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Review

Stuck in the Caterpillars’ Web: A Half-Century of Biocontrol Research and Application on Gregarious Lepidopteran Pests in Europe

by
Aleksandra Trajković
* and
Vladimir Žikić
Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, 18000 Niš, Serbia
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(4), 2881; https://doi.org/10.3390/su15042881
Submission received: 31 December 2022 / Revised: 27 January 2023 / Accepted: 1 February 2023 / Published: 5 February 2023
(This article belongs to the Special Issue Biocontrol for Sustainable Crop and Livestock Production)
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Abstract

:
Unraveling multiple layers of collective behavior outside the well-known isopteran and hymenopteran societies was a tall order for the scientific community, especially in the case of gregarious juveniles in the order Lepidoptera. Often protected with a solid silk shelter, devoid of reproductive division of labor or conventional forms of parental care, caterpillar aggregations have rarely been considered in terms of economic importance. Of over 60 European communal species, 24 can be associated with voracious feeding habits, and thus be irruptive or pestilential, depending on the extent and severity. This review retrieves 59 cases of biocontrol against Hyphantria cunea (Drury), Euproctis chrysorrhoea (L.), Malacosoma neustria (L.), Thaumetopoea pityocampa (Denis and Schiffermüller), T. processionea (L.) and Yponomeuta malinellus (Zeller) and classifies them in predefined research and application subcategories. The percentage-wise distribution of the utilized or explored biocontrol agents was projected at 35.59% in favor of parasitoids and predators. Falling between fundamental and applicative disciplines, biocontrol, especially in its early days, built a global reputation of being underreported. To provide guidance for future research regarding the group, the functional trait-based concept used in this study is complemented with preliminary outcome assessment.

1. Introduction

Though not the leader in the overall implementation of biocontrol, Europe has long-standing experience with developing pest management strategies and providing expertise for pest outbreaks around the globe. Over the last 50 years, the continent has spawned many regulating bodies and national research systems devoted to bringing successful biocontrol agents (BCAs) from the laboratory to the field. Apart from the legislation-domain sovereignty of European countries and the environmental risks, the pivotal element of integrated pest management (IPM) is often faced with defensive traits of the target species. Focusing on gregarious arboreal species with pest status, this article recapitulates to biological control that was explored or employed in dealing with both residential and imported species, regardless of the BC category. The contribution can be seen through experiments and applications related to biological control in the territory of Europe or the participation of European experts in biocontrol programs abroad.
Biological control, as per its most bendable definition, employs living agents in maintaining populations of pestilential organisms at manageable levels. Naturally, the exact meaning of both “pestilential organism” and “manageable levels” refer directly to any damage to the human economy and overall humankind well-being [1]. Historically, the utilization and the public acceptance of biological control have been fluctuating irregularly [2] entangled in geopolitical factors, economic outlook, and most importantly, the newest community and industry attitudes toward chemical control. Historically, the latter was dictated by the current primary interest of practitioners and the general public, which shifted between environmental consciousness and convenience on multiple occasions during the 20th century [3,4]. The very start of what we now call classical biological control [5], which employes an exotic biological control agent (BCA), did in fact involve a lepidopteran pest: in 1883, Riley successfully orchestrated an intercontinental transfer of Apanteles (=Cotesia) glomeratus from England to the United States to suppress the populations of the invasive cabbage white butterfly, Pieris rapae L. [6]. The outstanding result of the treatment generated a welcoming attitude towards biocontrol: the lack of natural enemies for an invasive species can be easily surpassed with human assistance. This viewpoint was, however, quickly abandoned, especially after several biological control failure stories surfaced, i.e., the intentional and unintentional introductions in Hawaii, USA, a massive native moth-loss event, discussed by Zimmerman [7]. The omnipresent polarity on the topic of biological control was soon replaced with a more realistic approach that accounts for nontarget impact and phenological incompatibilities driven by geographic differences [8].
As authors in the field [9,10,11,12] elaborated, the branching of scientific disciplines involved in biological control, the expansion of biopesticide market, emphasis on cultural practices in integrated pest management (IPM), integrated crop management (ICM) and integrated plant protection (IPP) expectedly diluted the concept of what can be perceived as biological control sensu stricto. Of the principles proposed by Steneberg et al. [13], only the ones promoting virus inclusion (nuclear polyhedrosis viruses present across the order Lepidoptera) and excluding bioprotection are applicable to the scope of this review. Further information on the fundamental background of biocontrol, and in much greater detail, can be found in [13,14,15,16,17].
Instead of analyzing biological control research and application in Europe on the merits of a certain BC category, nature of the BCA, or particular agriculture or market segment, this article assesses biocontrol efforts within the given framework by systematizing publications on targeting caterpillar species that display same functional properties. The inability to cohesively track down and document cases of microbial and macrobial BCA utilization was thoroughly described while reporting on evaluating environmental risks of biological control introductions in Europe (ERBIC) [18], where it is clearly denoted that a major part of data acquisition came through personal communication with biocontrol practitioners. The sovereignty-based approach in regulating BCAs within European countries also brought inconsistent standards in both research and application, which is additionally blurred by the dearth of explicit data on biological control successes and failures, particularly in the commercial domain. Resources that can render great service to both practitioners and those in search of a particular data record include CABI and IOBC publications, such as Gerber and Schaffner [19], Kabuluk et al. [20], and many others available in online and printed formats.

