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Review

Approaches to Integrated Pest Management in Orchards: Comstockaspis perniciosa (Comstock) Case Study

by
Katarzyna Golan
,
Izabela Kot
*,
Katarzyna Kmieć
and
Edyta Górska-Drabik
Department of Plant Protection, University of Life Sciences in Lublin, Leszczyńskiego 7, 20-069 Lublin, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(1), 131; https://doi.org/10.3390/agriculture13010131
Submission received: 25 November 2022 / Revised: 27 December 2022 / Accepted: 31 December 2022 / Published: 4 January 2023
(This article belongs to the Special Issue Role of Agriculture in Implementing Concept of Sustainable Food System)
Review Reports Versions Notes

Abstract

:
Insect pests have major effects on agricultural production and food supply. Pest control in conventional crop management in orchards is mainly based on agrochemicals, which entails economic, health and environmental costs. Other approaches, such as biological methods or products based on biologically active substances and sex pheromones used for mating disruption, have faced some implementation challenges, particularly in relation to invasive insect species. The key for appropriate insect pest management is to identify the species and understand its biology and behaviour. Pest management systems should monitor, detect and inform fruit growers about changes in insect distribution, population ecology, possible damage level and economic loses. Comstockaspis perniciosa (San José scale—SJS) is a model example of a pest against which the method of integrated pest management should be adopted. This review presents a case study to support this statement.

1. Introduction

The armored scales (Hemiptera: Coccomorpha: Diaspididae) are sap-sucking, often concealed insects. There are approximately 2600 described species of Diaspididae worldwide [1], of which at least 200 are pests of agricultural crops, forest trees, ornamentals and greenhouse plants [2]. They are among the most invasive insects in the world, since they can be readily transported with plant material. Moreover, they are small and cryptic in habit, and thus go largely unnoticed and uncollected in natural habitats [3]. Armored scale insects are a morphologically distinct and homogenous group with extreme sexual dimorphism. Male nymphs have five instars, including two pupa-like quiescent stages, and adult males have a distinct head, thorax, an abdomen and one pair of wings. They live for a day or less and never feed [1]. Female nymphs have three instars, and the crawler instar (first instar) is the only one that is mobile. Adult females are morphologically reduced, sessile, legless, wingless and do not have a clear head and body [4]. The bodies of the older nymphs and females have a protective covering, the so-called ‘scale’, consisting of a waxy secretion, which is shaped with a pygidium. The scale-like covering either may occur as a discharge adhering to the cuticle or as a structure detached from the body [5]. This cover offers protection from direct contact with insecticides, which affects the effectiveness of chemical control. Furthermore, efforts to manage invasive insects, including scales, are often non-species-specific and provide short-lived effects [6]. The mouth parts of Diaspididae consist of piercing stylets that penetrate cells of mesodermal parenchyma in leaves and stems as well as mesocarp cells in fruits. Chlorosis, necrosis, reduced productivity, retarded development of the plants and their susceptibility to microbes and other insects is observed as a consequence of their feeding [7]. Because they feed on the parenchyma tissues of the host plants, they do not produce honeydew [8].
The control of the armored scale insects is based mainly on application of synthetic insecticides. The use of natural enemies and their efficacy is dependent on the correct identification of both the armored scale and its natural enemies, while the morphological identification of scale insects is based on microscopic cuticular characters of adult females, which requires expertise [9]. Parasitoids associated with Diaspididae belong to the families of Aphelinidae, Encyrtidae and Signiphoridae, with Aphelinidae being most numerously represented [10].
