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Review

Arthropod Pest Management in Strawberry

Department of Entomology, Gulf Coast Research and Education Center, University of Florida, Wimauma, FL 33598, USA
*
Author to whom correspondence should be addressed.
Insects 2022, 13(5), 475; https://doi.org/10.3390/insects13050475
Submission received: 8 March 2022 / Revised: 11 May 2022 / Accepted: 17 May 2022 / Published: 19 May 2022
(This article belongs to the Topic Integrated Pest Management of Crops)

Abstract

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Simple Summary

Strawberry is a commercially important crop which is produced and consumed globally. As there is an increase in economic significance of strawberry production, growers across the globe face challenges in protecting the crop against insect and mite pests. The damage from insect pests results in significant yield loss which adversely affects the strawberry industry. To overcome this situation, management of pests is warranted with reduced impact on the environment and beneficial organisms. Even though insecticide-driven management practices predominate in the strawberry production system, the use of non-chemical alternatives is also gaining importance. The current review is aimed at discussing the important pests of strawberry and various integrated pest management practices adopted worldwide to reduce the damage impact and improve production.

Abstract

The strawberry crop endures economic losses due to feeding injury from a number of phytophagous arthropod pests. A number of invasive pests have posed challenges to crop protection techniques in the strawberry cropping system recently. It is increasingly evident that sole reliance on chemical control options is not sustainable. In this review, current challenges and advances in integrated pest management of various strawberry pests are presented. Key pests discussed include thrips, mites, lygus bug, spotted wing drosophila, seed bug, weevils, aphids, whiteflies, and armyworms. Several integrated pest management techniques that include use of intercropping, resistant cultivars, irradiation with gamma rays, use of spectral sensitivity of pests, biological control agents and natural enemies, and biorational pesticides have recently been reported to be useful in managing the various strawberry pests. With the increase in world production of strawberry, several techniques will be necessary to manage the pest complex of strawberry.

1. Introduction

The strawberry, Fragaria × ananassa Duchesne (Rosales: Rosaceae) management practices presented in this review focus mostly on the integrated pest management techniques that have been utilized globally within the last 10 years to tackle strawberry pest issues. In recent years, development of resistance to several plant protection products used for managing arthropod pests in strawberries has been reported [1]. In addition to pesticide resistance development, the incidence of strawberry pests expanding their invasive range has increased [2,3,4,5,6]. Strawberry remains a high-value crop worldwide and the number of countries producing this crop is on the rise, as is evident from the increase in its global production of 7.6 million kg in 2014 to 8.9 million kg in 2019 [7]. Demand for organic strawberry is also on the rise, which in turn has increased the requirement for information regarding alternative pest management options. Growers that succeed in producing strawberry sustainably in spite of global competitive markets are poised to generate substantial revenue for their regional and national economies. However, there has been a gap in knowledge about the latest developments worldwide with regards to review articles covering recent strawberry arthropod pest management. Upon searching for review articles on Web of ScienceTM and Google Scholar, several articles were found that covered management tactics but had the following issues: (1) covered only a single pest; (2) were older than 10 years; (3) were geographically limited to Northern and Central Europe or the United States. Therefore, the aim of this review article is to present alternative management tactics for major arthropod pests of strawberry occurring globally, with potential for implementation in strawberry pest management.

2. Strawberry Pests and Their Management

2.1. Thrips

Thrips (Thysanoptera: Thripidae) form a complex of species that routinely infest strawberry, at both vegetative and reproductive stages. Pest thrips species cause damage by feeding on leaves, flowers, or fruits, resulting in reduced crop yield and quality. Particularly in strawberry, thrips feeding leads to bronzing, cracking, and cat-facing injuries on the fruits [5,8]. Although thrips-vectored tospovirus and non-viral diseases are common in other cropping systems, such instances of transmission have not yet been reported in strawberry [9]. Even though only 1% of all the thrips species are considered to be serious pests, they cause immense damage to strawberry production worldwide [9,10,11]. The major thrips species that are pests of strawberry include Frankliniella intonsa (Trybom), Thrips tabaci Lindeman, Frankliniella occidentalis Pergande, Frankliniella bispinosa Morgan, Thrips palmi Karny, Frankliniella schultzei Trybom, Thrips fuscipennis Haliday, T. imaginis Bagnall, T. atratus Haliday, and Thrips major Uzel [8,12,13,14,15]. Scirtothrips dorsalis Hood is an invasive pest in the southeastern USA, which became established in this region on strawberry crops in 2015 [5]. Within a few years of invasion in the USA, S. dorsalis has rapidly spread across strawberry and horticultural crop-producing regions of the country [16].
Thrips such as S. dorsalis or F. occidentalis are notoriously difficult to manage due to their small size (1–2 mm) and high reproductive capacity. Moreover, their ability to hide in small spaces within plants also makes management challenging [17]. In addition, there is a high probability of movement of thrips to new geographic areas through the trade of plant materials such as cuttings, seedlings, potted plants, and fresh fruits. Continuous monitoring of thrips pests in the field is essential to implement timely management strategies. Biocontrol agents such as Neoseiulus cucumeris Oudemans, Stratiolaelaps scimitus (Womersley), Amblyseius swirskii Athias-Henriot (Arachnida: Phytoseiidae), and Orius spp. are found to be effective in thrips management along with adequate insecticide spray treatments [18,19,20]. Additionally, foliar-dwelling entomopathogenic nematodes, Thripinema spp. (Tylenchida: Allantonematidae) are also effective in controlling thrips population [18]. Cultural control methods include eliminating the alternative host or weeds in and around the main crop which can serve as reservoirs for thrips [16].
Thrips management in strawberry is mainly insecticide-driven. Conventional insecticides such as spinetoram, cyantraniliprole, flupyradifurone, imidacloprid + lambda cyhalothrin, and bifenthrin are found to be effective in managing thrips population [10,21]. Research findings suggest that three consecutive applications of neem extract reduced the thrips population by more than 70% in strawberry, which makes it an alternative for the reduced use of synthetic pesticide [22]. However, repeated application of insecticides induces insecticide resistance in thrips, especially with F. occidentalis developing resistance to organophosphate, carbamate, and pyrethroid insecticides [23,24]. As a result, it is critical to apply these insecticides in rotation to slow down resistance development in thrips. Additionally, over usage of synthetic pesticides can also affect the beneficial insects. Hence it is important to incorporate an integrated pest management approach for thrips which includes cultural and biological control methods with adequate spray treatments.

