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Morphological and DNA Barcoding Evidence for Invasive Pest Thrips, Thrips parvispinus (Thripidae: Thysanoptera), Newly Recorded From India

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  • National Institute of Biological Sciences (NCBS) Tata Institute of Fundamental Research (TIFR)

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South East Asia pest thrips species, Thrips parvispinus (Karny), is a serious pest on a number of agricultural and horticultural crops in a number of plant families. Based on an integrated approach of morphology and DNA barcoding, invasion of this serious pest is reported first time from India on papaya plantations. Molecular data have corroborated with the morphological identification. Haplotyping data suggested that the Indonesia may be a probable source of invasion of this pest to India. © The Author 2015. Published by Oxford University Press on behalf of the Entomological Society of America.
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Morphological and DNA Barcoding Evidence for Invasive Pest Thrips, Thrips parvispinus
(Thripidae: Thysanoptera), Newly Recorded From India
Kaomud Tyagi, Vikas Kumar,
1
Devkant Singha, and Rajasree Chakraborty
Centre for DNA Taxonomy, Zoological Survey of India, Kolkata 700 053, West Bengal, India
1
Corresponding author, e-mail: vikaszsi77@gmail.com
Subject Editor: Roland Muehlethaler
J. Insect Sci. (2015) 15(1): 105; DOI: 10.1093/jisesa/iev087
ABSTRACT. South East Asia pest thrips species, Thrips parvispinus (Karny), is a serious pest on a number of agricultural and horticultural
crops in a number of plant families. Based on an integrated approach of morphology and DNA barcoding, invasion of this serious pest
is reported first time from India on papaya plantations. Molecular data have corroborated with the morphological identification.
Haplotyping data suggested that the Indonesia may be a probable source of invasion of this pest to India.
Key Words: invasive pest, thrips, COI, new record, papaya
Members of insect order Thysanoptera with two recognized suborders,
the Terebrantia and Tubulifera, are commonly called thrips. Out of
nearly 6,000 known species, a few have been documented as economi-
cally important, i.e., pollinator, predator, pest, and vector for plant vi-
ruses (Lewis 1997, Pappu et al. 2009, ThripsWiki 2015). As insect
vectors, thrips are sole transmitters of Tospoviruses (genus Tospovirus,
family Bunyaviridae) affecting a number of plant species in unrelated
plant families across the globe (Riley et al. 2011). The peculiarity in
tospoviruses transmission by thrips is that larvae can acquire the vi-
ruses, while adult can transmit (Whitfield et al. 2005).
Hence identification of both adults and larvae thrips is of prime impor-
tance for pest and vector management. Considering their minute size, cryp-
tic behavior, high degree of similarity of various developmental stages,
polymorphism, intraspecific variations, and complex morphology make
morphological characters of limited use to nonspecialist for accurate and
speedy identification especially those of pest and vector species (Asokan
et al. 2007). Nuclear markers like ribosomal ITS have also been used for
molecular identification in thrips (Toda and Komazaki 2002, Rugman-
Jones et al. 2006, Farris et al. 2010). However, mitochondrial COI (DNA
barcoding, Hebert et al. 2003) has been found to be the most suitable for
molecular identification within the genus Thrips (Glover et al. 2010). DNA
barcoding has been widely used in thrips identification (Rugman-Jones
et al. 2010, Kadirvel et al. 2013), development of species specific markers,
and phylogenetic analysis (Buckman et al. 2013). Integration of both mor-
phological and DNA barcoding data may be immense use for accurate spe-
cies identification and phylogenetic analysis (Mound et al. 2010).
Thrips parvispinus,amemberof“Thrips orientalis group” (Mound
2005), is a widespread pest thrips species of quarantine importance and
has been recorded from Thailand to Australia (Mound and Collins 2000)
as a serious pest on a number of unrelated plant families. It is reported on
papaya in Hawaii, greenhouse Gardenia plants in Greece, vegetable
crops like chili, green beans, potato, and eggplant from other countries
(Murai et al. 2009). Identification of an invasive pest is the first step
which unlocks the barriers for further research in planning appropriate
management strategies for the pest involved. The objective of this article
is to report invasive pest, T. parvispinus from India based on specimens
collected on papaya and elucidation of probable source of invasion.
Materials and Methods
Specimens were collected and stored in 70% ethanol at 80
C.
