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First incursion in Europe of bamboo white scale Kuwanaspis howardi (Hemiptera: Diaspididae), with a review of Kuwanaspis species detected in Britain

Authors:
  • Fera Science Limited, York, United Kingdom

Abstract

Kuwanaspis howardi (Cooley) (Hemiptera: Diaspididae) is a scale insect native to East Asia that feeds on bamboo. A large infestation of K. howardi was found in January 2015 at the Royal Horticultural Society’s Garden, Wisley, Surrey, on mature Fargesia nitida (Chinese Fountain Bamboo) plants that were planted in 1988. Kuwanaspis howardi has previously been intercepted by the Plant Health and Seeds Inspectorate on Phyllostachys vivax plants imported from China at a nursery in Hampshire, in April 2002. These are the first findings of this scale insect in Britain and Europe. The biology, geographical distribution and potential economic importance of K. howardi are discussed. In addition, the status of four other non-native Kuwanaspis species recorded in Britain is reviewed; one species, K. pseudoleucaspis (Kuwana) has established widely on ornamental bamboo outdoors and on indoor plantings in England since at least the 1960s. Fargesia is recorded as a new host genus for K. howardi and Drepanostachyrum, and Himalayacalamus as new host genera for K. pseudoleucaspis.
FIRST INCURSION IN EUROPE OF BAMBOO WHITE SCALE
KUWANASPIS HOWARDI (HEMIPTERA: DIASPIDIDAE), WITH
A REVIEW OF KUWANASPIS SPECIES DETECTED IN BRITAIN
C. MALUMPHY
1
&A.SALISBURY
2
1
Fera Science Limited, National Agri-Food Innovation Campus, Sand Hutton, York YO41 1LZ,
U.K. chris.malumphy@fera.co.uk
2
Entomology, Royal Horticultural Society’s Garden, Wisley, Nr Woking, Surrey GU23 6QB
andrewsalisbury@rhs.org.uk
ABSTRACT
Kuwanaspis howardi (Cooley) (Hemiptera: Diaspididae) is a scale insect native to
East Asia that feeds on bamboo. A large infestation of K. howardi was found in
January 2015 at the Royal Horticultural Society’s Garden, Wisley, Surrey, on
mature Fargesia nitida (Chinese Fountain Bamboo) plants that were planted in 1988.
Kuwanaspis howardi has previously been intercepted by the Plant Health and Seeds
Inspectorate on Phyllostachys vivax plants imported from China at a nursery in
Hampshire, in April 2002. These are the first findings of this scale insect in Britain
and Europe. The biology, geographical distribution and potential economic
importance of K. howardi are discussed. In addition, the status of four other non-
native Kuwanaspis species recorded in Britain is reviewed; one species,
K. pseudoleucaspis (Kuwana) has established widely on ornamental bamboo
outdoors and on indoor plantings in England since at least the 1960s. Fargesia
is recorded as a new host genus for K. howardi and Drepanostachyrum and
Himalayacalamus as new host genera for K. pseudoleucaspis.
INTRODUCTION
On the 25th January 2015 several stems of a single large Chinese Fountain
Bamboo (Fargesia nitida (Mitford), Poaceae: Bambusoideae) plant growing out-
doors at the Royal Horticultural Society’s Garden (RHS), Wisley, Surrey, England
(GU23 6QB) were found by W. McCutcheon (RHS Horticulturalist) to be encrusted
with an extensive population of scale insects (Plate 6, Fig. 1). The plant had been in
situ since June 1988 and appeared to be healthy despite the scale infestation. Samples
of infested stems were submitted to The Food and Environment Research Agency
(now Fera Science Limited), where the scale was identified as Kuwanaspis howardi
(Cooley) (Hemiptera: Diaspididae). This scale insect is native to East Asia where it is
recorded as a pest of bamboo (Wang, Varma & Xu, 1998). It is commonly known as
‘Bamboo White Scale’ (Miller & Davidson, 1990) or ‘Woolly Bamboo Scale’ (Gogua,
1975). This appears to be the first known incursion (FAO, 2009) of this scale insect in
Europe as it was not recorded in a recent review of the scale insects on bamboo in the
Western-Palaearctic region by U
¨lgentu
¨rk, Porcelli & Pellizzari (2014) or in the
comprehensive review of non-native scale insects established in Europe by Pellizzari
& Germain (2010). It is not recorded from Europe by ScaleNet, an online catalogue
of the scale insects of the world (Garcı
´a Morales et al., 2016), nor on EUROPHYT
(2015). In addition, scale insect specialists were contacted in France, the Netherlands
and Italy (details provided in the acknowledgments) who confirmed that they had no
unpublished records of K. howardi. A small number of adult female K. howardi had
been previously intercepted by the Plant Health and Seeds Inspectorate (PHSI) (now
part of the Animal and Plant Health Agency (APHA)) at a commercial nursery in
BR. J. ENT. NAT. HIST., 29: 2016 97
Hampshire on Chinese timber bamboo Phyllostachys vivax McClure (Poaceae)
plants imported from China, in April 2002. This finding was not considered an
‘incursion’ as there was no evidence of breeding. No statutory action was taken to
control the scale as it was considered to pose a negligible economic and
environmental risk in Britain (see Discussion).