2.2. Mites

Tetranychus urticae Koch, Tetranychus cinnabarinus Boisduval, Phytonemus pallidus Banks, and Polyphagotarsonemus latus Banks (Trombidiformes: Tarsonemidae) are common mite pests in strawberry, with T. urticae being the most consistently occurring pest of open-field and high tunnel strawberry [1,25,26,27]. With a round and soft body, T. urticae have a body length of 350 to 1000 µm and are sexually dimorphic, where males can be distinguished from females by the conical tapering of the caudal end and the larger size of females [28]. Tetranychus urticae have two large dark areas on their abdomen and have variable body color including red, orange, green, and yellow [26]. These T. urticae adults and nymphs feed on plant cell chloroplasts and typically develop on the adaxial side of leaves where they can form complex webbing. Feeding causes pale chlorotic spots, known as stippling, to appear on the leaves due to the depletion of mesophyll cells, resulting in the breakdown of plant tissue [28,29]. Tetranychus urticae uses its stylet to secret enzymes from its salivary gland to aid in the breaking down of plant cells [30]. Additionally, T. urticae are capable of arrhenotokous parthenogenesis which means that a virgin female can lay unfertilized eggs that will hatch into males when mature males are unavailable initially during host colonization. Therefore, a single unfertilized female can quickly establish a bisexual population on the host plant [31].
Monitoring and sampling of T. urticae is the key to its management. Several management options for T. urticae exist for strawberry growers. Steam treatments of transplants can be an effective way of reducing mite populations in the early phase of transplanting. Temperatures of 48 °C have been shown to completely kill adult females after 2.7 h of exposure and eggs after 1.9 h of exposure [32]. Several predatory mites belonging to the family Phytoseiidae are sold commercially as biological control agents [33]. A commonly used mite predator, Phytoseiulus persimilis Athias-Henriot, is a spider mite specialist. It is known to cause a swift decline of T. urticae populations after application. If miticides are applied in conjunction with mite predators, it is recommended that growers wait for 7–10 days before releasing the phytoseiid mites onto strawberry plants [26].
Management options using pesticides are available for both conventionally [34] and organically grown strawberry. Organic products containing azadirachtin, paraffinic oil, Metarhizium anisopliae strain F52, potassium salts of fatty acids, Isaria fumosoroseus Apopka strain 97, unsulfonated residue of petroleum oil, neem oil, heat-killed Burkholderia rinojensis strain A396, and heat-killed Chromobacterium subtsugae strain PRAA4-1 and spent fermentation media are viable options for management [35,36].
P. pallidus is a smaller, clear-bodied mite that is ~250 µm in body length. Their eggs are also clear, oval, and have a smooth surface, and are typically glued to the edge of the leaf trichomes or trichomes of the fruit calyx, typically on the underside. Unlike T. urticae, these mites are not visible without magnification. Phytonemus pallidus prefer to feed on young foliage and are typically found on strawberry trifoliates that are still folded and developing near the crown [37]. Feeding causes the plant to have a stunted appearance (compact leaf mass) until the plant eventually turns brown and dies [26]. Flowers can be damaged at high pest levels, resulting in browning and drying. Fruits may also be affected by feeding damage and will appear undersized. High densities may prevent fruit from being produced entirely [28,37]. Adults can overwinter in the crown of strawberry but in warmer climates they can continue to reproduce through the winter and females are capable of parthenogenesis [38,39].
Research findings suggest that similar control methods for T. urticae likely affect P. pallidus. Research conducted using hot water treatments found that soaking P.-pallidus-infested strawberry runners at 46 °C for 6.5 min killed P. pallidus [40]. Moreover, commercially available generalist phytoseiid mites such as Neoseiulus californicus McGregor and Neoseiulus cucumeris Oudemans have been shown to control phytophagous mites on strawberry [28,39]. For the management of P. pallidus in strawberry, prevention of pest infestation and pest establishment is a better tactic than crop rescue, owing to limited miticide compounds available and lack of effective pest suppression. Many miticides labeled for T. urticae are not labeled for P. pallidus management in strawberry; therefore, manufacturer labels of miticides should be thoroughly referenced before being included in chemical control programs.

2.3. Tarnished Plant Bug

The tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) (Hemiptera: Miridae) is one of the most damaging pests of strawberry [41]. Lygus hesperus Knight is an economically important pest of strawberry on California’s central coast, whereas Lygus rugulipennis Poppius affects the late season strawberry production in the UK. Lygus spp. has a very broad host range, attacking over 25 economic and 117 weed hosts [42]. Strawberry is not a preferred host; however, Lygus spp. migrate from unmanaged areas during the late spring as seasonal rains diminish and establish themselves in strawberries and other crops [43]. Lygus spp. have piercing-sucking mouthparts and cause economic damage to strawberry primarily by feeding on the achenes, or seeds of developing fruit [44]. This feeding causes malformation of the fruit, resulting in symptoms described as “cat-facing”. There is evidence that oviposition by Lygus spp. into the ripening fruit can also cause cat-facing [43]. Both adult and nymphal Lygus spp. feed on strawberry and contribute to economic damage.
Adults are about 6 mm long and are a green-brown color with a reddish tint on the forewings. They have a characteristic triangle in the center of the back that is pale green. Young nymphs are pale green. Older nymphs develop five black spots on the back: four arranged between the wing buds and one in the middle of the abdomen. Eggs are oviposited into plant tissue. Methods for sampling Lygus spp. in strawberry have been developed [45,46]. Hand-held vacuum devices and beating trays such as a 12-inch (30 cm) embroidery hoop can be used to sample Lygus spp. [47]. In addition, degree day models can be used to predict the establishment of Lygus spp. populations in strawberry [48].
Lygus lineolaris is primarily controlled in conventional strawberry production with broad spectrum insecticides, including pyrethroid, organophosphate, and neonicotinoid insecticides [49,50]. In addition, newer modes of action including a butenolide (flupyradifurone), a growth regulator (novaluron), and a pyridinecarboxamide (flonicamid) are registered for use against Lygus spp. on strawberry. Entomopathogenic fungus, Beauveria bassiana (Balsamo-Crivelli) Vuillemin can also contribute to Lygus spp. management [51]. An effective push-pull strategy has been described for Lygus rugulipennis management in strawberry using synthetic semiochemicals [52]. The authors found hexyl butyrate (HB) to be an effective push element and L. rugulipennis female sex pheromone combined with phenylacetaldehyde was used as the pull element.
Intensive insecticide use to manage Lygus spp. is disruptive to biological control programs directed at the management of twospotted spider mites and contributes to the development of populations of Lygus spp. that are resistant to insecticides [51]. Augmentative releases of the native egg parasitoid, Anaphes iole Girault (Hymenoptera: Mymaridae) and Leiophron uniformis (Gahan) (Hymenoptera: Braconidae) have been evaluated for management of Lygus spp. [53]. The authors found that A. iole has potential as an inundative biocontrol release agent in strawberry owing to high (~80%) parasitism of L. hesperus at high release rates. However, the potential of L. uniformis as a biocontrol agent needs further investigation as the parasitism of L. hesperus also reached 97% at high release rates (100 parasitoids/150 nymphs in cage), but the L. uniformis oviposition rate declined with an increase in parasitoid density, unlike in the case of A. iole. Lygus spp. have been observed to oviposit proportionally more eggs into the fruit (46.5% of eggs laid) than in other parts of the plant, but in young fruits where inter-achene distance was the minimum, parasitism by A. iole was lower (25.4%) than in more developed fruit [43]. The authors concluded that the fruit offered a refuge for Lygus spp. eggs from parasitism by A. iole, necessitating alternate strategies for management.
Tractor-mounted suction machines, or bug vacs, have been evaluated alone and in combination with insecticide applications for management of Lygus spp. [54,55,56]. A clear advantage of integrating bug vacs with insecticidal control has not been demonstrated over sole reliance on insecticides, and in some cases, bug vacs can damage the strawberry crop. Moreover, the use of trap crops in combination with insecticide sprays or physical control methods can increase the efficiency in Lygus spp. management. The studies in [41,57] found that vacuuming Lygus spp. from the trap crop reduced damage on adjacent strawberry more than directly vacuuming the crop. In addition, trap crops such as alfalfa (Medicago sativa L.), can serve as a refuge for natural enemies [58,59].