2. Collective Behavior of Larval Lepidoptera

According to Costa and Fitzgerald [21], over 300 species in the order Lepidoptera, distributed in about 25 families, live in single-generation cohort, formerly known as a form of parasociality, in larval societies. This publication, together with its precedents [22,23,24,25,26], represents the most exhaustive account on the topic of their demography. Initiated by egg clustering, characterized by several different feeding and communication mechanisms, presence of a shelter and of varying duration, larval aggregations have evolved through independent events. As all performance-based traits, juvenile gregariousness is similar to a double-edged sword to the one who possesses it. Ehrlich [27] elucidates vastly different levels of invasion success in Pieris brassicae (L.) and P. rapae (L.), where singly deposited eggs might lead to a lifetime of laborious thermoregulation for the caterpillar, but at the same time, greatly reduced risk of parasitoid attack or pesticide exposure. Caterpillars, depending on the species in question and the level of cohort behavioral complexity (patch-restricted, nomadic, or central-place foraging), live with or without a structured shelter. Predominantly built of silk threads and host plant parts, the web, sometimes also referred to as a nest or a tent, facilitates feeding and accelerates the already present mechanisms. This particular type of shelter is often called a communal web, which can, depending on the species, vary in size, robustness, and position on the host plant.
In European lepidopteran fauna, the gregarious taxonomic assemblage brings together Erebidae (Ocnogyna spp., Euproctis spp., Hyphantria cunea), Lasiocampidae (Malacosoma spp., Eriogaster spp., Chondrostega Lederer, 1858), Noctuidae (Oxicesta spp.), Notodontidae (Thaumetopoea spp., Phalera spp.), Nymphalidae (Nymphalis spp., Aglais spp., Araschnia levana (L.), Melitaea spp., Euphydryas spp.), Papilionidae (Aporia crataegi (L.)) and Pieridae (Pieris brassicae), Saturnidae (Saturnia spp.), Yponomeutidae (Yponomeuta spp., Scythropia crataegella). As evident (Table 1), gregariousness encompasses Microlepidoptera and Macrolepidoptera, both moths and butterflies, and is not by any means an implication of a species’ ability to colonize, invade or damage its host plant in the way that qualifies it as a pest. This is made obvious by the fact that many nymphalid web caterpillars, i.e., Euphydryas aurinia (Rottemburg), are butterflies strongly endangered throughout their range. Notes on biology, identification, damage, and host plants of European lepidopteran pests can be found summarized in [1].
It should be noted that the list provided in Table 1 does not represent a complete inventory of the gregarious Lepidoptera, particularly in the family Erebidae. As discussed by Costa and Pierce [26], egg clustering and sociable living of young instars is very common in the former family Lymantriidae (now Erebidae: Lymantriinae). Species such as Lymantria spp., Penthophera morio, Calliteara spp. and others were intentionally omitted from the overview as they display either early dispersal or are not viewed as communal in the literature, since their gregariousness is overshadowed by other, more prominent traits. Other omissions include Microlepidoptera, except Yponomeutidae, and several congeners of Malacosoma, Melitaea and Ocnogyna whose taxonomic status is obscure or there are no data regarding their juveniles. Additionally, there are numerous standpoints of what does and does not constitute collective behavior, as well as several interpretations of the terms gregarious, sociable, communal, pre–, para–, and quasisocial, all in-depth elaborated through multiple functional traits within the abovementioned references [26,29].

3. Pestilential or Phytophagous?

As discussed by Bernal and Medina [30], it should be emphasized that a “pest” is a human construct, born out of several agricultural conflicts in producing high-yield yet herbivore- and pathogen-resistant strains. The herbivore-to-pest transition is, in fact, facilitated through, e.g., maximizing the available plant foliage [31]. In those terms, the gregarious Lepidoptera display many levels of agricultural importance. As mentioned, some of the species pose no threat to the economy, while others position themselves as minor, major or even key pests because of their feeding preferences and adaptability to highly disturbed habitats. Naturally, species alternate between pest categories over the course of time, or are a nuisance to one country, yet a rare species for another, as exemplified by Phalera bucephala L., sometimes referred to as the “rarest pest” in literature [32]. Another representative is Euproctis similis (Füssli), whose ability to break out locally and sporadically made it shift frequently between economic importance statuses. The ability of a certain species to penetrate an area and break out is tightly associated with the ecological stability of the area in question. The methods for dealing with infestations changed dramatically over the course of the last century, a topic thoroughly elaborated on, among others, by Whitten [33], Kogan [34] and Flint and Bosch [35]. Table 2 outlines paramount dendrophilous gregarious species in Europe, with references to the market sectors in which they are considered a nuisance.
To adhere to the concept that accounts for the majority of the pestilential Lepidoptera in larval societies, which implies an arboreal habitat and damage to market sectors of the same group (see Table 1) and thus similar physical, cultural and chemical methods of population suppression, this overview does not deal with species such as Ocnogyna baetica (Rambur), endemic to the Mediterranean region, whose caterpillars forage cultivated fields of legumes and cereals [64], or Pieris brassicae, a major vegetable crop pest and a model organism in many biological disciplines, whose regulation has often been intermixed with the control of other Brassicaceae pests, such as Mamestra brassicae (L.) in IPM programs [65].

