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First record of the brown marmorated stink bug Halyomorpha halys (Stål , 1855) in Algeria and its presence in North Africa (Heteroptera: Pentatomidae)

Authors:
  • Independent researcher
  • Conservation des forêts Skikda Algerie
  • Natural History Museum Milan - Italy

Abstract

In the last decades the Asiatic brown marmorated stink bug Halyomorpha halys (Stål, 1855) (BMSB) infested North America and recently Europe, where it was recorded in many countries. The new record from Algeria is recent (2021) and concerns an adult photographed in the city of Skikda at the Mediterranean coast of the country. There is a penetration of pests in Algeria by commercial business, mainly from Spain and Morocco, probably in the area of the port. Skikda is connected to other Mediterranean ports from coast to coast on a daily basis.
Revista gaditana de Entomología, volumen XII núm. 1 (2021): 147-154 ISSN 2172-2595
147
Torsten van der Heyden*, Amar Saci** & Paride Dioli***
* Immenweide 83, 22523 Hamburg, Germany; email: tmvdh@web.de. ORCID:
https://orcid.org/0000-0003-4138-7160
** Conservation des forêts de la wilaya de Skikda, cité Bouabbaz, Skikda, Algérie, 21000; email:
amarsaci21@gmail.com.
*** Department of Entomology, Natural History Museum, Corso Venezia 55, 20121 Milan, Italy;
email: paridedioli@virgilio.it. ORCID: https://orcid.org/0000-0002-4274-0926
Abstract. In the last decades the Asiatic brown marmorated stink bug Halyomorpha halys (Stål,
1855) (BMSB) infested North America and recently Europe, where it was recorded in many
countries. The new record from Algeria is recent (2021) and concerns an adult photographed in the
city of Skikda at the Mediterranean coast of the country. There is a penetration of pests in Algeria
by commercial business, mainly from Spain and Morocco, probably in the area of the port. Skikda
is connected to other Mediterranean ports from coast to coast on a daily basis.
Key words: Heteroptera; Halyomorpha halys; invasive species; first record; pest; distribution;
Algeria; North Africa.
Primer registro de Halyomorpha halys (Stål, 1855) en Argelia y su presencia en el norte de
África (Heteroptera: Pentatomidae)
Resumen. En las últimas décadas, la chinche asiática parda marmorada Halyomorpha halys (Stål,
1855) (BMSB) infestó América del Norte y recientemente Europa, donde se registró en muchos
países. El nuevo registro de Argelia es reciente (2021) y se refiere a un adulto fotografiado en la
ciudad de Skikda en la costa mediterránea del país. Existe una penetración de plagas en Argelia por
el tráfico comercial, principalmente desde España y Marruecos y probablemente a través del puerto.
Skikda está conectado con otros puertos mediterráneos a diario.
Palabras clave: Heteroptera; Halyomorpha halys; especie invasora; primer registro; plaga;
distribución; Argelia; Norte de África.
urn:lsid:zoobank.org:pub:2730F16C-CCD8-45C8-AD32-1E8A4E0F5095
First record of the brown marmorated stink bug Halyomorpha
halys (Stål, 1855) in Algeria and its presence in North Africa
(Heteroptera: Pentatomidae)
INTRODUCTION
The brown marmorated stink bug
Halyomorpha halys (Stål
, 1855)
(BMSB) is considered a key pest of fruit
orchards and legume crops in its native
countries China, Japan, Korea and
Taiwan (Lee et al., 2013).
INTRODUCCIÓN
La chinche parda marmorada
Halyomorpha halys (Stål, 1855)
(BMSB) se considera una plaga clave de
los huertos de frutas y cultivos de
leguminosas en sus países de origen
China, Japón, Corea y Taiwán (Lee et
al., 2013).
