Ceroplastes cirripediformis Comstock, 1881

Joshi, Sunil, Bhaskar, Haseena, Poon, V. S. Aashiq, Mala, B. R. Jayanthi, Jayanthi, P. D. Kamala, Pai, Sachin G., Thite, Sachin V., Sood, Ajay K., Kedar, Santosh C., Sridhar, V., Deepthy, K. B., Navik, Omprakash & Rachana, R. R., 2021, Occurrence and spread of Ceroplastes cirripediformis Comstock (Hemiptera Coccomorpha: Coccidae) in India, Zootaxa 5039 (4), pp. 561-570 : 562-568

publication ID	https://doi.org/ 10.11646/zootaxa.5039.4.7
publication LSID	lsid:zoobank.org:pub:B09C6289-2C7F-437D-B687-87746E5FDCEE
persistent identifier	https://treatment.plazi.org/id/03F587A3-FF9D-FFCF-FF00-F89BA6A5C5DD
treatment provided by	Plazi
scientific name	Ceroplastes cirripediformis Comstock, 1881
status

Treatment

Ceroplastes cirripediformis Comstock, 1881 View in CoL

Material examined with states given in chronological order of invasion:

INDIA: Karnataka: Bengaluru, Bhuvaneshwari Nagar, 12.9231° N, 77.5482° E, 15 ♀♀ on Passiflora sp. (Passifloraceae) , 11.iii.2009, Sunil Joshi coll.; Sanjay Nagar, 13.0369° N, 77.5785° E, 10 ♀♀ on Annona muricata L. ( Annonaceae ), 1.v.2010, Sunil Joshi coll.; Anand Nagar, 13.0313° N, 77.5913° E, 10 ♀♀ on Alternanthera sp. (Amaranthaceae) , 5.vi.2012, Sunil Joshi coll.; Hebbal, 13.0354° N, 77.5988° E, 15 ♀♀ on Pseudoeranthemum artopurpureum Guillaumin (Acanthaceae) , 3.iv.2015, Sunil Joshi coll.; Amrutha Nagar, 13.0585° N, 77.5970° E, 5 ♀♀ on Epipremnum aureum (Linden & André) G.S. Bunting (Araceae) , 28.iii.2015, Sunil Joshi coll.; Bhuvaneshwari Nagar, 12.9231° N, 77.5482° E, 5 ♀♀ on Impatiens sp. (Balsaminaceae) , 11.iii.2016, Sunil Joshi coll.; Ashwath Nagar, 13.0200° N, 77.5763° E, 6 ♀♀ on Nerium oleander L. ( Apocynaceae ), 12.vii.2016, Sunil Joshi coll.; Devanahalli, 13.2437° N, 77.7172° E, 6 ♀♀ on Crossandra infundibuliformis L. ( Acanthaceae ), 12.iii.2017, Srinivasa coll.; Hebbal, 13.0294° N, 77.5850° E, 2 ♀♀ on Impatiens sp. (Balsaminaceae) , 27.ii.2017, Harish coll.; Hebbal, Veterinary College, 13.0294° N, 77.5850° E, 7 ♀♀ on Jacaranda mimosifolia D. Don (Bignoniaceae) , 15.iii.2017, Harish coll.; same location, 4 ♀♀ on Tabebuia sp. (Bignoniaceae) , 15.iii.2017, Harish coll.; same location, 9 ♀♀ on Tecoma stans (L.) Juss. ex Kunth ( Bignoniaceae ), 15.iii.2017, Harish coll.; Bhuvaneshwari Nagar, 12.9231° N, 77.5482° E, 5 ♀♀ on Pelargonium sp. (Geraniaceae) , 8.ix.2017, Sunil Joshi coll.; same location, 15 ♀♀ on Plectranthus prostratus Gürke (Geraniaceae) , 11.ix.2017, Sunil Joshi coll.; Devanahalli, 13.2437° N, 77.7172° E, 12 ♀♀ on Clerodendrum sp. (Lamiaceae) , 19.ix.2017, Harish coll.; same location, 20 ♀♀ on Hibiscus rosa-sinensis L. ( Malvaceae ), 19.ix.2017, Harish coll.; same location, 10 ♀♀ on Ficus sp. (Moraceae) , 19.ix.2017, Harish coll.; Ramanagara, 12.7209° N, 77.2799° E, 20 ♀♀ on Eugenia sp. (Myrtaceae) , 2.i.2018, Srinivasa coll.; same location, 7 ♀♀ on Syzigium sp. (Myrtaceae) , 2.i.2018, Srinivasa coll.; Yelhanka, 13.0801° N, 77.5785° E, 4 ♀♀ on Mangifera indica L. ( Anacardiaceae ), 15.viii.2018, Sunil Joshi coll.; Bhuvaneshwari Nagar, 12.9231° N, 77.5482° E, 15 ♀♀ on Philodendron sp. (Araceae) , 15.viii.2018, Sunil Joshi coll.; Bengaluru North, Hesaraghatta, 13.1500° N, 77.4900° E, 3 ♀♀ on Psidium guajava L. ( Myrtaceae ), 25.ix.2019, Jayanthi Mala coll.; same locality, 5 ♀♀ on Chrysanthemum sp. (Asteraceae) , 22.vii.2021, V. Sridhar coll.; Hebbal, Veterinary college campus, 13.0294° N, 77.5850° E, 4 ♀♀ on Pseudoeranthemum artopurpureum Guillaumin (Acanthaceae) , 11.viii. 2021, Omprakash Navik coll.; Bengaluru, Kodigehalli, Ganesh Nagar Layout, 13.0697° N, 77.5788° E, 6 ♀♀ on Ipomoea nil (L.) Roth. ( Convolvulaceae ), 27.vii.2021, Rachana coll.

