First record of the lawn chinch bug Blissus insularis Barber (Hemiptera: Blissidae) in Europe
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Phytoparasitica (2021) 49:539–545
https://doi.org/10.1007/s12600-021-00903-1
SHORT COMMUNICATION
First record of the lawn chinch bug Blissus insularis Barber
(Hemiptera: Blissidae) in Europe
Arlindo Lima & Tatiana Valada &
Maria Filomena Caetano & José Carlos Franco &
Ana Paula Ramos
Received: 6 January 2021 / Accepted: 22 February 2021 / Published online: 5 March 2021
# The Author(s), under exclusive licence to Springer Nature B.V. 2021
Abstract Since October 2019, chinch bugs have been Keywords Chinch bugs . St. Augustinegrass . Lawn
detected in large sunken dead patches of St. pests . Invasive species . Portugal
Augustinegrass (Stenotaphrum secundatum) lawns in
different locations of Lisbon and Setubal districts, in
Portugal. Based on morphological and molecular stud-
Introduction
ies, using mitochondrial Cytochrome C Oxidase subunit
I (COI) gene, the collected insects were identified as
The St. Augustinegrass, Stenotaphrum secundatum
Blissus insularis (Hemiptera, Heteroptera, Blissidae).
(Walter) O. Kuntze (Poaceae: Panicoidae), is a perennial
This is the first record of this noxious chinch bug species
grass that includes fertile diploids and sterile polyploids.
in Europe and in the Palaearctic region.
Since the beginning of botanical explorations, the com-
mon diploid type has been found as a coastal pioneer on
both sides of the Atlantic and later one triploid form of
this species first appeared in the Cape of Good Hope
A. Lima (*) : A. P. Ramos region (Sauer 1972). St. Augustinegrass was introduced
LEAF, Linking Landscape, Environment, Agriculture and Food,
School of Agriculture, University of Lisbon, 1349-017 Lisbon, in Asia, Australia, New Zealand, Pacific islands and
Portugal some areas of USA and Europe, mainly with horticul-
e-mail: arlindolima@isa.ulisboa.pt tural purposes, and became a popular turf grass in many
of the warmer regions of world, for its climatic adapta-
A. P. Ramos
e-mail: pramos@isa.ulisboa.pt tion and tolerance to different conditions, from full sun
to moderate shade (Sauer 1972; Macfarlane and Shelton
T. Valada : M. F. Caetano : A. P. Ramos 1986; Cherry 2001; Aldous et al. 2014; OGTR 2018). In
LPVVA, Laboratório de Patologia Vegetal “Veríssimo de
Portugal, besides being commonly used in public and
Almeida”, School of Agriculture, University of Lisbon,
1349-017 Lisbon, Portugal private lawns, mainly in central and south regions,
S. secundatum is occasionally found as a sub-
spontaneous plant in humid or salty places (Franco and
T. Valada
Afonso 1998).
e-mail: tvalada@isa.ulisboa.pt
M. F. Caetano When properly planted and maintained, a healthy and
e-mail: mffcaetano@isa.ulisboa.pt vigorous lawn of St. Augustinegrass produces a dense
carpet of textured grass blades and has a high capacity to
J. C. Franco
CEF, Forest Research Centre, School of Agriculture, University of adapt to the soil and local environmental conditions,
Lisbon, 1349-017 Lisbon, Portugal supporting small populations of insect pests, such as
e-mail: jsantossilva@isa.ulisboa.pt weevils, web worms, army worms, cut worms, or
540 Phytoparasitica (2021) 49:539–545
nematodes. However, chinch bugs (Hemiptera, long and 1.0 mm wide, with a ratio of length/width
Heteroptera, Blissidae) can cause significant damage between 2.8 and 3.1 (Leonard 1966). The antennae are
to St. Augustinegrass lawns in many regions (Kerr long and slender, consisting of four segments. Females
1966; Sweet 2000). Chinch bugs are sap-sucking spe- are slightly longer and larger than males and have an
cies of the genus Blissus Burmeister that feed on phloem obvious slit on the rounded abdomen, where the ovipos-
tissues above and below the soil surface, causing grad- itor rests instead an oval plate as in males. The head is
ual yellowing and eventual dead patches of turf usually narrower than the posterior margin of the
(Leonard 1966). These insects seem to prefer open pronotum. They are fuscous to black in colour with
sunny areas, especially those with abundant thatch black and white wings, antennae variously infuscate,
(Vázquez and Buss 2006; Reinert et al. 2011). legs reddish-yellow, often with a dark burnt orange tint.