The purpose of this communication is to report the first findings of K. howardi in
Europe and to review its geographical distribution, biology and economic
importance. In addition, the status of four other non-native Kuwanaspis species in
Britain is reviewed.
Slide mounted specimens of K. howardi are deposited at Fera.
Kuwanaspis howardi (Cooley) – Bamboo White Scale (Plate 6, Figs 1–4)
Synonymy: Chionaspis howardi Cooley 1898; Duplachionaspis howardi (Cooley);
Kuwanaspis howardi (Cooley); K. phyllostachydis Borchsenius & Hadzibejli 1950;
K. howarai (Cooley), misspelling of species epithet; K. howadi (Cooley), misspelling
of species epithet.
DETECTION AND IDENTIFICATION
The following description of the adult female and nymphs is based on observations
made of specimens found in Britain. Adult female cover white, elongate, pyriform,
oyster-shell or mussel-shell shaped, slightly convex, 1.0–1.5 mm long; exuviae (shed
skins) apical, yellow or tan (Plate 6, Fig. 2). The scales remain attached to the host
long after they have died and the older scale covers become discoloured as they are
contaminated with debris and fungi. Adult female body is elongate, yellow or orange
(Plate 6, Fig. 3); eggs and first instars (crawlers) are bright yellow (Plate 6, Fig. 4).
The scale is found primarily at the base of the stems, particularly at the nodes. Many
of the female scales had a single hymenopteran parasitoid emergence hole in the
dorsal surface, although no live parasitoids were observed and therefore the species
could not be determined. Male scales were not observed in the samples submitted to
the laboratory, which may be because male scales often form separate colonies.
During the summer these male colonies can appear ‘woolly’ or ‘fluffy’ with
abundant, dorsal, loose, wax strands (Bustshik, 1958). Male covers are smaller than
the female covers, and are elongate, white, with two median longitudinal ridge;
exuviae skin marginal and yellow.
In life, K. howardi is indistinguishable from K. pseudoleucaspis (Kuwana), a species
that is widely established outdoors in the UK, occasionally found on bamboo plants
grown indoors, and intercepted on imported bamboo plants (see details below).
Authoritative identification of the two species can only be achieved by microscopic
examination of slide-mounted teneral adult females.
