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Review

A Review of the Arrival, Effects, and Management of Bagrada hilaris in South America: The Case of Chile

by
Marta V. Albornoz
,
Camila C. Santander
and
Armando Alfaro-Tapia
*
Centro Regional de Investigación e Innovación para la Sostenibilidad de la Agricultura y los Territorios Rurales, Ceres, Pontificia Universidad Católica de Valparaíso, Quillota 2260000, Chile
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(10), 1072; https://doi.org/10.3390/horticulturae10101072
Submission received: 13 September 2024 / Revised: 4 October 2024 / Accepted: 5 October 2024 / Published: 8 October 2024
(This article belongs to the Section Insect Pest Management)
Browse Figure
Versions Notes

Abstract

:
Biological invasions are partly defined by their ability to spread rapidly within invaded regions, posing threats to biodiversity and local species assemblages. The painted bug, Bagrada hilaris (Hemiptera, Pentatomidae) (Burmeister, 1835), originally described as being from India, is an important pest worldwide, mainly due to the serious economic losses incurred and the large number of zones invaded. Since its initial detection in Chile in 2016, the invasive and destructive paint bug has started its invasion to the east and invaded new areas in South America. Without adequate control methods, the insect may threaten brassica crop production, resulting in yield losses greater than 70% in recently infested areas. The extraordinarily wide range of the B. hilaris invasion has necessitated studies describing its biology and ecology, as well as highlighting the urgent need for effective and long-term management techniques. Hence, thoroughly revising the data on this pest in new areas that have been invaded, as well as in the area of origin, is expected to enable the development of management programs. This review incorporates information on B. hilaris in South America, including the invasion, ecology, and potential management approaches, which may allow for efficient integrated pest management, mainly in Chile. Lastly, researchers are expected to break the bottlenecks of some key issues, offering valuable perspectives for identifying strategies that warrant additional research as potential biological control agents for B. hilaris in South America, utilizing either augmentative or conservation biological control approaches, as well as semiochemicals and cultural practices.

1. Introduction

One of the most important concerns in the 21st century regarding worldwide food security is biological invasions. Invasive alien species (IAS) and agriculture are closely related, which has facilitated the invasion of many agricultural pests beyond their native ranges [1,2]. Pests can reduce yields, increase management costs, and lead to the use of agrochemicals [3]. The painted bug, Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae), is one of the most destructive pests affecting commercial brassica crops [4,5], with a great number of biological and ecological traits that have increased its invasiveness [6,7]. These traits include the fact that B. hilaris does not lay its eggs in clusters and is the only known Pentatomidae (Hemiptera) species to oviposit in soil [8]. In addition, the nymphs and adults represent the mobile life stages with aposematic coloring; generally, they can be found in groups [9]. On the other hand, abiotic and biotic factors contribute to the threat posed by this species. It has been observed that B. hilaris is well-adapted to warm conditions, with the highest survival rate between 24 and 35 °C [10]. In addition, no effective control methods, such as pheromone traps, successful biological control, or other nonchemical management practices, exist for this pest [11].
B. hilaris is native to eastern and southern Africa and Asia, and it is considered one of the major important pests of oilseed brassica crops [4,12]. It is a multivoltine species with 10–12 generations per year that thrives under warm, dry conditions [4]. Feeding damage may be characterized by the presence of circular chlorotic patches or spots on leaf surfaces [4,13,14]. In the western hemisphere, this pest was first reported in Los Angeles County (CA) in 2008 [15], and it subsequently spread throughout Southern California, Arizona, and New Mexico [16]. This pest was not present in South America until December 2016, when it was recorded in Central Chile, reported for the first time near the city of Santiago de Chile (Quilicura), and subsequently in Argentina [6,17]; however, it has not yet been recorded in other South American countries. Since then, B. hilaris has increased in both number and spatial distribution, which are unambiguous indications that the insect is in the spreading stage of invasion. As a result of the continuous invasion of B. hilaris [7,11], applied research has started to examine several elements of its biology and ecology. Models based on the invasion of B. hilaris and global warming have previously been used to predict the possible invasion of this species in Chile [18] and South America [7]. However, there are no reports based on field data. For instance, there is no evidence about its thermal fitness [10] nor its relationship to the distribution and accessibility of biotic resources (e.g., host plants) [11,19,20]. Hence, knowledge of the bioecology of B. hilaris is crucial to understanding the processes underlying its successful establishment and dissemination, as well as for the proposal of management strategies.
Many strategies have been developed and implemented to manage B. hilaris. These include chemical control, such as the use of pesticides (pyrethroids, organophosphates, and recently, neonicotinoids) [11,13,21], cultural practices to prevent its spread, and biological control [22,23]; however, the existing literature does not indicate the specific methods used in South America. Research on biological control has demonstrated potential, as certain insect parasitoids, such as Gryon aetherium Talamas (Hymenoptera Scelionidae) [24,25], and predators, such as Eriopis chilensis, Hippodamia variegata (Coleoptera, Coccinellidae) [26], and Chrysoperla externa (Neuroptera, Chrysopidae) [27], have been identified as potential natural enemies of this pest. As a result, multiple studies around the world have evaluated different pest management techniques (e.g., biological control, botanical insecticides, cultural management, and the sterile insect technique) in an effort to prevent serious harm and significant economic losses [11,13,25,28,29,30]. Nevertheless, knowledge about this invasive species that has recently invaded areas such as South America is still developing. We thoroughly examine, unravel, and discuss relevant scientific information regarding the current status of B. hilaris in South America in this study, including its bioecology, its natural enemies, and the management techniques that have been attempted and/or used to control this pest since it was initially recorded in 2016, as well as potential management approaches.