According to Dellapé and Thomas (2021), the genus The body is setose with somewhat recurved shorter
Blissus currently consists of more than 30 species, most of setae and often less dense long erect setae. Wing dimor-
which occur in North, Central or South America, with a phism occurs within the genus, so populations can con-
few species known from the Palaearctic region, including sist of long-winged forms (macropterous), in which the
some host-specific of economically important grasses. In wings reach almost the end of the abdomen, and short-
North America, the most important species are winged forms (brachypterous), where the wings extend
B. leucopterus leucopterus (Say), B. leucopterus hirtus for less than half the length of the abdomen, or both.
Montandon, B. insularis Barber and B. occiduus Barber, They have a long rostrum with four segments and the tip
which may have overlapping ranges of plant hosts and reaches at least the level of mesocoxae (Leonard 1966;
geographic distribution (Anderson et al. 2006; Leonard Slater 1979; Schuh and Weirauch 2020).
1966; Tashiro 1987; Vittum et al. 1999). These chinch The taxonomic identification of lawn chinch bug is
bugs are closely related and considered pests of turfgrass, based on the adults’ body size, pubescence, general col-
but with different host preferences. While B. leucopterus our patterns, the colour of the posterior and anterior lobe
leucopterus and B. leucopterus hirtus are important pests of the pronotum, mouthpart morphology (total length and
of Bermudagrass (Cynodon dactylon (L.) Persoon), fescue length of individual segments), complemented, in some
(Festuca spp.), Kentucky bluegrass (Poa pratensis L.), cases, with host range and geographic distribution
perennial ryegrass (Lolium perenne L.) and zoysiagrass (Leonard 1966, 1970; Slater and China 1961; Slater and
(Zoysia japonica Steudel.), creeping bentgrass (Agrostis Baranowski 1990; Hoffman 1996; Sweet 2000;
stolonifera L.) (in this last case, only for B. leucopterus Anderson et al. 2006; Larson and Scudder 2018).
hirtus), B. occiduus is a pest only of buffalograss In October 2019, the Laboratório de Patologia Veg-
(Bouteloua dactyloides (Nutt.) Columbus). Blissus etal “Veríssimo de Almeida” (LPVVA), School of Ag-
insularis feeds on Bahiagrass (Paspalum notatum riculture, University of Lisbon, was asked to investigate
Flugge), Bermudagrass, centipedegrass (Eremochloa a new phytosanitary problem in St. Augustinegrass
ophiuroides (Munro) Hack.) and zoysiagrass, and is the lawns, at Seixal in Setubal district. Samplings in the
only Blissus species reported as a common pest of St. affected areas (Fig. 1) showed the damaged lawns were
Augustinegrass (Tashiro 1987; Reinert et al. 1995; associated with large numbers of chinch bugs that were
Chandra et al. 2011; Eickhoff et al. 2004). identified as B. insularis. Here we report for the first
Blissus insularis is considered the most damaging time the presence of this chinch bug in Portugal and
pest of St. Augustinegrass (Cherry 2001), being able to present the results of a survey carried out in Lisbon and
build up very large populations, with more than 2000 Setubal districts, to assess its distribution in the region.