DNA isolation and amplification of partial fragment of mtCOI gene,
purification of amplified PCR products, and sequencing were per-
formed as earlier protocol using non-destructive techniques (Buckman
et al. 2013, Kumar et al., 2014). Voucher specimens have been retrieved
after DNA isolation and mounted in Canada balsam onto glass slides
and identified as T. parvispinus using the morphological keys (Mound
2005). The voucher specimens have been submitted to National
Zoological Collections, Zoological Survey of India, Kolkata, India.
Eleven DNA sequences generated in this study were aligned against
80 sequences of T. parvispinus from Indonesia as retrieved from
National Centre for Biotechnology Information. Further, the generated
sequences were submitted to GenBank database to acquire the acces-
sion numbers for T. parvispinus (KM485659–KM485667) and Thrips
orientalis (KM507077–KM507078). T. orientalis is used as it is a
member of the Thrips orientalis group.” Frankliniella schultzei
(KC513151) is used as outgroup. Evolutionary genetic divergences
with Kimura-2-parameter model and neighbor-joining (NJ) phyloge-
netic tree were constructed in MEGA 6.0 with 1,000 bootstrap replica-
tions (Tamura et al. 2013). Haplotyping was carried out in DNaSP, and
median joining networks were produced in Network 4.1 (Bandelt et al.
1999, Librado and Rozas 2009).
Results and Discussion
Morphological Data. Thrips parvispinus (Karny)
Isoneurothrips parvispinus Karny, 1922: 106.
Diagnosis. Body brown, head, and thorax paler than abdomen. Legs
yellow, forewings brown with pale base. Head broader than long, ocel-
lar pair III arising at the anterior margin of ocellar triangle; postocular
setae I and IV longer than III (Fig. 1). Antennae seven segmented, seg-
ments III and IV each with forked sense cone. Pronotum with two pairs
of posteroangulars setae and two pairs of posteromarginal setae
(Fig. 1). Metanotum reticulate medially and with faint internal reticules;
median setae long and placed behind the anterior margin; campaniform
sensilla absent (Fig. 2). Fore wing first and second vein with continuous
row of setae (Fig. 3). Posterior margin of tergite VIII without comb, a
few microtrichia present laterally. Abdominal sternites III–VI with
accessory setae, absent on II and VII.
Male. Body yellow. Posterior margin of tergite VIII without comb.
Abdominal sternites II–VI each with pore area.
Material examined. Thirteen females, two males, India: Karnataka:
Bangalore, 10.ii.2014, Kamlajayanti (Reg. No. 5618/H17 to 5628/H17,
5994/H17, 5998/H17, 5999/H17, 6000/H17 to 6001/H17).
V
C
The Author 2015. Published by Oxford University Press on behalf of the Entomological Society of America.
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Molecular Data
Homology search using BLAST search option resulted in 99–100%
similarity to T. parvispinus sequences from Indonesia. W e analyzed 91
partial mtCOI sequences of T. parvispinus and T. orientalis in this study.
Out of which 11 sequences were generated in this study and rest of the 80
sequences were retrieved from National Centre for Biotechnology.
Complete dataset after trimming have 604 nucleotides, which shows 89
variable sites with 87 parsimony informative sites. However, the dataset
of 89 sequence of T. parvispinus yielded only 14 variable sites out of
which 10 were parsimony informative.
Analysis of 89 sequences of T. parvispinus yielded four haplotypes
(Hap_1 to Hap_4) (Fig. 4). Hap_1 and Hap_3 were from Indonesia.
Hap_2 includes 18 sequences from India and Indonesia. Hap_4 is rep-
resented by a single specimen from India (Table 1). The data show that
there is no host-plant or geographical locality specific haplotyping. The
total number of segregating sites between four derived haplotypes
varies from 1 to 13 (Table 1). Further, out of 14 segregating sites, 11
were detected as synonymous changes and 3 as nonsynonymous
changes corresponding to nine transitions and five transversions. The
analysis of NJ tree yielded two major clades with high bootstrap sup-
port; clade I includes 89 sequences of T. parvispinus from Indonesia
and India, while clade II is represented by two sequences of T. orientalis
(Fig. 5). F. schultzei is used as outgroup. NJ tree provided here is only
to segregate two species based on the reciprocal monophyly criteria and
not to interpret phylogeny of genus Thrips.
Both morphological and molecular evidences verify that the speci-
mens collected on papaya represents T. parvispinus. The presence of
this pest species on an economically important crop plant like papaya in
India raise serious issues and is a concern for quarantine authorities.