4. Criteria for Identifying BC Cases

This review minimizes ambiguity in selecting biological control practice and research cases by classifying published data within one or both of the following categories: (1) research (1.1 rearing for natural enemies; 1.2 BCA selection; 1.3 susceptibility, efficiency, optimization in laboratory experiments and other) and (2) application (2.1 field experiments; 2.2 open field implementation). Secondly, the terms “gregariousness” and “collective behavior” are herein and in Table 1 applied according to Costa and Pierce [26] and Costa and Fitzgerald [66]. Certain caterpillar species do display collective feeding, but are described as loosely gregarious, e.g., Tyria jacobaeae, which was, interestingly, used as a BCA for the noxious tansy ragwort (Senecio vulgaris) in many parts of North America [67], but excluded from this study. The studied assemblage consists of species currently present in Europe (both residential and invasive species), pestilential in agriculture or forestry in at least one part of their range in the given time span, and that display collective behavior with or without constructing a silk shelter in at least three instars during the development. Lastly, at least a portion of research, experimental or implementation phase for the target species must have been performed within the European geographical territory. A great number of potentially irruptive taxa were omitted from the case retrieval due to lack of public records, technical reports in foreign languages, obsolete pest status or the fact that of all defined subcategories, the only available data were confirmation of natural enemies’ presence or miscellaneous findings. To filtrate the records further, multiple publications from the same laboratory and same group of authors that deal with the same method, agent, and outbreak were treated as a single BC instance.

5. Species-Wise Overview and Current Status

While the abovementioned criteria, when applied to all species listed in Table 1, lead to exclusion of certain taxa, the six remaining species provide an insightful outline of how biological control developed methodologically, both in practice and reporting-wise. Assigning the surveyed literature to adequate subcategories revealed that of 59 retrieved cases, 24 dealt with rearing for natural enemies, 11 with optimization and susceptibility testing, 9 with open field implementation, 12 with field trials, and only 3 with BCA selection. Since the latter involves export (or import), the low number of selection studies is understandable, especially if one considers the fact that the “golden era of exotic species introduction” took place several decades before the target time frame of this review.

5.1. Hyphantria cunea Drury

Continuously expanding its range, H. cunea can be described as one of the most well-adapted species in the class Insecta, which is largely due to its generalist habits, extreme tolerance of various environmental factors, and aggregated living conditions. According to the EPPO global database, H. cunea feeds on many economically important crop plants (over 600 host plants worldwide [68]), although with varying degrees of success. Declared a quarantine pest in Tunisia (2012), Israel (2009) and Belarus (1994), the species is being monitored throughout South America, New Zealand, and Europe. Known for its characteristic tent-like webs that spawn across the tree crotches, the noxious caterpillar can completely defoliate its host plant. While hardwood recovers rather efficiently [69], fruit and nut industries may endure severe yield losses [70]. Voltinism in H. cunea has gone through several shifts as the species spread further from its native areal [71], and thus the number of generations ranges from one, i.e., Canada, two (majority of European countries), and three or four in southern US populations [72], following the temperature gradient. The severity of the outbreaks throughout Asia (although Japanese populations had a significantly milder economic impact) resulted in a higher frequency of publications regarding genetics, genomics, control options and ecology of the pest [73,74]. The introduction pathway is believed to be hitchhiking during the international and intercontinental transfer of various non-plant materials. European interest in population dynamics, invasiveness, natural enemies, and rearing techniques for H. cunea sparked around the time of the first encounter with the species, which took place in Hungary, 1940. Franz [75] discusses the use of previously reported nuclear polyhedrosis virus (NPV) [76] in field tests that employ epizootics without being adequately documented. Tadić and Warren [77] gave a global perspective on natural enemies through compiling records from all three continents, discussing spreading dynamics and local efforts on suppressing the pest. This study was succeeded by Szalay-Marzso [78] who anthologized findings on the biology of Eastern European populations and discussed natural enemies (Coleoptera: Coccinellidae and some Neuroptera as egg predators; over 30 larval and pupal parasitoids from Diptera: Tachinidae, and Hymenoptera: Ichneumonidae, Braconidae and Chalcididae, over 30 bird and insect entomophages from Hungary, and several viral and protozoan entomopathogens). Additionally, it was proposed that natural biological control impact in the newly infested areas and the original range is incomparable, citing much higher percentage of population loss for the same class of BCAs in favor of native natural enemies. Sullivan and Sullivan [79] reviewed the Eurasian and North American status of H. cunea considering tachinid fly parasitism and noted many undocumented introductions from and into Europe. Kuzmanova et al. [80] isolated several strains of Bacillus thuringiensis from dead forest pest larvae, selected them according to morphology and characterization and tested their effectiveness against H. cunea and Thaumetopoea pityocampa in the field with a 100% mortality success. As B. thuringiensis var. kurstaki treatments became more refined, novel formulations of bioinsecticides emerged in the industry and underwent trials that compared them to the commercial standards before appearing on the market. In Serbia, a product named D-stop was tested on, among other target species, H. cunea, where it proved almost equally efficient as the widely applied Foray 48 B. [81,82,83]. Draganova [84] tested the susceptibility of third instar H. cunea to fungus Beauveria bassiana (Bals.-Criv.) Vuill. in experimental invasion, while Chkhubianishvili et al. [85] explored infecting H. cunea with Steinernema feltiae (Filipjev) and Heterorahabditis bacteriophora Poinar, two entomopathogenic nematodes (USAID, Israel strains) in Romania. In Moldova, Stîngaci et al. completed multiple laboratory optimization studies with baculoviruses [86,87,88,89].