2.4. Beetles

Sap beetles: Although commonly referred to as sap beetles, this strawberry pest consortium is made up of several genera and species. Based on research findings, Haptoncus luteolus (Erichson), Lobiopa insularis (Castelnau), and Carpophilus fumatus Boheman (Coleoptera: Nitidulidae) are considered to be the major species of sap beetles associated with strawberry fruit damage [60,61].
The adults are attracted to and feed on ripening fruit, followed by egg laying by the females in the soil surrounding the fruit [62]. The sap beetle larvae emerge from eggs in the soil and feed on the fruits until pupating in the soil. When presented with green, semi-ripe, and ripe strawberry, L. insularis clearly show preference for semi-ripe and ripe fruits [63]. The sap beetle L. insularis is a polyphagous species that is associated with significant economic losses (20–70%) due to strawberry fruit damage in the USA, Brazil, and Argentina [60,64,65,66]. In addition to causing direct feeding damage by burrowing into the semi-ripe and ripe strawberry, these sap beetles facilitate secondary pest infestations of fruit flies, Drosophila spp. (Diptera: Drosophilidae) and phytopathogens such as fungi, Rhizopus stolonifer (Mucoraceae) [63].
Although pyrethroids such as bifenthrin and fenpropathrin are labeled for use in strawberry, the best management practice for sap beetle suppression is maintaining field sanitation by removing ripe fruits promptly from fields [62]. Since the larvae hatching from eggs in the soil tend to infest the fruits closest to the soil, strawberry grown on raised beds with fruits never hanging close to the soil surface will remain least affected by sap beetle infestation and population establishment. In fact, strawberry cultivars that hold ripe fruit off the ground were found to sustain significantly less damage from sap beetles when compared to cultivars that have ripe fruit touching the ground [63]. Moreover, limiting the use of fungicides by following an environmental-model-based spray program approach can contribute to 55% reduction in Stelidota geminate (Say) infestation in open-field strawberry [67].
Weevils: The black vine weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae) was reported as an invasive pest of strawberry in Finland and human activities were mainly held responsible for aiding the spread of this wingless beetle there [2]. Typical of root-feeding weevil pests, the larvae of O. sulcatus reduce plant growth by feeding on the strawberry roots, which in acute cases may lead to plant wilting and death [68]. In the UK, neither chemical nor biological control tactics suppressed this pest but host plant resistance in one cultivar “Symphony” showed lower feeding and oviposition by the adult O. sulcatus feeding on the leaves of this cultivar [68]. The root weevil species complex affecting strawberry includes O. sulcatus, strawberry root weevil, O. ovatus L., clay-colored weevil, O. singularis L., cribrate weevil, Otiorhynchus cribricollis Gyllenhal, Fuller’s rose beetle, Pantomorus cervinus Boheman, Woods weevil, Nemocestes incomptus Horn, Barypeithes pellucidus Boheman, and obscure root weevil, Sciopithes obscurus L. [69,70]. Cultural management of root weevils includes keeping strawberry beds free of weeds and grass. Additionally, pesticide spray or dust which contains pyrethroids acts as an effective chemical control option. For biological control, use of entomopathogenic nematode, Steinernema kraussei (Steiner, 1923), is found effective [71].
The strawberry blossom weevil, Anthonomus rubi Herbst (Coleoptera: Curculionidae) is an economically important pest of strawberry. In addition to strawberry plants, A. rubi tend to feed and reproduce on raspberries and rarely on blackberries [72]. A. rubi is considered to be a key pest of strawberry in the UK and throughout Europe, Asia, and North Africa [73,74]. Additionally, recent reports document that A. rubi has been established in the Lower Mainland region of British Columbia, Canada [74]. Adults of A. rubi are relatively smaller, ranging from 2.5 to 3.0 mm in length. Female A. rubi oviposit eggs singly inside the developing flower buds. Soon after oviposition, the females cut off the bud stalk to prevent bud development and facilitate larval development [75]. The feeding activity of adult A. rubi results in small deep holes on berries at different stages, causing significant yield losses.
Research findings suggest that yellow sticky traps combined with synthetic attractants are efficient for adult monitoring and mass trapping of A. rubi [76]. For management, periodic removal of severed buds or adults is found to be effective [76]. Parasitoid wasps from the families Braconidae (Ichneumonoidea) and Pteromalidae (Chalcidoidea) have been recorded as parasitoids of the larval stages of A. rubi in Europe [74,77]. However, more studies are warranted to understand the efficacy of these natural enemies as potential biocontrol agents.
Scarab beetles: In perennial strawberry fields, other root-feeding beetle species include Popillia japonica Newman, Anomala orientalis Waterhouse, Amphimallon majalis Razoumowsky, and Maladera castanea Arrow (Coleoptera: Scarabaeidae) [71,72]. Their management options include crop rotation with “Saia” oats, Avena strigosa Schreb and “Garry” oats, Avena sativa L., and applying neem oil or insecticidal soaps [71,78].

2.5. Spotted Wing Drosophila

Drosophila suzukii Matsumura (Diptera: Drosophilidae), a native pest of Asia, has invaded fruit crops in Europe and USA and infests unripe strawberry fruits by laying eggs inside the fresh fruit before harvest, using their serrated ovipositor [79]. It has now been reported from the strawberry production regions of Brazil and Africa also [3,80]. This species is particularly devastating as it completes several generations during a field season and is capable of causing farmgate value losses of more than USD 500 M [81]. Resistance to insecticides is an ever-present threat; therefore, alternative pest management tactics are being investigated. It was found that the fruit fly, Drosophila melanogaster Meigen, a related species, shows aversion to UV light during oviposition [82]. Inspired by this finding, studies were conducted to understand the spectral sensitivity of D. suzukii. It was concluded that there is a preference in females for near-UV range (340, 365, 405 nm) but avoidance of the blue-green light spectrum (430–565 nm) [83]. This study conducted using strawberry fruit shows potential in utilizing the preferential phototactic response to ultra-violet light versus visible light in D. suzukii. Another valuable development comes from the investigation of 107 strawberry cultivars, where the authors reported three cultivars that had significantly reduced adult D. suzukii emergence until 17 days post-exposure [84]. Additionally, efficacy of multiple natural enemies on immature D. suzukii has been studied in both the strawberry and blueberry system. In strawberries, Orius insidiosus (Say) (Hemiptera: Anthocoridae) along with Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) resulted in 81% reduction of D. suzukii [85].

2.6. Aphids and Whiteflies

Several pests infest strawberry depending on the pest management program, proximity to other host crops, and field sanitation situation. Aphids (Hemiptera: Aphididae) and whiteflies (Hemiptera: Aleyrodidae) infesting strawberry fall in this category and cause yield loss due to feeding on strawberry leaves. Feeding leads to reduction of plant vigor and vector plant viral diseases (strawberry decline disease) and limits the productivity of the crop by production of honeydew which leads to sooty mold [86,87,88]. Several aphid species infest cultivated strawberry around the world including Aphis ruborum (Börner and Schilder), Chaetosiphon fragaefolii Cockerell, Aphis forbesi Weed, Aphis gossypii Glover, Myzus persicae Sulzer, and Macrosiphum euphorbiae Thomas. Whitefly species infesting strawberries include Trialeurodes vaporariorum Westwood, Aleyrodes spiraeoides Quaintance, and Bemisia tabaci Gennadius [51,87].
Aphid parasitoids such as Aphelinus varipes (Foerster) (Hymenoptera: Aphelinidae) and Aphidius colemani Viereck (Hymenoptera: Braconidae) have been found to be associated with aphid pests and are viewed as important tools in the integrated pest management of aphids in strawberry [88]. Several predators such as syrphid flies (Diptera: Syrphidae), green lacewings (Neuroptera: Chrysopidae), and lady beetles (Coleoptera: Coccinelidae) are effective in suppressing aphid and whitefly populations. Irradiation of boxed fresh fruits with gamma rays (100 Gy) has also shown efficacy in management of B. tabaci and T. vaporariorum [89]. Additionally, biotechnological traps based on an entomopathogenic fungus, Isaria fumosorosea (Wize) Brown and Smith, have been found to be effective in controlling B. tabaci adults in strawberry [90].

2.7. Seed Bug

Seed bug, Neopamera bilobata Say (Hemiptera: Rhyparochromidae) is native to North America and has emerged as an occasional pest of strawberry in USA, Mexico, and Brazil, as they feed on the achenes of green or mature fruits, leading to fruit injury commonly described as “cat-facing” or drying and brown staining of strawberry [91,92,93,94]. Both adults and nymphs are actively feeding stages; these injuries make the fruits unmarketable, especially since adults feed on ripe fruits only whereas nymphs feed on both unripe and ripe fruits [89]. Fruit availability throughout the field season due to production of day-neutral strawberry cultivars and dry and warm climate favors the development of multiple generations of N. bilobata [95]. Although there are some broad-spectrum insecticides available for management of N. bilobata, intercropping high-tunnel strawberry with garlic or undercropping with Chinese chives can suppress N. bilobata populations by 64% and 47%, respectively [96]. Traditional plant breeding resulting in strawberry fruits having seeds recessed into the fruit may provide protection against these achene feeders because of limited accessibility of the seeds [95].

