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The multicolored Asian lady beetle, Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae), a not so new invasive insect in Colombia and South America

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Abstract. The first reports of the multicolored Asian lady beetle Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) in Colombia appeared in 2011. However, based on museum insect specimens, the introduction of H. axyridis in Colombia occurred in 1989 or earlier, making it the second oldest record of the species in South America after the deliberate releases of the species in Argentina in 1986. Currently in Colombia, H. axyridis is well established and is here recorded from the States of Antioquia, Caldas, Cauca, Cundinamarca, Nariño, Tolima and Valle del Cauca. Resumen. Los primeros reportes de la mariquita multicolor asiática Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) aparecieron en el 2011. Sin embargo, con base en colecciones de insectos en museos, la introducción de H. axyridis en Colombia ocurrió en 1989 o antes, haciendo que este sea el segundo registro más antiguo de esta especie en Sur América, después de las liberaciones intencionales de la especie en Argentina en 1986. Actualmente en Colombia, H. axyridis está bien establecida y aquí se reporta en los departamentos de Antioquia, Caldas, Cauca, Cundinamarca, Nariño, Tolima y el Valle del Cauca.
CENTER FOR SYSTEMATIC ENTOMOLOGY, INC., Gainesville, FL
The multicolored Asian lady beetle, Harmonia axyridis (Pallas, 1773)
(Coleoptera: Coccinellidae), a not so new invasive insect in Colombia
and South America
Takumasa Kondo
Corporación Colombiana de Investigación Agropecuaria (CORPOICA)
Centro de Investigación Palmira, Calle 23, Carrera 37, Continuo al Penal
Palmira, Valle, Colombia
Guillermo González F.
Santiago, Chile,
Date of Issue: February 28, 2013
0283
INSECTA
MUNDIA Journal of World Insect Systematics
Takumasa Kondo and Guillermo González F.
The multicolored Asian lady beetle, Harmonia axyridis (Pallas, 1773) (Coleoptera:
Coccinellidae), a not so new invasive insect in Colombia and South America
Insecta Mundi 0283: 1-7
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1
0283: 1-7 2013
The multicolored Asian lady beetle, Harmonia axyridis (Pallas, 1773)
(Coleoptera: Coccinellidae), a not so new invasive insect in Colombia
and South America
Takumasa Kondo
Corporación Colombiana de Investigación Agropecuaria (CORPOICA)
Centro de Investigación Palmira, Calle 23, Carrera 37, Continuo al Penal
Palmira, Valle, Colombia
takumasa.kondo@gmail.com
Guillermo González F.
Santiago, Chile,
willogonzalez@yahoo.com
Abstract. The first reports of the multicolored Asian lady beetle Harmonia axyridis (Pallas, 1773) (Coleoptera:
Coccinellidae) in Colombia appeared in 2011. However, based on museum insect specimens, the introduction of H.
axyridis in Colombia occurred in 1989 or earlier, making it the second oldest record of the species in South America
after the deliberate releases of the species in Argentina in 1986. Currently in Colombia, H. axyridis is well established
and is here recorded from the States of Antioquia, Caldas, Cauca, Cundinamarca, Nariño, Tolima and Valle del Cauca.
Resumen. Los primeros reportes de la mariquita multicolor asiática Harmonia axyridis (Pallas, 1773) (Coleoptera:
Coccinellidae) aparecieron en el 2011. Sin embargo, con base en colecciones de insectos en museos, la introducción de
H. axyridis en Colombia ocurrió en 1989 o antes, haciendo que este sea el segundo registro más antiguo de esta especie
en Sur América, después de las liberaciones intencionales de la especie en Argentina en 1986. Actualmente en
Colombia, H. axyridis está bien establecida y aquí se reporta en los departamentos de Antioquia, Caldas, Cauca,
Cundinamarca, Nariño, Tolima y el Valle del Cauca.
Introduction
While studying insects on a citrus orchard in Palmira, in the State of Valle del Cauca, Colombia, the
first author photographed a species of coccinellid on the twigs of Tahiti Lime, Citrus latifolia Tanaka
(Fig. 1). The species was identified as the multicolored Asian lady beetle Harmonia axyridis (Pallas,
1773) (Coleoptera: Coccinellidae) by the second author. Specimens of H. axyridis collected in Colombia
were compared with Chilean, Argentinean, Peruvian and Brazilian specimens.
Harmonia axyridis is a rather characteristic species with white pronotum with black “M” shaped
design, frequently separated into four or five spots, and yellow to red elytra, with nine spots (2:3:3:1),
and a common scutellar one, although sometimes some or all spots are reduced or absent. It can be
distinguished from other similar species of Coccinellidae known from Colombia and more widely in South
America by the following combination of features: (i) body glabrous and 6 to 8 mm long; (ii) frequently
with wrinkles anterior to elytral apex; (iii) apex of middle and hind tibia without apical spurs; and (iv)
postcoxal area of first abdominal ventrite with an oblique dividing line. As the name suggests, the multi-
colored Asian lady beetle has numerous color morphs, and this may be the reason why the species has
eight junior synonyms and numerous subspecies (Koch 2003). Michie et al. (2010) indicated that the
plasticity of color pattern observed in H. axyridis f. succinea is an adaptation to increase the melanic
area of the elytra, and hence activity level, when the insect is exposed to cold temperatures, and that its
plasticity has helped this particular morph to be so successful and may also have contributed to its
invasive success.