5.2. Euproctis chrysorrhoea (L.)

Indigenous to Europe, E. chrysorrhoea was accidentally introduced to the USA and Canada by the end of the 19th century. According to the EPPO database, brown-tail moth still holds quarantine status in Mexico (2018) and Canada (2019) At the time known as Nygmia phaerorrhoea (Donovan) (=Euproctis chrysorrhoea) (former Lymantridae) the species was subjected to the first ever augmentative biocontrol treatment, reinforcement of the existing US Trichogramma sp. parasitoid populations with shipments from Europe. Tothill [90], who pioneered biological control practice in North America, reports on introduction of insect enemies targeted at E. chrysorrhoea, even though the initial intention was to control the spongy moth, Lymantria dispar (L.). The outbreak was effectively suppressed, although today’s experts in the field suggest that this introduction [91,92] was too venturesome, and even a liability to the ecosystem [93,94]. Across Europe, several research teams [95,96,97,98] reported on parasitoid complex, predators and protozoic diseases. Bulgarian researchers dealt with microsporidian infections, predominantly with Nosema sp. [99,100] and Entomophaga aulicae (Reichardt) [101]. The latter entomopathogenic fungus was, after its initial report for Serbia in 2015, assessed as a significant control agent by Tabaković-Tošić and Milosavljević [102], who also investigated E. aulicae presence in Bosnia and Herzegovina two years later [103]. Sidor et al. recorded an NPV infection [104], while Kelly et al. [105] published NPV spray testing in laboratory conditions and followed up with a field test the same year [106]. Further work was devoted to NPV mass production exploration [107] and another series of field trials after several attempts failed due to tachinid attacks and other causes [108]. The UK group of authors also discusses natural enemies in detail as well as their interaction with initiating epizootics. In Romania, NPV formulations were tested in field trials [109], effectively on older instars. In the Netherlands, [110], Hungary [111], and Italy [112], B. thuringiensis treatments were sufficient to treat native range local outbreaks, while certain areas required a combined approach with pesticides [113]. Mietkiewski [114] explored several fungi—Beauveria bassiana, Paecilomyces farinosus (Holmsk.) and Verticillium (=Lecanicillium) lecanii Zare and Gams—as well as their potential to maintain their pathogenicity in overwintering nests.

5.3. Malacosoma neustria L.

The European tent caterpillar is a widely distributed polyphagous species holding a “forest tree defoliator” title (EPPO). Depending on the part of its range, M. neustria causes significant damage to both cultivated and wild ornamental and fruit trees. Easily recognized by its solid white webbings, the caterpillars share natural enemies and parasitoid complexes with L. dispar, H. cunea and E. chrysorrhoea. [115]. Out of the studies that qualified for this literature survey, the first laboratory NPV pathogenicity test came from Magnoler [48], and was followed by a series of field tests, reported a decade later [116]. Zannati [117] reported on egg parasitoids, namely Ablerus celsus (Walker) (Aphelinidae), Anastatus bifasciatus (Geoffroy) (Eupelmidae), Ooencyrtus masii (Mercet), O. tardus (Ratzeburg) (Encyrtidae), Telenomus laeviusculus (Ratzeburg) (Scelionidae), and Trichogramma embyiophagum (Hartig) (Trichogrammatidae). This paper also concluded that the top-down control is not the primary population shaping factor during local outbreaks in Bulgaria, with highest levels of mortality being reported for A. celsus. Isolates of nucleopolyhedrosis virus were thoroughly described, characterized and tested in field trials in Latvia [118,119,120,121,122] Draganova et al. [123] found and reported on several entomopathogenic fungi that infect M. neustria, among other forest pests. In Italy, various formulations of Bacillus thuringiensis var. kurstaki were evaluated in field experiments [124,125]. Žikić et al. [50] provided records on natural enemies from an outbreak population in Greece. Caterpillars of M. neustria were, together with those of T. processionea and many other arboreal Lepidoptera outbreaks, a part of several studies regarding possible nontarget impacts of the fungus Entomophaga maimaiga. The entomopathogen was not found among the studied specimens, and thus showed high specificity for its target—the spongy moth, Lymantria dispar [126,127].

5.4. Thaumetopoea pityocampa (Denis and Schiffermüller, 1775)

The pine processionary moth, besides being of the most frequent causes of caterpillar dermatitis and related erucisms [128] and the culprit behind massive silk shelters on Pinus sp. (Cedrus in North Africa) [129] maintains its central position in scientific circles due to being a unique climate change indicator [130]. The population dynamics, spreading pattern, current status in the reinvaded areas and an in-depth discussion regarding the hastily abandoned BC research studies for both T. pityocampa and the oak processionary moth, T. processionea, together with a generous reference list, can be found in de Boer and Harvey [131]. Natural enemies, especially egg parasitoids, were recorded regularly in Bulgaria and Greece [132,133,134,135,136,137,138]. The dual nature of T. pityocampa (important pest for BC practitioners and model organism for climate change researchers) implied the necessity to delimit two streams of publications: work undertaken to estimate mortality to investigate the factors that can be calculated into predictions and population models and actual BC potential research [139]. NPV isolation and Beauveria pathogenicity were primarily investigated in the Asian part of the species range [140,141]. Integrated control of the pest was mostly carried out by physical means, e.g., removing and burning the nests [142] and Bacillus thuringiensis var. kurstaki, which was in routine control use in Italy since 1998 [143]. Triggiani and Tarasco reported on efficacy of entomopathogenic nematodes, Sternernema feltiae, and several egg parasitoids [144]. Its economic importance and medical significance, as well as range expansion. encouraged exploring different trap systems [145] and mating disruption [146] due to its proximity to urban and suburban areas. Barta et al. isolated Beauveria pseudobassiana (Rehner and Humber), B. varroae Rehner and Humber and Purpureocillium lilacinum (Thom) from the Bulgarian T. pityocampa population [147].