T. van der Heyden et al. First record of the brown marmorated stink bug Halyomorpha halys (Stål,
1855) in Algeria and its presence in North Africa (Heteroptera: Pentatomidae)
148
In 1996, it was accidentally introduced
into the United States of America
(Hoebeke & Carter, 2003) and a few years
after the first record in Pennsylvania, it
replaced Tortrix moths as key pest in fruit
orchards and caused farmers to
quadruplicate insecticide treatments
(Leskey et al., 2012).
In Europe, H. halys first appeared in
Liechtenstein in 2004 (Arnold, 2009) and
in Switzerland in the same year, but was
officially reported later (Wermelinger et
al., 2008; Haye et al., 2014). Subsequently
it spread throughout the continent and in
many islands, creating considerable
problems for crops (EPPO, 2021).
In North Africa there were a doubtful
record from Egypt (Gadalla, 2004) and
some findings in Morocco (Nouere et al.,
2019).
The recent record is the first for
Algeria. Based on bioclimatic models and
climate data, the presence of H. halys in
the northern parts of Algeria could have
been expected (Haye et al., 2015).
MATERIAL EXAMINED
ALGERIA Skikda, Lat: 36.866479
Lon: 6.906256, 05.X.2021, 1 spec. in the
city center, at night, attracted by the
artificial light on the wall of a house, photo
by Hidaya Benkassa, det. A.Saci (Fig. 1).
The species was observed also in July 2021
in the same area of the town.
MORPHOLOGY AND IDENTIFICATION
Adults (Fig. 1) are 12-17 mm long and
7-10 mm wide, brownish or greyish,
generally variable in size and colour, with
alternating light and dark bands on the
antennae, legs and the lateral margins of
the abdomen. The legs have completely
white tarsi. Ventrally the colour of adults
is variable, from ivory to dirty pink.
En 1996, se introdujo accidentalmente
en los Estados Unidos de América
(Hoebeke & Carter, 2003) y unos años
después del primer registro, reemplazó a
las polillas Tortrix como plaga clave en
frutales y provocó que se cuadruplicaran
los tratamientos con insecticidas (Leskey
et al., 2012).
En Europa, H. halys apareció por
primera vez en Liechtenstein en 2004
(Arnold, 2009) y en Suiza el mismo año,
aunque publicado más tarde
(Wermelinger et al., 2008; Haye et al.,
2014). Más tarde se extendió por todo el
continente y muchas islas, dando
problemas en los cultivos (EPPO, 2021).
En el norte de África hubo un registro
dudoso de Egipto (Gadalla, 2004) y
algunos hallazgos en Marruecos (Nouere
et al., 2019).
Este es el primer dato de Argelia. En
base a modelos y datos bioclimáticos, se
podría haber esperado la presencia de H.
halys en el norte de Argelia (Haye et al.,
2015). MATERIAL EXAMINADO
ARGELIA - Skikda, Lat: 36.866479 Lon:
6.906256, 05.X.2021, 1 ex. en el centro de
la ciudad, de noche, atraído por la luz
artificial en la pared de una casa, foto de
Hidaya Benkassa, det. A.Saci (Fig. 1). La
especie fue observada también en julio de
2021 en la misma zona de la localidad.
MORFOLOGÍA E IDENTIFICACIÓN
Los adultos (Fig. 1) miden 12-17 mm
de largo y 7-10 mm de ancho, parduscos o
grisáceos, generalmente de tamaño y
color variables, con bandas alternas claras
y oscuras en las antenas, patas y márgenes
laterales del abdomen. Patas con tarsos
completamente blancos. Ventralmente, el
color de los adultos es variable, desde el
marfil hasta el rosa sucio.
Revista gaditana de Entomología, volumen XII núm. 1 (2021): 147-154 ISSN 2172-2595
149
overwintering in houses and other man-
et al., 2013).
Vétek et al. (2014).
DISCUSSION
from Morocco (Nouere et al., 2019).
al. (2018).
El sternum es de color marfil al
emerger, pero con el tiempo cambia a
rojo, especialmente en los machos, y
varía según la exposición al sol. En
otoño, los adultos comúnmente se
agregan en grandes cantidades para
pasar el invierno en casas y otras
estructuras artificiales antes de mudarse
a los edificios (Maistrello et al., 2016).
