CAB Reviews 2018 13, No. 058

Entomopathogenic as biocontrol agents of pests in orchards

Tim Belien

Address: Zoology Department, Fruittuinweg 1, B-3800 Sint-Truiden, Belgium

Correspondence: Tim Belien. Email: [email protected]

Received: 11 June 2018 Accepted: 14 November 2018 doi: 10.1079/PAVSNNR201813058

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2018 (Online ISSN 1749-8848)

Abstract

Entomopathogenic nematodes (EPNs) are increasingly being used as biological control of insect pests due to their successful biocontrol activity against various economically important insect pests. Despite the growing success of EPNs, their effective use in orchards remains rather scarce. The principal limiting factors for the practical implementation of EPNs in Integrated Pest Management (IPM) programmes in orchards are their reduced control activity and persistence due to low-temperature regimes and desiccation, in particularly when applied against aboveground pest stages. However, recent advances in formulation technology, application strategy (with emphasis on improved persistence of the applied EPNs) and gradually acquired knowledge on optimal implementation strategies already have extended – and in the future most likely will further expand – the practical adoption of EPNs in pest management programmes in orchards. A successful implementation of EPNs in orchards requires that their usage fits into an IPM strategy. Interactions between EPNs and other biological or chemical control agents can be synergistic, additive or antagonistic, depending on the specific chemical and biological agents, as well as their rates and timing and host species. In this article, the most important aspects and features of EPN applications in orchards are reviewed.

Keywords: Entomopathogenic (EPN), Orchard, Application strategy, Insect pest, Integrated pest management (IPM)

Review Methodology: We searched the following databases: Web of Science (v.5.29) and PubMed (NCBI) (Keyword search terms used: entomopathogenic nematode, fruit, orchard, insect pest, biocontrol). In addition, we used the references from the articles obtained by this method to check for additional relevant material. We also obtained information from our own (field) research experiences.

Introduction and are currently mass produced on an economic scale, this review is focused on them. These Entomopathogenic nematodes (EPNs) are increasingly EPNs kill with the aid of a mutualistic symbiosis being used as a biological control of insect pests due with a bacterium ( spp. and to their successful biocontrol activity against various spp. for EPN genera and Heterorhabditis, economically important insect pests [1]. EPNs are soil- respectively) [3]. Driven by the desirability of reducing inhabiting, lethal insect parasites that belong to the Phylum pesticide usage, the past decades extensive research has Nematoda from the families (genera led to the discovery of many efficacious isolates/strains Steinernema and Neosteinernema) and Heterorhabditidae and significant advances in mass production and formu- (genus Heterorhabditis). More recently, the genus Oscheius lation technology [4]. Currently, , from the family Rhabditidae was also identified as EPN Steinernema feltiae, Steinernema kraussei, Steinernema [2]. However, as only species of the genera Steinernema glaseri, Steinernema riobrave, Heterorhabditis bacteriophora

