.; Lauraceae: Laurus nobilis L.; Mal- Photo: M. Jansen. vaceae: Malva sp.; Moraceae: Ficus carica L., Morus alba L.; Punicaceae: Punica granatum L.; Rosaceae: effective predatory role of an alien Coccinellidae of Cydonia sp., Malus sp., Prunus armeniaca L., P. cv, the genus Delphastus Casey, 1899 found in Campan- P. domestica L., Pyracantha coccinea M.Roem.; Pyrus ia and finds a single Mt haplotype in the Italian pop- pyraster (L.) Burgsd., Pyrus sp.; Salicaceae: Salix ulations studied. This strongly suggests that OSW sp.; Vitaceae: Parthenocissus tricuspidata (Siebold & could have reached Italy either by a single invasion Zucc.) Planch., Vitis vinifera L. cv. The most recent event or by multiple invasive events from the same contribution (Nugnes et al. 2018) updates the OSW haplogroup source. The same authors (Nugnes knowledge about new host plants with Ailanthus et al., 2018) report OSW also in Campania, Liguria altissima (Mill.) Swingle, Arbutus unedo L., Citrus and Lazio and Montenegro (Radonjić et al. 2014, medica L., Citrus reticulata Blanco, Clematis vitalba Radonjić & Hrnčić 2017). The accidental find in a L., Pistacia vera L., Rosa × damascena Herrm. and single garden centre in Split, Croatia, in 2012 (Šimala R. banksiae R.Br. (Ranunculaceae, Anacardiaceae, & Masten Milek 2013) proves that the species may Simaroubaceae). This study introduces the possible easily spread to otherDownloaded countries from in Brill.com09/29/2021 the Mediterranean 09:03:18PM via free access
Aleurocanthus woglumi Ashby, 1915 or citrus blackfly Fig. 33. Aleurocanthus spiniferus. Male puparium with Figs 3, 9, 11, 15, 16, 21, 30 10 submarginal spines on each side. Photo: M. Jansen. Aleurocanthus woglumi originates from Southeast Asia and has spread throughout Asia and to the Diagnostics of A. camelliae, A. spiniferus Central Pacific, Southern Africa, Central America and A. woglumi and parts of North and South America. It is absent The puparia are very similar in appearance and have from EPPO member countries. The species is high- several characters in common: ly polyphagous and recorded from at least 80 host plant species in 40 families (Khan et al. 1985; Ser- • Cuticle dark brown to black; rano et al. 1993; Dubey & Sundararaj, 2004; Martin • Venter smooth with a transparent submarginal & Lau, 2011; Dubey & Ko, 2012; Gillespie, 2012). row of dark papillae; Citrus species are the main hosts of economic im- • Presence of a submarginal row of pointed, portance. The taxonomy and a description of the smooth and single stout spines (Fig. 6); puparium and adult are given by Caballero (1992). • The presence of a white wax fringe (Figs 1, 2).
Table 2. Microscopic differences between puparia of Aleurocanthus species independent of the sex, after Kanmiya et al. (2011), Dubey & Ko (2012) and Gillespie (2012), and observations of M. Jansen. Character A. woglumi A. camelliae A. spiniferus Number of marginal teeth per 3.5–5 (rarely 6) (Fig. 11) 6–8 in female, 7–10 in male (rarely 6) 7–11 (rarely 12) 0.1 mm/100 μm (Fig. 12) Crenulation: total number of About 130 Teeth lined with loose Teeth lined with narrow gaps marginal teeth gaps,158–196 205–242 Ratio of longest spines: length (1 : 28)–(1 : 48) (Figs 9, 21) (1 : 7)–(1 : 14) (Figs 25, 31) (1 : 9)–(1 : 17) (Figs 6, 26) of spine to basal width Width of white wax fringe to Narrow fringe: about 0.1x Intermediate: 11.2–15.8% of Wide fringe: 17.3–30% of width of black disk disk (Fig. 3) puparial width (Fig. 1) puparial width (Fig. 2) Submedian abdominal Sockets not in line: 2nd Sockets of 2nd to 5th spines Sockets not in line, 2nd and spines* placed distal and 4th placed lined up roughly linearly 4th placed distal and 3rd and proximal (Fig. 27) 5th proximal (Fig. 26) Cephalic eye spot Sharply defined Clearly defined, placed very Weakly defined, placed closer closely to 3rd cephalothoracic to 3rd submarginal spine than submarginal spine (Fig. 25) to the 2nd (Fig. 24) Microscopic papillae 3–5 duct-like papillae present 3–5 microscopic papillae Microscopic papillae outside submarginal spines lined outside submarginal (arrow) are situated between between each two spines near spines between each two submarginal spines (Fig. 28) abdomen; 2 between frontal spines (Fig. 29) spines (Fig. 30)