5.5. Thaumetopoea processionea (L.)

T. processionea challenged biocontrol practitioners and forestry workers during the past century through its life cycle specificities and susceptibility to control measures that apparently varied heavily between seasonal reports [148]. Ceianu and Dissescu [149] report the Bacillus thuringiensis treatments as routine control in Romania, but also denote two parasitoids Carcelia iliaca (Ratzeburg) (Tachinidae) and Pimpla rufipes Fabricius) (Ichneumonidae), also a predator Calosoma sycophanta (L.) (Carabidae) as most prominent natural enemies. Seventy years ahead, much more is known about the phenology and the effect that chemical control has on the present natural enemies and their role in shaping the populations’ range. The mentioned natural enemies are known from the rest of continental Europe and the United Kingdom as well [150]. More parasitic taxa were reared and reported from the Netherlands [151], two egg parasitoids from Italy, Trichogramma sp. and Anastatus bifasciatus [152], Bulgaria [153], Germany [154], and others. In 2008, a group of researchers [155] screened multiple populations for entomopathogenic microsporidia and isolated Endoreticulatus sp., which was ultimately suspended in water and tested through inoculative treatments in a field trial. The results showed low prevalence. While aerial control with Btk (Bacillus thuringiensis var. kurstaki) was optimized in Quercus forests across Spain, Germany, and Italy [156,157,158,159], Straw and Forster [160] focused on the effectiveness of Btk ground treatments in the UK. For a historical overview on range, expansion and damage, see Groenen [161]. Cosic et al. [162] explored substitution hosts for rearing a promising parasitoid, Oenocyrtus spp., in IPM programs for several forest lepidopteran pests, including T. processionea.

5.6. Yponomeuta malinellus (Zeller)

Of the entire Palearctic genus Yponomeuta, only Y. malinellus was treated as a quarantine or key pest in apple orchards in North America, where it apparently arrived through nursery stock shipments and quickly adapted to new conditions. The lepidopteran was recorded in multiple outbreak events in British Columbia, Canada, as well as Oregon and Washington, USA during the last decade of the 20th century [163]. Beginning their life cycle as L1 (first instar) leaf miners, small, yet voracious caterpillars continue the development on several Rosaceae species, most notably Malus domestica Miller [164]. With their ability to defoliate and completely cover the infected trees with dense silk webs, the species posed a great threat to agriculture and horticulture, which eventually led to an impactful intercontinental collaboration between European and Canadian biological control research centers. In the joint effort of establishing an efficient biological control program, Kuhlmann et al. [59] intensively searched for appropriate natural enemies, which resulted in urgent transfers of two selected BCAs, Ageniaspis fuscicollis (Dalman) (Encyrtidae) and Herpestomus brunnicornis (Gravenhorst) (Ichneumonidae), hymenopteran parasitoids with egg–larval and larval–pupal modes of action, which established with great success [165]. Almost simultaneously, international branches of the USDA and European Parasite Laboratory, Behoust, France (EPL), as well as Russian, Swiss, and German laboratories, performed multiple expeditions to collect the selected native natural enemies A. fuscicollis, Diadegma armillata (Gravenhorst) and H. brunnicornis [60] In both cases of BCA implementation, no prior laboratory studies were conducted. Canadian authorities published the first comprehensive risk assessment in 1998, continued to monitor local and sporadic outbreaks [166], and amended it in 2014, stating that Y. malinellus should no longer be considered a quarantine or key pest in apple orchards. Although locally pestilential, the species did not require specialized suppressing treatments in its native range. Cossentine and Kuhlmann [167] noted that in the majority of its natural and colonized range, Y. malinellus populations remained neutral either by natural enemies’ regulation or collaterally, due to the Btk treatments previously applied for Cydia pomonella (L.) (Tortricidae) infestations [168]. Apart from exporting BCAs, Europe contributed with susceptibility and optimization studies [160,161,162,163,164,165,166,167,168,169,170] as well as rearing records [163,171,172,173,174]. Entomopathogenic BCAs or bioinsecticides containing living agents are hitherto not assessed in Europe.