The Coccinellidae, whose members are commonly known as ladybirds, ladybugs or lady beetles, is a
cosmopolitan family with approximately 6,000 described species to date (Vandenberg 2002), including
1400 South American species (González 2010). The life cycle of Coccinellidae includes a spring or summer
larval period of approximately one month, followed by a short period of pupation and an adult life of
many months, including a period of hibernation in cold and temperate areas. The majority of the
Coccinellidae are diurnal predators and they are associated largely with soft-bodied insects such as
2 INSECTA MUNDI 0283, February 2013 KONDO AND GONZÁLEZ
Coccoidea and Aphidoidea. Other species feed on Acari (e.g., those of the tribe Sthetorini), Psylloidea
(e.g., those of the tribes Coccinellini and Ortaliinae), Aleyrodidae (e.g., those of the tribe Serangiini), and
some others prey on coccinellid larvae (Vandenberg 2002). Although coccinellids usually are considered
beneficial as they control agricultural pests and many species are mass reared and sold for that purpose,
members of the subfamily Epilachninae are phytophagous, feeding especially on cucurbits and legumes,
and some are considered important agricultural pests, e.g., Epilachna paenulata (Germar, 1824) (Diaz et
al. 2010) and E. varivestis Mulsant, 1850 (Nakamura and Shiratori 2010). Furthermore, species of the
tribe Halyziini feed on fungi of the genus Erysiphales (Vandenberg 2002).
The multicolored Asian lady beetle as a predator
Harmonia axyridis is a well-known predator of aphids and other soft-bodied arthropods (Koch 2003).
In soybean production systems in the USA, H. axyridis plays an important role in controlling the soy-
bean aphid Aphis glycines Matsumura, 1917 (Hemiptera: Aphididae) (Douglas et al. 2004). Numerous
releases of H. axyridis as a classical biological control agent were made in the USA dating back to as
early as 1916 (Gordon 1985, apud Koch 2003). However, the first established population in the USA (in
the State of Louisiana) was documented in 1988 (Chapin and Brou 1991, apud Koch 2003; Hahn and
Kovach, 2004). Thereafter, H. axyridis rapidly expanded its range in North America, and now is found in
much of the continental USA and southern Canada (Koch 2003).
The multicolored Asian lady beetle as a pest
Harmonia axyridis may cause negative impacts that can be classified into three general categories: 1)
impacts on non-target arthropods; 2) impacts on fruit production; and 3) impacts as a household invader
(Koch and Galvan 2008). Harmonia axyridis has received particular attention because it is often used as
Figure 1. Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in copula on a twig of Citrus latifolia Tanaka.
Palmira, Valle del Cauca, Colombia. Photo by T. Kondo.
INSECTA MUNDI 0283, February 2013 3
HARMONIA AXYRIDIS IN COLOMBIA
a biological control agent and because it is thought to displace native coccinellids through resource
competition wherever it is introduced (Koch et al. 2006). However the multicolored Asian lady beetle is a
generalist predator that preys on a wide variety of non-target insects, including the monarch butterfly
Danaus plexippus (L., 1758) (Lepidoptera: Nymphalidae), and is known as an intraguild predator, that
may feed on other coccinellids and on Chrysoperla carnea (Stephens, 1836) (Neuroptera: Chrysopidae)
(Koch et al. 2004; Koch and Galvan 2008). The insect is also known as a pest. In the State of Ohio, USA,
H. axyridis has been reported to attack fruits such as apples, grapes and peaches, and to bite people
(Kovach 2004). Their bite often causes allergic reactions in humans (Huelsman and Kovach 2004). On
the other hand, H. axyridis is considered an urban pest in temperate climates, where large numbers of
beetles invade homes in search of places for overwintering. In Ohio (USA), H. axyridis is considered as a
serious nuisance pest to homeowners during fall, winter, and early spring (Huelsman and Kovach 2004).
Introduction and distribution in South America
Harmonia axyridis was intentionally introduced to the province of Mendoza in Argentina in the late
1990s, and it was later found in Buenos Aires (Argentina) and in Curitiba (Brazil) (Grez et al. 2010).
Hitherto, in South America, H. axyridis has been reported from Argentina (Buenos Aires) (Grez et al.
2010; Saini 2004), (Mendoza) (Grez et al. 2010), Brazil (Curitiba) (Grez et al. 2010), (Parana) (Almeida
and Silva 2002), (Minas Gerais) (Queiroz-Rezende 2010), Chile (Santiago and Valparaiso) (Grez et al.
2010), Paraguay (Caaguazú, Itapúa and Cordillera) (Silvie et al. 2007), Peru (Tumbes and Lima) (G.
González personal observation, apud Grez et al. 2010; Iannacone and Perla 2011), Ecuador (Gonzalez
and Kondo 2012) and Uruguay   (Nedv d and Krej ík 2010). Based on studies of climatic similarities
between South America and locations in Asia which were analyzed using the climate matching software,
CLIMEX, and a biome matching method, Koch et al. (2006) predicted that most of South America is
suitable for establishment of H. axyridis. Furthermore, Grez et al. (2010) suggested that H. axyridis
would soon colonize other areas of South America. As predicted by various authors (Koch et al. 2006;
Grez et al. 2010, Poutsma et al. 2008, apud Martins et al. 2009), H. axyridis was reported recently from
Colombia in the State of Valle del Cauca by Brown et al. (2011) based on a personal communication, and
by Amat-Garcia et al. (2011) based on specimens collected in Bogota in the State of Cundinamarca on
Croton bogotanus Cuatrec., 1935 (misspelled as Croton bogotensis) (Euphorbiaceae). Here we reconfirm
the presence of H. axyridis in Colombia based on newly collected material and museum specimens, and
try to estimate a time of its introduction into Colombia.
Materials and Methods
Collection data on H. axyridis was gathered from nine insect collections (8 in Colombia and 1 in
Chile; see depositories below). Species identification was carried out by the authors based on direct
observation, or based on photographs of coccinellids sent by collaborators (see Acknowledgment sec-
tion). Specimens deposited at the Museo Entomológico Francisco Luis Gallego were kindly identified by
Mr. John A. Quiroz. This study was carried out at insect collections or museums located in Cali, Palmira
(State of Valle del Cauca), Bogota (State of Cundinamarca), Medellin (State of Antioquia), Pasto (State of
Nariño), and Santa Marta (State of Magdalena), and only covers a small area of the Colombian territory.
Depositories
CEUNP: Colección Entomológica de la Universidad Nacional, sede Palmira, Palmira, Valle del Cauca,
Colombia.
CIAT: Insect Collection, International Center for Tropical Agriculture, Palmira, Valle del Cauca, Colom-
bia.