2. Host Plant Range, Crop Damage, and Economic Impacts

One of the reasons for the successful establishment of an IAS pest in a new area is the abundance of host plants. These plants provide essential resources where they can feed, shelter, and reproduce [31]. Brassica (Brassicaceae) hosts (Figure 1), such as cauliflower (Brassica oleracea L. var. botrytis), cabbage (B. oleracea L. var. oleracea), broccoli (B. oleracea L. var. italica), kale (B. oleracea var. sabellica L.), rapeseed (Brassica napus L.), pakchoi (B. rapa subsp. chinensis L.), mizuna (B. rapa L. var. japonica), red mustard (B. juncea L.), arugula (Eruca sativa Mill), and radish (Raphanus sativus), as well as weeds of this family, such as mustard (Hirschfeldia incana L.), shepherd’s purse (Capsella bursa-pastoris L.), wild radish (R. raphanistrum L.), and Alyssum (Lobularia maritima L.), have been proposed to be the most suitable host plants for B. hilaris [11,32,33,34]. The fitness of this insect pest is substantially higher on these preferred hosts compared to plant species from other families, including Fabaceae, Amaranthaceae, Solanaceae, Poaceae, Apiaceae, and Asteraceae (Figure 1) [11], according to field and laboratory experiments. In brassicas, the damage caused by B. hilaris varies with both the plant’s morphology and its maturity [4,13,19]; for instance, leafy plants that do not form shoots (e.g., arugula) are attacked throughout the growing season [4]. In contrast, in cabbage and broccoli, B. hilaris prefers the youngest leaves, reproductive structures, and growing tips [35]. In this case, the main damage caused by B. hilaris occurs when the first true leaves of the host plant begin to develop; in this period, the plants are at the stage of greatest susceptibility [21], causing death in seedlings and leading to the generation of acephalous plants (without crown formation) or plants with multiple crowns, which makes their commercialization impossible [13]. It has been suggested that the attraction to newly emerged plants is determined by the unsaturated volatile hydrocarbons (diterpene hydrocarbons) emitted by the seedlings of Brassica species, providing host location cues [36], such as brassicadiene [37].
According to [4], at least 96 plant species from 25 families have been described as hosts of B. hilaris, of which at least 87 are present in Chile [32,33,34] (Table 1). Within this group of host plants, 31 correspond to crops (vegetables and fruit trees), 7 are used as forage plants, and 9 are cultivated for ornamental use. Considering only the area cultivated, this pest could damage more than 563,000 hectares (ha) in Chile [7]. The large number of hosts, the adaptability of this insect to different environments, and its interactions with the communities in which it establishes [38] have made B. hilaris a pest of great economic importance [14,19,35].
Table 1. List of plant species evaluated as Bagrada hilaris hosts. Adapted from [4] with new records of potential host plants in Chile [32,33,34,39]. The list shows the use, area cultivated, and distribution of the host plants in Chile.
Table 1. List of plant species evaluated as Bagrada hilaris hosts. Adapted from [4] with new records of potential host plants in Chile [32,33,34,39]. The list shows the use, area cultivated, and distribution of the host plants in Chile.
Plant FamilyScientific NamePlant
Type/Use		ReferenceSurface Cultivated in Chile/haRegional Distribution
in Chile
AmaranthaceaeBeta vulgaris L. subsp. maritimaWeed[33] Atacama—Valparaíso
Beta vulgaris L.Crop [4,34]1937Arica—La Araucanía
Chenopodium álbum L.Weed[4,32] Arica—Magallanes
Spinacia oleracea L.Crop[4]1161Atacama—Magallanes
AmaryllidaceaeAllium cepa L.Crop[34]8607Arica—La Araucanía
AnacardiaceaeMangifera indica L.Crop[4,34]10Arica
Apiaceae Daucus carota H.Crop[4]3038Arica—Los Lagos
AsteraceaeCarduus pycnocephalus L.Weed[34] Coquimbo—Los Lagos
Carthamus oxyacantha M.Weed[4,34] Coquimbo—Araucanía
Chrysanthemum sp. L.Ornamental [4,34] Atacama—Los Lagos
Cynara scolynus L.Crop[4]1535Arica—La Araucanía
Cynara cardunculus L.Weed[33] Coquimbo—Biobio
Dahlia sp. L.Ornamental[4,34] Atacama—Magallanes
Lactuca sativa L.Crop[4,34]8309Arica—Los Lagos
Lactuca serriola L.Weed[33] Antofagasta—La Araucanía
Schkuhria pinnata L.Weed[4] Arica—Coquimbo
Sonchus arvensis L.Weed[4] Magallanes
Sonchus asper L.Weed[33] Arica—Magallanes
Sonchus oleraceus L.Weed[33] Arica—Magallanes
BrassicaceaeBarbarea verna M.Weed[4] Metropolitana—Los Lagos
Brassica campestris L.Weed[4,32] Valparaíso—Biobio
Brassica juncea L.Crop[4,34]0.02Metropolitana
Brassica oleracea L. var. acephalaCrop[4,34] 27.2Arica—Los Lagos
Brassica oleracea L. var. botrytisCrop[4,33]1803.4Arica—La Araucanía
Brassica oleracea L. var. capitataCrop[4,33]2901.3Arica—Los Lagos
Brassica oleracea L. var. gemmiferaCrop[4]100Arica—La Araucanía