Tamil Nadu: Tandigudi, 10.3093° N, 77.6435° E, 6 ♀♀ on Euonymus angulatus Wight (Celastraceae) , 6.vi.2017, Sunil Joshi coll.; same location, 11 ♀♀ on Terminalia catappa L. ( Combretaceae ), 7.vi.2017, Sunil Joshi coll.; same location, 10.3093° N, 77.6435° E, 9 ♀♀ on Cycas sp. (Cycadaceae) , 7.vi.2017, Sunil Joshi coll.; same location, 5 ♀♀ on Codiaeum sp. (Euphorbiaceae) , 8.vi.2017, Sunil Joshi coll.; same location, 5 ♀♀ on Euphorbia hirta L. ( Euphorbiaceae ), 8.vi.2017, Sunil Joshi coll.

Maharashtra: Amaravati, Ganesh colony: 20.9211° N, 77.7464° E, 6 ♀♀ on Punica granatum L. ( Punicaceae ), 6.ii.2018, Sunil Joshi coll.; same location, 9 ♀♀ on Ixora sp. (Rubiaceae) , 9.ii.2018, Sunil Joshi coll.; same location, 19 ♀♀ on Gardenia jasminoides J. Ellis (Rubiaceae) , 9.ii.2018, Sunil Joshi coll.; Shegaon, 20.7930° N, 76.6910° E, 6 ♀♀ on Hamelia patens Jacq. (Rubiaceae) , 15.v.2018, Sunil Joshi coll.; same location, 16 ♀♀ on Citrus limon L. ( Rutaceae ), 16.v.2018, Sunil Joshi coll.; same location, 5 ♀♀ on Manilkara zapota (L.) P. Royen ( Sapotaceae ), 17.v.2018, Sunil Joshi coll.; same location, 10 ♀♀ on Solanum nigrum L. ( Solanaceae ), 17.v.2018, Sunil Joshi coll.; Pandharpur, 17.6806° N, 75.3155° E, 12 ♀♀ on Pyrostegia venusta Miers (Bignoniaceae) , 14.i.2021, Sachin Thite coll.

Gujarat: Talala: 21.0556° N, 70.5295° E, 5 ♀♀ on Pseudoeranthemum artopurpureum Guillaumin (Acanthaceae) , 5.xii.2018, Sunil Joshi coll.