Kuwanaspis howardi was originally described by Cooley from specimens taken at
quarantine in Washington D.C., USA, on imported bamboo (Cooley, 1898). A
detailed morphological description and illustration of K. howardi adult female is
provided by Balachowsky (1954), and the immature stages are described by Howell
& Tippins (1973). A detailed illustrated glossary of morphological terms for the
Diaspididae is available in Miller & Davidson (2005). There are currently 20 species
assigned to the genus Kuwanaspis and keys for the identification of adult female
Kuwanaspis species are provided by Ferris (1942), Balachowsky (1954), Chou (1982),
Hu (1982), and Suh & Hodges (2007). There is no published key for the British
98 BR. J. ENT. NAT. HIST., 29: 2016
Diaspididae but the three named species may be separated using the following
couplets:
1. With less than 10 perivulvar pores on each side of the body (scale cover very
long and slender, about 2.5 mm long, sides straight, parallel, sometimes curved,
usually found on foliage) ........... Kuwanaspis hikosani (Kuwana)
With more than 20 perivulvar pores on each side of body (scale cover shorter
and broader, about 1.5 mm long, usually found on stems) ..........2
2. Venter of abdominal segment 1 with transverse row of small-sized macroducts
.......................... Kuwanaspis howardi (Cooley)
Venter of abdominal segment 1 with macroducts restricted to marginal areas
and not forming a transverse row . . . Kuwanaspis pseudoleucaspis (Kuwana)
HOST RANGE AND BIOLOGY
Kuwanaspis howardi is oligophagous on bamboo, feeding on plants assigned to five
genera. The nomenclature of bamboo plants has changed significantly in recent
decades and here it follows The Plant List (2015). Poaceae: Arundinaria sp.; Bambusa
multiplex (Lour.) Raeusch. ex Schult.; Bambusa sp.; Fargesia nitida (Mitford) Keng f.
ex T.P.Yi (recorded here for the first time); Phragmites sp.; Phyllostachys aurea
Rivie
`re & C.Rivie
`re; P. bambusoides Siebold & Zucc.; P. dulcis McClure; P. edulis
(Carrie
`re) J.Houz.; P. nigra (Lodd. ex Lindl.) Munro; P. reticulata simonsonii
(Krasn.) Ginkul (unresolved name); P. violascens Rivie
`re & C. Rivie
`re;
P. viridiglaucescens (Carrie
`re) Rivie
`re & C.Rivie
`re; and Phyllostachys sp. (Garcı
´a
Morales et al., 2016).
In the Caucasus and Crimea K. howardi has two generations per year and
overwinters as second instar nymphs. In the first half of May females lay about 32–60
eggs over 20–50 days. Eggs hatch in 12–14 days with larvae emerging at the end of
May (Borchsenius & Hadzebejli, 1950). Bustshik (1958) observed a mass flight of
adult males in mid-July. Kuwanaspis howardi also has two generations each year in
China (Zhejiang Province) but overwinters as the fertilized adult female (Gang &
Liu, 2000). The first nymphal instars, or crawlers, are the primary dispersal stage and
move to new areas of the plant, or are dispersed by wind or animal contact.
Mortality due to abiotic factors is high in this stage. Dispersal of sessile adults and
eggs occurs through human transport of infested plant material.
The population found at Wisley in January 2015 consisted of eggs, first and
second-instar nymphs, and adult females. There were egg-laying females and first
instars actively crawling over the bamboo. No males were observed. The biology of
the scale in Britain remains unclear and requires further investigation. Three natural
enemies have been recorded attacking K. howardi: a parasitoid wasp Encarsia citrina
(Crawford) (Hymenoptera: Aphelinidae), Heather Ladybird Chilocorus bipustulatus
(L.) (Coleoptera: Coccinellidae) and predatory mite Androlaelaps casalis (Berlese)
(Mesostigmata: Laelapidae) (Garcı
´a Morales et al., 2016).
GEOGRAPHICAL DISTRIBUTION
Kuwanaspis howardi is native to East Asia and has been spread to the Caucasus
region, Middle East, North America and to the Bonin Islands in the Pacific
(Nakahara, 1982; Danzig & Pellizzari, 1998; Tao, 1999; Watson, 2002).
Orient: China; Korea. Palaearctic: Azerbaijan; China; Georgia; Iran; Japan;
Russia; and Ukraine. Nearctic: USA. Oceania: Bonin Islands.
BR. J. ENT. NAT. HIST., 29: 2016 99
ECONOMIC IMPORTANCE
Kuwanaspis howardi is recorded as a serious pest of bamboo in China (Wang,
Varma & Xu, 1998) and Georgia (Gogua, 1975), and is included in a list of diaspid
pests by Miller & Davidson (1990). Large populations may reduce host vigour, cause
chlorosis and lower the value of individual ornamental plants. The culms of the
bamboo turn white as they become encrusted with scales giving the plants an
unsightly appearance. However, it is of no economic importance in Florida (Dekle,
1977) and a large population of the scale found at one site in the UK had no
noticeable impact on the host plant.