http://www.cabi.org/cabreviews 2 CAB Reviews and are the most commonly borer (Synanthedon exitiosa) [18, 19]. This nuance could used and successfully applied nematodes due to the fact be explained by the ‘habitat specialist’ hypothesis stating that they can easily be produced in liquid culture [5]. that certain ambush type nematodes such as S. carpocapsae However, effective practical usage of EPNs on a commercial are adapted to life in media other than mineral soil, scale has experienced both successes and failures [6]. e.g. peat, leaf, litter or woody environments where they The key of success is to be able to achieve a predictable, are able to cruise [20]. A frequently limiting factor of reliable and consistent control activity against the target orchard environments for the successful application of pest. In general, the reached control efficacy of biological EPNs is the temperature, as (host-seeking) activity of EPNs control agents largely depends on environmental con- generally requires temperatures in the range of 15–25°C ditions, and this certainly also applies for EPNs. Indeed, (depending on EPN species) [21]. This is a challenge as besides the pathogenicity for the targeted insect and the EPNs are often targeting overwintering life stages of pest host finding or foraging strategy of the EPN, the outcome insects, like for instance codling moth Cydia pomonella [21]. of an EPN application is influenced to a great extent by Therefore, cold-active EPN species, like, e.g. S. kraussei, environmental parameters such as temperature, moisture, provide an interesting potential for further developments soil type, exposure to ultraviolet light, salinity and organic into EPN-based pest control strategies in orchard environ- content of soil, means of application, agrochemicals and ments [22]. others [7]. This article is focused on the current status of Table 1 displays an overview of the currently existing EPN applications in orchard systems. In this respect, an EPN applications targeting pests (potentially) present in orchard is defined as an area of land devoted to the orchards. Root-feeding larvae (like, e.g. plum/pecan/ cultivation of fruit or nut trees. As orchards typically chest/hazelnut Curculio , white grubs and the are unprotected without any possibility to control climato- polyphagous black vine Otiorhynchus sulcatus)are logically conditions (in contrast to, e.g. greenhouse probably the best known underground EPN-target crops), they represent a challenging environment for EPN pests [8]. There is an ongoing research effort to investigate applications. The principal limiting factors of nematodes the potential control of many other pests occurring in in orchards are low temperature (<15°C) and desiccation orchards with a focus on targeting subterranean pest life [6]. The use of EPNs for successful control of a number stages. The past decade interesting results were obtained of orchard insect pests has been reported in several for, e.g. underground life stages of (among others) sawflies reviews [1, 6–10]. In this article, the most important (Hoplocampa sp.) [23–25], fruit flies (Tephritidae, aspects and features of EPN applications in orchards are Drosophilidae) [7, 26, 27] or Lepidoptera with a larvae/ reviewed. pupae stage in the soil like the peach fruit moth Carposina sasakii [28]. However, not all targeted soil inhabiting pests in orchards turned out to be susceptible in these studies. EPN Targeting Subterranean Pest Stages in For instance, EPNs were found to fail in parasitizing the Orchards woolly apple aphid Eriosoma lanigerum because their symbiotic bacteria are suppressed [29]. EPNs targeting The most ‘climatologically stable’ habitat in an orchard subterranean pest stages can be applied with conventional environment and also the natural habitat of nematodes is spray equipment for soil treatments (e.g. herbicide the soil. Hence, not surprisingly, many of the current suc- delivery equipment) or through an irrigation system [30]. cessful EPN applications are targeting subterranean pest However, in order to increase the efficacy of EPN stages [6, 7, 11]. The soil of many orchard environments treatments, specific application strategies have been devel- appears to be an excellent natural habitat for EPNs oped throughout various studies the past decade (see as numerous EPNs could be sampled and isolated from also further under Application strategies). A certain soil orchard soils in various studies the past decades (e.g. see moisture level for EPN survival and movement is required, [12–16]). Within a favourable range of temperatures, adeq- but too much moisture may cause oxygen deprivation uate humidity and a susceptible host, effective control of and restrict movement [30, 31]. The ideal moisture underground pest stages generally requires EPNs with a content for nematode host infectivity was reported to mobile foraging strategy (cruisers and intermediate foraging be about 30% [32]. Soil parameters are also important strategies) [7]. Indeed, according to the ‘foraging strategy’ for EPN applications targeting underground pests. The paradigm, cruise foragers tend to move actively through soil texture in orchards often has a high clay content, soil, and use distant volatile cues to assist in host-finding. which limits nematode movement and aeration, which, Ambush foragers, in contrast, tend to remain near the soil in combination, can result in reduced nematode survival surface where they lift their body into the air which faci- and efficacy [33, 34]. In a recent study, it was shown that litates attachment to passing insects [17]. However, there modifying the soil in planting sites improved EPN presence are exceptions such as S. carpocapsae, which is typically and control activity against the root weevil Diaprepes described as an ambusher but has been shown to provide abbreviatus in a citrus orchard [35]. Also the soil pH good control of deep dwelling, cryptic or immobile pests, can have an impact as pH of 10 or higher is likely to be like for instance its usage for controlling the peachtree detrimental to EPN applications, whereas a soil pH in