Kerala: Thrissur: Cherpu, 10.4380° N, 76.1476° E, 5 ♀♀ on Citharexylum spinosum L. ( Verbenaceae ), 11.iv.2019, Haseena Bhaskar coll.; Nellikunnu, 10.5161° N, 76.2361° E, 7 ♀♀ on Malpighia emarginata DC. (Malpighiaceae) , 15.vi.2019, Haseena Bhaskar coll.; same location, 9 ♀♀ Lannea coromandelica (Houtt.) Merr. (Anacardiaceae) , 12.x.2019, Haseena Bhaskar coll.; Thrissur, 10.5276° N, 76.2144° E, 3 ♀♀ on Nyctanthes arbortristis L. ( Oleaceae ), 10.i.2020, Sachin G. Pai coll.; Idukki, Ramakkalmedu, 9.7966° N, 77.2271° E, 15 ♀♀ on Passiflora edulis Sims. (Passifloraceae) , 12.x.2019, Haseena Bhaskar coll.; Palakkad, Nelliampathy, 10.5348° N, 76.6928° E, 17 ♀♀ on Passiflora edulis Sims. (Passifloraceae) , 5.ii.20, Haseena Bhaskar coll.

Himachal Pradesh: Palampur, 32.1109° N, 76.5363° E, 5 ♀♀ on Duranta erecta L. ( Verbenaceae ), 10.vii.2020, Ajay Sood coll.

Uttar Pradesh: Lucknow: 26.2647° N, 82.0727° E, 12 ♀♀ on Cestrum diurnum L. ( Solanaceae ), 2.vii.2021, Santosh Kedar coll.; 26.2647° N, 82.0727° E, 9 ♀♀ on Cannabis sativa L. ( Cannabaceae ), 2.vii.2021, Santosh Kedar coll.

Appearance in life ( Fig. 1 View FIGURE 1 ): Eggs gleaming bright orange ( Fig. 1K View FIGURE 1 ). First-instar nymph lacking wet wax, possessing only dorsal dry white wax which has a narrow horizontal slit ( Fig. 1L View FIGURE 1 ). Second-instar nymph with developing brown nucleus ( Fig. 1M View FIGURE 1 ). Adult female with wet wax a dirty yellowish white ( Fig. 1N View FIGURE 1 ), with dorsal heptagonal plate, seven lateral plates, dark brown nuclei, cephalic filaments trifurcate, anterolateral and posterolateral filaments simple, posterolateral filaments and caudal filaments bifurcate, white stigmatic bands near both pairs of spiracles, anterior bands directed dorsally; body length 3.8 mm (range 2.6–4.1), width 2.4 mm (range 1.8–3.2), height 2.0 mm (range 0.8–3.2). The scale insect was collected on a wide range of host plants infesting upper and lower leaf surfaces, stems, tendrils, collar region, etc. ( Fig. 1A View FIGURE 1 to J).

Appearance of slide-mounted adult female ( Fig. 2 View FIGURE 2 ): Body circular to elliptical, 3.8–5.9 mm long, 0.5–5.0 mm wide.

Dorsum. Derm entirely membranous except for heavily sclerotized caudal process ( Fig. 2A View FIGURE 2 ). Caudal process short, wider than long, 0.3–0.4 mm long, 0.4–0.6 mm wide. Derm with eight clear areas, without setae. Dorsal setae mainly capitate ( Fig. 2B View FIGURE 2 ), each 2.9–8.8 µm long, mostly slightly longer than width of basal socket, which is 4–5 µm wide, very sparse throughout the dorsum but more numerous on marginal areas. Dorsal pores ( Fig. 2C View FIGURE 2 ): loculate microducts of the intermediate type, those with 2 or 3 satellite loculi most abundant and widespread; those with 1 satellite loculus most frequent in submarginal region, otherwise scarce; those with 4 satellite loculi scarce; each microduct surrounded by a small clear area, forming a spotted derm pattern. Simple microducts not seen on any of the mounted specimens. Preopercular pores forming a transverse band of 9–16 pores. Anal plates ( Fig. 2D View FIGURE 2 ) little longer than wide, each plate 100–105 µm long, combined width 95–98 µm; each plate with 3 large dorsal setae measuring 38–40 µm, 41–45 µm and 35–37 µm; and one smaller apical seta, 10–13 µm long. Anal fold ( Fig. 2E View FIGURE 2 ) with four small anterior margin setae, each measuring 8–10 µm, and one lateral margin seta, 15–17 µm long. Anal tube 160–170 µm long, 1.6x longer than anal plate.