GGPC: Guillermo González Personal Collection, Santiago, Chile.
ICN: Instituto de Ciencias Naturales, Universidad, Nacional de Colombia, Bogotá, Colombia.
MECP: Museo de Entomología, Corporación Colombiana de Investigación Agropecuaria, Centro de
Investigación Palmira, Palmira, Valle del Cauca, Colombia.
4 INSECTA MUNDI 0283, February 2013 KONDO AND GONZÁLEZ
MEFLG: Museo Entomológico Francisco Luis Gallego, Universidad Nacional de Colombia, Sede Medellín,
Medellín, Colombia.
UDENAR: Colección de insectos, Universidad de Nariño, Facultad de Ciencias Agrícolas, Pasto, Nariño,
Colombia.
UNAB: Museo Entomológico Facultad de Agronomía, Universidad Nacional de Colombia, Sede Bogotá,
Bogotá, Cundinamarca, Colombia.
UVCO: Museo de Entomología, Universidad del Valle, Cali, Valle del Cauca, Colombia.
Material studied. Harmonia axyridis (Pallas). Colombia: Antioquia: Amalfi, Bosque, 26.x.2000, coll.
O. Ruíz, det. John A. Quiroz, 1 specimen (No. 7465: 10); Cañón del río Porce, 18.iii.1998, coll. J. G.
Hurtado, det. John A. Quiroz, ex. insect net, 1 specimen (No. 7465: 29); Copacabana, Relleno Sanitario,
Curva de Rodas, 24.x.2000, coll. D. Acevedo, det. John A. Quiroz, 4 specimens (No. 7465: 11-14); La
Unión, 01.iii.1998, coll. J. Jaramillo, det. John A. Quiroz, ex. insect net, 1 specimen (No. 7465: 30);
Medellín, 03.xi.1998, coll. R. Vélez, det. John A. Quiroz, ex. Preying upon aphids on Jacaranda caucana,
6 specimens (No. 7465: 1-6), Medellín, Univ. Nacional de Colombia, 28.ii.1998, coll. A. Rodríguez, det.
John A. Quiroz, ex. plant locally called Morera, 1 specimen (No. 7465-20); Medellín, Univ. Nacional de
Colombia, 04.iv.1998, coll. A. Rodríguez, det. John A. Quiroz, ex. plant locally called Nacedero, 1 speci-
men (No. 7465: 21); Medellín, Univ. Nacional de Colombia, 25.iv.1998, coll. A. Rodríguez, det. John A.
Quiroz ex. plant locally called Nacedero, 1 specimen (No. 7465: 22); Medellín, Univ. Nacional de Colom-
bia, 13.v.1998, coll. A. Rodríguez, det. John A. Quiroz, ex. Amaranthus sp., 1 specimen (no. 7465: 23);
Medellín, Univ. Nacional de Colombia, 01.iii.1998, coll. A. Rodríguez, det. John A. Quiroz, ex. grass, 1
specimen (No. 7465: 24); Medellín, Universidad Nacional de Colombia, 26.ii.1998, coll. A. Rodríguez, det.
John A. Quiroz, ex. grass, 1 specimen (No. 7465: 25); Medellín, Univ. Nacional de Colombia, 9.iv.1998,
coll. A. Rodríguez, det. John A. Quiroz, ex. Cajanus cajan, 3 specimens (No. 7465: 26-28); Medellín, Univ.
Nacional de Colombia, 12.iv.1998, coll. D. Terrazas, det. John A. Quiroz, ex. Symphytum officinale, 1
specimen (No. 7465: 31); Rionegro, 24.ii.1998, coll. A. Rodríguez, det. John A. Quiroz, ex. corn, 5 speci-
mens (No. 7465: 15-19); Santa Fé de Antioquia, 30.ix.2000, coll. R. Gaviria, det. John A. Quiroz, ex.
caugth on flight, 1 specimen (No. 7465: 9) (MEFLG); Caldas: Manizales, 05°04'N,75°, 31'W, 2216 m
a.s.l., 27.iv.2005, colls. Luque N. & Jamaica D., ex. Sweeping net, 2 specimens (UNAB); Cauca: Bolivar,
03.vi.1994, coll. Deisy Martínez, ex. Pastos, 1 specimen (UDENAR); Cundinamarca: Bogotá, Universidad
Nacional de Colombia, 04°38’07"N, 74°04’57"W, 2600 m a.s.l., 03.viii.2011, coll. D. Suarez, ex. Croton
bogotanus (Euphorbiaceae), 1 specimen; Silvania, Finca el Altillo, 04°24’N, 74°23'W, 1470 m a.s.l., 20.v.2001,
colls. C. Forero & E. Rodríguez, 1 specimen; Caquezá, Girón de Blancos, 04°24’30"N, 73°63’50"W, 1740 m
a.s.l., 16.xi.2003, coll. A. Forero (UNAB); Bogotá, Universidad Nacional de Colombia, Bofota Campus,
24.vi.2011, coll. Edwin Ariza, 4 specimens (No. 054076, 054077, 054078, 054079) (ICN); Nariño: San
José, 18.i.1990, coll. L. Miranda, ex. Foliage, 2 specimens; La Union, 08.xii.1994, coll. Carlos Solarte, ex.
Light trap, 1 specimen; Yaquanquer, 27.iii.2002, coll. Oswal Estrada, ex. Potato, 1 specimen; Chachagüi,
coll. Adriana Ch., 01.x.1989, ex. Foliage, 1 specimen (UDENAR); Tolima: Espinal, 04°09’10"N, 74°12’19"W,
322 m a.s.l., 26.iv.2005, coll. L. Camilo, 1 specimen; Espinal, 04°09’10"N, 74°12’19"W, 322 m a.s.l., 26.iii.2005,
coll. M. Velandia, ex. Captured in flight, 1 specimen (UNAB); Valle del Cauca: Cali, Dapa, 1700 m
a.s.l., 14.vii.2002, coll. Ana María Correa, 1 specimen (UVCO); La Unión, 04°32’N, 73°03’W, 975 m a.s.l.,
27.iv.2005, coll. A. Sánchez, ex. Meadow, 1 specimen (UNAB); Palmira, Corporación Colombiana de
Investigación Agropecuaria (CORPOICA), Centro de Investigación Palmira, 29.xii.2011, coll. H. Rodriguez,
ex. Citrus sp., 1 specimen; Valle del Cauca, Caicedonia, finca Jamaica, 29.xii.2011, coll. H. Rodriguez, ex.