http://www.cabi.org/cabreviews Table 1 Overview of currently known tested EPN applications targeting pests in orchards Habitat of targeted Pest Nematode species1 pest stage Reference Commercial application?2 Apple sawfly () H. bacteriophora, S. carpocapsae, S. feltiae Underground and [23, 24] Yes (mentioned as target in commercial aboveground: foliar products but effective practice is unclear) Banana stem borer (Odoiporus longicollis) S. carpocapsae Aboveground: cryptic [82] Yes Banana root borer weevil (Cosmopolites H. indica, S. carpocapsae, S. karii Underground [83, 84] Yes sordidus) Black vine weevil (Otiorhynchus sulcatus) H. bacteriophora, S. kraussei, H. marelatus, Underground [5, 79, 85, 86] Yes, mainly in berries (occasionally in S. feltiae orchards) Borers – clearwing moths (Lepidoptera: H. bacteriophora, S. carpocapsae, S. feltiae Underground and [18, 19, 55, Yes Sesiidae) aboveground: cryptic 87–89] Chestnut moth (Cydia splendana) H. bacteriophora, S. feltiae, S. weiseri Underground [90, 91] Yes Chestnut weevil (Curculio elephas) H. bacteriophora, S. carpocapsae, S. feltiae, Underground [91] Yes (but usage in fruit production orchards S. siamkayai, S. weiseri unclear) Citrus mealybug (Planococcus citri) H. bacteriophora, H. zealandica, S. yirgalemense Underground and [52, 92] Yes (but usage in fruit production orchards aboveground: foliar, unclear) cryptic http://www.cabi.org/cabreviews Citrus root weevil (Pachnaeus litus) H. bacteriophora, S. carpocapsae, S. riobrave Underground [93] Yes Codling moth (Cydia pomonella) S. carpocapsae, S. feltiae, H. zealandica Aboveground: cryptic [40, 44, Yes (and fruit bins) 94–96] Diaprepes root weevil (Diaprepes S. riobrave, H. bacteriophora, H. indica Underground and [38, 39] Yes abbreviatus) aboveground: epigeal False codling moth (Thaumatotibia H. bacteriophora, H. zealandica, S. yirgalemense Underground [97–99] No leucotreta) Filbertworm moth (Cydia latiferreana) S. kraussei, H. marelatus, S. carpocapsae, Underground [100, 101] Yes Fruit flies (Tephritidae) H. bacteriophora, H. marelatus, S. feltiae Underground [7, 26, 65, Yes (mentioned as target in commercial 102, 103] products but effective practice is unclear) Fruit flies (Drosophila suzukii) S. kraussei, H. bacteriophora, S. carpocapsae, Aboveground: cryptic, [26, 27, 104] No S. feltiae epigeal Goat moth (Cossus cossus) S. carpocapsae, S. weiseri Aboveground: cryptic [105] Yes Hazelnut weevil (Curculio nucum) H. bacteriophora, S. feltiae, S. carpocapsae Underground [106–108] Yes Litchi longhorn beetle (Aristobia testudo) S. carpocapsae Aboveground: cryptic [109] No Litchi stem borer (Arbela dea) S. carpocapsae Aboveground: cryptic [28] No Mediterranean flat-headed rootborer S. feltiae Underground [50] Yes (Capnodis tenebrionis) Navel orangeworm (Amyelois transitella) S. carpocapsae, S. feltiae (less active) Aboveground: cryptic, [110, 111] Yes epigeal Oriental fruit moth (Grapholita molesta H. bacteriophora, S. carpocapsae, S. feltiae, Aboveground: cryptic [112, 113] Yes (=Cydia molesta)) S. rarum, S. riobrave, H. marelatus (and in fruit bins) Palm borer (Paysandisia archon) S. carpocapsae Aboveground: cryptic [114] Yes Peach fruit moth (Carposina sasakii) H. bacteriophora, S. carpocapsae Underground [28] Yes Pear sawfly (Hoplocampa brevis) H. bacteriophora, S. carpocapsae, S. feltiae Underground and [25] Yes (mentioned as target in commercial aboveground: foliar products but effective practice is unclear) 3 Belien Tim Pecan weevil (Curculio caryae) S. carpocapsae, H. marelatus (only lab tests), Underground [115, 116] Yes H. megidis (only lab tests) Plum curculio (Conotrachelus nenuphar) S. feltiae, S. riobrave (S. carpocapsae was less Underground and [7, 24, 117] Yes (mentioned as target in commercial effective) aboveground: foliar products but effective practice is unclear) Plum fruit sawfly (Hoplocampa flava) H. bacteriophora, S. carpocapsae, S. feltiae Underground [28, 118] Yes (mentioned as target in commercial products but effective practice is unclear) 4 CAB Reviews the range of 4–8 is normally compatible for EPN applications [34].