Brassica oleracea L. var. itálica Crop[4,33,34]2289.1Arica—La Araucanía
Brassica oleracea L. var. oleraceaCrop[39]2640Arica—La Araucanía
Brassica napus L.Crop[39]32,650Biobio—Los Lagos
Brassica rapa L. subsp. chinensisCrop[39]20Metropolitana
Brassica rapa L. subsp. japonicaCrop[39]5Metropolitana
Brassica rapa L. subsp. oleiferaWeed[4,34] Biobio—Los Lagos
Brassica rapa L. subsp. rapaPasture[4,34] Biobio—Los Lagos
Brassica rapa L. subsp. narinosaWeed[4] Arica—Magallanes
Brassica rapa L. subsp. nipposinicaWeed[4] Arica—Magallanes
Capsella bursa-pastoris L.Weed[4,33,34] Arica—Magallanes
Descurainia sophia L.Weed[4,34] Metropolitana—Magallanes
Descurainia nuttallii C.Weed[33] Antofagasta—Magallanes
Descurainia pimpinellifolia B.Weed[32] Antofagasta—Maule
Eruca sativa L.Crop[4,33] Coquimbo—La Araucanía
Hirschfeldia incana L.Weed[4,33,34] Atacama—Araucanía
Lepidium latifolium L.Weed[4,34] Antofagasta—Maule
Lepidium auriculatum R. and K.Weed[32] Antofagasta—Magallanes
Lepidium pseudodidymum T.Weed[32] Valparaíso—Magallanes
Lobularia marítima L.Ornamental[4,34] Tarapacá—Los Lagos
Matthiola sp. A.Ornamental[4,34] Antofagasta—Coquimbo
Raphanus sativus L.Crop[4,33,34] Valparaíso—Maule
Raphanus raphanistrum L.Weed[4,33,34] Antofagasta—Los Lagos
Sisymbrium irio L.Weed[4,34] Arica—Magallanes
Cannabaceae Cannabis sativa L.Crop[4,34] Arica—Los Lagos
CapparaceaeCapparis spinosa L.Ornamental[4,34] Arica—Valparaíso
ConvolvulaceaeConvolvulus arvensis L.Weed[4] Arica—Los Lagos
Cuscuta reflexa R.Weed[34] Arica—Los Lagos
CucurbitaceaeCitrullus lanatus T.Crop[4]2842Atacama—Biobio
Cucumis melo L.Crop[4]2919Atacama—La Araucanía
Momordica dioica R.Crop[4,34] Coquimbo—La Araucanía
EuphorbiaceaeRicinus communis L.Weed[4,34] Arica—Los Lagos
FabaceaeArachis hypogaeaCrop[34] Valparaíso—Ñuble
Indigofera sp. L.Weed[4,34] Arica
Medicago sativa L.Pasture [4,34] Arica—Magallanes
Medicago polymorpha L.Pasture[34] Arica—Los Rios
Phaseolus vulgaris L.Crop[4,34]12,942Arica—Los Lagos
Phaseolus lunatus L.Crop[4,34] Arica—Los Lagos
Pisum sativum L.Crop[4,34]1800Arica—Los Lagos
Robinia pseudoacacia L.Ornamental[4,34] Valparaíso—Biobio
Trifolium alexandrinum L.Pasture[4,34] Arica—Magallanes
Trifolium resupinatum L.Pasture[34] Arica—Magallanes
Vicia sp. L.Crop[4,34]1790Arica—Los Lagos
Vigna mungo L.Crop[4,34]550Coquimbo—Los Lagos
LinaceaeAbelmochus sculentus L.Crop[4,34] Experimental in Chile
Alcea sp. L.Ornamental[4] Antofagasta—Aysén
Gossypium sp. LOrnamental[4,34] Experimental in Chile
Linum usitatissimum L.Crop[34]250Valparaíso—Ñuble
Malva sylvestris L.Weed[39] Antofagasta—Maule
MoraceaeMorus alba L.Ornamental[4,34] Coquimbo—La Araucanía
PlantaginaceaePlantago major L.Weed[34] Arica—Los Lagos
PoaceaeAvena sativa L.Crop[4]71,685Valparaíso—Magallanes
Cynodon dactylon L.Weed[4,34] Arica—Biobio
Hordeum vulgare L.Crop[4]30,000Atacama—La Araucanía
Oryza sativa L.Crop[4]20,700Metropolitana—Biobio
Sorghum bicolor L.Crop[4,34] Valparaíso—La Araucanía
Tritricum aestivum L.Crop[4,34]216,733Coquimbo—Los Lagos
Zea mayz L.Crop[4,34]56,792Arica—Los Lagos
PolygonaceaeRumex dentatus L.Weed[34] Atacama—Aysén
RutaceaeCitrus sp. L.Crop[4,34]24,000Arica—Biobio
SolanaceaePhysalis peruviana L.Crop[4,34]5.5Arica—Maule
Solanum lycopersicum L.Crop[4,32,34]9302Arica—Los Lagos
Solanum tuberosum L.Crop[4,34]26,986Coquimbo—Magallanes
TheaceaeCamellia sinensis L.Ornamental[4,34] Atacama—Magallanes
Since the arrival of this insect in Chile (2016) [17], heavy damage has been recorded, mainly among small growers [40,41]. Preliminary assessments carried out by Instituto de Investigaciones Agropecuarias (INIA) recorded losses of up to 35 ha in areas cultivated with different species of brassicas, mainly arugula in the Lampa locality. In 2017, 781.87 ha were surveyed in the Metropolitana region, of which around 55% of the surface (430.5 ha) was already affected, while in the Valparaíso region, around 39% of the surface (21.3 ha) was affected (Servicio Agricola Ganadero [39]). Estimates made according to the cost per hectare of the cabbage production process in Chile [42] indicate that the economic loss of net profit margin of one hectare affected by B. hilaris would be equivalent to USD 6400. To date, while the associated symptomatology has been observed in Brassica crops, the economic damage has been minor, probably due to the chemical control carried out. However, a high abundance of this species has been found in weeds associated with crops [39]. Research carried out in Centro Ceres showed approximately 20% plant loss in cabbage crops at the time of transplanting in the Central Valley of Chile [32]. Similar results have been recorded in the United States, with losses in the range of 4–20% in no-till crops and 2–10% in transplanted crops [14,19,43]. At present, this insect is still considered a quarantine pest in Chile, and its control is mandatory [39,44].