6. Outcomes and BCA Representation

Estimation of success or failure of biological control can be perceived in several ways. For instance, one can base its assessment on the criteria of target species: whether or not the population has been suppressed and what the contribution of all individual attempts in the given time frame is. The retrieved studies encompassed in this review, vastly different in terms of motives, are assessed according to the defined subcategories, based on the successful completion, long-term impact, and implementation in the commercial domain. Rearing for natural enemies (RNR studies), which also includes inspecting for mortality causes in search of fungi, microsporidia, or other pathogens, is omitted, as the research belongs to the fundamental portion of biological control.
Decisive designation of biological control treatment, or an entire program, as successful or unsuccessful, implies that all cases have similar or at least uniform scenarios that lead to the need for population suppression, including the methodology and subclass of the biological control itself. This generalization is, at least in the scope of this review, practically unachievable as 59 different attempts to explore, initiate or design effective control strategies came with completely different circumstances, such as the nature of the target species, the status of the ecosystem, extent and severity of the outbreak and history of pesticide use in the given area. Additionally, it has been shown and exemplified (see Introduction) that even validating the BCA presence and spreading dynamics after the introduction requires time and extensive knowledge about the factors that shape the impact of the control. This is where the detailed, timely reporting, comparative studies and stacking up of the evidence on the present biotic and abiotic interactions takes a pivotal place in forming grounds for broader overviews. In this manner, it would be possible to explicitly differentiate between programs in which the agent is unfavorably selected, method requires major adjustments or are cost ineffective on one side, and programs that should receive further attention on the other.
The specificity of the discussed mode of life, especially if supported by a physical barrier of a silken shelter, implied modifications in control measures ranging from dissecting the webs and thus providing chemical or biological agent entrance, to individually designed transmission studies that take specialized communication signals of social caterpillars into account [175]. As schematized in Figure 1, parasitoids and predators constitute the majority of utilized or explored BCAs, which is in accordance with the high number of RNR publications. It should be noted that the percentage for Bacillus thuringiensis is probably much higher; however, the treatments were not meticulously reported. Even though Btk is a part of regular aerosol treatments in many European countries, performance studies and collateral impact records would greatly increase the chance to obtain successful individual assessments, as many arboreal, tent-constructing species have highly similar ecological profiles [176].
The literature excerpts analyzed in this review only encompassed six of over 20 species of economic, environmental, and public health interest (Table 1), which points out that the realistic status of biocontrol in Europe, regarding this species repertoire, needs to be extended to include all species categorized as potential pests. Due to the accumulating evidence on climate changes–range expansion relation, it can be expected that the irruptive species benefit from the current worldwide ecosystem sensitivity and shift their pest status.
The growing interest in harmonizing regulative in individual European countries, especially for exotic species introduction, is reflected through the newly adopted changes in microbial pest control (Farm to Fork: new rules for micro-organisms used in plant protection products, EU 2022). As discussed in Waage and Greathead [177], Europe’s lag behind other continents in terms of BC implementation can be explained not only through the rigorous legislative but also through the mere lack of reasonably appropriate scenarios for exotic introductions, at least in the domain of gregarious arboreal Lepidoptera. The uncontainable outbreaks that require such drastic measures often come hand in hand with severely damaged biodiversity due to the homogeneity of monoculture crops, and, consequently, the lack of natural enemies in the given area. The analysis of 59 recent studies showed a promising number of RNR studies in the European continent, as well as the uncertainty of local outbreaks and range expansion predictions around the globe, provides a solid base for the continuance of once extremely fruitful intercontinental collaboration. Although the CABI (Centre for Agriculture and Bioscience International, formerly CIBC) and European laboratories of the USDA mediated in the majority of the projects, the individual contribution of national research teams is not negligible. The evident shift of fundamental biological disciplines towards a more applicable sphere will likely, once again, consolidate the scientific community, the industry sector, and the practitioners around the same objective.

Author Contributions

Conceptualization, A.T. and V.Ž.; writing—original draft preparation, A.T.; writing—review and editing, V.Ž.; supervision, V.Ž. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Ministry of Education, Science, and Technological Development of the Republic of Serbia (contract 451-03-68/2020-14/200124).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank Marijana Ilić Milošević and Saša Stanković for discussions on data interpretation and their technical assistance. Insightful feedback of the three anonymous referees is also gratefully acknowledged.

Conflicts of Interest

The authors declare no conflict of interest.