Kuwanaspis recorded in Britain
There are no Kuwanaspis species native to Britain or Europe. Five species of
Kuwanaspis have been found in Britain on growing plants, but only three of these
have been identified to species. Two morphologically distinct species (referred to as A
and B) could not be keyed out satisfactorily and require further research. Two
species have been found breeding in Britain: K. pseudoleucaspis is fairly widespread;
K. howardi is currently only known from a single location.
Kuwanaspis hikosani Kuwana – Armoured Thread Scale
Kuwanaspis hikosani was originally described from specimens collected from
Phyllostachys bambusiodes in Japan. It is native to Asia and has been recorded from
China, Japan, Korea, and has been introduced to the U.S.A. There is an old record
of this species being found in Turkey (Bodenheimer, 1953). It is oligophagous on
bamboo (Poaceae) and is recorded feeding on: Arundinaria simonii (Carr.) Riv.;
Bambusa sp.; Phyllostachys bambusoides;P. edulis;P. nigra (Lodd. ex Lindl.) Munro;
and Sasa sp..
It has been found on two occasions in England: Hampshire, commercial nursery,
on Phyllostachys vivax imported from China, 17.iv.2002, leg. Robin Whittaker of the
PHSI (together with K. howardi); Surrey, commercial nursery, on Phyllostachys
aureosulcata McClure (new host) imported from China, 3.v.2006, leg. Justine Walker
of the PHSI.
Kuwanaspis howardi (Cooley) – Bamboo White Scale
The first known incursion and interception in Europe are reported above.
Kuwanaspis pseudoleucaspis (Kuwana) – Bamboo Diaspid
Kuwanaspis pseudoleucaspis was described from specimens collected from Bambusa
sp. in Japan (Kuwana, 1902, under the junior homonym Leucaspis bambusae). It
occurs in Europe, Asia, Central Asia, North America, Bermuda, Hawaii, and New
Zealand. In Europe and the Mediterranean region it has been recorded from Algeria,
Croatia, France, Germany, Italy, Morocco, Poland, Portugal, Russia, Slovenia,
Sweden, Turkey, Ukraine, and the United Kingdom. This species was apparently the
first exotic bamboo scale introduced into Europe (U
¨lgentu
¨rk, Porcelli & Pellizzari,
2014) and has become widely established since at least 1900 (Pellizzari & Germain,
2010). It was first collected in Britain from Arundinaria growing outdoors at the
Royal Botanic Gardens, Kew, Surrey, in 1961, although it was already well
100 BR. J. ENT. NAT. HIST., 29: 2016
established and no import connection was recorded (Boratynski & Williams, 1964).
Fera have recent records of K. pseudoleucaspis found in botanical collections in
Surrey and Devon, and under glass in South Yorkshire. It has also been intercepted
on many occasions at nurseries in England on bamboo plants imported from China,
USA and Italy. It is oligophagous on Poaceae, feeding on plants assigned to 10
genera: Arundinaria;Bambusa; Cynodon;Fargesia;Paspalum;Phyllostachys;
Pleioblastus;Sasa;Semiarundinaria; and Sinobambusa. In addition it has been
recorded by Fera in the UK on Drepanostachyrum and Himalayacalamus.Itisa
serious pest of bamboo in China (Wang, Varma & Xu, 1998), but in Europe even
high infestations do not apparently affect the vigour of the host plant (U
¨lgentu
¨rk,
Porcelli & Pellizzari, 2014).
Kuwanaspis sp. A
Intercepted on one occasion in England: Lancashire, a public garden in a college,
on Fargesia lushuiensis Hsueh & T.P.Yi imported from China, 21.ii.2007, leg. Keith
Warwick of the PHSI.
Kuwanaspis sp. B
Intercepted on one occasion in England: Hampshire, Southampton Container
Port, on P. aureosulcata imported from China, 13.iii.2015, leg. Andrew Gaunt of the
PHSI. The scale covers were exceptionally long and narrow.
DISCUSSION
This is the first published record of K. howardi being found in Britain and Europe,
and the pathway of introduction is unknown. The plants may have been infested
with K. howardi since 1988 when they were originally planted at Wisley, as they are
easily overlooked, being highly cryptic and hidden at the base of the culms. It
appears to have a negligible impact on ornamental bamboo, and can easily be
confused with K. pseudoleucaspis which is already widespread in Europe. The heavily
infested bamboo plants at the RHS Garden have been removed, not because of the
presence of the scale insect but as part of normal garden maintenance. However, it is
possible that other bamboo plants at the gardens and in the vicinity are infested at
low levels.