Margin. Marginal setae ( Fig. 2F View FIGURE 2 ) each about 2 or more times longer than submarginal setae, length 23–30 µm; with 5–7 between eyespots and, on each side, 1–5 between eyespots and anterior stigmatic setae, 2 or 3 between stigmatic clefts, and about 5 or 6 on each side of abdomen; anal lobes each with 3–6 larger setae, each 40–50 µm long. Stigmatic setae ( Fig. 2G View FIGURE 2 ) conical to lanceolate, each cleft with a group of 27–59 setae in 3 or 4 irregular rows, but group narrow and extending out of cleft along margin; most stigmatic setae each 16–22 µm long but with about 3–5 larger setae near centre of each group, each 24–31 µm long and 25–30 µm wide at base. Eyespots each 27–29 µm wide.

Venter. Derm entirely membranous. Pregenital disc-pores ( Fig. 2H View FIGURE 2 ) abundant around genital opening (segment VII) and across preceding segments, distributed as follows: mesothorax with 2 or 3 pairs medially and 2–4 at the base of each coxa; metathorax, 1 or 2 pairs medially and 1–3 near base of each coxa; abdominal segment I, 0–2 pairs; II, 2–4 pairs, III, 2–5 pairs, IV, 10–15 pairs; area from segment V to genital fold with several pairs. Spiracular pores ( Fig. 2I View FIGURE 2 ), each with five loculi, in a band of 100–200 pores between spiracle and margin; each band with few pores extending medially past peritreme. Ventral microducts normal, cruciform ( Fig. 2J View FIGURE 2 ), seen mostly on submarginal area of head and thorax. Ventral tubular ducts ( Fig. 2K View FIGURE 2 ) each with a long inner ductule and a small glandular end; in a group of 11–26 in cephalic region and 17–33 medially and mediolaterally on posterior abdominal segments. Ventral setae: with a pair of preopercular setae, each 50–56 µm long; submarginal setae about twice as frequent as marginal setae, each 6–9 µm long ( Fig. 2L View FIGURE 2 ). Antennae ( Fig. 2M View FIGURE 2 ) each with 7 segments; usually with 1 or 2 distinct pseudoarticulations in segment III; each antenna 200–320 µm long. Clypeolabral shield about 150–190 µm long and 110–150 µm wide. Spiracles ( Fig. 2N View FIGURE 2 ): width of each anterior peritreme 50–60 µm, that of each posterior peritreme 55–65 µm. Legs ( Fig. 2O View FIGURE 2 ) well developed, each with a distinct tibio-tarsal articulatory sclerosis; each claw without a denticle; claw digitules both broad. Dimensions of metathoracic legs (in µm): coxa 40–130; trochanter+femur 92–160; tibia 85–120; tarsus 55–77, and claw 15–25. Tarsal digitules 40–42 µm, claw digitules 30–38 µm long.

Interspecific comparisons: Hodgson and Peronti (2012) stated that C. cirripediformis is similar to C. sinensis Del Guercio ; however, C. sinensis is not known to occur in India. Within the area under study, C. cirripediformis is most similar to C. rusci (Linnaeus) .

In life, C. cirripediformis can be separated from C. rusci (characters of C. rusci given in parentheses) by its: (i) dirty yellow wet wax (dull pinkish white); (ii) heptagonal dorsal plate surrounded by seven lateral plates (octagonal domed dorsal plate surrounded by eight quadrate plates); (iii) diffused brown dorsal nucleus (very well-defined, red dish dorsal nucleus with a depressed margin); (iv) without darker coloration at the junction of marginal area of plates (reddish at the junction of marginal area of plates); (v) without fine radiating lines at dorsal plate margin (usually with numerous fine radiating pinkish lines).

When slide mounted, C. cirripediformis can be separated from C. rusci (characters of C. rusci given in parentheses) because of its (i) seven antennal segments (six segments); (ii) claw without a denticle (usually with a denticle); (iii) capitate dorsal setae (bluntly spinose dorsal setae); (iv) with 5–7 marginal setae between the eye spots (6–15 marginal setae between the eye spots).