3. South America Invasion: The Case of Chile

The first finding of B. hilaris in South America was recorded in Chile in 2016 in the commune of Quilicura, Metropolitan Region. It was presumably introduced by land or air, as the first specimens were collected close to the Pan-American Road and near the international airport of Santiago de Chile [17]. In this country, the species quickly expanded its population and began to spread throughout the Central Valley [41], with incredibly rapid expansion in both the longitudinal and altitudinal directions [6]. This altitudinal record indicated its high probability of invading other countries, such as Argentina, where a single adult specimen was found in Mendoza in 2021 at 950 m. [45]. Upon its arrival in 2016–2017, this species caused severe economic damage in brassica crops [39] and was even recorded as biting a 3-year-old girl in the Lampa locality (Metropolitana region) [46]. In terms of its distributional range, this species covered around 650 km during the first two years of its invasion, reaching 500 km to the north and 150 km to the south [6], suggesting a more aggressive invasion than in other latitudes, such as the United States and Mexico [13,47]. In this context, the SAG—the state agency responsible for pest surveillance in Chile—has developed an active survey and implemented the verification of complaints nationwide to detect the presence of these insects in traps, crops, and weeds. To date, this species has been detected in the regions of Atacama, Coquimbo, Metropolitan, Valparaiso, O’Higgins, and Maule, extending by approximately 950 km (Figure 1) in 6 years [48]. Considering the recent arrival of the species in South America, B. hilaris is restricted to colonizing coastal zones at latitudes between 15° and 40° [7,18], a region that is strongly affected by climate change [49]. This scenario has led to the prediction of an increase in the potential distribution of B. hilaris, where the South American region may be the most affected [5,6,7]. In Chile, the effects of climate change are most noticeable in terms of the decline in precipitation and extremely high temperatures; as a consequence, this region may experience increasingly severe droughts [50,51]. It has been observed that high temperatures typically cause this species to become active, affecting its behavior (e.g., walking, and mating), suggesting that it feeds more effectively on brassica crops when the temperatures are high [10,20]. Therefore, the economic losses linked to declines in farmland productivity, management costs, and the availability of water resources for crop irrigation could grow as a result of these extreme occurrences and the impact of B. hilaris [7,11,17].

4. Current Advances in Management Methods: Practical Implementations

4.1. Chemical Control

To keep the populations of B. hilaris below the threshold of economic damage, which is considered the concentration at which preventive actions should be taken to avoid economic losses [52], the main strategy applied is the use of chemical insecticides [21,40,53]. Their use has generated increased production costs while also negatively impacting natural enemy populations and human health [54]; furthermore, they are not available to organic farmers [55]. B. hilaris adult feeding may cause large economic losses in newly transplanted crops, forcing growers to resort to contact insecticides to protect seedlings and their yields [4,13,35]. Contact insecticides are effective in controlling B. hilaris [11]. Several tests have been conducted with pyrethroid and carbamate insecticides, which have shown rapid effects and high efficacy [11,35,53], as well as neonicotinoids and organophosphates [11,56]. However, their efficiency is conditioned by the behavior of this pest, as the insects may fly or shelter in the soil, making their control difficult [13].
In countries such as the United States, pyrethroids are used as the main group of insecticides for the control of B. hilaris adults, given their high efficacy as contact insecticides [53]. In Chile, control of B. hilaris is mandatory, according to resolution No. 1.577/2017 issued by the SAG [44]. At present, 25 active ingredients have been authorized, which belong to 10 chemical groups, including neonicotinoids, pyrethroids, and organophosphates (Table 2) [39].
Of the authorized insecticides, more than 90% are toxic to bees and other beneficial arthropods [39]. Their possible non-target impacts may disrupt the existing integrated pest management systems in brassica crops that depend on inoculation agents and/or conservation biological control [11,57]. It is known that chemical insecticides can exert negative effects on natural enemies by causing their deaths or affecting their development, longevity, reproduction, and behavior [58]. For instance, in [59], it was reported that neonicotinoids such as thiamethoxam led to reduced parasitism by Gryon genus parasitoids and had detrimental effects on parasitoids of the Trissolcus genus [60]. Both genera have been reported as parasitoids of the Bagrada insect [28,61,62]. Even in agroecosystems that rely strongly on chemical control, arthropod pest populations can be efficiently managed through the combination of natural enemies with selective insecticides [63]. Therefore, selective pesticides may be highly beneficial for crop management, particularly for conservation biological control (CBC) strategies through integrated pest management (IPM) [40,63,64]. For instance, it has been observed that ethiprole was less toxic than sulfoxaflor + lambda-cyhalothrin, thiamethoxam + lambda-cyhalothrin, and chlorpyrifos to Telenomus podisi Ashmead, Trissolcus hyalinipennis Rajmohana and Narendran, and Trissolcus teretis Johnson (Hymenoptera: Scelionidae) [65], while diflubenzuron, flubendiamide, and lufenuron were categorized as selective to Te. podisi and Trissolcus basalis Wollastonn [66]. Meanwhile, insecticides such as cyantraniliprole, chlorantraniliprole, deltamethrin, chlorfenapyr, spinosad, azadiracthin, and spiromesifen are compatible with insecticide-resistant adult Eriopis connexa Germar (Coleoptera, Coccinellidae) [67]. Thus, future studies must be directed toward studying natural enemies and selective insecticides that may help manage arthropod pest populations, even in agroecosystems that are highly dependent on chemical control.