One of the armored scale insect species, Comstockaspis perniciosa (Comstock, 1881) (San José scale, SJS) previously known as Quadraspidiotus perniciosus (Comstock), fits in with the characteristics mentioned above. It is a cosmopolitan and highly polyphagous species, with a tendency towards rapid and mass colonisation of host plants. It is considered the most serious pest of fruit trees in Europe and several other countries in the world [11]. C. perniciosa is native to eastern Asia and was brought to North America, where it was first discovered in San José, California in 1880 [12]. Currently, it is common in the Palearctic and Nearctic regions, as well as in South America, Australia and New Zealand [13]. The San José scale had been the object of quarantine regulations in European countries; however, due to its spread over most of the continent, the European Commission decided not to qualify this species as a quarantine pest anymore [14]. Many abiotic and biotic factors affect the spread and evolution of C. perniciosa; nevertheless, temperature seems to be the most relevant [11].
The list of San José scale host plants includes at least 193 plant genera, with Malus, Morus, Prunus, Pyrus, Ribes, Rubus and Vaccinium being crucial due to their economic importance [1]. This species is described as a major pest, causing severe damage to almond and peach trees in Greece [15,16] and Ukraine [17], pears (destruction of trees) in Kazakhstan [18] and China [19], sour-cherry trees in Hungary [20] and apple trees in New Zealand [21], India [22], Romania [23], Kazakhstan [24], Chile [25], Portugal [26] and Poland [11].
The overwintering stage is the so-called black cap nymph (immature first instar), which occurs on the bark of tree trunks and branches. Hibernation of adult females or second-stage nymphs has sometimes been observed; however, only black cap nymphs were recorded to survive the low temperatures during the winter [11]. Development resumes in spring, and nymphs of C. perniciosa undergo several moults and the scales grow in diameter. The female’s scale covering is circular, while the male’s becomes elongated. The female’s body is soft, yellow in colour and without wings or legs. Its covering is grey, reaching a diameter of 2 mm. Males are winged, 1 mm long and the body colour is yellow, with a dark band across the back. They fly for 2–3 days, mate with females and subsequently die. Females are viviparous and have a high fertility rate. First-instar nymphs, commonly referred to as crawlers (mobile stage), are oval, yellow and about 0.3 mm long. Only this stage is capable of dispersing and colonising new areas. They walk on bark, leaves or fruits until they find a suitable place to settle. They are active for less than one day, and factors such as temperature, humidity, dustiness, population density and host plant species have an impact on crawlers’ settlement [27]. Within 24 h of hatching, they settle and insert their mouthpart into the host plant tissues, their antennae and legs undergo atrophy, they feed on sap and they start to produce cover. Feeding nymphs secrete a white waxy covering (white cap nymph), which turns black (black cap nymph) and then grey before maturation. According to the literature, two or three generations occur per year in the northern hemisphere [11,14,28,29] and three or four in the southern [25,30] hemisphere. Sometimes, single generations become so numerous that they overlap, and insects completely cover tree branches. Scale insects, including the San José scale, show low dispersal ability, and they spread by wind, birds, other insects or by infested seedlings in the nursery.
C. perniciosa, as all armored scales, feed on the content of individual parenchyma cells [31]. During feeding, sap accumulates in tree bark tissues, causing the surface to swell and the bark to crack. This results in a decrease in tree vigour, growth and productivity [32]. Long-lasting feeding, without pest control, can lead to the death of twigs or even the entire tree. Infested fruits have a slight depression and reddish-purple blotches around the feeding sites. This causes distortions, cracking and premature fruit dropping, ultimately reducing the quality and size of the yield (fruits are not marketable). Red spots may form around the scale within 24 h of crawler settling, but can also develop several weeks later. At present, the control of C. perniciosa is mainly based on the dormant application of mineral oils in wintertime against overwintering stages and the application of insecticides during the growing season. Summer treatments with mineral oils during the growing season are also possible due to improvements in refinement of oils, which are safer to plants. Nevertheless, there are still many precautions recommended (e.g., avoiding large spray droplet sizes by using the right equipment and spray pressure; oils must be sprayed directly on the insect due to their low residual activity, and oils cannot be sprayed when temperatures are below 5 °C or above 28 °C degrees and the relative humidity is above 90%) whenever using an oil on a woody plant to avoid plant injury (phytotoxicity) [33]. Furthermore, considering that the European Commission has proposed “Sustainable Use of Plant Protection Products” regulation with an objective to cut pesticides by 50% by 2030, and the fact that pesticide use against the San José scale is limited to period of crawler occurrence (the most sensitive stage to insecticide), this review updates key information on management practices [34]. Our approach was to review the current state of knowledge regarding monitoring and infestation assessment methods, the application of insecticides and nonchemical control methods to help develop control strategies of this pest.