El traslado a lugares de hibernación
generalmente aumenta a mediados de
octubre, continúa hasta noviembre y
generalmente se detiene cuando las
temperaturas exteriores están por debajo
de los 9° C (Lee et al., 2013).
H. halys tiene cinco estadios ninfales
cuya longitud es de 2,4 mm, 3,7 mm, 5,5
mm, 8,5 mm y 12 mm, respectivamente.
La cabeza y el tórax de los dos primeros
estadios son en su mayoría negros y el
abdomen es de color rojo amarillento,
mientras que los estadios tres (Fig. 2) y
cuatro tienen una cabeza y tórax de color
negro pardusco con fuertes espinas y un
abdomen blanco con manchas y suturas
rojizas. El quinto estadio tiene una
cabeza y tórax de color negro pardusco
con espinas cortas lateralmente, un brillo
metálico y abdomen blanco amarillento
cubierto densamente de punteado
metálico negro y manchas y suturas
rojizas. Las tibias de los estadios 3-5
muestran una banda blanca. Los ojos de
todas las etapas ninfales son de color
negro rojizo. Vétek et al. (2014)
describen los genitales de ambos sexos.
DISCUSIÓN
En este momento, hay dos citas para
el norte de África: el primero fue en
Egipto (Gadalla, 2004), seguido de
registros de Marruecos (Nouere et al.,
2019). No hay nuevos registros en
Egipto después de la cita de Gadalla
(op.cit.) y su presencia en ese país sigue
T. van der Heyden et al. First record of the brown marmorated stink bug Halyomorpha halys (Stål,
1855) in Algeria and its presence in North Africa (Heteroptera: Pentatomidae)
150
widely distributed (EPPO, 2021).
pomegranate tree nearby.
siendo dudosa de acuerdo con
Cianferoni et al. (2018).
En Marruecos, la especie se encontró
durante investigaciones sobre plagas y
enfermedades del arándano (Vaccinium
corymbosum) realizadas en 2019 en las
regiones de Souss-Massa y Loukkos,
pero a día de hoy sigue sin estar
ampliamente distribuida (EPPO, 2021).
En Argelia (Skikda) el dato actual es el
primero para este país. El BMSB se vio
por primera vez en julio de 2021.
Alrededor del lugar de observación hay
pequeños jardines públicos con varias
especies, incluida Washingtonia sp. y
Ailanthus altissima en los terraplenes.
Además, hay un árbol de azufaifo y un
granado cerca.
Durante los últimos 20 años, ha habido
una progresiva penetración de plagas por
Figures 1-2. 1. Adult of Halyomorpha halys (Stål, 1855), Skikda, Algeria, 05.X.2021. (Photo:
Hidaya Benkassa); 2. Head and thorax of third instar of Halyomorpha halys (Stål
, 1855). (Photo:
Paride Dioli).
Revista gaditana de Entomología, volumen XII núm. 1 (2021): 147-154 ISSN 2172-2595
151
plausible.
(Bernon, 2004).
al., 2014).
el tráfico comercial en los países de la
ribera norte del Mediterráneo
conectados vía puertos.
El clima mediterráneo favorece
claramente la presencia continuada de H.
halys y, por tanto, también se propaga
por medios de transporte entre los países
de esta región. Por ello, también es
plausible una progresiva expansión
desde Italia (puerto de Génova) hacia el
oeste hacia Francia, España, Portugal
(Grosso-Silva et al., 2020) y, a través del
Estrecho de Gibraltar, Marruecos y
Argelia.