4.2. Biological Control

While seven years have passed since B. hilaris arrived in Chile, the number of natural enemies, such as parasitoids and predators, is unknown. It is anticipated that the number of recorded natural enemies of B. hilaris will increase in the coming years. To develop an effective biological control program, it is necessary to determine whether there are natural enemies of the pest inhabiting the invaded area [29,57]. In order to decrease the crop yield losses caused by pest activity and lessen the effects of pest management on the environment and public health, more robust and sustainable approaches are urgently needed. B. hilaris is a difficult species to manage [57]. One of the main reasons is that this species deposits its eggs in the soil [13], so they might be better protected from insecticides and natural enemies; therefore, the implementation of new management strategies is necessary [11]. Since its detection in the western hemisphere in 2008, in the United States, and later in South America, the painted bug B. hilaris has become a severe threat in newly infested areas, especially during the first few years of its presence. In addition, biological control may effectively reduce the B. hilaris populations in non-crop habitats where insecticides are not typically applied [68]. Indeed, a range of arthropods have been recorded as natural enemies of B. hilaris, and many of them have been investigated as biological control agents (Table 3). Overall, several efforts have been made to study and use parasitoids of eggs, mainly from the genera Telenomus Haliday, Trissolcus Ashmead, Gryon Haliday (Hymenoptera, Scelionidae) [11,28,57,68,69], and Ooencyrtus Ashmead (Hymenoptera, Encyrtidae) [70,71], as well as adult parasitoids of the Tachinidae family (Diptera). However, little is known about the predators of B. hilaris [11,57].
As biological control agents, parasitoids frequently have a significant effect in terms of pest density reduction [72]. Egg parasitoids from Pakistan (origin area) have been recorded as possible classical biocontrol agents [73]. G. aetherium, previously named Gryon gonikopalense and Tr. hyalinipennis, were recorded as candidates for classical biological control programs [57] after the invasion in the United States, showing that the coexistence of both species may have an additive effect on the control of B. hilaris, as G. gonikopalense forages in the ground, while Tr. hyalinipennis likely searches above ground level in natural conditions [74]. On the other hand, Ooencyrtus lucidus Triapitsyn and Ganjisaffar (Hymenoptera, Encyrtidae) have been recorded as potential candidates for biological control programs in California [71]. Similar cases have been recorded from field surveys in Mexico, where the following three species of Scelionidae (Hymenoptera) have been identified as parasitoids of B. hilaris eggs: Gryon myrmecophilum Ashmead, Te. podisi, and Tr. basalis [75]. In South America, the possible use of parasitic wasps such as G. aetherium as biological control agents for B. hilaris is currently being considered, especially in Chile, where natural parasitism by this species has been recorded [24]. It has been shown that G. aetherium commonly displays greater host search efficiency and host specificity—traits that are considered important in preventing non-target host attacks [57]. In addition, the production of progeny is influenced by maternal age and host deprivation [76]. On the other hand, as with most other free-living insects, bugs of the Pentatomidae family are attacked by a wide range of generalist predators [77]. These include some ladybirds (Coleoptera, Coccinellidae), Chrysoperla sp. (Neuroptera, Chrysopidae), and some hoverflies (Diptera, Syrphidae) [26,27,78,79]; however, few studies supporting their effectiveness have been published. Therefore, an assessment is a crucial initial step in developing a biological control program, serving to ascertain whether the natural enemies in the invaded range can effectively control the pest. The investigation of predation and parasitism in invasive pests provides valuable insights for the preservation of natural enemy populations, which can be utilized to enhance biological control strategies.
Table 3. Guilds of natural enemies recorded as biological control agents for Bagrada hilaris. Each species’ presence in Chile is highlighted.
Table 3. Guilds of natural enemies recorded as biological control agents for Bagrada hilaris. Each species’ presence in Chile is highlighted.
GuildOrderFamilySpeciesRecorded as Natural
Enemies of B. hilaris		Recorded in Chile
ParasitoidsDipteraSarcophagidaeSarcophaga kempi[11,80]No
TachinidaeAlophora sp. *[11,80]Yes
Alophora indica[80,81,82]No
Alophora pusilla[81]No
Phasia sp. [11]Yes
HymenopteraEncyrtidaeOoencyrtus californicus[57]No
Ooencyrtus lucidus[71]No
Ooencyrtus sp.[4]No
ScelionidaeGryon aetherium[24,57,83]Yes
Gryon myrmecophilum **[75]
Gryon gonikopalense **[73]
Gryon sp. [80,82]unknown
Idris elba[84]No
Psix sp.[82]No
Telenomus podisiWalker unpublished cited by [4]No
Telenomus samueli[85]No
Trissolcus basalis[61,83,86,87]No
Trissolcus erugatus[57]No
Trissolcus hullensis[61,87]No
Trissolcus hyalinipennis[61,88]Yes
Trissolcus sp.[85]Yes
Trissolcus utahensis[61,87]No
Typhodytes sp.[80]No
TrichogrammatidaeTrichogramma sp.[78]Yes
PredatorsAcarinaErythraeidaeBochartia sp.[89]No
AraneaeThomisidaeMisumenops temibilis[78,79]Yes
ColeopteraCarabidaeCincindela sp.[78,79]Yes
CoccinellidaeAdalia angulifera[78,79]Yes
Adalia bipunctata[78,79]Yes
Eriopis chilensis[78,79]Yes
Eriopis connexa chilensis[78,79]Yes
Eriopis eschscholtzi[78,79]Yes
Hippodamia convergens[78,79]Yes
Hippodamia variegata[78,79]Yes
MelyridaeCollops vittatus[90]No
DermapteraForficulidaeForficula auricularia[4]Yes
HemipteraNabidaeNabis punctipennis[78,79]Yes
PentatomidaePodisus maculiventris[90]No
ReduviidaeRhynocoris segmentarius[4]No
Sinea diadema[4]No
Zelus renardii[78,79]Yes
HymenopteraFormicidae Linepithema humile[78,79,90]Yes
Monomorium ergatogyna[91]No
Solenopsis xyloni[91]No
MantodeaCoptopterygidaeCoptopterix gayi[78,79]Yes
NeuropteraChrysopidaeCrysoperla defreitasi[78,79]Yes
* The genus Alophora is currently a synonym of the genus Phasia [92]. ** The species Gryon myrmecophilum and G. gonikopalense correspond to G. aetherium [83].