2.8. Lepidopteran Pests

The major lepidopteran pests of strawberry include Spodoptera frugiperda (J.E. Smith), Spodoptera eridania Cramer, Spodoptera exigua (Hübner), Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae), Duponchelia fovealis Zeller (Lepidoptera: Crambidae), Ancylis comptana (Frölich), and Acleris comariana (Lienig and Zeller) (Lepidoptera: Tortricidae) [26,97,98,99]. The armyworm and cutworm pests may infest strawberry to feed on young foliage. S. exigua mostly damages strawberries planted in summer and fall. The immatures of S. exigua initially feed on strawberry foliage and eventually kill the plants by attacking the crown. Monitoring of S. exigua can be achieved through deploying pheromone traps [97]. Management can be achieved through cultural practices and biological control agents such as Hyposoter exiguae (Viereck) or application of commercial formulations of Bacillus thuringiensis [26,71].
In fact, in the case of an invasive pest, synthetic pesticides may not even be registered for use in the invasive range, in which case microbial insecticides may play an important role in the IPM of such pests. For example, [6] reported that D. fovealis, which is a recently invasive strawberry pest in Brazil, could not be managed with synthetic chemical products due to lack of product registration. As an alternative, commercial products based on the entomopathogenic fungus B. bassiana were tested and found to be compatible for the IPM of D. fovealis along with biological control agents such as the predatory stink bug, Podisus nigrispinus Dallas (Hemiptera: Pentatomidae) and the multicolored Asian lady beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). A. comariana (Lienig and Zeller) (Lepidoptera: Tortricidae) is a common lepidopteran pest that attacks strawberry crops. A three-year study conducted in Denmark found that strawberry cropping practices had a significant impact on A. comariana management. A. comariana was more dominant on conventional farms than on organic farms and also the infestation was significantly higher in older fields compared to newer fields [99].

3. Conclusions

Augmentative biological control has emerged as an effective tool to manage several strawberry pests such as thrips, mites, plant bugs, weevils, spotted wing drosophila, aphids, whiteflies, and various lepidopteran pests (Table 1). However, conservation biological control tactics are yet to be utilized for strawberry pest management widely. The lack of adoption of conservation biological control can be attributed to the limited field research and cost-benefit analysis available. Since a successful conservation biological control program will require habitat manipulation to provide a physiological and behavioral advantage to natural enemies, future research programs need to be focused on these aspects. Laboratory research findings need to be expanded to large-scale field studies and supported with information regarding cost to promote adoption of this technology.
With the growing demand for organic strawberry across the globe, biological control has the potential to provide a sustainable pest management solution. We have a wealth of baseline information regarding potential of different species of flowering plants to function as insectary plants around strawberry fields. For example, pollen from strawberry, Urtica urens, Lamium amplexicaule, Convolvulus arvensis, Sonchus oleraceous, and Galega officinalis supports the development of predatory mite, N. californicus, to adulthood but does not support its reproduction [100]. For development and reproduction, N. californicus need to be supplemented with prey items such as T. urticae and thrips. This information can assist in the adoption of habitat manipulation programs that can sustain the development and reproduction of natural enemies to minimize chances of pest resurgence in strawberry fields.