Kuwanaspis pseudoleucaspis has been established outdoors in southern Britain
since the 1960s but has not been recorded damaging plants, and it is considered here
that K. howardi will have a similar negligible economic and environmental impact in
Britain.
Three exotic scale insects (Balanococcus kwoni Pellizzari & Danzig, Chaetococcus
bambusae (Maskell) and Trionymus bambusae (Green)) have been found breeding on
bamboo in Britain since the 1990s (Malumphy, 2015) and there are many other
exotic species found on bamboo in Europe (U
¨lgentu
¨rk, Porcelli, & Pellizzari, 2014).
There is therefore a continual risk of further introductions of unregulated exotic
scale insects due to international trade in bamboo plants.
ACKNOWLEDGEMENTS
I thank Jean-Franc¸ ois Germain of the Laboratoire de la Sante
´des ve
´ge
´taux,
Montferrier-sur-Lez, France, Daniele Matile of the Muse
´um National d’Histoire
BR. J. ENT. NAT. HIST., 29: 2016 101
Naturelle,Paris,France and Maurice Jansen of the Netherlands Ministry of
Economic Affairs, Wageningen, for providing information on the status of
Kuwanaspis in Europe. This work was partially funded by the Department for
Environment, Food and Rural Affairs.
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Borchsenius, N. S. & Hadzibejli, Z. K. 1950. Hard scales of the genus Kuwanapis MacG.
(Homoptera, Coccoidea) injurious to bamboo in the Caucasus and the Crimea. [In
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Bustshik, T. N. 1958. A contribution to the comparative morphology of the males of the scale
insects (Homoptera, Coccoidea, Diaspididae). [In Russian] Trudy Vsesoyuznogo Entomo-
logicheskogo Obshchestva. Akademiya Nauk SSSR, Moscow 46: 162–269.
Chou, I. 1982. Monograph of the Diaspididae of China. Vol. 1. [In Chinese] Shanxi Publ. House
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Cooley, R. A. 1898. New species of Chionaspis and notes on previously known species.
Canadian Entomologist 30: 85–90.
Danzig, E. M. & Pellizzari, G. 1998. Diaspididae. 172–370. In: Koza
´r, F. (Ed.), Catalogue of
Palaearctic Coccoidea. Plant Protection Institute, Hungarian Academy of Sciences,
Budapest, Hungary. 526pp.
Dekle, G. W. 1977 (1976). Florida Armored Scale Insects. Arthropods of Florida and
Neighbouring Land Areas. Volume 3. 345pp. Florida Department of Agriculture and
Consumer Services, Division of Plant Industry.
EUROPHYT, 2015. European Union Notification System for Plant Health Interceptions.
http://ec.europa.eu/food/plant/plant_health_biosecurity/europhyt/index_en.htm [accessed
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measures 5: 1–27.
Ferris, G. F. 1942. Atlas of the scale insects of North America. (Series 4) (Volume 4) Nos. 385–
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of Bamboo Research 19: 78–80.
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´a Morales, M., Denno, B., Miller, D. R., Miller, G. L., Ben-Dov, Y. & Hardy, N. B. 2016.
ScaleNet: A Literature-based model of scale insect biology and systematics. http://
scalenet.info (Accessed: 1 January 2016).
Gogua, G. G. 1975. Results of testing Fozalon, DDVP and other organophosphorus pesticides
against Kuwanaspis howardi. [In Russian.] Subtropicheskie Kul’tury 2: 98–100.
Howell, J. O. & Tippins H. H. 1973. Immature stages of Kuwanaspis howardi (Homoptera:
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SHORT COMMUNICATION
Lundy Ciidae (Coleoptera: Tenebrionoidea), July 2014. – This note confirms the
presence of Octotemnus glabriculus (Gyllenhal) and Cis bilamellatus Wood on Lundy
and adds Cis vestitus Mellie
´to the island’s list. It reports the apparent use of Stereum
rugosum (Pers.) Fr. as a breeding host by C. vestitus.