The recent invasion in the South American region has renewed the interest in biological control, particularly CBC, as a sustainable and effective pest management strategy. This approach emphasizes habitat management, involving the manipulation of non-host plants inside and outside crops that may directly affect pests through their behavior and by providing food and shelter to natural enemies [63,64]. As insects use plant volatiles to locate potential hosts for feeding and oviposition, some non-host plants (aromatic and ornamental plants) may release volatiles with repellent and deterrent properties as a defense against insect attacks. As demonstrated by [93], non-host plants such as coriander (Coriandrum sativum L.), cardinal (Pelargonium hortorum Bailey), ivy cardinal (Pelargonium peltatum L.), rose geranium (Pelargonium graveolens L’Her. ex Ait), mint (Mentha spicata L.), and thyme (Thymus vulgaris L.), when sown along the row border, showed good efficiency in decreasing the incidence of B. hilaris on the leaves and the severity of damage over two seasons, namely, winter and summer. The authors proposed that the combination of these plants in the field has repellent potential against pests. Additionally, the flowers of these plants can help maintain and preserve natural enemies, such as insect parasitoids [94,95]. Therefore, the conservation of natural enemies, such as parasitoids, and the increased use of strip flowers adjacent to crops represent low-cost measures to improve the food supply for flower-visiting insects while sustaining agricultural productivity and reducing environmental damage [96]. Therefore, combining the manipulation of B. hilaris’ behavior and the use of plants to improve the fitness of parasitoids and predators may offer a long-lasting pest control strategy.
On the other hand, planting a trap crop that is highly attractive to the pest can help to protect the main crop from damage. For instance, trap crops such as E. sativa have been shown to be attractive to B. hilaris [97]. Similarly, it was found that B. juncea was successful as a trap crop in cabbage fields, serving to keep B. hilaris away from the main crop [98]. Therefore, the identification of repellent and attractive plants can help us in the implementation of “push-pull” strategies [99,100] using a combination of behavior-modifying stimuli to manipulate the distribution and abundance of pests and/or natural enemies [101], aiming at reducing the density of B. hilaris and the resulting crop damage through increasing the functional biodiversity [102] while simultaneously promoting the presence of natural enemies [24]. It should be noted that the Bagrada bug, unlike other phytophagous pests of brassica crops, has shown a preference for plants in the seedling stage [14]; therefore, the trap crop should be placed together with the crop of commercial interest. On the other hand, the repellent activity of parsley (Petroselinum crispum L.), C. sativum, and P. hortorum, as well as their essential oils, was observed regarding a B. hilaris population established in Chile. Notably, the response to these repellents appears to differ between male and female B. hilaris, suggesting a potential sex-based variation in its behavior [103]. Nevertheless, this approach appears promising for the management of B. hilaris and may be a viable option for other stink bug species [104]. It would also be interesting to study the chemical ecology of plant volatiles to incorporate this information into integrated pest management programs.
Another alternative for the control of B. hilaris is entomopathogenic fungi. In Chile, Baeuveria pseudobassiana (Hypocreales: Clavicipitaceae) and Metarhizium robertsii (Hypocreales: Clavicipiceae) have been shown to be effective in the control of this pest under laboratory conditions [79,105]. In the United States, a study [106] has shown the control capacity of Zoophthora radicans regarding B. hilaris. In turn, Lecanicillium lecanii was found to be highly effective against painted bug nymphs [107], suggesting that L. lecanii is more effective than Metarhizium anisopliae. On the other hand, entomopathogenic nematodes (EPNs) were found as potential candidates to control B. hilaris. From six native Chilean EPN isolates of the genera Heterorhabditis and Steinernema, all caused great mortality against B. hilaris adults and nymphs, of which S. feltiae was the most effective (with around 98% mortality) [108].
In addition, semiochemicals have been utilized in various ways to control insect pests. These methods include monitoring and detection, suppressing population growth through repellent effects, mating disruption, mass trapping, and attract-and-kill techniques [109]. It is known that species of the Pentatomidae family produce mixtures of chemical compounds, the function of which is to prevent the rest of the population from warning of the presence of immediate danger or to serve as alarm or aggregation pheromones [104,110]. However, little information is available about the chemical compounds involved in B. hilaris’ behavior [36,111] and its use in management programs. It is known that long-distance mate localization by B. hilaris is mediated by sex and/or aggregation pheromones, which consist of a mixture of volatile chemicals, mainly esters, terpenoids, and alcohols [111]. Notably, (E)-2-octenyl acetate appears to play a crucial role in intraspecific interactions, functioning as both a sex pheromone for adults and an aggregation pheromone for nymphs [112]. In this sense, mating disruption may be an efficient strategy for its control and may be included in the overall integrated pest management programs for brassicas since sex pheromones are the most used compounds for the control and monitoring of pests in the field [113]. Interestingly, mating pairs of B. hilaris inflict significantly greater feeding damage than individual insects, suggesting a synergistic effect on feeding behavior [20]. This finding, coupled with observations that male irradiation by Gy. may disrupt this behavior [30], underscores the potential for these strategies in the management of B. hilaris. While the use of semiochemicals for pest control shows promise, knowledge gaps remain regarding their specific roles in the behavior of B. hilaris and their optimal deployment in agricultural settings. Further research exploring the intricacies of semiochemical signaling in B. hilaris, particularly in the context of mating and feeding, could unlock novel and effective strategies for controlling this important pest in crops.