insects/0.1 m2 (Reinert and Kerr 1973). Nymphs and
adults of B. insularis are phloem feeders on
S. secundatum causing wilting, chlorosis, stunting and Materials and methods
death of damaged plants. At the beginning of the attacks,
damage is limited to small patches of dead grass, and Sampling
eventually expands, with entire lawns killed as time
progresses (Vázquez and Buss 2006; Reinert et al. 2011). Samples were collected, between October 2019 and
Adult members of the genus Blissus are small and October 2020, in different locations of Lisbon and
somewhat elongated insects, measuring 2.0 to 4.0 mm Setubal districts: Seixal (38°37′33.0”N 9°06′58.9”W;Phytoparasitica (2021) 49:539–545 541
October 2019), Oeiras (38°41′58.2”N 9°16′28.8”W; specimens collected at Almada, using the DNeasy Blood
38°41′38.3”N 9°18′01.1”W; 38°41′13.4”N 9°18′56.3”W; and Tissue® kit (QIAGEN, Hilden, Germany). The pro-
November 2019 and July 2020), Almada (38°40′03.2”N tocol provided by the manufacturer was followed, with the
9°14′25.0”W; November 2019), Cascais (38°41′50.7”N following modifications: initial sample washed with ultra-
9°26′28.4”W; June 2020), Tapada da Ajuda (38°42′ pure sterilized water, followed by instant freeze in liquid
27.5”N 9°10′56.3”W; June 2020), Sesimbra (38°26′ nitrogen to improve cell lysis and addition of 4 μL of
41.7”N 9°06′10.1”W; July 2020), Loures (38°49′53.8”N RNase A after the incubation period (approx. 1 h at
9°10′16.9”W; September 2020) and Grândola (38°27′ 56 °C). Polymerase Chain Reaction (PCR) was conducted
26.9”N 8°51′43.3”W; October 2020). using the primers LCO1490 5’-GGTCAACAAATCAT
Adults and nymphs of chinch bugs (Fig. 2a and Fig. AAAGATATTGG-3′ and HCO2198 5’-TAAACTTC
2b) were collected on damaged lawns of St. AGGGTGACCAAAAAATCA-3′ (Folmer et al. 1994)‚
Augustinegrass, placing a 4–6 cm × 4–6 cm square of which extracted a fragment of 658 bp of the COI region.
lawn in a bucket full of water and waiting for them to Each 25 μL PCR reaction tube contained 12.5 μL of
float to the top (Shetlar and Andon 2012). The collected DreamTaq™ MasterMix (2x) solution (Thermo Fisher
specimens were preserved in ethanol 70% for morpho- Scientific, Lithuania), 9.5 μL of ultra-pure sterilized water,
logical and molecular studies. Voucher’s specimens 1 μL of each specific primer (each with a concentration of
were deposited in the collection of LPVVA. 10 μM) and 1 μL of DNA (approx. 5 ng). The PCR cycle
program was as follows: initial denaturation at 95 °C for
Morphological studies two minutes, followed by 40 cycles of denaturation at
95 °C for half a minute, annealing at 46 °C for a minute,
For species identification, four adult females and four extension at 72 °C for one minute and a final extension at
adult males (macropterous form), from each of the 10 75 °C for five minutes. PCR cycles were conducted on a
studied locations (i.e., 80 insects), were studied under S1000 Bio-Rad Thermal Cycler. Quality of the PCR
stereomicroscope (Leica MZ 12.5), and their images reactions was verified on an agarose gel (0.5X TBE).
were captured at magnifications from ×20 to ×62.5 with DNA sequences were obtained through Sanger sequenc-
a camera mounted in a system with motorized z-axis ing protocol. Amplification of COI fragments was made
drive and inbuilt montaging software (Leica MC 170 on an ABI 3730 XL sequencer at Stabvida (http://www.