2. Monitoring and Treatment Decisions

The presence of SJS is mostly detected on twigs and branches during pruning and on fruits during harvest or packing. Scouting the trees during the dormancy period allows one to detect infested plants and determine the level of infestation [14]. If the presence of SJS is detected, monitoring methods should be applied. Searching for crawlers and immobile instars on twigs, leaves and fruits, the application of sticky tape traps for crawlers, and pheromone traps for winged males are the most commonly used methods in SJS monitoring [11,14,35,36,37]. Assessing the number of SJS per fruit and the percentage of infested fruits allows one to estimate the degree of orchard infestation, and also provides feedback on the treatments applied. Results of the research conducted in Portugal demonstrated that 64.5% and 100% of fruits were infested in commercial and abandoned apple orchards, respectively [36].
Most San José scale specimens overwinter in the third phase of the first nymphal instar, known as the black cap stage. Winter survival is high, reaching more than 80% in untreated orchards [31]. This usually results in a well-synchronised emergence of the first generation of adults and crawlers in spring [38]. Adult males live for only a few days, while adult females produce offspring during a period of six weeks. In this way, successive generations overlap and all stages can occur on the tree at the same time during summer [30,31,38].
Research conducted in the 1970s and 1980s on SJS phenology and sex pheromones enabled the use of synthetic pheromones to detect and monitor male activity [39,40,41,42,43,44]. Since then, this method has been widely used by scientists and fruit growers around the world [14,45,46,47,48]. SJS sex pheromone compounds include (Z)-3,7-dimethy1-2,7-octadien-1-y1 propanoate and 7-methyl-3-methylene-7-octen-1-y1 propanoate. Synthetic sex pheromones have also been found to have a kairomonal effect on the SJS parasitoid Encarsia perniciosi (Hymenoptera: Aphelinidae) [49]. Observations of male activity under field conditions of North America and Greece indicated a lower flight temperature threshold of approx. 17 °C [26,42,45]. Pheromone lures, which are effective for 4 to 6 weeks, can be placed in delta (closed) traps, open-tent (sticky-board) traps or wing-shape traps [14]. Hoyt et al. [39] found tent traps to be more efficient than closed traps. However, the study by Rychla [29] suggested the comparable effectiveness of wing and delta traps, with the latter being more convenient to handle. Recently, there has been an increased interest in the use of digital sensors for pest monitoring [50,51]. A trap attached to a wireless networked digital camera (self-counting trap) can be used for scale insect monitoring, which has been proven for the California red scale, Aonidiella aurantii (Maskell) [37]. This type of trap for SJS catching is available on the market. It is a helpful time-saving tool for growers; however, more research is needed in this field. In commercial orchards, pheromone traps are commonly applied to establish the time of the first male capture, referred to as biofix [14,38]. This date is used for the accumulation of degree days. SJS traps should be placed in spring and located at a height of about 2 m in the northeastern part of the tree [39]. Badenes-Perez et al. [38] demonstrated that in Kern County, CA, USA, the relative density of trapped males was positively correlated with the crawler population density of the first generation. In Greece, Deligeorgidis et al. [46] did not find any relationship between captured adults and nymphs. On the other hand, a study of Mague and Reissig [52] in Wayne County, NY, USA, showed an inverse relationship between the cumulative pheromone trap catch of males and the total direct count of crawlers on trees. The discrepancies in the results could be related to different weather conditions between various US states and Europe. Other factors affecting observations may involve the number of generations developing each year and/or host species (almond, apple cv. Red Chief, apple cv. McIntosh, respectively).