4.3. Cultural Control Practices

Agronomic cultural control practices, such as the elimination of host weeds present in production areas and surrounding sites, mitigate the impacts of B. hilaris [11]. Other management measures include composting crop debris to reduce pest carryover between crops [13], and soil solarization, a technique involving the application of a slim, see-through plastic sheet over damp soil during periods of intense heat [114], which may reduce the number of pests that develop in the soil. In addition, avoiding the use of seedlings from infected nurseries is critical to reduce the spread and potential outbreaks of B. hilaris populations [20]. Another management strategy is to vary the planting times of brassica crops to avoid pest damage [56,115]. This practice consists of carrying out constant monitoring of the pest; in this way, it is possible to know when the peaks of appearance are so that they can be considered when carrying out the transplant in seasons when there is a low population of B. hilaris [32]. Early detection is important, as the population of B. hilaris grows exponentially [116].

5. Conclusions and Future Directions

The control of IAS may be particularly challenging when they have already established themselves in entire regions and triggered population outbreaks. The management of such species requires a comprehensive approach that considers the specific ecosystem, landscape, and management objectives. With a focus on Chile, we provided a timely assessment of the most recent developments and the effective use of management strategies aimed at B. hilaris. Progress in combining compatible preventive and curative pest control strategies will make control by growers and pest control researchers more cost-effective when managing the invasive paint bug. Over the last few years, significant technological advances have been made in the areas of pest detection, pest surveillance, pest feeding damage assessment, and the timely formation and application of management decisions. Effective management strategies for B. hilaris in Chile should consider a range of factors, including the specific environmental conditions, as well as the life history and behavioral requirements of the pest [117] and its natural enemies [25,28,55,68,69,76,83]. Chemical control measures, while potentially effective in the short term, may have detrimental effects on non-target species. As a result, biological control emerges as a highly promising approach for managing this invasive pest. Both native natural enemies and introduced agents show potential in effectively controlling B. hilaris populations. Promoting natural enemy populations already present in the invaded region can contribute to the suppression of B. hilaris and provide insights into CBC and its application in agroecosystems. Providing suitable habitats, such as flowering plants or hedgerows, can attract and support natural enemies, thus enhancing their efficacy. However, this strategy still has serious limitations that hinder its wider adoption for biocontrol. On the other hand, the additive (or synergistic) action of natural enemies combined with repellent plants could provide a suitable option for the management of this species. Finally, as discussed earlier, semiochemicals offer targeted control options with minimal environmental impacts. For example, deploying synthetic pheromones to disrupt mating communication can be highly effective. In the same way, pheromone-baited traps can aid in monitoring population levels and guiding management decisions. Therefore, successfully managing B. hilaris in newly invaded areas requires a multifaceted approach that integrates various strategies. Prioritizing research into classical biological control agents while simultaneously implementing conservation biological control, semiochemical applications, and cultural practices offers the most sustainable and effective long-term solution.

Author Contributions

Conceptualization, M.V.A. and A.A.-T.; resources, M.V.A. and A.A.-T.; writing—original draft preparation, A.A.-T.; writing—review and editing M.V.A., C.C.S. and A.A.-T.; project administration, M.V.A. and A.A.-T.; funding acquisition, M.V.A. and A.A.-T. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Agencia Nacional de Investigación y Desarrollo (ANID) through Concurso de Fortalecimiento al Desarrollo Científico Tecnológico de Centros Regionales, Project No. R23F0003. Moreover, Armando Alfaro-Tapia was funded by the ANID postdoctoral grant (FONDECYT) No. 3230599.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing does not apply to this article.

Acknowledgments

We thank Christian R. González from Universidad Metropolitana de Ciencias de la Educación, Chile, for his support in confirming the species of the Tachinidae (Diptera) family and Hector Moya for the maps drawing. Thanks also to Jeniffer K. Alvarez-Baca for their invaluable feedback on the manuscript and to Sarai A. Gallardo-Araya for his assistance with references. We are also grateful to two anonymous reviewers for their critical comments and suggestions.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this review.