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Sustainability 15 02881 g001 550
Figure 1. Percentage representation of used biological control agents (BCAs) sorted by classes: parasitoids and predators of all taxonomic affiliations; Bacillus thuringiensis var. kurstaki (Btk) in all preparations, nuclear polyhedrosis viruses (NPVs), fungal/microsporidian treatments; entomopathogenic nematodes (EPNs); see Table 3 and Table 4 for data references.
Figure 1. Percentage representation of used biological control agents (BCAs) sorted by classes: parasitoids and predators of all taxonomic affiliations; Bacillus thuringiensis var. kurstaki (Btk) in all preparations, nuclear polyhedrosis viruses (NPVs), fungal/microsporidian treatments; entomopathogenic nematodes (EPNs); see Table 3 and Table 4 for data references.
Sustainability 15 02881 g001
Table
Table 1. European Lepidoptera species displaying collective behavior (regardless of the aggregation type), their taxonomic affiliation, and reported host plants (* irruptive species, capable of an outbreak; ** pestilential species, had any category of pest status in the last 50 years, has economic or medical importance).
Table 1. European Lepidoptera species displaying collective behavior (regardless of the aggregation type), their taxonomic affiliation, and reported host plants (* irruptive species, capable of an outbreak; ** pestilential species, had any category of pest status in the last 50 years, has economic or medical importance).
Taxon 1Host Plant 2
Yponomeutidae
Yponomeuta cagnagella (Hübner) *Euonymus sp.
Y. evonymella (L.) *Prunus padus, P. serotina
Y. gigas Rebel *Salix sp., Populus sp.
Y. irrorella (Hübner)Euonymus sp.
Y. mahalebella Guenée *Prunus mahaleb
Y. malinellus Zeller **Malus sp., Pyrus sp.
Y. padella (L.) *Rosaceae
Y. plumbella (Denis and Schiffermüller) *Euonymus sp.
Y. rorrella (Hübner) *Salix sp., Populus sp.
Y. sedella TreitschkeCrassulaceae
Scythropia crataegella L. *Rosaceae
Lasiocampidae
Malacosoma alpicola Staudingerpolyphagous on herbs
M. castrensis (L.)polyphagous on herbs
M. franconica (Denis and Schiffermüller) *polyphagous on herbs
M. laurae Lajonquièrepolyphagous on herbs
M. neustria (L.) **polyphagous on woody Aceraceae, Rosaceae, Salicaceae, Fagaceae, Ulmaceae and Oleaceae
Eriogaster arbusculae Freyeralpine Salicaceae, Betulacae, Rosacae and Ericaceae
E. catax (L.)Prunus spinosa, Crataegus sp., Quercus sp., Salix sp., Ulmus sp.
E. lanestris (L.) *woody Rosaceae and Betulaceae, Corylaceae, Salicaceae and Tiliaceae
E. rimicola (Denis and Schiffermüller)
Chondrostega vandalicia (Millière)
C. pastrana Lederer		Quercus sp.
polyphagous on herbs
polyphagous on herbs
Notodontidae
Phalera bucephala (L.) *Fagaceae, Ulmaceae, Aceraceae, Betulaceae, Salicaceae, Tiliaceae, Caprifoliaceae
P. bucephaloides (Ochsenheimer) *Quercus sp.
T. pinivora (Treitschke) *Pinaceae, Cupressaceae
T. pityocampa (Denis and Schiffermüller) **Pinaceae
T. processionea (L.) **Fagaceae, Juglandaceae
T. solitaria (Freyer) **Pistacia sp.
T. wilkinsoni Tams **Pinaceae, Cupressaceae
Erebidae
Ocnogyna corsica (Rambur)polyphagous on herbs and grasses
O. baetica **(Rambur)Fabaceae, Apiaceae, Poaceae
Euproctis chrysorrhoea (L.) **polyphagous on woody Rosaceae, also on Aceraceae, Betulaceae, Fagaceae, Juglandaceae, Oleaceae, Eleagnaceae, Vitaceae, Grossulariaceae and others
E. similis Fuessly *polyphagous on woody Rosaceae, also on Betulaceae and Fagaceae
Noctuidae
Oxicesta chamoenices (Herrich-Schäffer)Euphorbia sp.
O. geographica (Fabricius)Euphorbia sp.
O. serratae (Zerny)Euphorbia sp.
Endromidae
Endromis versicolora (L.)Betulaceae, Rosaceae, Tiliaceae
Saturniidae
Saturnia pavonia (L.)polyphagous in herb and shrub layer
S. pavoniella (Scopoli)polyphagous in herb and shrub layer
S. spini (Denis and Schiffermüller)Prunus spinosa and other Rosaceae
Nymphalidae
Aglais io L.Urtica sp.
A. urticae L.Urtica sp.
A. ichnusa (Bonelli)Urtica sp.
M. arduinna (Esper)Centaurea sp.
M. athalia (Rottemburg)Plantaginaceae, Scrophulariaceae
M. aurelia NickerlPlantaginaceae
M. britomartis AssmannPlantaginaceae, Scrophulariaceae
M. cinxia L.Plantaginaceae, Asteraceae, Scrophulariaceae
M. deione GeyerPlantaginaceae
M. diamina (Lang)Scrophulariaceae, Valerianaceae, Plantaginaceae
M. didyma (Esper)Scrophulariaceae, Valerianaceae, Plantaginaceae
M. parthenoides KefersteinPlantaginaceae, Scrophulariaceae
M. phoebe (Denis and Schiffermüller)Asteraceae
M. telona FrühstorferCirsium sp., Centaurea sp.
M. trivia (Denis and Schiffermüller)Verbascum sp.
M. varia Meyer-DürPlantaginaceae, Scrophulariaceae
Euphydryas aurinia (Rottemburg)Caprifoliaceae, Gentianaceae, Dipsacaceae
E. cynthia (Denis and Schiffermüller)Plantago alpina, Viola calcarata and others
E. desfontainii (Godart)Dipsacaceae
E. iduna (Dalman)Scrophulariaceae, Plantaginaceae
E. intermedia (Ménétriés)Caprifoliaceae, Scrophulariaceae
E. maturna (L.)Fraxinus excelsior, Scrophulariaceae, Plantaginaceae, Valerianaceae, Oleaceae, Adoxaceae
Araschnia levana (L.)Urticaceae
Nymphalis antiopa (L.)Salicaceae, Betulaceae, Ulmaceae, Aceraceae, Oleaceae, Cannabaceae, Moraceae, Corylaceae, Rosaceae, Tiliaceae, Urticacae
N. polychloros (L.)Salicaceae, Ulmaceae, Rosaceae,
N. vaualbum (Denis and Schiffermüller)Betulacae, Salicacae, Ulmaceae
N. xanthomelas (Esper)Salicaceae, Ulmaceae, Anacardiaceae
Pieridae
Pieris brassicae (L.) **Brassicaceae, Resedaceae, Solanaceae, Tropaeolaceae
Aporia crataegi (L.) **woody Rosaceae and Betulaceae, Juglandaceae, Fagaceae, Salicaceae, Ericaceae
1 Modified from [26] to suit the criteria and the scope of the study. 2 As per HOSTS—A Database of the World’s Lepidopteran Host plants [28].
Table
Table 2. Summary of the most important arboreal Lepidoptera species considered for the literature survey (* market sectors defined as per European Commission, agriculture and rural development; ** the selected references represent only a portion of available data and offer multiple other outbreak information and sources cited therein).
Table 2. Summary of the most important arboreal Lepidoptera species considered for the literature survey (* market sectors defined as per European Commission, agriculture and rural development; ** the selected references represent only a portion of available data and offer multiple other outbreak information and sources cited therein).
TaxonGeographical OriginMarket Sector *Outbreak Region(s) ** References
Hyphantria cunea (Erebidae)Nearcticpome fruits, stone fruits, grapes, vegetables, ornamental trees, forestryEurope [36,37]
Asia [38,39,40,41]
New Zealand [42]
Euproctis chrysorrhoea (Erebidae)Europepome fruits, stone fruits, forestryEurope [43,44,45]