Author Contributions

Conceptualization, S.L. and H.A.S.; writing—original draft preparation, S.L., H.A.S., M.G., G.K. and J.D.M.; writing—review and editing, S.L.; funding acquisition, S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by “USDA National Institute of Food and Agriculture Hatch Project No. FLA-GCR-005888”.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bi, J.L.; Niu, Z.M.; Yu, L.; Toscano, N.C. Resistance status of the carmine spider mite, Tetranychus cinnabarinus and the twospotted spider mite, Tetranychus urticae to selected acaricides on strawberries. Insect Sci. 2016, 23, 88–93. [Google Scholar] [CrossRef] [PubMed]
  2. Tuovinen, T. Risk of invasive arthropod pests related to climate change in the northernmost small fruit production area in EU. In Proceedings of the Workshop on Berry Production in Changing Climate Conditions Cultivation Systems, Geisenheim, Germany, 29 October 2008; COST-Action 863. Volume 838, pp. 151–154. [Google Scholar]
  3. Andreazza, F.; Haddi, K.; Oliveira, E.E.; Ferreira, J.A.M. Drosophila suzukii (Diptera: Drosophilidae) arrives at Minas Gerais State, a main strawberry production region in Brazil. Fla. Entomol. 2016, 99, 796–798. [Google Scholar] [CrossRef] [Green Version]
  4. Lue, C.H.; Mottern, J.L.; Walsh, G.C.; Buffington, M.L. New record for the invasive spotted wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in Anillaco, western Argentina. Proc. Entomol. Soc. Wash. 2017, 119, 146–150. [Google Scholar] [CrossRef]
  5. Panthi, B.R.; Renkema, J.M.; Lahiri, S.; Liburd, O.E. The short-range movement of Scirtothrips dorsalis (Thysanoptera: Thripidae) and rate of spread of feeding injury among strawberry plants. Environ. Entomol. 2021, 50, 12–18. [Google Scholar] [CrossRef] [PubMed]
  6. Araujo, E.S.; Benatto, A.; Rizzato, F.B.; Poltronieri, A.S.; Poitevin, C.G.; Zawadneak, M.A.C.; Pimentel, I.C. Combining biocontrol agents with different mechanisms of action to control Duponchelia fovealis, an invasive pest in South America. Crop Prot. 2020, 134, 105184. [Google Scholar] [CrossRef]
  7. FAO. FAOSTAT Agricultural Statistics Database. 2019. Available online: http://www.fao.org/faostat/en/#data/QC/visualize (accessed on 5 May 2021).
  8. Strzyzewski, I.L.; Funderburk, J.E.; Renkema, J.M.; Smith, H.A. Characterization of Frankliniella occidentalis and Frankliniella bispinosa (Thysanoptera: Thripidae) injury to strawberry. J. Econ. Entomol. 2021, 114, 794–800. [Google Scholar] [CrossRef] [PubMed]
  9. Morse, J.G.; Hoddle, M.S. Invasion biology of thrips. Annu. Rev. Entomol. 2006, 51, 67–89. [Google Scholar] [CrossRef] [Green Version]
  10. Abdelmaksoud, E.M.; Elrefai, S.A.; Mahmoud, K.W.; Mohammed, S.M. The effectiveness of some pesticides in the control of thrips and red spider mites on strawberry plants. Arab. Univ. J. Agric. Sci. 2020, 28, 329–335. [Google Scholar] [CrossRef]
  11. Nielsen, H.; Sigsgaard, L.; Kobro, S.; Jensen, N.L.; Jacobsen, S.K. Species composition of thrips (Thysanoptera: Thripidae) in strawberry high tunnels in Denmark. Insects 2021, 12, 208. [Google Scholar] [CrossRef]
  12. Renkema, J.M.; Evans, B.; Devkota, S. Management of flower thrips in Florida strawberries with Steinernema feltiae (Rhabditida: Steinernematidae) and the insecticide sulfoxaflor. Fla. Entomol. 2018, 101, 102–108. [Google Scholar] [CrossRef] [Green Version]
  13. Gremo, F.; Bogetti, C.; Scarpelli, F. The thrips damaging to strawberry. L’Inf. Agrar. 1997, 53, 85–89. [Google Scholar]
  14. Buxton, J.H.; Easterbrook, M.A. Thrips as a probable cause of severe fruit distortion in late-season strawberries. Plant Pathol. 1998, 37, 278–280. [Google Scholar] [CrossRef]
  15. Steiner, M.Y.; Goodwin, S. Management of thrips (Thysanoptera: Thripidae) in Australian strawberry crops: Within-plant distribution characteristics and action thresholds. Aust. J. Entomol. 2005, 44, 175–185. [Google Scholar] [CrossRef]
  16. Kumar, V.; Kakkar, G.; Seal, D.R.; McKenzie, C.L.; Colee, J.; Osborne, L.S. Temporal and spatial distribution of an invasive thrips species Scirtothrips dorsalis (Thysanoptera: Thripidae). Crop Prot. 2014, 55, 80–90. [Google Scholar] [CrossRef]
  17. Hansen, E.A.; Funderburk, J.E.; Reitz, S.R.; Ramachandran, S.; Eger, J.E.; McAuslane, H. Within-plant distribution of Frankliniella species (Thysanoptera: Thripidae) and Orius insidiosus (Heteroptera: Anthocoridae) in field pepper. Environ. Entomol. 2003, 32, 1035–1044. [Google Scholar] [CrossRef] [Green Version]
  18. Kumar, V.; Kakkar, G.; McKenzie, C.L.; Seal, D.R.; Osborne, L.S. An overview of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) biology, distribution and management. In Weed and Pest Control-Conventional and New Challenges; Soloneski, S., Larramendy, M., Eds.; IntechOpen Limited: London, UK, 2013; pp. 53–77. [Google Scholar]
  19. Sampson, C.; Bennison, J.; Kirk, W.D. Overwintering of the western flower thrips in outdoor strawberry crops. J. Pest Sci. 2001, 94, 143–152. [Google Scholar] [CrossRef] [Green Version]
  20. Arthurs, S.; McKenzie, C.L.; Chen, J.; Dogramaci, M.; Brennan, M.; Houben, K.; Osborne, L. Evaluation of Neoseiulus cucumeris and Amblyseius swirskii (Acari: Phytoseiidae) as biological control agents of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) on pepper. Biol. Control 2009, 49, 91–96. [Google Scholar] [CrossRef]
  21. Lahiri, S.; Panthi, B. Insecticide efficacy for chilli thrips management in Strawberry, 2019. Arthropod Manag. Tests 2020, 45, tsaa046. [Google Scholar] [CrossRef]
  22. Monteon-Ojeda, A.; Damian-Nava, A.; Hernandez-Castro, E.; Cruz-Lagunas, B.; Romero-Rosales, T.; San, J.L.J.; Ibarra-Cortes, K.H. Biorational and conventional insecticides efficacy to control thrips (Frankliniella occidentalis Perg.) on strawberries (Fragaria X ananassa Duch.) at Morelos state, Mexico. AGRO Product. 2021, 14, 59–68. [Google Scholar]
  23. Zhao, G.; Liu, W.; Brown, J.M.; Knowles, C.O. Insecticide resistance in field and laboratory strains of western flower thrips (Thysanoptera: Thripidae). J. Econ. Entomol. 1995, 88, 1164–1170. [Google Scholar] [CrossRef]
  24. Jensen, S.E. Insecticide resistance in the western flower thrips, Frankliniella occidentalis. Integr. Pest Manag. Rev. 2000, 5, 131–146. [Google Scholar] [CrossRef]
  25. Renkema, J.M.; LeFors, J.A.; Johnson, D.T. First report of broad mite (Acari: Tarsonemidae) on commercial strawberry in Florida. Fla. Entomol. 2017, 100, 804–806. [Google Scholar] [CrossRef] [Green Version]
  26. Liburd, O.; Rhodes, E. Management of strawberry insect and mite pests in greenhouse and field crops. In Strawberry-Pre-and Post-Harvest Management Techniques for Higher Fruit Quality; Asao, T., Asaduzzaman, M., Eds.; IntechOpen Limited: London, UK, 2019. [Google Scholar] [CrossRef] [Green Version]
  27. Easterbrook, M.A.; Fitzgerald, J.D.; Solomon, M. Biological control of strawberry tarsonemid mite Phytonemus pallidus and two-spotted spider mite Tetranychus urticae on strawberry in the UK using species of Neoseiulus (Amblyseius) (Acari: Phytoseiidae). Exp. Appl. Acarol. 2001, 25, 25–36. [Google Scholar] [CrossRef]
  28. Vacante, V. The Handbook of Mites of Economic plants: Identification, Bio-Ecology and Control; CABI: Oxfordshire, UK, 2016; pp. 1–865. [Google Scholar]
  29. Sato, M.E.; Da Silva, M.Z.; De Souza Filho, M.F.; Matioli, A.L.; Raga, A. Management of Tetranychus urticae (Acari: Tetranychidae) in strawberry fields with Neoseiulus californicus (Acari: Phytoseiidae) and acaricides. Exp. Appl. Acarol. 2007, 42, 107–120. [Google Scholar] [CrossRef] [PubMed]
  30. Bensoussan, N.; Zhurov, V.; Yamakawa, S.; O’Neil, C.H.; Suzuki, T.; Grbić, M.; Grbić, V. The digestive system of the two-spotted spider mite, Tetranychus urticae Koch, in the context of the mite-plant interaction. Front. Plant Sci. 2018, 9, 1206. [Google Scholar] [CrossRef]
  31. Tuan, S.J.; Lin, Y.H.; Yang, C.M.; Atlihan, R.; Saska, P.; Chi, H. Survival and reproductive strategies in two-spotted spider mites: Demographic analysis of arrhenotokous parthenogenesis of Tetranychus urticae (Acari: Tetranychidae). J. Econ. Entomol. 2016, 109, 502–509. [Google Scholar] [CrossRef]
  32. Renkema, J.; Dubon, F.; Peres, N.; Evans, B. Twospotted spider mites (Tetranychus urticae) on strawberry (Fragaria × ananassa) transplants, and the potential to eliminate them with steam treatment. Int. J. Fruit Sci. 2020, 20, 978–991. [Google Scholar] [CrossRef]
  33. Howell, A.D.; Daugovish, O. Biological control of Eotetranychus lewisi and Tetranychus urticae (Acari: Tetranychidae) on strawberry by four phytoseiids (Acari: Phytoseiidae). J. Econ. Entomol. 2013, 106, 80–85. [Google Scholar] [CrossRef]