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Horticulturae 10 01072 g001
Figure 1. Bagrada hilaris in Chile: (a) Adult female on cabbage crop. (b) Aggregation and feeding of B. hilaris on weeds Sonchus oleraceus. (c) Damage symptoms in cabbage. (d) Current distribution in Chile. The map shows the locality in which B. hilaris was first recorded.
Figure 1. Bagrada hilaris in Chile: (a) Adult female on cabbage crop. (b) Aggregation and feeding of B. hilaris on weeds Sonchus oleraceus. (c) Damage symptoms in cabbage. (d) Current distribution in Chile. The map shows the locality in which B. hilaris was first recorded.
Horticulturae 10 01072 g001
Table 2. Pesticides authorized for the official control of Bagrada hilaris in Chile [39]. Information according to the pesticide class and label is denoted by (*), as follows: (a) Ib (red) highly dangerous; (b) Ib (red) very dangerous; (c) II (yellow) Moderately dangerous; (d) III (blue) not very dangerous; and (e) IV (green) products that do not normally pose a hazard. Visas for use in organic agriculture are shown. Data up to date as of 2021.
Table 2. Pesticides authorized for the official control of Bagrada hilaris in Chile [39]. Information according to the pesticide class and label is denoted by (*), as follows: (a) Ib (red) highly dangerous; (b) Ib (red) very dangerous; (c) II (yellow) Moderately dangerous; (d) III (blue) not very dangerous; and (e) IV (green) products that do not normally pose a hazard. Visas for use in organic agriculture are shown. Data up to date as of 2021.
Chemical GroupActive IngredientCommercial NameToxicological
Classification (*)		Visa
Anthranilic amides/NeonicotinoidsChlorantraniliprole/ThiamethoxamVoliam flexi 30+D24+BB2:E43IV (Green) (e)No
Anthranilic amides/PyrethroidsChlorantraniliprole/λ-cyhalothrin Ampligo 150 ZCII (Yellow) (c)No
Anthranilic diamidesCyantraniliproleAzyraIV (Green) (e)No
Benzoylphenyl ureasNovaluronRimon 10 ECIV (Green) (e)No
CarbamatesMethomylBalazo 90 SPIb (Red) (b)No
Greko 90 SPIb (Red) (a)No
Kuik 90 SPIb (Red) (b)No
NeonicotinoidsAcetamipridMospilan III (Blue) (d)No
Quilate 700 WPII (Yellow) (c)No
ImidaclopridAbsoluto 20% SLIV (Green) (e)No
Absoluto 70% WPIV (Green) (e)No
Confidor forte 200 SLIII (Blue) (d)No
Imaxi 350 SCII (Yellow) (c)No
Imidacloprid 200 SL AgrospecIV (Green) (e)No
Imidacloprid 70% WP AgrospecIII (Blue) (d)No
NupridII (Yellow) (c)No
ThiamethoxamActara 25 WGIV (Green) (e)No
Neonicotinoids/Benzoylphenyl ureasAcetamiprid/NovaluronCormoran ECII (Yellow) (c)No
Neonicotinoids/PyrethroidsAcetamiprid/λ-cyhalothrinGladiador 450 WPII (Yellow) (c)No
Imidacloprid/β-cyhalothrinConnect 112.5 SCIII (Blue) (d)No
Imidacloprid/DeltamethrinMuralla delta 190 ODII (Yellow) (c)No
Thiamethoxam/λ-cyhalothrinEngeo 247 ZCII (Yellow) (c)No
Orbita SCII (Yellow) (c)No
OrganophosphatesAcephateOrthene 75 SPIII (Blue) (d)No
ChlorpyrifosChlorpirifos 48% ECII (Yellow) (c)No
Chlorpirifos S 48OII (Yellow) (c)No
Chlorpyrifos 480 ECII (Yellow) (c)No
ProfenofosSelecron 720 ECII (Yellow) (c)No
Pyrethroidsα-cypermethrinMageosIII (Blue) (d)No
OverkillII (Yellow) (c)No
β-cyfluthrinBulldock 125 SCIII (Blue) (d)No
Predector 125 SCII (Yellow) (c)No
BifenthrinTalstar 10 ECII (Yellow) (c)No
TrippII (Yellow) (c)No
γ-cyhalothrinBullIV (Green) (e)No
λ-cyhalothrinInvicto 50 CSII (Yellow) (c)No
Karate con tecnología zeonII (Yellow) (c)No
KnockoutIII (Blue) (d)No
Zero 5 ECII (Yellow) (c)No
PermethrinPermetrina 50 CEII (Yellow) (c)No
Rayo 50 ECII (Yellow) (c)No
TetranortriterpenoidsAzadirachtinNeem-XIV (Green) (e)Yes
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Albornoz, M.V.; Santander, C.C.; Alfaro-Tapia, A. A Review of the Arrival, Effects, and Management of Bagrada hilaris in South America: The Case of Chile. Horticulturae 2024, 10, 1072. https://doi.org/10.3390/horticulturae10101072

AMA Style

Albornoz MV, Santander CC, Alfaro-Tapia A. A Review of the Arrival, Effects, and Management of Bagrada hilaris in South America: The Case of Chile. Horticulturae. 2024; 10(10):1072. https://doi.org/10.3390/horticulturae10101072

Chicago/Turabian Style

Albornoz, Marta V., Camila C. Santander, and Armando Alfaro-Tapia. 2024. "A Review of the Arrival, Effects, and Management of Bagrada hilaris in South America: The Case of Chile" Horticulturae 10, no. 10: 1072. https://doi.org/10.3390/horticulturae10101072

APA Style

Albornoz, M. V., Santander, C. C., & Alfaro-Tapia, A. (2024). A Review of the Arrival, Effects, and Management of Bagrada hilaris in South America: The Case of Chile. Horticulturae, 10(10), 1072. https://doi.org/10.3390/horticulturae10101072

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