HD). For each studied specimen, the general colour stabvida.com). Each sequence was blasted against the
pattern and the colour of the posterior and anterior lobe sequences of Blissus species available in GenBank
of the pronotum were registered. The body length (from (www.blast.ncbi.nlm.nih.gov) for a species match.
the tip of the clypeus to the posterior-most part of the
body), body width (maximum width across humeral
angles in dorsal view and maximum width of body in Results and discussion
ventral view at right angles to the body length) and
rostrum length were measured, using the software Leica Observed symptoms and damage
Application Suite version 4.12.0. In addition, the rostral
segments lengths of six females and six males were At all the sampled lawns, symptoms included stunting
measured in wet mounted microscope slides under an (failure of leaf sheaths and internodes to elongate prop-
optical microscope (Leica DM 2500) equipped with a erly), reddish to yellowish feeding marks behind leaf
reticule eyepiece calibrated with a stage micrometer. sheaths and a yellowish streaking on the leaves. Sunny
The identification of the studied specimens was areas were often most heavily infested. Severely dam-
based on Slater and Baranowski (1990) and Anderson aged plants died or were badly stunted, with leaves at
et al. (2006). the growing point wilted or dead (Fig. 1).
Molecular studies Morphological studies
For the amplification of the mitochondrial Cytochrome C The collected adults of chinch bugs consisted of both
Oxidase subunit I gene (COI) total DNA was extracted macropterous and brachypterous forms (Fig. 2a). They
from legs of two specimens collected at Seixal and two are grey to black and hirsute, with the body covered with542 Phytoparasitica (2021) 49:539–545 Fig. 1 Damage caused by Blissus insularis on a St. Augustinegrass lawn: left - infested lawn displaying discolored patches, which are usually circular in shape; right - detail of the initial stage of a discolored patch of lawn fine silver-grey semi-erect hairs. The pronotum posteri- respectively. The abdomen of females was slightly longer or lobe is black, strongly contrasting with the grey and larger than that of males, with the resting ovipositor colour of the anterior lobe (Fig. 2c). In the macropterous instead an oval plate as in males (Fig. 2e). Adult females adults, the wings are white, with a distinctive triangular- were 0.98 to 1.16 mm (1.05 ± 0.06 mm) wide, whereas shaped black marking in the middle of the outer edge of adult males were narrower, ranging from 0.80 to 0.99 mm each wing (Fig. 2d). (0.92 ± 0.04 mm). The maximum width across humeral In the macropterous specimens, the adult female and angles in dorsal view ranged between 1.07 and 1.19 mm male lengths ranged from 3.03 to 3.78 mm (3.57 ± (1.11 ± 0.4 mm), in females and between 0.95 and 0.14 mm) and from 2.84 to 3.50 mm (3.19 ± 0.13 mm), 1.01 mm (1.00 ± 0.2 mm), in males. Fig. 2 Morphology of Blissus insularis: a) macropterous and pronotum (dorsal view); d) forewing hemelytron and membranous brachypterous adults (dorsal view); b) 2nd, 3rd, 4th and 5th hindwing (dorsal view); e) abdomen (ventral view; left: female, instar-nymph (dorsal view); c) anterior and posterior lobe of the right: male); f) rostrum (ventral view). Scale bar: 0.25 mm
Phytoparasitica (2021) 49:539–545 543
The rostrum extends at least below the attachment and Baranowski 1990; Anderson et al. 2006). The re-
point of the third pair of legs and sometimes the tip sults of the molecular studies confirmed they belong to
reaches the abdomen (Fig. 2f). Overall, rostrum length the genus Blissus, but did not allow the identification at
was higher in adult females, than in males. The rostrum the species level. In fact, previous analysis of the COI
length measured between 1.44 and 1.77 mm (1.62 ± gene of heteropteran species by several authors (Jung
0.07 mm), in females and between 1.41 and 1.71 mm et al. 2011; Raupach et al. 2014; Kim and Jung 2018)
(1.50 ± 0.06 mm), in males. The mean length of the four revealed that the mean maximum intraspecific distance
individual rostrum segments differed between genders: of the compared species was around 1.8%, while the
409.7 μm and 370.5 μm (segment 1); 525.2 μm and average minimum interspecific distance of congeners
478.2 μm (segment 2); 351.4 μm and 329.3 μm (seg- was 3.5%. According to Park et al. (2011), these values
ment 3); and 377.5 μm and 349.3 μm (segment 4), for are congruent with the enormous diversity of this taxon,
females and males, respectively. where there are countless species ordinarily morpholog-
ically similar and closely related.