EPN Targeting Aboveground Pest Stages in 2 Orchards

The past decades many research efforts have also focused on the development of EPN applications against above- ground pest stages [36]. In this respect, three aboveground habitats in orchards can be distinguished: epigeal, foliar and cryptic habitats [7]. The epigeal habitat is on the soil (occasionally in orchards) unclear) (usage in fruit productionunclear) orchards surface, the foliar habitat is on the canopy/leaves, while orchards). Yes, mainly in garden/grassland Yes cryptic habitats include, but are not limited to, bark cracks/ ll cases the most effective solutions for control the holes, under bark and leaf litter, in prop piles, fruit bins, nut shells and pruning wounds [7, 36]. While EPNs with a 124] 132] Yes, in greenhouse crops (ornamentals) – – mobile foraging strategy (cruisers and intermediate 119 127] foraging strategies) can be effective in all these types of [56, 126, [130 aboveground habitats, EPNs with a sit and wait foraging strategy (ambushers) will be most effective in cryptic and soil surface habitats [7]. Because of their sensitivity to desiccation and UV degradation, EPNs are most suitable for application to soil or cryptic (protected) habitats [37]. In Table 1, the habitat of pest life stages controlled by EPN applications is indicated for a list of orchard pests. A well-known example of an EPN application targeting a foliar, epigeal aboveground: foliar, epigeal pest with a (partial) soil-dwelling life stage (epigeal habitat) Habitat of targeted pest stage Reference Commercial application? Underground [7, 68, Aboveground: cryptic [28, 125] No Aboveground: cryptic, Underground [128, 129] Yes (usage in fruit production orchards Underground and in orchards is that of Diaprepes root weevil in citrus

, (D. abbreviatus) [38, 39]. This weevil lays its eggs on leaves, , and after hatching, larvae drop to the ground and enter the ,

, soil. Because neonate D. abbreviatus larvae are highly S. feltiae , , S. feltiae susceptible to EPNs, soil surface treatments with EPNs , while they are entering the soil result in high control H. zealandica , S. arenarium efficacies. An example of an EPN application targeting a pest , with a life stage in a cryptic habitat in orchards is codling S. carpocapsae S. scarabaei

, moth (C. pomonella) [40, 41]. Their caterpillars are ,

1 fruit-boring/feeding pests, but when they are fully grown, H. megidis H. ferruginophorus S. carpocapsae H. indica , , , , S. carpocapsae

, they leave the fruit in search of protected (cryptic) habitats in which they spin their cocoons and pupate. EPN S. abbasi S. glaseri , , applications (after harvest) directed at such potential (overwintering) cryptic habitats (bark cracks, leave litter) can have a significant impact on the population next spring S. feltiae S. longicaudum H. indicia S. glaseri S. bicornutum H. bacteriophora H. bacteriophora S. carpocapsae H. bacteriophora H. bacteriophora [40, 42]. Fruit bins that are in the orchard during the time when diapause-destined larvae are seeking cryptic habitats

) can also provide overwintering sites. As a consequence,

, EPN treatments by submersion or drenching these fruit bins have also been found to be efficacious in controlling the codling moth population in an orchard environment ) [43, 44]. The foliar habitat is the most challenging Aromia bungii Phyllophaga environment for aboveground pest control by EPN treat- ,