Distribution, host plants, damage and associated insects: The earliest collection of C. cirripediformis in India was in 2009 on a home-grown passion fruit vine, but authoritative identification, after slide-mounting several specimens, was made only in 2017 and the pest was officially documented in India during 2018 (ICAR - NBAIR, 2019). The species was found to be spreading slowly to different geographical areas in India. Since 2009, this pest has been collected from 46 host plants belonging to 30 families from seven Indian states viz., Karnataka, Kerala, Tamil Nadu, Maharashtra, Gujarat, Himachal Pradesh and Uttar Pradesh. Ceroplastes cirripediformis is widely distributed in the Nearctic, Neotropical, Palaearctic, Indo-Australian and Oriental regions, with distribution records from 32 countries on different continents ( García Morales et al. 2016). Wang et al. (2020) evaluated the effects of climatic variables on distribution patterns of C. cirripediformis , produced a global risk map and predicted its spread to more regions, including India; however, our collection data indicate that the pest was present in India well before it was recorded in China ( Li et al. 2018). Recently, the DNA barcode of this species was submitted to the NCBI gen bank (accession number: MW988113 View Materials from Kerala, India) and a kind of pest alert was issued in a local newspaper ( Muringatheri, 2021).

Out of 46 recorded host plants, 25 were ornamentals grown in home yards, 13 fruit crops, 3 weeds, 3 medicinal and 2 avenue trees, indicating the adaptability of this scale to establish and breed in different ecosystems. It was recorded for the first time on two plant families ( Oleaceae and Punicaceae ) and there were 13 new host plants recorded [ Cannabis sativa L., Cestrum diurnum L., Clitoria ternatea L., Crossandra infundibuliformis L., Epipremnum aureum (Linden & André) G.S. Bunting , Ipomoea nil (L.) Roth., Ixora sp. , Nyctanthes arbor-tristis L., Plectranthus prostates Gürke , Punica granatum L., Pyrostegia venusta Miers , Tecoma stans (L.) Juss. Ex Kunth and Terminalia catappa L.]. The most serious damage in southern parts of India was found in Kerala at Idukki, Ramakkalmedu, where complete drying and death of the two-year-old passion fruit crop occurred over fifteen acres; while in northern India (in Lucknow, Uttar Pradesh), 500 m 2 plots of C. diurum and C. sativa suffered crop losses of 78 and 22 per cent, respectively. Four ant species viz., Oecophylla smaragdina Fabricius , Camponotus compressus (Fabricius) , Tapinoma melanocephalum (Fabricius) and Paratrechina sp. ( Hymenoptera : Formicidae ) were found attending the scale insect. The hymenopterans viz., Coccophagus sp. (Aphelinidae) , Metaphycus sp. (Encyrtidae) , Tetrastichus sp. (Eulophidae) and Scutellista sp. (Pteromalidae) were found parasitizing this scale insect at different locations, however the percent parasitism was always insignificant.

Management: At present the main objective should be prevention of further spread of this scale insect to other host plants, through the complete destruction of infested plant parts; constant monitoring of home yard gardens, parks and fruit orchards for new infestations; recording and use of natural enemies, and use of organic chemicals to control at heavily infested sites.

Discussion: During the last few years, India has experienced several introductions of sternorrhynchan species, of which mealybugs viz., Phenacoccus solenopsis Tinsley ( Hodgson et al. 2008) , Paracoccus marginatus Williams and Granara de Willink ( Muniappan et al. 2008) and Phenacoccus manihoti Matile Ferrero (Joshi et al. 2020) demonstrated rapid population growth after introduction, while other species viz., Phenacoccus madeirensis Green ( Shylesha & Joshi, 2012) , Pseudococcus jackbeardsleyi Gimpel and Miller ( Mani et al. 2013) , and the soft scale insects viz., Trijuba oculata (Brain) ( Joshi & Rameshkumar, 2017) and Pulvinaria urbicola Cockerell (Joshi, 2017) are maintaining moderate population sizes on several or limited hosts for years after their first introductions. In contrast to these, there are few species of sternorrhynchans like the aphid, Wahlgreniella nervata (Gillette) ( Joshi et al. 2014) and soft scales like Kilifia acuminata (Signoret) and Protopulvinaria longivalvata Green ( Joshi & Rameshkumar, 2017) which were recorded only a few times after their first reports in India. On the other hand, there are other species of introduced soft scales that seem to be self-restricted, like Hemilecanium theobromae Newstead [which is restricted to a relatively unimportant host plant ( Joshi & Kondo, 2020)] and Platylecanium nepalense Takagi [which is confined to a particular geographic area (Joshi & Firake, 2019)]. The invasion of C. cirripediformis seems to have gone through a lag phase, when it persisted in low numbers (since 2009) for about a decade, and now its population is exploding, expanding its host and geographical ranges. Lag times in biological invasions have been studied well in some plant and animal species ( Crooks & Soulé, 1999; Crooks, 2005; Kelly et al. 2021) that have demonstrated similar population changes after their introductions. The establishment of this scale insect warrants special attention in India as it is a potentially damaging plant pest and has a broad host range across many plant families and including many crops.