San José scale mobile crawlers are deprived of waxy cover only within approximately 24 h of hatching [11]. Subsequently, they become sessile and start to produce a waxy sac, making the next larval instars and females less vulnerable to environmental stresses and insecticide treatments [53]. Therefore, knowledge of peak mobile crawler activity is fundamental for effective management. Their presence can be confirmed by searching for crawlers on branches, leaves and fruits [31]. Various studies reported different crawler densities depending on the estimation method used. Wearing and de Boer [30] found up to 31.6 crawler per cm2 of bark, while approximately 100 nymphs per 100 cm2 were detected by Mague and Reissig [54]. A three-minute count of crawlers on apple bark using a hand lens showed the presence of up to 500 individuals depending on generation and management model [31]. On the other hand, 8.5 to 65.2 nymphs per fruit were recorded in a commercial and unsprayed orchard in Portugal, respectively [36]. Monitoring crawlers in the field is problematic due to their size and difficulties in their identification; thus, it is also possible to use sticky tape traps to assess their abundance. It is known that armored scale crawlers mostly remain on the same plant on which they emerged. They move mainly vertically on the tree for several hours after emergence covering distances of up to 3 m, but often settle within 1 m of their sessile mother. Hence, sticky tapes placed around the branches allows one to evaluate crawler activity and density [27,36,38]. Double-sided sticky traps are recommended for use in commercial orchards as an effective and practical tool for monitoring SJS nymphs [55]. On the other hand, sticky-tape traps have been shown to be labour-intensive, and are therefore not widely selected for treatment decisions by growers and their consultants [38].
Research on insect phenology in correlation with temperature, referred to as growing degree days (DD), led to the development of insect models. They are a useful tool for predicting insect development and timing of treatments [56]. The degree-day accumulation method can be used to predict the appearance of subsequent developmental stages [14,56,57]. SJS phenology is not consistent across studies. The low temperature threshold in many studies was set at 10.5 °C [14,29,44,55,58] or 10.6 °C [31,37]; however, other values were also reported, e.g., 7.3 °C [28] and 10 °C [26,52,54]. Seasonal DD accumulation should begin when daily temperatures exceed the developmental threshold of 10.5 °C. It usually starts on January 1 (e.g., Arizona, southern Utah) or March 1 (e.g., western Colorado, Idaho, northern Utah) depending on temperature conditions [14]. For SJS the most important thing is the precise timing of the treatment, which controls the first generation of crawlers and can prevent fruit infestation. Since insect activity varies from year to year depending on weather conditions, calculating DD can help in scouting operations, e.g., setting traps or looking for crawlers. The baseline temperature and accumulation start date for calculating DD for the San José scale vary in the literature; therefore, it is difficult to compare the results calculated for different stages and generations (Table 1). In general, pheromone traps should be placed approximately at the pink stage of apple [11,14]; biofix (first male catch) was recorded at 84–140 DD, while the first crawlers were recorded at 196–294 DD. This indicates the need to develop the SJS model independently for different regions.

3. Application of Insecticides

Of all phytophagous insects of apple orchards, C. perniciosa is a key pest in many commercial orchards almost all over the world. Without proper control, it causes tree death within a few years [25,59,60,61,62,63,64,65,66,67,68,69]. Effective control with chemicals is not satisfactory, due to its behaviour and differences in susceptibility between individual developmental stages [25,70,71].
Numerous attempts to control SJS resulted in the development of lime-sulphur spray, which was the first widely used insecticide spray in the United States, extensively applied for SJS control until 1922. Felt [72] documented that properly prepared and applied lime-sulphur applications gave satisfactory results in controlling SJS populations in orchards. In turn, the entire US apple industry was threatened in 1914 with extinction when lime-sulphur applications did not provide protection due to SJS resistance [73]. Petroleum oil has been used to reduce the abundance of various pest species since 1871 [74]. However, promising results regarding C. perniciosa control using lime sulphur have significantly slowed down research on the use of oils for SJS control. Ackerman [75], in his landmark study, proved that oil emulsions were more effective in SJS control compared to lime-sulphur. As a result, oils have become the dormant spray of choice in SJS control, and are also essential components in the control of this pest in current eradication programmes.