Citrus sp., 1 specimen (GGPC); Palmira, 27.xi.2001, coll. Ángela Rojas, 1 specimen; Palmira, 5.xi.2002,
coll. O. Londoño, 1 specimen; Palmira, 1001 m a.s.l., 05.ix.2007, coll. O. Cárdenas, No. 12, 1 specimen;
Palmira, 15.ix.2007, 1000 m a.s.l., coll. G. Arroyo, No. 19, 1 specimen; Palmira, 06.ix.2007, 1200 m a.s.l.,
coll. N. Melo, No. 18, ex. Grass, 1 specimen; Palmira, 1000 m a.s.l., 22.x.2006, coll. F. Campuzano, No.
16, ex. Leaf litter, 1 specimen; Palmira, 1000 m a.s.l., 8.xii.2007, coll. A. Duran, No. 8, ex. On ground, 1
specimen; Palmira, 1000 m a.s.l., 20.ix.2006, coll. A. Vega, 1 specimen; Palmira, 1000 m a.s.l., 03.x.2006,
coll. R. Bolarta, No. 45, ex. Corn, 1 specimen; Palmira, 100 m a.s.l., 12.xi.2007, coll. E. Arbeláez, #18, ex.
Leaf litter, 1 specimen; Palmira, 1000 m a.s.l., 27.iv.2005, coll. J. Gutiérrez, 1 specimen; Palmira, ICA,
12.viii.2000, coll. Grupo CBA, ex. Cotton, 1 specimen; Palmira, 10.xi.2006, coll. S. Gómez, ex. Ground, 1
specimen; Palmira, 21.ix.2004, coll. L. López, ex. Shrub, 1 specimen; Buitrera, 26.v.2000, coll. Franco, 1
INSECTA MUNDI 0283, February 2013 5
HARMONIA AXYRIDIS IN COLOMBIA
specimen; ICA, 23.v.2000, coll. Rodríguez; Palmira, km 30, 16.v.2000, coll. Pastrana, 1 specimen; Palmira,
12.iv.2000, coll. Martínez, 1 specimen; Ingenio Providencia, 5.v.2000, coll. Rodríguez, 1 specimen (CEUNP);
Palmira, 13.xii.2000, coll. A. Trochez, ex. Citrus, 3 specimens; Palmira, viii.1999, coll. J. Barrera, ex.
Cotton, 1 specimen (MECP); Palmira, 19.iv.2003, coll. Fulvia Garcia, ex. Zea mays, 1 specimen; Yumbo,
06.v.2003, coll. Fulvia Garcia, ex. Gossypium hirsutum, 1 specimen (CIAT); Tuluá, 2.vii.2000, coll. A.
Madrigal, det. John A. Quiroz, ex. Gossypium hirsutum, 2 specimens (No. 7465: 7 & 8) (MEFLG).
Results and Discussion
The earliest collection date of H. axyridis in Colombia is from 1989, from a specimen collected in the
municipality of San José, in the State of Nariño, with several specimens collected in the 1990s in Bolivar
(Cauca), Chachagüi, La Unión, San José (Nariño), and Palmira (Valle del Cauca). There is a clear
increase in number of specimens in the 2000s, and a wider distribution in additional departments, namely,
Antioquia, Caldas, Cundinamarca and Tolima. This suggests that H. axyridis was introduced into Co-
lombia in the late 1980s, at least 22 years earlier than the first published reports of H. axyridis in
Colombia (Amat-Garcia et al. 2011; Brown et al. 2011) and since then it has expanded its distribution.
The earliest recorded introduction of H. axyridis in South America was in 1986 in Mendoza, Argentina
(García et al. 1999, apud Poutsma et al. 2008). This means that the introduction of H. axyridis into
Colombia was also one of the earliest introductions of the species into South America.
Harmonia axyridis is very common in the State of Valle del Cauca (T.K., personal observation). It has
displaced other coccinellids, such as Hippodamia convergens Guérin-Méneville, 1842 and Coleomegilla
maculata (De Geer, 1775) from a cassava orchard at the International Center for Tropical Agriculture
located in Palmira (M. P. Hernandez, personal communication). In Colombia, H. axyridis has not been
found yet in Santa Marta (Magdalena) (A. Arcila, personal communication) nor on San Andres island
(M. F. Maya, personal communication). The species appear to be closely associated with human activity,
e.g., farming and urban areas. Harmonia axyridis was likely introduced either accidentally on plant
material, or intentionally for biological control purposes, and not through natural expansion. Either
way, the coccinellid now appears to be widespread in many parts of Colombia. Further studies should be
carried out in other Colombian museums and in other States in order to get more accurate information
on the time and path of introduction of H. axyridis in Colombia.
Acknowledgments
Many thanks to Ángela Arcila (Corpoica, Centro de Investigación La Libertad), Ángela Melo (MEFLG),
Carmen Elisa Posso (UVCO), María del Pilar Hernández (CIAT), María Fernanda Maya Álvarez
(Universidad Nacional, Sede Caribe), Marilyn Belline Manrique (Universidad de Nariño), Carlos
Sarmiento (ICN), Andrea Amalia Ramos Portilla (UNAB), Francisco Serna (UNAB), John A. Quiroz
(MEFLG), Tito Bacca Ibarra (UDENAR), Pedro Antonio Ramos Racines (CEUNP), Santos Barrera
Lemus (CEUNP). Especial thanks to Penny Gullan (The Australian National University, Canberra,
Australia) and to Dr. M. Bora Kaydan (Çukurova Üniversity, Adana, Turkey) for kindly reviewing the
manuscript.
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INSECTA MUNDI 0283, February 2013 7
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Received January 6, 2013; Accepted February 6, 2013.