Key to adult females of the Indian species of Ceroplastes Gray. The View in CoL key does not necessarily reflect phylogenetic relationships.

Note: Although C. stipulaeformis has been recorded from India, it could not be included in the key as its original description by Haworth (1812) (probably inadequate) is not available and the description in De Lotto (1971) is very scant and does not provide any precise morphological characters for separating it from other species of Ceroplastes View in CoL . Slides of C. ajmerensis View in CoL and C. alami View in CoL , mounted and described by Avasthi and Shafee from the Department of Zoology, Aligarh Muslim University, Aligarh, Uttar Pradesh, India were obtained on loan for study but were found to have deteriorated; it was not possible to remount them, so their morphological character states were taken from Avasthi and Shafee (1986). All the remaining species were studied using slide-mounted specimens.

1(0) Ventral tubular ducts absent............................................................................. 2

- Ventral tubular ducts present............................................................................ 3

2(1) Interantennal setae numbering 2 pairs; legs reduced; dorsal tubular ducts present; anogenital fold with 3 pairs of anterior margin setae................................................................................. C. rubens Maskell View in CoL

- Interantennal setae numbering 7‒10 or more pairs; legs well developed; dorsal tubular ducts absent; anogenital fold without anterior margin setae................................................................ C. stellifer (Westwood) View in CoL

3(1) Ventral tubular ducts restricted to susbmarginal bands........................................................ 4

- Ventral tubular ducts dispersed on venter.................................................................. 5

4 (3) Tibio-tarsal sclerosis present; antenna 7 segmented; dorsum without quadrilocular pores; ventral tubular ducts each with long inner ductule............................................................... C. ajmerensis Avasthi & Shafee View in CoL

- Tibio-tarsal sclerosis absent; antenna 6 segmented; dorsum with quadrilocular pores; ventral tubular ducts each with greatly swollen, short inner ductule......................................................... .. C. floridensis Comstock View in CoL

5(3) Dorsal clear areas numbering 9 or more.................................................................... 6

- Dorsal clear areas numbering 8 or fewer................................................................... 7

6(5) Dorsum with 11 clear areas; claw digitules unequal, with 1 broad and other slightly narrower; stigmatic setae restricted to cleft; multilocular disc pores absent from near procoxae; with fewer than 15 marginal setae between anterior stigmatic furrows.................................................................................... C. ceriferus (Fabricius) View in CoL

- Dorsum with 9 clear areas; claw digitules equally broad; stigmatic setae spreading out of cleft onto margin; multilocular disc pores present near procoxa; around 40 marginal setae present between anterior stigmatic furrows.. C. pseudoceriferus Green View in CoL

7(5) Caudal process well developed, becoming very long and broad at base at maturity; most stigmatic setae with a pronounced flange around base; claw digitules dissimilar.............................................. C. destructor Newstead View in CoL

- Caudal process variable; stigmatic setae without a pronounced flange around base; claw digitules similar............... 8

8(7) Antenna 7 segmented; claw without a denticle; dorsal setae capitate; multilocular disc pores present on derm near each coxa.............................................................................. C. cirripediformis Comstock View in CoL

- Antenna 6 segmented; claw with a denticle; dorsal setae not capitate; multilocular disc pores absent from thoracic segments. ................................................................................................... 9

9(8) Dorsal setae bluntly spinose, margins almost parallel to slightly convergent with a very blunt apex, quite frequent throughout; dorsal dendritic microducts present; anterior margin of anogenital fold with 3 pairs of long setae; spiracular pores each with 5 loculi............................................................................... C. rusci (Linnaeus)

- Dorsal setae small and thick with bluntly pointed or truncate apices, sparse; dorsal dendritic microducts absent; anterior margin of anogenital fold with 4 pairs of setae; spiracular pores each with 5‒7 loculi................ C. alami Avasthi & Shafee View in CoL