North America [46,47]
Asia [48]
Malacosoma neustria (Lasiocampidae)Palearticpome fruits, ornamental shrubs, stone fruits, ornamental treesEurope [49,50]
Asia [51,52,53]
Thaumetopoea pityocampa
(Notodontidae)		Palearticforestry,
livestock farming		Europe [54,55]
Thaumetopoea
processionea
(Notodontidae)		Europeforestry,
livestock farming		Europe [56,57]
Yponomeuta
malinellus
(Yponomeutidae)		Paleartic,
Indomalayan		pome fruit, orchards, ornamental treesEurope [58]
North America [59,60]
Asia [61,62,63]
Table
Table 3. Number of selected cases dealing with research: rearing for natural enemies (RNR), biocontrol agent selection (BCAS); optimization and susceptibility (OPT) or application: field trials or experiments (FE) and open field implementation (OFI) for each investigated taxa, and references to the reports.
Table 3. Number of selected cases dealing with research: rearing for natural enemies (RNR), biocontrol agent selection (BCAS); optimization and susceptibility (OPT) or application: field trials or experiments (FE) and open field implementation (OFI) for each investigated taxa, and references to the reports.
TaxonResearchApplication
RNRBCASOPTFEOFI
H. cunea/1 [83]4 [80,84,85,86,87,88,89]1 [81,82,83]/
E. chrysorrhoea7 [93,94,95,96,97,98,99,100,104]/3 [106,107,127]4 [108,111,112,114]2 [109,113]
M. neustria3 [50,117,123]/1 [49]3 [116,118,119,120,121,122,124]1 [125]
T. pityocampa3 [132,133,134,135,136,137,138,144,147]//2 [83,144]2 [142,143]
T. processionea7 [150,151,152,153,154,155,163]/1 [162]2 [156,158]2 [157,160]
Y. malinellus4 [163,171,172,173,174]2 [59,60]2 [169,170]/2 [165,166]
Table
Table 4. Selected cases grouped in accordance with the subcategory of BC, general objective of the work undertaken and described within the provided references, and estimation of the success and further implementation based on the availability of follow-up.
Table 4. Selected cases grouped in accordance with the subcategory of BC, general objective of the work undertaken and described within the provided references, and estimation of the success and further implementation based on the availability of follow-up.
SubcategoryReference(s) *ObjectiveOutcome **
Biological control agent selection (BCAS)
1[59]selecting agents for intracontinental introduction, exportsuccessful
2[60]selecting agents for intracontinental introduction, exportsuccessful
3[81]comparing novel bioinsecticide efficiency to the standardsuccessful, commercially applied
Optimization and susceptibility (OPT)
1[80]selecting perspective strainsdiscontinued
2[84]pathogenicity testingsuccessful, not implemented *
3[85]pathogenicity testingsuccessful, not implemented *
4[86,87,88,89]larvicidal potential and formulation testingsuccessful, commercially applied
5[106]transmission and persistence testingsuccessful, continued
6[107]mass productionsuccessful, cost-ineffective
7[127]confirming host specificitysuccessful, implemented
8[49]investigating relative susceptibilitysuccessful, implemented
9[162]selecting agents and mass productionunknown
10[169]susceptibility in different phases of developmentsuccessful, implementation unknown
11[170]collecting BCAs from alternate hostsuccessful, implementation unknown
Field experiments (FE)
1[81,82,83]bioinsecticide efficiency testingsuccessful, commercially applied
2[108]formulation efficiency testingsuccessful, application unknown
3[114]strain efficiency testingunknown
4[111]synergistic effects investigationrecommendations for further research
5[112]efficiency testingsuccessful, implemented
6[116]laboratory trial confirmationsuccessful
7[118,119,120,121,122]pathogenicity, susceptibility, synergistic effectssuccessful, continued
8[124]formulation testing, comparison to standardsuccessful, commercially applied
9[83]bioinsecticide efficiency testingsuccessful, commercially applied
10[144]pathogenicity testingrecommendations for further research
11[156]susceptibility, comparison with standardsfurther adjustments recommended
12[158]commercial formulation testingsuccessful, recommendations for further research
Open field implementation (OFI)
1[109]formulation efficiency testingsuccessful, implementation unknown
2[113]dosage variation testingunknown
3[125]impact evaluationsuccessful, continued
4[142]reportsuccessful, continued
5[143]methodology variation testingrecommendations for further research
6[157]routine efficiency estimation, commercialsuccessful, continued
7[160]commercial formulation testingsuccessful, recommendations for further research
8[165]agent introductionsuccessful, continued
9[166]agent introductionsuccessful, continued
* One or more publications that either report on or refer to the described case.** successful: aligned with the motive of the study or experiment e.g., high mortality rate in laboratory or field trials, significant pathogenicity during new strain isolation, persistent agent in monitoring and follow-up studies; commercially applied: novel product placed on the market, or routinely used product tested in different conditions; discontinued: no further research on the topic (by the same groups of authors) was retrieved; continued: further research on the topic (by the same group of authors) available; not implemented: no field trials for performed laboratory experiments, or without gaining wider acceptance in practice; implemented: confirmed in field trials, continued; implementation unknown: in studies dealing with optimization of single or several steps of BC: the results is successful but it is not clear whether or not the method was accepted in practice, in field trials: no reports about the application of the tested agent/methodology are available; recommendations for further research: the result of the study led to new research directions.
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Trajković, A.; Žikić, V. Stuck in the Caterpillars’ Web: A Half-Century of Biocontrol Research and Application on Gregarious Lepidopteran Pests in Europe. Sustainability 2023, 15, 2881. https://doi.org/10.3390/su15042881

AMA Style

Trajković A, Žikić V. Stuck in the Caterpillars’ Web: A Half-Century of Biocontrol Research and Application on Gregarious Lepidopteran Pests in Europe. Sustainability. 2023; 15(4):2881. https://doi.org/10.3390/su15042881

Chicago/Turabian Style

Trajković, Aleksandra, and Vladimir Žikić. 2023. "Stuck in the Caterpillars’ Web: A Half-Century of Biocontrol Research and Application on Gregarious Lepidopteran Pests in Europe" Sustainability 15, no. 4: 2881. https://doi.org/10.3390/su15042881

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