Como la mayoría de los
pentatómidos fitófagos, H. halys es una
plaga polífaga con una gama
extremadamente amplia de plantas
hospedantes de muchas familias, con
preferencia por Fabaceae y Rosaceae
(Hoebeke & Carter, 2003; Bernon,
2004). Debido al clima favorable de la
costa mediterránea argelina, deberíamos
esperar un aumento de individuos de esta
especie. En el área de Skikda hay
muchos cultivos de frutas y hortalizas,
incluidas algunas especies botánicas
atacadas por H. halys. La especie
también parasita diversas plantas
ornamentales en jardines debido a que
las ninfas y los adultos se alimentan
chupando diferentes partes como brotes,
hojas, tallos, frutos, vainas o semillas.
Los adultos tienen preferencia por las
estructuras reproductivas, aunque los
sitios de alimentación pueden diferir
para algunas plantas hospedantes, p. ej.
Paulownia tomentosa, de la que se
alimenta principalmente de estructuras
vegetativas (Bernon, 2004).
En Asia, H. halys se ha citado de 106
plantas hospedadoras que pertenecen a
45 familias (Lee et al., 2013) y es
considerada como plaga periódica /
T. van der Heyden et al. First record of the brown marmorated stink bug Halyomorpha halys (Stål,
1855) in Algeria and its presence in North Africa (Heteroptera: Pentatomidae)
152
2012).
et al., 2016, 2018).
(Leskey et al., 2012).
attraction (Maistrello et al., 2018).
ocasional de Glycine max (soja), Malus
spp. (manzanas), Pyrus spp. (peras),
Prunus spp. (cerezas, albaricoques,
melocotones, ciruelas) (Yanagi &
Hagihara, 2008; Xu et al., 2014).
En los Estados Unidos un informe
registra 166 especies de plantas
hospedantes de BMSB, con algunas
utilizadas únicamente para la
alimentación y otras para la alimentación
y la oviposición (Leskey & Nielsen,
2018). En comparación con Asia, el
estatus de plaga se confirma para los
cultivos de frutales (manzanas, peras,
melocotones, uvas, cerezas), así como
Corylus avellana (avellana) y frutos
pequeños (Rubus spp., moras y
frambuesas; Vaccinium spp., arándanos;
Morus spp, moras) (Leskey et al., 2012).
En el caso de las frutas, el tipo de
daños y vulnerabilidad a menudo se
relaciona con el tipo de cultivo y varía
durante el período de crecimiento; la
alimentación al inicio de la temporada a
menudo causa la caída de la fruta, la
afectación del desarrollo o produce
deformidades, principalmente en las
peras (Maistrello et al., 2016, 2018). En
las manzanas, las lesiones debidas a la
alimentación incluyen hoyuelos,
depresiones y puntos negros que pueden
confundirse fácilmente con trastornos
fisiológicos como la mancha del corcho
y el hueso amargo (Leskey et al., 2012).
Además de ser una plaga agrícola,
dondequiera que ocurra H. halys, se ha
convertido en una plaga residencial y
molesta para los propietarios de
viviendas y empresas por su hábito de
utilizar edificios (casas, áticos, garajes,
oficinas, graneros, etc.) para pasar el
invierno (Hoebeke & Carter, 2003;
Inkley, 2012; Maistrello et al., 2016).
Este problema se agrava en zonas
rurales, donde se pueden encontrar miles
Revista gaditana de Entomología, volumen XII núm. 1 (2021): 147-154 ISSN 2172-2595
153
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ACKNOWLEDGEMENTS
reviewing the text in English.
de ejemplares en las casas (hasta 26.000
mil)
durante la temporada de invierno
(Inkley, 2012). Las molestias son
causadas por la presencia diaria en
grandes cantidades, manchas en paredes
y pisos, con excrementos y actividad
debido a la atracción de la luz
(Maistrello et al., 2018).
AGRADECIMIENTOS
Nos gustaría agradecer a Hidaya
Benkassa (Skikda, Argelia) por
permitirnos usar la foto del registro y a
Anja von Seth (Hamburgo, Alemania)
por revisar el texto en inglés.