Rhynchophorus ments in orchards [6, 7, 36]. The major limiting factor of EPN applications to leaf surfaces is the rapid desiccation of Hoplia Western flower thrips , ) , ) the applied EPNs, although several improvements in for-

(Continued) mulation and application strategy were developed the last decade (see further below). Hence, in general, only variable inconsistent results for pest control by foliar EPN treat- Melolontha Frankliniella occidentalis ( Popillia sp. ferrugineus ( The indicated EPN species were shown to display a certain level ofAvailable control effect as in commercially studies with product the for target primarily pests, but intended do usage not necessarily in represent in practise a in orchards (or in other crops against target pests which can also occur in Table 1 PestScarab , white grubs, chafers 1 Nematode species 2 pest in practice. Red palm weevil ( Red longicorn beetle ( Termites Thrips palmi ments in orchards have been reported so far [7, 24, 36].

http://www.cabi.org/cabreviews Tim Belien 5 EPN Application Strategies and Persistence in into an Integrated Pest Management (IPM) strategy. IPM Orchard Systems involves the (combined) use of many tactics to keep pest levels below an economic threshold, with a maximal A major advantage of EPNs as biological control agents contribution of natural enemies. Applied EPNs might is their ease of application using conventional spraying have undesirable non-target side effects on beneficial equipment. However, there is a variety of handling con- [8, 59]. On the other hand, the presence of siderations including volume, nozzle type, pressure and predators can reduce EPN populations either recycling time, spray distribution pattern and, notably, an by consuming the free-living EPNs, nematode-killed insects adequate agitation during application [37, 45]. In addition or by breaking down the integrity of nematode-killed to conventional spraying equipment, EPNs can be applied insects and causing unfavourable conditions for nematode using different irrigation systems [46]. Habitat modification, development [60]. There are a couple of studies on particularly the use of irrigation before and after treatment, the specific interactions between EPNs and beneficial and the use of strip mulches around tree bases are strategies arthropods in orchards. Exposure of developing larvae that enhance the persistence of EPNs in orchard environ- of two idiobiont parasitoids (Mastrus ridibundus and ments and consequently can increase or extend the control Liotryphon caudatus) of codling moth to infective juveniles activity of EPNs in orchards [39, 40, 47–49]. Other of S. carpocapsae within codling moth cocoons resulted described EPN application strategies in orchards include in clear mortality of these natural enemies. However, the use of an injection technique for soil-inhabiting pest diapausing fully grown parasitoid larvae were almost com- life stages [50] as well as baits and infected host cadavers pletely protected from nematode penetration within their [45, 51]. Moreover, various formulations and adjuvants for own tightly woven cocoons [61]. Moreover, M. ridibundus EPNs have been described for improving the persistence/ and L. caudatus females were able to detect and avoid application of EPNs in aqueous suspension including activ- ovipositing on nematode-infected cocooned codling moth ated charcoal, alginate and polyacrylamide gels, clay, peat, larvae [61]. Hence, compatibility of the two groups polyurethane sponge, vermiculite, water-dispersible gran- of biological control agents for codling moth requires ules, chitosan and other polymers [6, 30, 37, 45, 52, 53]. careful timing of applications. Out of three EPN species Notable examples in orchard systems are S. carpocapsae tested (S. carpocapsae, S. feltiae and H. bacteriophora), only applications for control of the lesser peachtree borer, S. carpocapsae was found to be capable of killing the Synanthedon pictipes, which were significantly improved by a beneficial predator Forficula auricularia, the European follow-up application of a sprayable gel (the gel is commonly earwig [62, 63]. However, earwigs were shown to be used for protecting structures from fire) [54, 55], and able to detect the presence of S. carpocapsae and therefore S. carpocapsae treatments resulting in high control levels avoid EPN-treated habitats. An earwig deterrent activity of the red palm weevil, Rhynchophorus ferrugineus, when in EPN-killed codling moth larvae that reduces the applied in a chitosan formulation [56]. Furthermore, EPN foraging of earwigs on insect cadavers containing EPNs applications to apple tree trunks for control of codling moth and allows nematodes to complete their life cycle was were improved when the treatments included the sprayable also shown [62]. Though, in another study, in pistachio fire gel or wood flour foam as a protecting agent [57]. orchards significantly fewer F. auricularia earwigs (and Improved efficacy, particularly for foliar applications, can Blapstinus discolor beetles) were found in S. carpocapsae- also be obtained by relying on leaf flooding with the addition treated plots, indicating a non-target infection [64]. of surfactants to increase leaf coverage [58]. On the other hand, significantly more isotomid collembo- An important and recurring aspect in the application lans, predatory anystid mites and gnaphosid spiders were strategy of EPNs in orchards is the concept of the so-called sampled under trees where nematodes were applied, ‘targeted applications’. This means that applications are only which could be explained by either direct predation (of made where the target pest (life stage) occurs (soil, cryptic EPNs) or indirect trophic effects. In a recent study on or foliar habitat). For instance, when soil inhabiting pests the Caribbean fruit fly, Anastrepha suspensa, single-EPN are targeted in orchards, in many cases, soil treatments are species treatments proved to be more effective than EPN directed at the soil under the canopy of the trees and not species mixtures, because of undesirable interactions of the between rows [8]. This is, for example, the case for the latter with the parasitoid Diachasmimorpha longicaudata successful implementation of EPN control of D. abbreviates, [65]. All in all, these examples make clear that the specific making these EPN treatments cost-competitive for con- outcome and impact of EPN applications on beneficial trolling this pest in citrus orchards [38, 39]. arthropods is, apart from its specific infection potential, notably dependent on the specific circumstances during and after the application. Is there a potential contact Interactions Between EPNs and Non-Target between applied EPNs and non-target organisms? Do the Beneficial Arthropods EPNs display sufficient persistence in order to result in a considerable effect? As for the target pests, these con- A successful implementation of EPNs in pest management siderations and spatiotemporal aspects (where and when programmes for orchards requires that their usage fits can EPNs reach the target in its particular habitat, with