The Ciidae is a family of obligately fungivorous beetles that typically live and
breed in the fruiting bodies of wood-rotting basidiomycetes with a poroid or smooth
hymenial surface (Orledge & Reynolds, 2005). There are 21 native and one
introduced ciid species on the British list (Orledge & Booth, 2006, 2012; see also
Orledge, 2009, for nomenclatural comments). Only two of these – the native
Octotemnus glabriculus (Gyllenhal) and the Australasian Cis bilamellatus Wood –
have been reported from Lundy (Orledge, 2012).
My visual search for ciid hosts during the BENHS recording meeting on Lundy,
5–8 July 2014, resulted in records for three ciid species exploiting basidiomycete
fruiting bodies growing on dead wood in Millcombe Valley. Specimens of each ciid
species were retained to confirm identification, and voucher specimens have been
deposited in the BENHS collections.
Two live males of O. glabriculus were found in Trametes versicolor (L.) Pila
´tona
dead fallen tree trunk at SS139441. A substantial number of small old basidiomycete
fruiting bodies on a dead standing Pinus trunk at the same location yielded ciids
subsequently determined as C. vestitus Mellie
´(four adults) and C. bilamellatus (four
adults). At SS140439 a small sample of Stereum rugosum (Pers.) Fr. fruiting bodies
growing on a dead Quercus branch was collected in the hope that subsequent
examination might reveal specimens of the Cis festivus (Panzer)/Cis vestitus species pair.
Eighteen days later two ciid larvae, but no adults, were noticed in this sample. Sixty
days after collection an unexpectedly high total of 21 C. vestitus adults, including one
teneral, were extracted, together with three ciid larvae and two ciid pupae.
BR. J. ENT. NAT. HIST., 29: 2016 103
Cis vestitus is here added to the Lundy ciid list, with the limited available evidence
suggesting that Millcombe Valley currently supports a good population of this
species. It is noteworthy that on mainland Britain S. rugosum generally yields
specimens of C. festivus rather than C. vestitus. The latter is typically found by
beating, or is recorded exploiting Stereum hirsutum (Willd.) Gray. Both ciids have
been recorded throughout England, Wales and Scotland, with by far the greater
number of records being for C. festivus (Orledge & Smith, in prep.).
In common with the larvae of the other members of the ‘Stereum ciid host-use
group’ (Orledge & Reynolds, 2005), those of C. vestitus develop in a relatively
restricted range of fungi. For C. vestitus only three fungus species – Stereum
gausapatum (Fr.) Fr., Stereum hirsutum and Peniophora quercina (Pers.) Cooke –
appear to have been recorded as breeding hosts (Koch, 1989; Reibnitz, 1999; Holter,
Milewski & Reibnitz, 1999; Orledge & Smith unpublished). The possibility that one
or two adult ciids might have been overlooked at the ‘18 day’ examination of the
Lundy S. rugosum sample must be acknowledged. However, their apparent absence
then, and the subsequent extraction of 21 adult C. vestitus, implies that C. vestitus
eggs and/or larvae were present at the time of collection and that this ciid is using
S. rugosum as a breeding host on Lundy. Certainly, the presence of a teneral adult
sixty days after collection demonstrates the ability of C. vestitus to develop in this
fungus.– GLENDA M. ORLEDGE, Department of Biology and Biochemistry,
University of Bath, Claverton Down, Bath BA2 7AY.
ACKNOWLEDGEMENTS
My grateful thanks both to the Lundy Manager, Derek Green, for his permission
for, and support of, the BENHS visit to Lundy in 2014, and to the Lundy warden,
Rebecca MacDonald, for facilitating the recording of invertebrates during this
meeting. I thank Craig Perl and Liam Crowley for field assistance on Lundy.
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PLATE 6. Fig. 1. Bamboo culm encrusted with Kuwanaspis howardi.BCrown copyright. Fig. 2. Kuwanaspis
howardi adult female scale cover. BCrown copyright. Fig. 3. Kuwanaspis howardi adult female body with scale
cover removed. BCrown copyright. Fig. 4. Kuwanaspis howardi first instar or crawler. BCrown copyright.
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