8 INSECTA MUNDI 0283, February 2013 KONDO AND GONZÁLEZ
... UU. y el sur de Canadá (Koch, 2003). En Colombia, la introducción de H. axyridis ocurrió en 1989 o antes y es el segundo registro más antiguo de la especie en Sur América, después de las liberaciones en Argentina en 1986 (Kondo & González, 2013). En la Foto: Guillermo León M. actualidad, se encuentra frecuentemente en varios cultivos del país, como algodón, soya, maíz y cítricos. ...
... La mariquita asiática H. axyridis parece estar estrechamente asociada a la actividad humana, tanto en la agricultura como en las zonas urbanas; probablemente fue introducida al país de forma accidental en algún tipo de material vegetal o intencionalmente con fines de control biológico, pero no a través de la expansión natural (Kondo & González, 2013). El H. axyridis es reconocido como un coccinélido muy voraz y está presente en muchas regiones de Colombia; debido a su alta voracidad como depredador y a su alta fecundidad y fertilidad, se reporta que Foto: Takumasa Kondo Figura 11. ...
... Un adulto de la mariquita asiática Harmonia axyridis busca larvas del minador de los cítricos para alimentarse. esta mariquita ha desplazado o compite por alimento con otros coccinélidos, como Hippodamia convergens Guérin-Méneville y Coleomegilla maculata (De Geer) en el Valle del Cauca (Kondo & González, 2013). ...
... UU. y el sur de Canadá (Koch, 2003). En Colombia, la introducción de H. axyridis ocurrió en 1989 o antes y es el segundo registro más antiguo de la especie en Sur América, después de las liberaciones en Argentina en 1986 (Kondo & González, 2013). En la Foto: Guillermo León M. actualidad, se encuentra frecuentemente en varios cultivos del país, como algodón, soya, maíz y cítricos. ...
... La mariquita asiática H. axyridis parece estar estrechamente asociada a la actividad humana, tanto en la agricultura como en las zonas urbanas; probablemente fue introducida al país de forma accidental en algún tipo de material vegetal o intencionalmente con fines de control biológico, pero no a través de la expansión natural (Kondo & González, 2013). El H. axyridis es reconocido como un coccinélido muy voraz y está presente en muchas regiones de Colombia; debido a su alta voracidad como depredador y a su alta fecundidad y fertilidad, se reporta que Foto: Takumasa Kondo Figura 11. ...
... Un adulto de la mariquita asiática Harmonia axyridis busca larvas del minador de los cítricos para alimentarse. esta mariquita ha desplazado o compite por alimento con otros coccinélidos, como Hippodamia convergens Guérin-Méneville y Coleomegilla maculata (De Geer) en el Valle del Cauca (Kondo & González, 2013). ...
Book
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Luego de varios años de investigación, se han encontrado y registrado las especies de insectos y ácaros que se asocian a los cultivos de cítricos en Colombia, y se presentan en este documento. Si bien este es un trabajo que debe continuar, el libro divulga los avances y conocimientos generados a la comunidad citrícola y las personas interesadas en el tema. La información didáctica del presente documento constituye una guía clara, valiosa y con suficientes fotografías que sirven de ayuda a los productores, los asistentes técnicos, los profesores y los estudiantes de agronomía, entomología y carreras afines, tanto para labores pedagógicas como para tomar decisiones sobre el manejo de plantaciones. Este documento presenta información sobre los programas de manejo integrado de plagas para cultivos de cítricos y se orienta a disminuir el uso de plaguicidas, reducir los costos de producción, aminorar el impacto ambiental y posibilitar la obtención de frutas con tecnologías limpias, que hoy en día son más apetecidas por los consumidores y tienen valor agregado. La producción de frutas obtenidas con el mínimo uso de pesticidas es una demanda creciente en el mundo, y la información consignada en este documento contribuye, en buena medida, al logro de este objetivo.
... Based on museum records Kondo and González (2013) concluded that introduction of H. axyridis into Colombia occurred in or before 1988, although the first reports of H. axyridis in this country appeared in 2011. Currently, the beetle is well established in Colombia and recorded from the states of Antioquia, Caldas, Cauca, Cundinamarca, Nariño, Tolima and Valle del Cauca. ...
... Currently, the beetle is well established in Colombia and recorded from the states of Antioquia, Caldas, Cauca, Cundinamarca, Nariño, Tolima and Valle del Cauca. Circumstantial evidence (Kondo and González 2013) suggested that it had displaced other coccinellids, such as H. convergens and Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae), in a cassava orchard at the International Center for Tropical Agriculture located in Palmira (M.P. Hernandez, personal communication). Interestingly, H. axyridis was among the 16 species of natural enemies found attacking the Asian citrus psyllid D. citri in the state of Valle del Cauca (Kondo et al. 2020). ...
Chapter
In Latin America different types of biological control, including documentation of natural control, and different biological control agents, entomopathogens and herbivores used in weed management, were applied since the mid-1800s. Numerous successes have been obtained since and importation, augmentative and conservation biological control of pests, weeds and plant diseases are implemented currently on millions of hectares of intensive and traditional crops, forestry, pastures, animal husbandry, and terrestrial and aquatic weeds. Programmes of particular interest are those concerning control of pests and plant diseases in crops typical for this region, such as asparagus, cassava, mate trees, maize, potato, and quinoa. The largest and the most interesting successful control programmes are presented, as well as several programmes that failed. Importation and augmentative biological control are used each on more than 30 million hectares in the region. Implementation of conservation biological control started as early as 1910 and is now an approach intensely researched in many countries. The first case of natural biological control was documented in 1884 and control of pests by naturally occurring beneficial organisms has been demonstrated extensively in the region. Latin America has provided many natural enemies for control of pests, diseases and weeds in other parts of the world and examples of introductions leading to success are presented. Agents provided for biological control of weeds have been especially successful. Finally, factors that hamper and stimulate use of biological control in the region are summarized.