Occurrence of T. parvispinus in other parts of India needs systematic
monitoring as it is likely to acquire pest status in future. Molecular evi-
dence for shared haplotype (H_2) between Indonesia and India indi-
cated that there is a flow of genetic material, and Indonesia may be a
probable source of invasion of this species to India. However,
Figs. 1–3. T. parvispinus, female (1) head and pronotum; (2) meso- and metanotum, (3) fore wing.
2 JOURNAL OF INSECT SCIENCE VOLUME 15
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molecular data on this species from other countries may be helpful to
trace exact route of invasion.
Acknowledgments
We are grateful to Director, Zoological Survey of India for his
encouragement and moral support and providing necessary facilities.
We are thankful to Dr. L. A. Mound (CSIRO, Australia) for his sug-
gestions, constant encouragement, and comments on earlier draft of
this manuscript. This study was supported by the SERB (Science and
Engineering Research Board), Department of Science & Technology,
Delhi, through DST Young Scientist Project entitled “Molecular
Systematics and Phylogeny of Economically Important Thrips
(Thysanoptera: Insecta) of India” (SR/FT/LS-24/2012) to K.T. and
ICAR (Indian Council of Agricultural Research) supported research
project outreach program on Management of Sucking Pests in
Horticultural Crops (ORP-SP) to V.K.
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Haplotypes 16 66 72 104 123 150 165 179 279 360 364 495 537 570
Hap_1 (Indonesia),
n ¼ 63
CAT AT T A G ATTTAT
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......... C. . . .
Hap_3 (Indonesia),
n ¼ 7
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... Moreover, analysis based on mtCOI produced fairly accurate relationships for lower taxonomic levels compared to multi-gene analysis (e.g., Wilson 2010; Boyle and Adamowicz 2015). The mtCOI sequences of T. parvispinus were first recorded by Tyagi et al. (2015), followed by Raghavendra et al. (2023) in India. Gleason et al. (2023), Palanisamy et al. (2023) and Khatun et al. (2024) recently provided mtCOI sequences for specimens from Canada, India (Tamil Nadu) and Bangladesh, respectively. ...
... Our study agrees with Raghavendra et al. (2023) that Hap1 [Hap8 in Raghavendra et al. 2023] and Hap3 [Hap7 in Raghavendra et al. 2023] are the two dominant haplotypes and are shared between countries. In addition, our study for the first time shows that Hap1 [Hap1 in Tyagi et al. 2015, Hap8 in Raghavendra et al. 2023, Hap1, Hap5, Hap10, 11 in Palanisamy et al. 2023 shares with the haplotypes from outside of Asia, including Ghana in Africa, the United States and Canada in North America. We suggest the global invasion of T. parvispinus associated with Hap1. ...
... We suggest the global invasion of T. parvispinus associated with Hap1. Tyagi et al. (2015) and Raghavendra et al. (2023) Raghavendra et al. (2023)] was found on Capsicum as well as on Carica papaya in 2014 (Tyagi et al. 2015). No host plant or geographical specificity in the haplotypes of T. parvispinus in our study concurs with Tyagi et al. (2015) and Raghavendra et al. (2023). ...
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... Thrips parvispinus (Karny) (Thysanoptera: Thripidae) is a significant quarantine pest with a global presence is native to Southeast Asian countries (Mound & Collins, 2000). Over the past two decades, its range has expanded to France, Greece, Hawaii, Mauritius, Reunion, Spain, Tanzania, the Netherlands, and India (Tyagi et al., 2015;Waterhouse, 1993;Zhang et al., 2011). In India, it was reported found on papaya from Bengaluru, Karnataka during 2015 and later on other plants like Brugmansia and Dahlia (Tyagi et al., 2015, Rachana et al., 2022Roselin et al., 2021;Nagaraju et al., 2021). ...
... Over the past two decades, its range has expanded to France, Greece, Hawaii, Mauritius, Reunion, Spain, Tanzania, the Netherlands, and India (Tyagi et al., 2015;Waterhouse, 1993;Zhang et al., 2011). In India, it was reported found on papaya from Bengaluru, Karnataka during 2015 and later on other plants like Brugmansia and Dahlia (Tyagi et al., 2015, Rachana et al., 2022Roselin et al., 2021;Nagaraju et al., 2021). This polyphagous pest affects various crops including beans, eggplant, papaya, pepper, potato, shallot, ornamental flowers and strawberry, causing substantial damage . ...
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... Thrips parvispinus (Karny) commonly called as Southeast Asia thrips is an invasive wide spread pest species first reported in India by Tyagi et al., (2015) on papaya from Bangalore. In the year 2021 an outbreak of Thrips parvispinus reported in Andhra Pradesh, Karnataka and Telangana causing 50-80 per cent yield loss in chilli crop.The species Thrips parvispinus completely dominated the common thrips species, Scirtothrips dorsalis. ...