Until the late 1940s, the damage caused by SJS was very severe. However, with the introduction of long-lasting chlorinated hydrocarbon insecticides, namely DDT and other persistent insecticides, SJS nearly disappeared from crops [12,76]. DDT, as a foliar spray for C. perniciosa control, started to be widely used in orchards in 1945 [77]. DDT was first applied to control codling moth and quickly replaced the previously used lead arsenate or cryolite. Until then, annual applications of dormant or delayed dormant sprays of oil, lime sulphur or mixtures thereof were necessary for SJS control to prevent serious losses [75]. These treatments often caused damage to plants in orchards by exerting a phytotoxic effect. In fact, growers often omitted or postponed the application of dormant sprays until the necessity for control became apparent because of a significant increase in scale infestation [12,78,79]. The studies conducted in the late 1940s indicated that two or more DDT cover spray applications inhibited the growth of the San José scale population despite skipping dormant sprays during the past 3 to 5 years. In turn, a significant increase in SJS population was recorded in the fruit orchards that were not sprayed with DDT [77].
The 1950s was another period of significant increase in the occurrence of San José scale in fruit crops, particularly in North America. SJS were present in orchards that were repeatedly treated with synthetic organic insecticides, due to the development of resistance, as well as probably the disruption of the natural enemy complex [80]. Research on the control of this pest has been revived following the development of many organophosphorus insecticides. The fact that growers have used even more than eight chemical treatments for many years, mainly with organophosphate (OP) insecticides, has contributed to the harmfulness and invasiveness of this pest since the 1980s. However, the incidence of this pest has increased, indicating a major resurgence attributed to growers switching from dormant diesel spray to potent synthetic chemical pesticides. This strategy yielded excellent results in reducing San José scale incidence in the early years, but later, in recent years, it led to pest resurgence and a disruption of the natural enemy complex, and possibly the development of pesticide resistance [12,63,79,80]. In consequence, the SJS was one of the first documented cases of insect resistance to synthetic insecticide in the USA [25]. Currently, SJS control in various regions of the world involves different protection strategies based primarily on integrated pest management and country-specific regulations. Buzzetti et al. [63] and González [80] observed increased SJS infestation levels in Chilean orchards in the early 21st century. Acetylcholinesterase (AChE) inhibitors from the group of organophosphate (OP) insecticides, such as chlorpyrifos and methidathion, have been frequently used in many orchards to control this pest, and chemical control programmes have included 6–8 applications per season [81]. According to literature data [12,63,79,80,82], organophosphate insecticides have been the main alternative for pest control in apple orchards since their introduction to the Chilean market in the 1960s. At the beginning of the 21st century, new requirements of importing markets have forced the use of more selective insecticide alternatives [63]. This shift in management strategy gave excellent results in reducing the incidence of San José scale in the early years, but subsequently, it caused pest resurgence [65]. At the end of the 20th century, the use of broad-spectrum insecticides such as methyl parathion and chlorpyrifos, which had previously kept SJS incidence to a minimum, was abandoned or reduced [83]. New regulations have limited the use of such products in many countries, but new chemical compounds have not shown the same degree of control [84].