... Harmonia axyridis, native to East Asia, nowadays has established populations in America, Europe, Africa, and New Zealand, and it is considered the most invasive ladybird on Earth [7]. Despite predictions of its potential invasive expansion, the presence of Harmonia axyridis and other non-native ladybird beetles in many countries of the Global South has usually been reported after populations are well-established [8]. Statistically, the use of citizen science records has proved exceptionally useful to discover new populations [9]. ...
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Fast and accurate taxonomic identification of invasive trans-located ladybird beetle species is essential to prevent significant impacts on biological communities, ecosystem functions, and agricultural business economics. Therefore, in this work we propose a two-step automatic detector for ladybird beetles in random environment images as the first stage towards an automated classification system. First, an image processing module composed of a saliency map representation, simple linear iterative clustering superpixels segmentation, and active contour methods allowed us to generate bounding boxes with possible ladybird beetles locations within an image. Subsequently, a deep convolutional neural network-based classifier selects only the bounding boxes with ladybird beetles as the final output. This method was validated on a 2, 300 ladybird beetle image data set from Ecuador and Colombia obtained from the iNaturalist project. The proposed approach achieved an accuracy score of 92% and an area under the receiver operating characteristic curve of 0.977 for the bounding box generation and classification tasks. These successful results enable the proposed detector as a valuable tool for helping specialists in the ladybird beetle detection problem.
... Harmonia axyridis is reported in most countries in South America (Amat-García et al. 2011;González and Kondo 2012;Koch et al. 2011;Kondo and González 2013;Nedvěd and Krejčík 2010;Saini 2004;Solano and Arcaya 2014). Based on factors such as climate and habitat, it has been predicted that H. axyridis would become established across broad areas of South America (Koch et al. 2006b). ...
... In South America, H. axyridis was introduced for biological control in the late 1980s in several countries (Chile, Argentina, Brazil and Colombia), but wild populations have only been reported more recently in these countries and also in Peru, Paraguay, Uruguay, Ecuador and Venezuela (Saini, 2004;Grez et al., 2010a;Nedv ed & Krej c ık, 2010;Amat-Garc ıa et al., 2011;Brown et al., 2011a;Gonz alez & Kondo, 2012;Kondo & Gonz alez, 2013;Solano & Arcaya, 2014). Nevertheless, in most of these countries the negative impacts have not been assessed and so it has not been described as invasive. ...
... In South America, H. axyridis was introduced for biological control in the late 1980s in several countries (Chile, Argentina, Brazil and Colombia), but wild populations have only been reported more recently in these countries and also in Peru, Paraguay, Uruguay, Ecuador and Venezuela (Saini, 2004;Grez et al., 2010a;Nedv ed & Krej c ık, 2010;Amat-Garc ıa et al., 2011;Brown et al., 2011a;Gonz alez & Kondo, 2012;Kondo & Gonz alez, 2013;Solano & Arcaya, 2014). Nevertheless, in most of these countries the negative impacts have not been assessed and so it has not been described as invasive. ...
Research
Biological invasions are one of the major threats to biodiversity. Usually highly disturbed anthropogenic habitats favour invasion by alien species such as the coccinellid Harmonia axyridis. The spread and impact of this species has been documented in Europe and North America, but no information exists for South America. The aims of this study were to: (1) document the process of invasion of H. axyridis in Chile, (2) compare the abundance of H. axyridis in different habitats with varying degrees of disturbance and (3) assess change in the coccinellid assemblages in alfalfa fields over the 6 years following invasion.
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Harmonia axyridis is a ladybird extensively used around the world for biological control of agricultural pests. However, it has become invasive in several countries, producing negative ecological and socio-economic impacts. Herein, we review the invasion history of the Harlequin Ladybird Harmonia axyridis (Pallas, 1773) in Ecuador. Although first reported in Ecuador in 2012, museum specimens date back to 2004 and it is currently established across the country, especially along the Andean region. Due to its invasive nature, further studies are urgently needed to evaluate possible impacts of H. axyridis on the Ecuadorian biodiversity and agroindustry.
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Harmonia axyridis (Coleoptera, Coccinellidae) is a globally invasive ladybird. It has been intentionally introduced in many countries as a biological control agent, whereas it has been unintentionally released in many others. Climatic factors are important in limiting the spread of H. axyridis. For example, very few records are known from tropical or desert regions. Currently , no published reports are known from Central America. Here, we report H. axyridis from Costa Rica, Guatemala, Honduras, Panama, and Puerto Rico. Specimens were either observed by the authors, discovered in dried insect collections, or retrieved from searching through online photographs available from the citizen science project iNaturalist and the photo-sharing website Flickr. These new records and the wide distribution of H. axyridis in Latin America suggest several invasion events, which have gone unnoticed until now. We stress the need for further, large-scale monitoring and show the advantage of citizen science to assess the presence of invasive alien species.
Article
The dragonfly Erpetogomphus sabaleticus Williamson, 1918 (Odonata: Anisoptera: Gomphidae) is for the first time reported preying on Diaphorina citri Kuwayama (Hemiptera: Liviidae). A compiled list of more than 63 species distributed in seven orders and seventeen families of arthropod (insects and spiders) natural enemies of D. citri is provided.