T. van der Heyden et al. First record of the brown marmorated stink bug Halyomorpha halys (Stål,
1855) in Algeria and its presence in North Africa (Heteroptera: Pentatomidae)
154
Lee, D.-H., Short, B. D., Joseph, S. V., Bergh, J. C. & Leskey, T. C. 2013. Review of the Biology,
Ecology, and Management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and
the Republic of Korea. Environmental Entomology, 42(4): 627-641.
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Recibido: 15 octubre 2021
Aceptado: 20 octubre 2021
Publicado en línea: 22 octubre 2021
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Polyphagous phytophagous organisms that shelter in man-made objects have a higher chance of becoming invasive fast-spreading pests, going undetected during phytosanitary checks and travelling with any type of goods. However, if the same organisms are also a household nuisance, they could be used in crowdsourcing surveys aimed at their early detection and to track their spread in real time. By participating in these surveys, people can be educated on the destructive potential of invasive species and on sustainable management options. Yet, in order to obtain good-quality data, useful to plant protection stakeholders, a one-to-one approach with people is crucial. The case study is the Italian invasion of Halyomorpha halys, among the most dangerous crop-threatening pests globally. A four-year survey that combined active search and a crowdsourcing approach, made the tracking of its spread and investigation of its spatio-temporal dynamics possible, showing the functionality of coordinated multi-actor approach in data collection. Keywords Invasive species, citizen science, crop and nuisance pest, population abundance, Brown Marmorated Stink Bug
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The regions in which Halyomorpha halys (Stål, 1855) occurs in Italy are summarized and ordered chronologically according to the date of the first record. Details and verification about the first Italian record from Liguria (often overlooked), that dates back to 2007 the introduction of H. halys in this country, are also given. First exact localities are listed for the Italian regions of Tuscany, Marche, Latium, Abruzzo, Campania, and Apulia, in which only general occurrence was known so far. We included also additional records from Trentino-Alto Adige, where the presence of H. halys has only recently been reported through a few data. Furthermore first records for Sweden, Central Macedonia (Greece), and Manitoba (Canada) are reported, as well as first intercepted specimens from Iceland.
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The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive pentatomid introduced from Asia into the United States, Canada, multiple European countries, and Chile. In 2010, BMSB populations in the mid-Atlantic United States reached outbreak levels and subsequent feeding severely damaged tree fruit as well as other crops. Significant nuisance issues from adults overwintering inside homes were common. BMSB is a highly polyphagous species with a strong dispersal capacity and high reproductive output, potentially enabling its spread and success in invaded regions. A greater understanding of BMSB biology and ecology and its natural enemies, the identification of the male-produced aggregation pheromone, and the recognition that BMSB disperses into crops from adjacent wooded habitats have led to the development of behavior-based integrated pest management (IPM) tactics. Much is still unknown about BMSB, and continued long-term collaborative studies are necessary to refine crop-specific IPM programs and enhance biological control across invaded landscapes. Expected final online publication date for the Annual Review of Entomology Volume 63 is January 7, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Early detection of invasive alien species and the ability to track their spread are critical for undertaking appropriate management decisions. Citizen science surveys are potentially valuable tools for quickly obtaining information on biodiversity and species distributions. The Asian brown marmorated stink bug, Halyomorpha halys, is an invasive pest of agricultural crops and a dwelling nuisance. Halyomorpha halys was first recorded in Italy in 2012 in Emilia Romagna, one of the most important fruit producing regions of Europe. To rapidly obtain data on its distribution in the newly invaded area, a survey that combined citizen science and active search was set up using multimedia channels. Data concerning when, where and how the bugs were spotted were collected, together with photographs and specimens. The survey detected established breeding populations in different areas of Northern Italy and Southern Switzerland, indicating a potentially high risk for crop damage that extends beyond the territories of first detection. Furthermore, new data on H. halys phenology, host plants, voltinism and behaviour were obtained. The importance of citizen science in early detection of introduced pest species is highlighted. This paper also provides a picture-based key to recognize H. halys from similar pentatomids in the world.
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http://www.cabi.org/isc/?compid=5&dsid=27377&loadmodule=datasheet&page=481&site=144
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