  34. Wang, Z.; Cang, T.; Wu, S.; Wang, X.; Qi, P.; Wang, X.; Zhao, X. Screening for suitable chemical acaricides against two-spotted spider mites, Tetranychus urticae, on greenhouse strawberries in China. Ecotoxicol. Environ. Saf. 2018, 163, 63–68. [Google Scholar] [CrossRef]
  35. Bernardi, D.; Botton, M.; da Cunha, U.S.; Bernardi, O.; Malausa, T.; Garcia, M.S.; Nava, D.E. Effects of azadirachtin on Tetranychus urticae (Acari: Tetranychidae) and its compatibility with predatory mites (Acari: Phytoseiidae) on strawberry. Pest Manag. Sci. 2013, 69, 75–80. [Google Scholar] [CrossRef]
  36. Whitaker, V.M.; Boyd, N.S.; Peres, N.A.; Desaeger, J.; Lahiri, S. Chapter 16. Strawberry Production. In Vegetable Production Handbook of Florida, 2020–2021 ed.; Dittmar, P.J., Freeman, J.H., Paret, M.L., Smith, H.A., Eds.; University of Florida/Institute of Food and Agricultural Sciences Extension: Gainesville, FL, USA, 2020; pp. 351–374. [Google Scholar]
  37. Croft, B.A.; Pratt, P.D.; Koskela, G.; Kaufman, D. Predation, reproduction, and impact of phytoseiid mites (Acari: Phytoseiidae) on cyclamen mite (Acari: Tarsonemidae) on strawberry. J. Econ. Entomol. 1998, 91, 1307–1314. [Google Scholar] [CrossRef]
  38. Fountain, M.T.; Harris, A.L.; Cross, J.V. The use of surfactants to enhance acaricide control of Phytonemus pallidus (Acari: Tarsonemidae) in strawberry. Crop Prot. 2010, 29, 1286–1292. [Google Scholar] [CrossRef]
  39. Patenaude, S.; Tellier, S.; Fournier, V. Cyclamen mite (Acari: Tarsonemidae) monitoring in eastern Canada strawberry (Rosaceae) fields and its potential control by the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae). Can. Entomol. 2020, 152, 249–260. [Google Scholar] [CrossRef]
  40. Hellqvist, S. Heat tolerance of strawberry tarsonemid mite Phytonemus pallidus. Ann. Appl. Biol. 2002, 141, 67–71. [Google Scholar] [CrossRef]
  41. Dumont, F.; Provost, C. Combining the use of trap crops and insecticide sprays to control the tarnished plant bug (Hemiptera: Miridae) in strawberry (Rosaceae) fields. Can. Entomol. 2019, 151, 251–259. [Google Scholar] [CrossRef]
  42. Schwartz, M.D.; Foottit, R.G. Revision of the nearctic species of the genus Lygus Hahn, with a review of the palearctic species (Heteroptera: Miridae). Ann. Entomol. Soc. 1998, 91, 895–896. [Google Scholar]
  43. Udayagiri, S.; Welter, S.C. Escape of Lygus hesperus (Heteroptera: Miridae) eggs from parasitism by Anaphes iole (Hymenoptera: Mymaridae) in strawberries plant structure effects. Biol. Control 2000, 17, 234–242. [Google Scholar] [CrossRef]
  44. Allen, W.W.; Gaede, S.E. The relationship of lygus bugs and thrips to fruit deformity in strawberry. J. Econ. Entomol. 1963, 56, 823–825. [Google Scholar] [CrossRef]
  45. Zalom, F.G.; Pickel, C.; Welch, N.C. Recent trends in strawberry arthropod management for coastal areas of the western United States. In Monitoring and Integrated Management of Arthropod Pests of Small Fruit Crops; Bostanian, N.J., Wilson, L.T., Dennehy, T.J., Eds.; Intercept: Andover, NH, USA, 1990; pp. 239–259. [Google Scholar]
  46. Zalom, F.G.; Pickel, C.; Walsh, D.B.; Welch, N.C. Sampling for Lygus hesperus (Hemiptera: Miridae) in strawberries. J. Econ. Entomol. 1993, 86, 1191–1195. [Google Scholar] [CrossRef]
  47. Bolda, M.A.; Daugovish, O.; Fennimore, S.A.; Koike, S.T.; Larson, K.D.; Marcum, D.B.; Zalom, F.G. Integrated Pest Management for Strawberries, 2nd ed.; University of California, Division of Agriculture and Natural Resources Publication: Davis, CA, USA, 2008; pp. 1–176. [Google Scholar]
  48. Zalom, F.; Bi, J.; Thompson, P. Managing Lygus Bugs in Strawberries. California Strawberry Commission, 2011. Available online: https://www.calstrawberry.com/Portals/2/Reports/ResearchReports/ProductionGuidelines/English/ManagingLygusBugsinStrawberries-2011.pdfver=2018-01-12-155446-573 (accessed on 24 March 2021).
  49. Zalom, F.G.; Bolda, M.P.; Dara, S.K.; Joseph, S.V. Strawberry Pest Management Guidelines. Lygus Bugs (Western Tarnished Plant Bug). 2018. Available online: https://www2.ipm.ucanr.edu/agriculture/strawberry/Lygus-Bug/ (accessed on 25 March 2021).
  50. Fitzgerald, J.; Jay, C. Chemical control of the European tarnished plant bug, Lygus rugulipennis, on strawberry in the UK. Crop Prot. 2011, 30, 1178–1183. [Google Scholar] [CrossRef]
  51. Dara, S. Managing strawberry pests with chemical pesticides and non-chemical alternatives. Int. J. Fruit Sci. 2016, 16, 129–141. [Google Scholar] [CrossRef]
  52. Fountain, M.T.; Deakin, G.; Farman, D.; Hall, D.; Jay, C.; Shaw, B.; Walker, A. An effective ‘push–pull’control strategy for European tarnished plant bug, Lygus rugulipennis (Heteroptera: Miridae), in strawberry using synthetic semiochemicals. Pest Manag. Sci. 2021, 77, 2747–2755. [Google Scholar] [CrossRef] [PubMed]
  53. Norton, A.P.; Welter, S.C.; Flexner, J.; Jackson, C.G.; Debolt, J.W.; Pickel, C. Parasitism of Lygus hesperus (Miridae) by Anaphes iole (Mymaridae) and Leiophron uniformis (Braconidae) in California strawberry. Biol. Control 1992, 2, 131–137. [Google Scholar] [CrossRef]
  54. Vincent, C.; Lachance, P. Evaluation of a tractor-propelled vacuum device for management of tarnished plant bug (Heteroptera: Miridae) populations in strawberry plantations. Environ. Entomol. 1993, 22, 1103–1107. [Google Scholar] [CrossRef]
  55. Pickel, C.; Zalom, F.G.; Walsh, D.B.; Welch, N.C. Efficacy of vacuum machines for Lygus hesperus (Hemiptera: Miridae) control in coastal California strawberries. J. Econ. Entomol. 1994, 87, 1636–1640. [Google Scholar] [CrossRef]
  56. Joseph, S.V.; Bolda, M. Evaluating the potential utility of an electrostatic sprayer and a tractor-mounted vacuum machine for Lygus hesperus (Hemiptera: Miridae) management in California’s coastal strawberry. Crop Prot. 2018, 113, 104–111. [Google Scholar] [CrossRef]
  57. Swezey, S.L.; Nieto, D.J.; Bryer, J.A. Control of western tarnished plant bug Lygus hesperus Knight (Hemiptera: Miridae) in California organic strawberries using alfalfa trap crop and tractor-mounted vacuums. Environ. Entomol. 2007, 36, 1457–1465. [Google Scholar] [CrossRef]
  58. Swezey, S.L.; Nieto, D.J.; Pickett, C.H.; Hagler, J.R.; Bryer, J.A.; Machtley, S.A. Spatial density and movement of Lygus spp. parasitoid Peristenus relictus (Hymenoptera: Braconidae) in organic strawberries with alfalfa trap crops. Environ. Entomol. 2014, 43, 363–369. [Google Scholar] [CrossRef]
  59. Hagler, J.R.; Nieto, D.J.; Machtley, S.A.; Swezey, S.L. Predator demographics and dispersal in alfalfa trap-cropped strawberry. Entomol. Exp. Appl. 2020, 168, 53–58. [Google Scholar] [CrossRef] [Green Version]
  60. Potter, M.A.; Price, J.F.; Habeck, D.H.; Schuster, D.J.; McCord Jr., E. A survey of sap beetles (Coleoptera: Nitidulidae) in strawberry fields in west central Florida. Fla. Entomol. 2013, 96, 1188–1189. [Google Scholar] [CrossRef]
  61. Fornari, R.A.; Junior, R.M.; Bernardi, D.; Botton, M.; Pastori, P.L. Evaluation of damage, food attractants and population dynamics of strawberry sap beetle. Hortic. Bras. 2013, 31, 380–385. [Google Scholar] [CrossRef] [Green Version]
  62. Loughner, R.L.; Loeb, G.M.; Schloemann, S.; Demchak, K. Evaluation of cultural practices for potential to control strawberry sap beetle (Coleoptera: Nitidulidae). J. Econ. Entomol. 2008, 101, 850–858. [Google Scholar] [CrossRef] [PubMed]
  63. de Souza, M.T.; de Souza, M.T.; Rizzato, F.B.; Zawadneak, M.A.C.; Cuquel, F.L. Feeding of Lobiopa insularis (Coleoptera: Nitidulidae) on strawberries. Crop Prot. 2019, 119, 180–184. [Google Scholar] [CrossRef]
  64. Fornazier, M.J.; Carmo, C.A.S.D.O.; Teixeira, C.P.; Pereira, E.B. Finding of the strawberry borer Lobiopa insularis in the State of Espirito Santo. EMCAPA Comun. Técnico 1986, 44, 3. [Google Scholar]
  65. Salles, L.A.B.; Williams, R.N. Broca-Do-Morango (Lobiopa insularis); Embrapa Clima Temperado; Circular Tecnica: Pelotas, Brazil, 1986; p. 17. [Google Scholar]
  66. Greco, N.; Cluigt, N.; Cline, A.; Liljesthrom, G. Life history traits and life table analysis of Lobiopa insularis (Coleoptera: Nitidulidae) fed on strawberry. PLoS ONE 2017, 12, e0180093. [Google Scholar] [CrossRef] [Green Version]
  67. Swett, C.L.; Butler, B.B.; Peres, N.A.; Koivunen, E.E.; Hellman, E.M.; Beaulieu, J.R. Using model-based fungicide programing to effectively control botrytis and anthracnose fruit rots in Mid-Atlantic strawberry fields and co-manage strawberry sap beetle (Stelidota geminate). Crop Prot. 2020, 134, 105175. [Google Scholar] [CrossRef]
  68. Labuschagne, L.; Wainwright, H.; Jennings, D.L. Evidence of variation in susceptibility to vine weevil (Otiorhynchus sulcatus) in strawberry cultivars. Acta Hortic. 1997, 2, 877–880. [Google Scholar] [CrossRef]