Molecular studies The extensive damage observed in St. Augustinegrass
lawns supports our identification since, as mentioned
The 633-bp sequences derived from three of the studied earlier B. insularis is the only Blissus species known as
individuals (Almada sample) were 100% identical to a common pest of St. Augustinegrass.
each other (GenBank accession MW435183), whereas
the sequence of the other one (Seixal sample) had Concluding remarks
99.69% similarity to the others, with two single-
nucleotide polymorphisms (SNPs) (GenBank accession The presence of B. insularis was confirmed in all 10
MW435184). Based on a megablast search of NCBI sampled locations, which indicates that this alien chinch
GenBank nucleotide database, the closest hits using bug has already established and dispersed within an area
both COI sequences had highest similarity to an uniden- whose limits are 13 Km North, 26 Km West and 38 Km
tified species of Blissus (GenBank HQ929023.1; Iden- Southeast from Lisbon. Eight of the sampled locations
tities = 603/606 (99.50%), 0 gaps) followed by are up to 26 Km from Lisbon, whereas the other two
B. leucopterus (GenBank KR040493.1; Identities = locations are up to 21 Km from Setubal. Both Lisbon
605/609 (99.34%), 0 gaps), B. arenarius (GenBank and Setubal have international ports, and Lisbon has an
KR038680.1; Identities = 604/609 (99.18%), 0 gaps), international airport. The importation of contaminated
B. occiduus (GenBank KR043512.1; Identities = 598/ plants was the possible pathway of invasion. This is the
609 (98.19%), 0 gaps) and Blissus canadensis most important pathway of alien Heteroptera in Europe
(GenBank KR043528.1; Identities = 562/608 (Rabitsch 2008).
(92.43%), 0 gaps). In contrast, the two COI sequences According to Rabitsch (2008, 2010), at least 16
of B. insularis available at the GenBank (KU242610.1 Heteroptera species are alien to Europe, of which about
and KU242609.1), referred in studies of culturing and 63% are of North America origin. No Blissus species is
characterization of the gut symbiont Burkholderia in included in that list. To the best of our knowledge, the
this bug species, showed a very high level of divergence documented presence of B. insularis in Portugal corre-
with the sequences of the studied specimens (GenBank sponds to the first report of this species both in Europe
KU242610.1; Identities = 337/673 (50.07%), 167 gaps), and in the Palaearctic region. The severe damages
as well as with any of the listed sequences of caused by this chinch bug in different locations of
B. leucopterus (e. g. GenBank KU242610.1 vs Lisbon and Setubal districts demand further studies on
KR040493.1; Identities = 334/679 (49.63%), 178 gaps), its bionomics and the development of effective pest
B. arenarius, B. occiduus or B. canadensis. management strategies.
Pest management of B. insularis populations has
Taxonomic identification been mostly based on the application of insecticides
and use of resistant cultivars of St. Augustinegrass, such
The morphological characteristics of the studied speci- as ‘Floratam’, ‘Floralawn’, ‘FX-10’ and ‘Captiva’.
mens of the lawn chinch bug collected in Portugal are in However, the existence of resistant populations of the
accordance with those described for B. insularis (Slater chinch bug has been reported (Genovesi et al. 2009;544 Phytoparasitica (2021) 49:539–545
Reinert et al. 2011; Vázquez et al. 2011; Milla-Lewis (Hemiptera: Lygaeidae). Journal of Economic Entomology,
97, 67–73.
et al. 2017).
Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R.
(1994). DNA primers for amplification of mitochondrial
Acknowledgments Thanks are due to Bruno Ferreira, Filipa cytochrome c oxidase subunit I from diverse metazoan in-
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Slater, J. A., & China, W. E. (1961). Blissus Burmeister, 1835 jurisdictional claims in published maps and institutional
(Insecta, Hemiptera): Proposed designation of a type species affiliations.You can also read