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Aims: Management of invasive southeast Asian thrips, Thrips parvispinus under laboratory conditions. Study Design: Completely Randomized Design. Place and Duration of Study: Regional Agricultural Research Station, Guntur, Andhra Pradesh during 2023. Methodology: Bio assays study was conducted with eleven insecticides for the Management of Thrips parvispinus under laboratory conditions following leaf dip method replicated thrice. Mortality and corrected mortality were assessed at 24 and 48 hours after treatment imposition by counting the number of dead and live adults. Results: Bio assay study revealed that the insecticide broflanilide 300 DC @ 64.0 ml/ha recorded significant high percent mortality of 93.3 at 48 hours after exposure. The insecticides fluxametamide 10 EC @ 400 ml/ha, tolfenpyrad 15 EC@ 1000 ml/ha, spinoterom 11.7 SC @ 500 ml/ ha and fipronil 5 SC @1000 ml/ha were at par with broflanilide 300 DC with 90.0, 90.0, 86.7 and 86.7 percent mortality, respectively. Lowest mortality of 6.0 percent was observed in untreated control where the leaves were agitated in distilled water. The corrected mortality was calculated and the insecticides broflanilide 300 DC (92.59 %), fluxametamide 10 EC (88.9), tolfenpyrad 15 EC (89.3), spinetoram 11.7 SC (85.9) and fipronil 5 SC @400 ml/acre (85.2) recorded high corrected mortality at 48 hours of post treatment.
... In India, the first recorded occurrence of T. parvispinus on papaya (Carica papaya) was documented in Karnataka in 2015 (Tyagi et al., 2015). Originally native to Southeast Asian countries, T. parvispinus has been reported in Australia, Thailand, North America, Europe, Malaysia, and Africa, establishing itself as a global and polyphagous pest (Waterhouse, 1993;Zhang et al., 2011;Lim, 1989). ...
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The Southeast Asian thrips, Thrips parvispinus (Thysanoptera: Thripidae), has recently invaded India, posing a significant threat to the country's chilli industry. Laboratory studies were conducted at the Department of Agricultural Entomology, College of Agriculture, Raichur, to understand the growth and development of this invasive pest on chilli. The study was conducted at controlled conditions of 25 ± 1 °C and a relative humidity of 65 ± 5%. The results revealed that the mean egg incubation period was 5.74±0.34 days, with egg dimensions measuring 0.23 ± 0.01 mm in length and 0.13±0.01 mm in breadth. The first and second larval instars lasted 2.16 ± 0.24 days and 3.76±0.42 days, respectively, with a total larval duration of 5.92 ± 0.66 days. The pre-pupal stage lasted 1.83 ± 0.23 days, while the pupal stage lasted 4.17 ± 0.50 days. Adult males had an average lifespan of 5.55 ± 0.46 days, whereas adult females lived for 10.18±0.47 days. The pre-oviposition, oviposition, and post-oviposition periods were 2.51±0.24 days, 3.58 ± 0.25 days, and 4.09±0.37 days, respectively. The mean fecundity was 15.53 ± 3.46 eggs per female. This study provides the first documented report on the biological parameters of T. parvispinus in the invaded regions.
... It sucks the sap from leaves, feeds on pollen, flowers and fruits of chillies resulting in upward curling of leaves, flower drop, curled-mis shaped fruits in chillies, capsicum, and other crops. In India, it was first reported by Tyagi et al. [4], followed by, Rachana et al. [5], Roselin et al. [6] and Verghese [7] in papaya, Dalhia rosea, Brugmansia sp. and chilli respectively. Nagaraj et al. [8] and Rachana et al. [9] reported other hosts i.e. cotton, bitter gourd, chrysanthemum, watermelon, mango, tamarind and marigold. ...
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The south east Asian pest thrips, Thrips parvispinus is re corded breeding in Europe for the first time, damaging Gardenia plants in Greece. Morphological variation in this species from various Asian countries is recorded and compared to the type specimens. As a result Isoneurothrips jenseni Karny, 1925 and Thrips (Isoneurothrips) taiwanus Takahashi, 1936 are placed as synonyms of Thrips parvispinus (Karny, 1922). In contrast, Thrips compressicornis (Sakimura), a species from the Marquesa Islands of the Pacific that has previously been associated with these taxa, represents a very different species. The quarantine significance of T. parvispinus is emphasised.
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