  69. Downes, W. The strawberry root weevil in British Columbia. In The 50th Annual Report of the Entomological Society of Ontario; Entomological Society of Ontario: Toronto, ON, Canada, 1920; Volume 36, pp. 84–88. [Google Scholar]
  70. Bomford, M.K.; Vernon, R.S. Root weevil (Coleoptera: Curculionidae) and ground beetle (Coleoptera: Carabidae) immigration into strawberry plots protected by fence or portable trench barriers. Environ. Entomol. 2005, 34, 844–849. [Google Scholar] [CrossRef] [Green Version]
  71. Reddy, P.P. Strawberry. In Sustainable Crop Protection under Protected Cultivation; Springer: Berlin/Heidelberg, Germany, 2016; pp. 245–260. [Google Scholar]
  72. Krauß, A.; Steen, C.; Zebitz, C.P.W. Phenology of the strawberry blossom weevil and damage in strawberries. In Proceedings of the 16th International Conference on Organic Fruit-Growing. Stuttgart-Hohenheim, Weinsberg, Germany, 17–19 February 2014; pp. 32–236. [Google Scholar]
  73. Innocenzi, P.J.; Hall, D.R.; Cross, J.V. Components of male aggregation pheromone of strawberry blossom weevil, Anthonomus rubi Herbst (Coleoptera: Curculionidae). J. Chem. Ecol. 2001, 27, 1203–1218. [Google Scholar] [CrossRef]
  74. Franklin, M.T.; Hueppelsheuser, T.K.; Abram, P.K.; Bouchard, P.; Anderson, R.S.; Gibson, G.A. The Eurasian strawberry blossom weevil, Anthonomus rubi (Herbst, 1795), is established in North America. Can. Entomol. 2021, 153, 579–585. [Google Scholar] [CrossRef]
  75. Aasen, S.S.; Trandem, N. Strawberry blossom weevil Anthonomus rubi Herbst (Col.: Curculionidae): Relationships between bud damage, weevil density, insecticide use, and yield. J. Pest Sci. 2006, 79, 169–174. [Google Scholar] [CrossRef]
  76. Tonina, L.; Zanettin, G.; Miorelli, P.; Puppato, S.; Cuthbertson, A.G.; Grassi, A. Anthonomus rubi on strawberry fruit: Its biology, ecology, damage, and control from an IPM perspective. Insects 2021, 12, 701. [Google Scholar] [CrossRef] [PubMed]
  77. Cross, J.V.; Hesketh, H.; Jay, C.N.; Hall, D.R.; Innocenzi, P.J.; Farman, D.I.; Burgess, C.M. Exploiting the aggregation pheromone of strawberry blossom weevil Anthonomus rubi Herbst (Coleoptera: Curculionidae): Part 1. Development of lure and trap. Crop Prot. 2006, 25, 144–154. [Google Scholar] [CrossRef]
  78. LaMondia, J.A.; Elmer, W.H.; Mervosh, T.L.; Cowles, R.S. Integrated management of strawberry pests by rotation and intercropping. Crop Prot. 2002, 21, 837–846. [Google Scholar] [CrossRef]
  79. Atallah, J.; Teixeira, L.; Salazar, R.; Zaragoza, G.; Kopp, A. The making of a pest: The evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proc. R. Soc. B 2014, 281, 20132840. [Google Scholar] [CrossRef] [Green Version]
  80. Boughdad, A.; Haddi, K.; El Bouazzati, A.; Nassiri, A.; Tahiri, A.; El Anbri, C.; Eddaya, T.; Zaid, A.; Biondi, A. First record of the invasive spotted wing Drosophila infesting berry crops in Africa. J. Pest Sci. 2021, 94, 261–271. [Google Scholar] [CrossRef]
  81. Bolda, M.P.; Goodhue, R.E.; Zalom, F.G. Spotted wing drosophila: Potential economic impact of a newly established pest. Berkeley CA Univ. Calif. 2010, 13, 5–8. [Google Scholar]
  82. Zhu, E.Y.; Guntur, A.R.; He, R.; Stern, U.; Yang, C.H. Egg-laying demand induces aversion of UV light in Drosophila females. Curr. Biol. 2014, 24, 2797–2804. [Google Scholar] [CrossRef] [Green Version]
  83. Fountain, M.T.; Badiee, A.; Hemer, S.; Delgado, A.; Mangan, M.; Dowding, C.; Davis, F.; Pearson, A. The use of light spectrum blocking films to reduce populations of Drosophila suzukii Matsumura in fruit crops. Sci. Rep. 2020, 10, 153–158. [Google Scholar] [CrossRef]
  84. Gong, X.; Bräcker, L.; Bölke, N.; Plata, C.; Zeitlmayr, S.; Metzler, D.; Olbricht, K.; Gompel, N.; Parniske, M. Strawberry accessions with reduced Drosophila suzukii emergence from fruits. Front. Plant Sci. 2016, 7, 1880. [Google Scholar] [CrossRef] [Green Version]
  85. Renkema, J.M.; Cuthbertson, A.G. Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries. BioControl 2018, 63, 719–728. [Google Scholar] [CrossRef]
  86. Ng, J.C.; Perry, K.L. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 2004, 5, 505–511. [Google Scholar] [CrossRef] [PubMed]
  87. Bonneau, P.; Brisson, J.D.; Tellier, S.; Fournier, V. Flight phenology and trap selection for monitoring potential viral vector Aphididae and Aleyrodidae (Hemiptera) in strawberry (Rosaceae) fields of Quebec, Canada. Can. Entomol. 2019, 151, 378–390. [Google Scholar] [CrossRef]
  88. Peña-Martinez, R.; Munoz-Viveros, A.L.; Vanegas-Rico, J.M.; Rodriguez, D.; Hernandez, R.A.T. Presence and distribution of Aphis ruborum with parasitoid Aphidius colemani in Mexico. Southwest. Entomol. 2020, 45, 949–956. [Google Scholar]
  89. Cho, S.R.; Koo, H.N.; Shin, S.; Kim, H.K.; Park, J.H.; Yoon, Y.S.; Kim, G.H. Gamma-ray irradiation control of whiteflies Bemisia tabaci (Hemiptera: Aleyrodidae) and Trialeurodes vaporariorum in the exportation of fresh strawberries. J. Econ. Entomol. 2019, 112, 1611–1617. [Google Scholar] [CrossRef]
  90. Cuellar-Sandoval, J.F.; Ortega-Martínez, L.D.; Hernández-Velázquez, V.M.; Cuellar-Zometa, J.F.; Torres-García, G.; Barrales-Cureño, H.J.; Salazar-Magallón, J.A. Agroecological basis for the design of biotechnological traps based on Isaria fumosorosea for the biological control of Bemisia tabaci in strawberry crops. Biocontrol Sci. Technol. 2019, 29, 1–18. [Google Scholar] [CrossRef]
  91. Brooks, A.N.; Watson, J.M.R.; Mowry, H. Strawberries in Florida: Culture, Disease, and Insects; University of Florida Agricultural Experiment Station: Gainesville, FL, USA, 1929; p. 523. [Google Scholar]
  92. Dellape, P.M. Biodiversidad, Relationships Genetics and Biogeographic Aspects of Rhyparochromidae (Lygaeoidea: Heteroptera) with Special Reference to the Genus Neopamera Harrington 1980. Master’s Thesis, Facultad de Ciencias Naturales y Museo, National University of La Silver, La Plata, Argentina, 2005. [Google Scholar]
  93. Kuhn, T.M.; Loeck, A.E.; Zawadneak, M.A.; Garcia, S.; Button, M. Parameters biological and fertility life table of Neopamera bilobata (Hemiptera: Rhyparochromidae) in strawberry. Brasilia 2014, 49, 422–427. [Google Scholar]
  94. Bernardi, D.; Andreazza, F.; Nava, D.E.; Baronio, C.A.; Botton, M. Duplo Ataque. Cultivar HF 2015, 95, 16–19. [Google Scholar]
  95. Talton, H.R.; Rhodes, E.M.; Chase, C.A.; Swisher, M.E.; Renkema, J.M.; Liburd, O.E. Effect of cultural practices on Neopamera bilobata in relation to fruit injury and marketable yields in organic strawberries. Insects 2020, 11, 843. [Google Scholar] [CrossRef]
  96. Hata, F.T.; Ventura, M.U.; Bega, V.L.; Camacho, I.M.; Paula, M.T. Chinese chives and garlic in intercropping in strawberry high tunnels for Neopamera bilobata Say (Hemiptera: Rhyparochromidae) control. Bull. Entomol. Res. 2019, 109, 419–425. [Google Scholar] [CrossRef]
  97. Asano, S.; Nagaoka, H.; Wada, Y.; Miyamoto, K. Influence of leaves on the biological activity of Bacillus thuringiensis formulation against the common cutworm, Spodoptera litura. Jpn. J. Appl. Entomol. Zool. 2004, 48, 307–314. [Google Scholar] [CrossRef] [Green Version]
  98. Bortoli, L.C.; Bertin, A.; Efrom, C.F.S.; Botton, M. Biology, fertility life table and effect of insecticides on Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in strawberry and grape. Rev. Bras. Frutic. Jaboticabal. 2012, 34, 1068–1073. [Google Scholar] [CrossRef] [Green Version]
  99. Sigsgaard, L.; Naulin, C.; Haukeland, S.; Kristensen, K.; Enkegaard, A.; Jensen, N.L.; Eilenberg, J. The effects of strawberry cropping practices on the strawberry tortricid (Lepidoptera: Tortricidae), its natural enemies, and the presence of nematodes. J. Insect Sci. 2014, 14, 122. [Google Scholar] [CrossRef] [PubMed]
  100. Ottaviano, M.F.G.; Cédola, C.V.; Sánchez, N.E.; Greco, N.M. Conservation biological control in strawberry: Effect of different pollen on development, survival, and reproduction of Neoseiulus californicus (Acari: Phytoseiidae). Exp. Appl. Acarol. 2015, 67, 507–521. [Google Scholar] [CrossRef] [PubMed]
Table 1. Summary table of pest management techniques for strawberry pests.
Table 1. Summary table of pest management techniques for strawberry pests.
Strawberry PestManagementReferences
Thrips
Scirtothrips dorsalis Hood
Frankliniella occidentalis Pergande
Biological Control
Predators:
  • Neoseiulus cucumeris Oudemans,
  • Stratiolaelaps scimitus (Womersley),
  • Amblyseius swirskii Athias-Henriot,
  • Orius spp.,
  • Thripinema spp.
Cultural Control
Eliminating the alternative host or weeds
Chemical Control
  • spinetoram,
  • cyantraniliprole,
  • flupyradifurone,
  • imidacloprid + lambda,
  • cyhalothrin, bifenthrin,
  • neem extract
[18,19,20]