* Note: Care should be taken not to confuse these spines with median and submedian spines (Fig. 26), which may be double in A. spiniferus as well. In A. woglumi, those from the cephalothorax do not reach beyond the margin, except the anterior pair. Moreover, the submarginal spines are sometimes doubled (Fig. 21) only on one half of the puparium. Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Table 3. Adult characters and puparium field view of threeAleurocanthus species based on EPPO/CABI 1997, Nguyen et al. 2010, Kanmiya et al. 2011, Sullivan et al. 2011 and own observations. Adults of A. spiniferus (Fig. 14) and A. woglumi cannot be distinguished morphologically (Gyeltshen et al., 2011). Character A. woglumi A. camelliae A. spiniferus Adult Length of adult Females 1.7 mm, males 1.35 Female 1.25–1.4 mm; male Females approximately 1.7 mm 0.9–1.1 mm mm; males up to 1.33 mm Male microscopic view: Not yet described (Fig. 15). Distally upcurved on dorsal Distally straight on dorsal aedeagus lateral view margin margin Male (Fig. 15): subgenital Not yet described Deeply incised on anterior Weakly depressed on anterior plate lateral view and ventral margins margin, rather convex on ventral margin Female microscopic view No discriminating characters No discriminating characters No discriminating characters (Fig. 16). described described described Puparium field view Width of white wax fringe Narrow, about 0.1x disk; Intermediate: 0.2–0.3x disk Wide, about 0.5x disk generally half as wide as in A. (Fig. 1); relatively narrow, (Fig. 2); relatively broad, spiniferus width 11.2–15.8% of width 17.3–30.0% of puparial width puparial width
Table 4. Differences between male and female puparia of three Aleurocanthus species. A. spiniferus A. woglumi A. camelliae Female Length: 1.24 mm; Length: 0.98–1.23 mm; Length: 1.08–1.28 mm; Width: 0.71 mm; Width: 0.62–0.85 mm; Width: 0.8–1 mm; 6–7 pairs of submarginal spines, 11 submarginal spines (Fig. 31), 11 submarginal spines (Fig. 32), posterior most third pair are doubled posterior most third pair with a posterior most third pair (n = 11) (Fig. 21) (Dubey & Ko 2012) single spine rarely doubled and then 12 spines Male Length: 0.99 mm; Length: 0.65–0.85 mm; Length: 0.8 mm; Width: 0.61 mm; Width: 0.39–0.57 mm; Width: 0.58 mm; 10 pairs of submarginal spines, none of 10 submarginal spines, posterior 10 submarginal spines (Fig. 33) them are doubled (Dubey & Ko 2012) most third pair with a single spine
The microscopic differences between the puparia (rarely 12). In rare cases where six teeth per 0.1 of these three species are summarised in Table 2. mm are found, the study of several specimens The differences between adult characters and the may be of help. differences in field views of puparia ofA. spi- • Female puparia are larger than male ones. Pu- niferus and A. camelliae are given in Table 3. Giv- paria of A. spiniferus and A. camelliae do not en the apparent resemblance among the puparia differ significantly in each sex (Table 4). On of the considered species, knowledge is required the other hand, the female and male puparia about the intra-specific variation of at least the next of A. woglumi are both wider (Fig. 11) than in characters: the other species.