At present, in addition to OP insecticides, the pesticide market offers a variety of other types of agents, including a class of neuroactive insecticides from the neonicotinoid group (nicotinic receptor agonists), which act as an insect neurotoxin; a class of chemicals called sulphoximines (sulphoxaflor), which affect the central nervous system of insects; and a class of pesticides known as tetronic acid insecticides. Juvenile hormone analogues and insect growth regulators (e.g., pyriproxyfen and buprofezin) are used in SJS population control in many countries in the world. These products prevent larvae from developing into their adult stage, or they act as chitin synthesis inhibitors. Insect growth regulators (IGR) buprofezin and pyriproxyfen, or neurotoxic sulphoxaflor, have recently been registered in Chile and North America and can be used in San José scale control [85,86]. According to Michigan State University, Lorsban® (chlorpyriphos), Esteem® (pyriproxyfen) and Centaur® (buprofezin) are the most effective insecticides for early-season SJS control [87]. Foliar preparations of Lorsban may be used for dormant or delayed-dormant C. perniciosa control, either alone or in combination with oil. Esteem works as an IGR by inhibiting egg development, and the application of Esteem with oil controls the overwintering stages of SJS. Centaur is an IGR insecticide that acts on insect nymph stages by inhibiting chitin biosynthesis, thereby interfering with insect moulting. Centaur can be used in single applications, with oil as an additive or a penetrant surfactant for effective control. In recent years, spirotetramat, another IGR, has been developed, which is used alone or in combination with thiacloprid in commercial formulations; acetamiprid and thiacloprid are other examples of recently introduced agents applied against C. perniciosa [81,88,89,90].
Local sprays of mineral oils have been used for many years against various groups of insects, but most commonly to control scale insects in horticulture [14,31,91]. Products recommended for this purpose are the so-called horticultural oils (e.g., superior, supreme, or other similar weight of petroleum oil). Oils block insect spiracles, causing them to die from asphyxiation. They may also interact with insect fatty acids and interfere its metabolism [33]. High efficacy (93% mortality of San José scale nymph) was shown for 6% soybean oil and 3% petroleum oil applied in the dormant season [31]. Even a single application of the above concentrations reduced pest population for subsequent years. A similar effect can be achieved with a soybean oil concentration <3%, but only after two consecutive years of application. The application of these oils also reduces the effect of tree dieback observed in orchards not protected with oils. Similar results were obtained by Mesbah et al. [92] who applied heavy and light mineral oils. The highest reduction in the C. perniciosa population infesting pear trees (mortality >90%) was obtained for a light oil called Caple-2 (applied in the summer season), followed by the heavy oils Albolium oil®, Marsona oil® and Moxy oil® (applied during the winter season). Mineral oils for the control of scale insects are comparable in efficacy to chemical pesticides and even superior in terms of protection of natural enemies and the environment. The effectiveness of mineral oils is closely related to the timing of application. The San José scale was controlled by the normal orchard practice of dormant spraying with diesel–oil emulsion and by the complex of natural enemies, including the dominant aphelinid parasitoid (Encarsia perniciosi Tower) [78,93]. According to Alston and coauthors [14], the best approach against the wintering stage is to use delayed-dormant sprays. Horticultural oils are recommended, but insecticide should be added if the SJS infestation rate is high. Timing of horticultural oil application against the crawler stage is also important for effective management of this species [14,91]. Recently, an increase in SJS population has been observed in many European countries and in the United States, probably due to a general decline in the use of dormant oil sprays, partly due to their increasing costs [29,63,78,79,84]. However, the spectrum of plant protection products used to control SJSs varies depending on the growing region and regulations. It is also important that fruits with ecologically based pest management are widely introduced and preferred by consumers, which reduces the use of chemical agents and the number of treatments and gives priority to nonchemical control.
The widespread use of toxic chemicals to control scale insects has caused many problems, such as the unsatisfactory effectiveness of C. perniciosa management programmes, development of insect resistance to insecticides, environmental pollution and reduced populations of natural enemies. Alternative, effective and environmentally safe nonchemical methods are urgently needed.