[16]


[10,21]



[22]
Mites
Tetranychus urticae Koch



















Phytonemus pallidus Banks
Physical Control
Steam treatment at 48 °C for 2.7 h for adults and 1.9 h for eggs.
Biological Control
Predators:
Phytoseiulus persimilis Athias-Henriot.
Neoseiulus californicus McGregor
Biopesticides:
  • Metarhizium anisopliae strain F52,
  • Isaria fumosoroseus Apopka strain 97,
  • heat-killed Burkholderia rinojensis strain A396,
  • heat-killed Chromobacterium subtsugae strain PRAA4-1
Chemical Control
  • azadirachtin,
  • paraffinic oil,
  • potassium salts of fatty acids,
  • unsulfonated residue of petroleum oil,
  • neem oil


Physical Control
Steam treatment at 46 °C for 6.5 min
Biological Control
Predators:
  • Neoseiulus californicus McGregor,
  • Neoseiulus cucumeris Oudemans
[32]


[26,33,100]


[34,35,36]
Tarnished Plant Bug
Lygus lineolaris (Palisot de Beauvois)
Lygus rugulipennis Poppius
Physical Control
Tractor-mounted suction machines
Biological Control
  • Beauveria bassiana (Balsamo-Crivelli) Vuillemin
  • Anaphes iole Girault
Cultural Control
Trap crop, Medicago sativa L.
Chemical Control
  • hexyl butyrate + phenylacetaldehyde for Push-Pull Strategy

  • flupyradifurone,
  • novaluron,
  • flonicamid,
  • pyrethroids,
  • organophosphates,
  • neonicotinoids
[54,55,56]


[51]

[53]

[41,58,59]

[52]


[49,50]
Beetles
Sap Beetles
Haptoncus luteolus (Erichson), Lobiopa insularis (Castelnau), Carpophilus fumatus Boheman, Stelidota geminate (Say)




Weevils
Otiorhynchus sulcatus F., O. ovatus L., O. singularis L., Otiorhynchus cribricollis Gyllenhal, Pantomorus cervinus Boheman, Nemocestes incomptus Horn, Barypeithes pellucidus Boheman, Sciopithes obscurus L.






Anthonomus rubi Herbst










Popillia japonica Newman, Anomala orientalis Waterhouse, Amphimallon majalis Razoumowsky, Maladera castanea Arrow

Host Plant Resistance
Cultivars with ripe fruits not touching the ground
Cultural Control
Field sanitation by removal of ripe fruits
Chemical Control
  • Pyrethroids
  • Limiting fungicide application by using environmental- model-based spray program.


Biological Control
Entomopathogenic nematode, Steinernema kraussei (Steiner, 1923)
Host Plant Resistance
Cultivar “Symphony” showed lower feeding and oviposition.
Cultural Control
Strawberry bed sanitation by removal of weeds and grass.
Chemical Control
  • Pyrethroids


Physical Control
  • Yellow sticky card combined with synthetic attractants for adult monitoring and mass trapping.
  • Periodic removal of severed buds or adults.
Biological Control
  • Braconidae
  • Pteromalus swederus


Cultural Control
Crop rotation with “Saia” oats, Avena strigosa Schreb and “Garry” oats, Avena sativa L.
Chemical Control
  • Neem Oil
  • Insecticidal Soaps

[63]

[62]

[62]

[67]



[68,71]










[76]


[77]

[74]


[71,78]
Spotted Wing Drosophila
Drosophila suzukii Matsumura
Physical control
Utilizing ultraviolet light; blue-green light spectrum (430–565 nm)

Biological control
Orius insidiosus (Say) along with Heterorhabditis bacteriophora Poinar
[83]



[85]
Aphids and Whiteflies
Aphid spp.





Trialeurodes vaporariorum Westwood
Bemisia tabaci Gennadius
Biological Control
  • Aphelinus varipes (Foerster)
  • Aphidius colemani Viereck
  • Syrphid flies
  • Green lacewings
  • Lady beetles


Physical Control
Irradiation of boxed fresh fruits with gamma rays (100 Gy)
Biological Control
  • Isaria fumosorosea (Wize)
  • Syrphid flies
  • Green lacewings
  • Lady beetles

[88]





[89]


[90]
Seed Bug
Neopamera bilobata Say
Cultural Control
Intercropping with garlic or undercropping with Chinese chives

Host plant resistance
Traditional plant breeding for varieties with seeds recessed into the fruit


[96]

[95]
Lepidopteran Pests
Spodoptera exigua (Hübner)







Duponchelia fovealis Zeller





Acleris comariana (Lienig and Zeller)

Physical control
Deploying pheromone traps
Biological control
Predator:
Hyposoter exiguae (Viereck)
Biopesticide:
Commercial formulations of Bacillus thuringiensis

Biological control
Beauveria bassiana (Balsamo-Crivelli) Vuillemin along with Podisus nigrispinus Dallas and Harmonia axyridis Pallas

Cultural Control
Improve strawberry cropping practices as less pest pressure experienced in organic strawberry and newer fields compared to conventional strawberry and older fields


[26]

[71,97]




[6]




[99]
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Lahiri, S.; Smith, H.A.; Gireesh, M.; Kaur, G.; Montemayor, J.D. Arthropod Pest Management in Strawberry. Insects 2022, 13, 475. https://doi.org/10.3390/insects13050475

AMA Style

Lahiri S, Smith HA, Gireesh M, Kaur G, Montemayor JD. Arthropod Pest Management in Strawberry. Insects. 2022; 13(5):475. https://doi.org/10.3390/insects13050475

Chicago/Turabian Style

Lahiri, Sriyanka, Hugh A. Smith, Midhula Gireesh, Gagandeep Kaur, and Joseph D. Montemayor. 2022. "Arthropod Pest Management in Strawberry" Insects 13, no. 5: 475. https://doi.org/10.3390/insects13050475

APA Style

Lahiri, S., Smith, H. A., Gireesh, M., Kaur, G., & Montemayor, J. D. (2022). Arthropod Pest Management in Strawberry. Insects, 13(5), 475. https://doi.org/10.3390/insects13050475

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