Conference Paper
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Strong inventories of cotton pests natural enemies were made in Paraguay by B. Michel and P. Prudent (1987 to 1992). Collections of the cotton entomofauna have been maintained, with visual observations during field visits of the national cotton program (PIEA) experimental plots. The new following predators have been identified: Oecanthus sp. (Orthoptera Oecanthidae), Acontiothespis brevipennis and A. concinna (Dictyoptera Mantodea, Hymenopodidae), Orthoderella ornata (Mantidae), Ceratocapsus paraguayensis and C. dispersus (Hemiptera, Coreidae), Oplomus sp. (Pentatomidae Asopinae), Castrida elegans granulatum (Carabidae), Phelister rufinotus (Histeridae), Trox suberosus (Coleoptera, Trogidae). Among 2167 specimens of Coccinellidae identified by C. Duverger, 2052 (94.7%) belonged to Pullus gillae, 85 were identified as Hyperaspis festiva, 17 were Pullus loewi, 13 belonged to Naemia (Eriopis) connexa and 8 to Cycloneda sanguinea species. None of Scymnus have been identified. The genus Pullus, very similar, is dominant. Inside the Reduviidae family (Harpactorinae) the following species were identified by J.M. Bérenger: Zelus longipes, very common, Z. laticornis, Z. ruficeps, Z. armillatus, Atrachelus cinereus ssp. crassicornis and Apiomerus apicalis. Podisus nigrispinosus is a common Pentatomidae predator on Alabama argillacea. Harmonia axyridis has been identified as an adult for the first time in Paraguay in cotton field in Caaguazu and Coronel Bogado, in January 2006. Larvae have been observed-also on cotton-in Caaguazu. Larvae and one adult have been observed in Caacupe in January 2007. Until now, this species, known as an invasive coccinellid from Asia, has been mentioned in the South American literature in Argentina (Buenos Aires) at the end of 2001 by Saini and in Curitiba-PR (Brazil) 2002 by de Almeida and da Silva (UFPR). We have observed larvae on cotton in Cascavel-PR in may 2006. The potential intraguild predation by this species has to be documented in the future.
Article
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153 T he multicolored Asian ladybeetle, Harmo-nia axyridis Pallas (Coleoptera; Coccinellidae), has become a well-known nuisance insect in North America (see other sym-posium summaries in this issue). Despite these nega-tive aspects, H. axyridis also plays a beneficial role by suppressing pests in a variety of cropping sys-tems (Koch 2003). The recent arrival of the soy-bean aphid, Aphis glycines Matsumura (Homoptera: Aphididae) into North American soybean production systems has created a situa-tion in which the positive and negative aspects of this insect are highlighted. Here we discuss some recent studies exploring the role of H. axyridis in biocontrol of soybean aphid. The soybean aphid is a major new invasive pest of soybean (Glycine max L.) in North America. First discovered in July 2000 in Wisconsin and adjoining states, it is currently distributed in 21 U.S. states and parts of Canada. In 2003, more than 42 million acres of soybean in the North Cen-tral United States were infested, and more than 7 million acres were treated with insecticides to con-trol A. glycines (Landis et al. 2003). Populations exceeding 24,000 aphids per plant and 40% losses in seed yield have been reported (DiFonzo and Hines 2002). Aphis glycines overwinters on plants in the genus Rhamnus (buckthorn), with summer generations occurring on soybean. The exotic in-vasive shrub Rhamnus cathartica appears to be the key overwintering host for A. glycines in Michi-gan. Fall migration to R. cathartica by A. glycines gynopare and production of oviparae and over-wintering eggs in the field has been observed with subsequent production of fundatrices and alate viviparous females and migration to soybean the following spring (Ragsdale et al. 2004). Alates ar-rive in soybean in early-to mid-June, soon after crop emergence (Fox 2002). Natural enemies play a key role in suppressing soybean aphid populations (Fox et al. 2004). In China, where soybean aphid outbreaks are rare, coccinellids are among the most common natural enemies; however, soybean aphid colonies also typi-cally experience parasitism rates of 40% (G. Heimpel, University of Minnesota personal obser-vation). In the United States, 22 predator taxa are reported to attack soybean aphid, with generalist predators including Harmonia axyridis, Coccinella septempunctata, and Orius insidiosus dominat-ing the natural enemy community (Fox and Landis 2003, Rutledge et al. 2004). The arrival of the soy-bean aphid in North America has created a vast new prey base for H. axyridis in soybean, a habi-tat formerly devoid of aphid prey. In soybean aphid outbreak years, soybean fields support large num-bers of H. axyridis that can subsequently cause problems for homeowners and fruit producers. In 2001-2003, we conducted a series of predator exclusion tri-als to examine the in-fluence of predation on soybean aphid popu-lations. In early season trials in 2001-2002, we used clip cages to protect establishing aphids from predation for 24 h (Fox and Landis, unpublished); for midseason trials, we used 1-m 3 field cages to investigate predator impacts on aphid population growth over 7 days (Fox et al., in press). In 2004, H. axyridis con-stituted 66% of the early season predator community, with all preda-tors combining to reduce aphid density by 26-56% over exclusion cages. However, in 2002, H. axyridis emerged before aphids were present, and adults did not remain in soybean. In midseason trials, H. axyridis had recolonized fields and constituted 57% of the total predator community in 2001, contributing to a 54% re-duction in aphid abundance. In 2002 and 2003, predator reduction of aphid density was very high (>90 in both years). In 2002, H. axyridis Fig. 1. Multicolored Asian lady beetle (Harmonia axyridis Pallas) attacking soybean aphid (Aphis glycines Matsumura) (Photo: D. A. Landis).
Article
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In this work, we document the presence of Harmonia axyridis in Chile, an invasive coccinellid species that has had negative effects in other regions of the world, such as: impacts on non-target arthropods, invasions of houses and fruit damage. This species has been found in the last three years in the Metropolitan and Valparaíso regions, in crops, pine plantations and inside houses. We warn about the consequences of the introduction of this species to Chile and claim to take actions to avoid its spread in the country.
Article
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The generalist predator Harmonia axyridis Pallas, 1772, is an effective and voracious biological control of pests, especially of aphids. However, worldwide is considered a threat to fruit production, in the reduction of beneficial fauna native and as a household pest. It has been detected from 90 of the last century in several South American countries, mainly in Argentina, Brazil, Uruguay, Colombia and Chile. Its invasion in Peru in recent years includes the arrival, establishment and spread in different urban, agricultural and natural ecosystems. The aim of this study was to determine the characteristics of the invasion of H. axyridis and an environmental risk assessment in Peru. The study was non-probabilistic, not experimental, and cross-sectional chance in 20 towns of Lima, Callao and Madre de Dios, Peru from January to March 2011 to search for different species of Coccinellidae, using standard procedures for collecting entomological. It was recorded aphid-prey specie, and specie and family plant associated. Of the total individuals of coccinellid collected, the 48.60% were H. axyridis, Cycloneda sanguine (29.01%), Hippodamia convergens (7.37%), Prodilis inclytus (3.81%), Eriopis connexa (3.56%) and other seven species (7.66%). Harmonia axyridis, C. sanguinea and H. convergens were surveyed in the following families and locations: 14:14, 13:14 and 4:4, respectively. With regard to the environmental risk assessment of H. axyridis was used van Lenteren protocol that assesses the magnitude and likelihood of risk based on their ability to establish, dispersal potential nontarget habitats, host range, and direct and indirect effects. The environmental risk index (ARI) was 77 points from a maximum of 125. The results show a reduction in frequency relative percentage of other species of coccinellids, especially H. convergens and an increase in H. axyridis related to high voracity as a predator, and a high fertility and fecundity. It includes an annotated list of the main species of Coccinellidae collected.