http://www.cabi.org/cabreviews 6 CAB Reviews sufficient persistence the hours and days after the treat- Conclusion/Summary ment) will ultimately determine if the EPN application has a final significant impact or not. This importance of Despite the growing success of EPNs as biological control specific biotic and abiotic parameters in the application agents of an increasing number of target insect pests, conditions was also illustrated in a study bridging lab- their effective use in orchards remains rather scarce. oratory and field trials on side effects of EPNs on two Higher costs and inferior performance of EPNs compared soil-borne beneficial arthropods in pome fruit, i.e. velvet with chemical insecticides in many situations, as well as mites (Allothrombium fuliginosum) and earwigs (F. auricularia) inconsistent performance of EPNs, due to their large [66]. While S. carpocapsae and S. kraussei applied as dependence on a variety of biotic and abiotic parameters, sole treatment were only slightly to moderately harmful are the greatest impediments to the adoption of EPNs for both beneficial arthropods, significant increased in IPM programmes in orchards. However, recent advances mortality rates were obtained after EPN treatments in in formulation technology, application strategy (with combined use with an adjuvant (improving the contact emphasis on improved persistence of the applied EPNs) by facilitating the penetration of EPNs to the target and gradually acquired knowledge on optimal implemen- (cryptic) habitats and delaying potential desiccation of tation strategies already have extended – and in the future EPNs) [66]. Hence, successful effective implementations most likely will further expand – the effective integration of EPNs in IPM programmes in orchards in future requires EPNs in pest management programmes in orchards. thorough insights into the spatiotemporal characteristics of pests and beneficial arthropods as well as tools and strategies to enhance the persistence and contact with the Acknowledgements target organism (as also described in the previous section of this review). The author wish to thank all fruit growers allowing field trials in their orchards, providing invaluable expertise and experiences on pest control in fruit growing practice. The Agentschap voor Innovatie en Ondernemen (VLAIO) EPN Combined with Other Crop Protection is gratefully acknowledged for funding major parts of Agents applied research projects executed by pcfruit vzw. IPM control of pest insects in orchards involves the com- bination of different control tactics. 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