• The number and position of the spines. Cor- Morphological resemblance with other bett (1935) showed that specimens of A. spin- organisms iferus from Rosa sp. possess six pairs of sub- Depending on the experience of the diagnostician marginal spines posterior to the transverse other Aleurocanthus species may be confused with moulting suture, all arising in different places, A. spiniferus or A. woglumi. Kanmiya et al. (2011) whereas specimens from Citrus spp. show noted that, compared to A. spiniferus and A. camelliae: seven pairs of spines, the four and fifth pairs being close together. In females of A. woglumi • Aleurocanthus hibisci Corbett, 1935 has longer the third posterior-most pair of the submar- cephalothoracic spines and closely arranged ginal row of spines is usually doubled, whereas 9th and 10th submarginal spines. males have a single spine in that position. • Aleurocanthus gordoniae Takahashi, 1941 has a • The number of marginal teeth per 0.1 mm perfectly circular vasiform orifice and areduced (=100 μm) (Figs 11, 12) varies: within popula- number of abdominal spines: 8 abdominal tions of A. woglumi from 3.5 to 5 (rarely 6) pairs (2 submedian + 6 subdorsal) whereas and within A. spiniferus from (rarely 6) 7 to 11 A. spiniferus and A. camelliae have 10 pairs. Downloaded from Brill.com09/29/2021 09:03:18PM via free access
Discussion fication of Aleurocanthus species is always tentative Although the presence of spines is a shared common and needs confirmation by a specialist. character of the genus Aleurocanthus, the variation of the shape and the number of spines may be an indication for distinguishing several genera. The Acknowledgements species which are ascribed to the genus (e.g., Evans We acknowledge the help of Dr Anil Kumar Dubey 2008 and others) may partly include synonyms and of the Indian Agricultural Research Institute, New already collected specimens may include new spe- Delhi (India) for his valuable textual suggestions. cies. Recent studies have revealed that a considerable Many thanks also to the members of the EPPO- number of species of the genus Aleurocanthus are Panel for Diagnostics in Entomology and the not yet described (e.g., Dubey & Ko 2012, Gillespie EPPO-Secretariat (Paris) who gave suggestions to 2012 and unpublished results). A lot of material col- improve the text. We also wish to thank Dr Ken- lected by various workers is waiting for identifica- kichi Kanmiya, Institute of Comparative Studies tion or is present in various collections of museums of International Cultures and Societies, Kurume, and research institutes. As in other Aleyrodid gen- Fukuoka, Japan, for his confirmation of the iden- era, host-induced variations are observed. These are tification ofAleurocanthus camelliae. Jean Francois changes in the morphological structures of puparia Germain (Anses, Lab de la Santé des Végétaux, depending on the host plant on which they develop. Unité d’Entomologie et Plantes Invasives, CBGP, This complicates species description and species Montferrier-sur-Lez, France) is acknowledged for identification. the pictures of Cerataphis brasiliensis. With the help Therefore, newly discovered characters will con- of Ernst Neering, Wageningen, the Netherlands, tribute to an improvement of the species descriptions it was possible to study adults and puparia of A. and a better discrimination between species and spe- woglumi. The Florida Division of Plant Industry, cies groups. Single species or groups of species within Florida Department of Agriculture and Consumer the genus may even actually represent different gen- Services, Bugwood.org, provided pictures of puparia era. Much of the collected material now available of Aleurocanthus woglumi on the plant. Thanks also in collections of workers, museums and research to Natalie Hummel, Louisiana State University Ag- institutes all over the world, is waiting for identifica- Center, Bugwood.org, for permission to use the pic- tion. The study of this material and of the natural ture of puparia of Aleurocanthus woglumi. Finally, we occurrence, together with field-oriented ecological would like to acknowledge the Puglia Region grant studies may result in the recognition and description CoBIAs/AGG2016 - Apulia Region - Controllo Bio- of new and cryptic species. logico per Incremento contro A. spiniferus. These challenges can only be solved by combining all available data. Studying morphological structures in relation to their intraspecific variation may be a challenge as the making of a good slide of a bleached References specimen is already a challenge in itself. Support of Alam, M.Z., A. Ahmed, S. Alam & M.A. Islam, 1965. A re- molecular tools such as barcoding, sequencing and view of research Division of Entomology (1947–1964). phylogenetic studies and the study of type mate- — Dacca Agricultural Information Service & East Pak- rial are needed to clarify the taxonomy and status of istan Agricultural Research Institute, pp. 1–272. species of this genus. The quality of older type mate- Anonymous, 1974. New United States records — orange rial, which in the case of Aleurocanthus is present in spiny blackfly,Aleurocanthus spiniferus (Quaintance). various countries, may complicate the study as well. — Hawaii Co-operative Economic Insect Report 24: For single species, transplantation experiments may 585 (R.A.E. Services A 1975 Vol. 63 No 781). be needed to elucidate the relation of a certain white- Anonymous, 2000. Council Directive 2000/29/EG of 8 fly with various plant hosts. New species descriptions May 2000 on protective measures against the intro- based on new or additional characters and a critical duction into the Community of organisms harmful to plants or plant products and against their spread within consideration of already existing species descriptions the Community + Annexes I–IX. — Official Journal of are needed. Normally the puparium is used for iden- the European Community L 169, 43: 1–112. tification purposes but in such a study all instars are Anonymous, 2010. Identification d’aleurodes d’intérêt of importance. agronomique. Methode officielle d’analyse 0007. — Most species live in the Oriental Region and the Ministère de l’Alimentation de l’Agriculture et de la majority of species can be distinguished based on Pêche, 1–23. small differences in the number of spines (Dubey & Anonymous, 2017a. EPPO A1 List of pests recommended Ko 2012). As there is no key available for all the de- for regulation as quarantine pests(version 2017-09). — scribed Aleurocanthus species of the world or even for Available at: https://www.eppo.int/QUARANTINE/ the species of major geographical regions, an identi- listA1.htm [accessed 9 March 2018]. Downloaded from Brill.com09/29/2021 09:03:18PM via free access
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