Article
Resumen: Se actualiza toda la bibliografía taxonómica relativa a Coccinellidae de América del Sur desde el año 1945 a la fe-cha. Adicionalmente, se incluye una lista de nuevos registros de especies del continente, por países. Se citan por primera vez 14 especies para Argentina, tres para Bolivia, una para Brasil, dos para Chile, tres para Ecuador, 25 para Paraguay, 21 para Perú, una para Uruguay y una para Venezuela. Asimismo, se proponen las nuevas combinaciones Calloeneis signata (Kors-chefsky) comb. nov., Tenuisvalvae rosariensis (Gordon & Canepari) comb. nov. y Zagreus hexasticta (Crotch) comb. nov. Adicionalmente se nombra Hyperaspis gordoni n. nom. para la especie H. brethesi Gordon y Canepari, nombre preocupado. Palabras clave: Coleoptera, Coccinellidae, taxonomía, bibliografía, distribución geográfica, América del Sur. An update on the literature of the South American Coccinellidae, with new records (Insecta: Coleoptera) Abstract: A compilation is made of all the taxonomic literature on the South American Coccinellidae from the year 1945 to the present. Additionally, a list is given of new species records from the continent, by countries. A number of first country records are presented: 14 species are new to Argentina, 3 to Bolivia, 1 to Brazil, 2 to Chile, 3 to Ecuador, 25 to Paraguay, 21 to Peru, 1 to Uruguay and 1 to Venezuela. The following new combinations are proposed: Calloeneis signata (Korschefsky) comb. nov., Tenuisvalvae rosariensis (Gordon & Canepari) comb. nov., Zagreus hexasticta (Crotch) comb. nov. and Hyperaspis gordoni n. nom. (for the species H. brethesi Gordon and Canepari, name preoccupied). Introducción El conocimiento de los Coccinellidae de América del Sur ha tenido un fuerte impulso durante los últimos 35 años gracias a los trabajos de Robert D. Gordon, quien ha publicado revisio-nes de subfamilias, tribus y géneros, describiendo alrededor de 500 nuevas especies. Muchos otros especialistas han pu-blicado también trabajos, lo que permite hoy en día disponer de tratamientos taxonómicos modernos para aproximadamen-te un 70% de la fauna de Coccinellidae de América del Sur. Lamentablemente no existen trabajos que permitan dar una visión panorámica de la fauna de Coccinellidae del subconti-nente, ya que la última lista disponible y bibliografía completa data ya de 65 años (Blackwelder, 1945) y consideraba 735 especies para el área. Por otro lado, muchas de las especies descritas o revisa-das recientemente se basan en uno o dos ejemplares, ya sea porque se revisaron solo los tipos de especies ya descritas, o por corresponder a descripción de nuevas especies basadas en ejemplares muy limitados. Con ello, el conocimiento de la distribución geográfica de las especies no ha sido resuelto, en especial en América tropical donde algunas especies se distri-buyen sobre extensas áreas que en muchos casos cubren va-rios países. Durante los últimos cinco años el autor ha estado traba-jando en la implementación de sitios web dedicados a Cocci-nellidae de Chile, Argentina, Perú y Paraguay. En el contexto de ese proyecto, muchas personas e instituciones han colabo-rado poniendo a disposición sus colecciones o colectas o enviando material bibliográfico al autor, lo cual ha permitido establecer la existencia de aproximadamente 1.400 especies descritas a la fecha para la región, de las cuales alrededor de 400 se encuentran documentadas en los sitios web indicados. Esta trabajo actualiza toda la bibliografía taxonómica publicada con posterioridad a Blackwelder (1945). Adicio-nalmente recopila 72 primeras citas de especies para 9 países de América del Sur. Cabe hacer notar que gran parte de esta información ya se encuentra disponible mediante publicacio-nes no formales en Internet (González, 2006, 2008 y 2010; González y Vandenberg, 2007; Castillo y Miró, 2010). Fi-nalmente para las especies incluidas en esta lista, se incluye la distribución geográfica conocida, ya sea por la literatura o por ejemplares revisados por el autor.
Article
Harmonia axyridis (Pallas), an Old World Coccinellini, is reported as es-tablished in southeastern Louisiana. A few specimens were also collected in eastern Mis-sissippi. The species is described, illustrated, and compared to //. dimidiala (F.) and II. quadripunctata (Pontopiddian). A lady beetle, not previously known to be established in the United States, was col-lected near Abita Springs, St. Tammany Parish, and in other southeastern Louisiana parishes. A few specimens were also col-lected in eastern Mississippi. Harmonia ax-yridis (Pallas) occurs in southern Siberia, and Washington from 1978 to 1982 (Gordon 1985, P. W. Schae-fer, pers. comm.). Specimens were also re-leased in Connecticut in 1985 during a study of the potential of H. axyridis to control Matsucoccus resinosae Bean and Godwin (McClure 1987). Japan was the country of origin of the specimens released in Louisiana and Mis-sissippi. A single release of 32 specimens was made in Shreveport, Bossier [sic] Par-ish, on August 24, 1979, and eight releases of 3781 specimens were made in Leland and Stoneville in Washington County, Missis-sippi, from July 12 to October 23, 1980 (P. W. Schaefer, pers. comm.). There were no subsequent reports that this species had be-come established.