4. Nonchemical Control

Botanical insecticides, often referred to as green pesticides, are a group of nonchemical agents that have been widely tested to control many pest species. There are several studies confirming the high efficacy of plant extracts against representatives of the family Diaspididae [94,95]. Fitiwy et al. [94] documented the effectiveness of an insecticide extracted from the seed kernels of neem tree (Azadiractha indica Jussieu) and tree tobacco (Nicotinia glauca Graham) in controlling the armored scale A. aurantii, a species related to C. perniciosa, feeding on orange trees. The high efficacy of azadirachtin against this insect species was also confirmed in other studies [95,96]. Although there has been no research on the use of essential oils directly on C. perniciosa, literature data indicate that some essential oils are highly effective against this group of insects. Formulations prepared from the essential oils of Ambrosia maritima L., Origanum minutiflorum O. Schwarz & P.H. Davis, Cymbopogon nardus (L.) Rendle and Cymbopogon citratus (DC.) Stapf. can be used as green insecticides against Aulacaspis tubereularis (News.) (Diaspididae). Among them, O. minutiflorum was the most effective, and caused more than 88% of insect mortality. Essential oil preparations affect scale insects both by contact and systemically. After spraying, the oil solution forms a barrier on the insect covers, which prevents their respiration. Residues of the essential oil solution can also penetrate plant tissues, be transported throughout the plant and consequently kill sucking insects [96].
The presence of the San José scale on fruits is a serious problem, not only for fruit growers and organic food producers, but also for their exporters. Attempts have been made to use ultrasound to eliminate C. perniciosa from the fruit surface, but the expected phytosanitary effect was not achieved. The insufficient effectiveness of this method was attributed to the specific morphological structure of the insect [97]. In contrast, good results were achieved by Endarto and Wicaksono [98] using high-pressure water (HPW with pressure 1000 psi). This method allowed them to destroy all stages of the pest present on the fruits. According to the authors, an additional preventive effect can be achieved by adding calcium polysulphide to the water, which, by changing the microclimate of the environment, discourages mobile nymphs (crawlers) from infesting the sprayed trees. This method is easy and low-cost, as well as safe for nontarget plants and arthropods, because it consists of washing the trees (mainly the stem part) using only water without pesticide. In the 1990s, an attempt was also made to remove C. perniciosa by fumigation [99]. Fumigation with methyl bromide (32 g/m3) killed all infesting stages of this species on ‘Red Delicious’ apples in normal storage after 31 days and in controlled-atmosphere cold storage after 137 days. Total scale mortality on another apple variety (‘Winesap’) occurred after almost six months in both types of storage, if they had been previously fumigated. Moreover, the dosage required for 100% insect mortality can be detrimental to fruit quality [100]. Given the concern regarding fumigant residues, this type of method has not been implemented. The study of Chu [101] carried out in various storage options of fruits infested with SJS showed that temperature and atmosphere had discernible effects on the survival of these herbivores.
C. perniciosa populations are limited by natural enemies. There are many species of parasitoids and predators that are to a higher or lesser extent specialised against C. perniciosa. Data on the occurrence and role of these beneficial organisms come predominantly from India, as well as Pakistan, Greece and Romania, and they mainly include various species of ladybird (Coleoptera: Coccinnellidae) and chalcid wasps (Hymenoptera: Chalcidoidea).
Among predatory beetles, 10 species were recorded, 9 of which were ladybirds of the genus Chilocorus. The literature also indicates single species of ladybird from the following genera as natural enemies of the San José scale: Coccinella, Lindorus, Oenopia, Pharoscymnus, Platynaspis and Sticholatis; as well as a beetle from the family Cybocephalidae: Cybocephalus fodori Endrödy-Younga (Table 2).
There are not many concrete, quantitative data on the contribution of natural enemies to the control of San José scale in commercial orchards. According to Hix [102], their abundance in orchards is rather low. Therefore, repeated attempts have been made to introduce and colonise some species of natural enemies of C. perniciosa. An example of an introduced parasitoid is Prospaltella perniciosi Tower. This parasitoid was introduced in Greece in 1968 from France, and then was brought to the United States. Within 2 to 10 years, the parasitoid was found be well established, mainly in peach, apple and pear orchards. However, the level of pest parasitism was not satisfactory, and varied from 2 to 5% [103]. Similar results were obtained by the authors when conducting a study on a native parasitoid species, Aphytis spp. On the other hand, a much higher efficiency of natural SJS enemies was shown by Trandafirescu et al. [104], who used three predator species together with three parasitoid species and were able to reduce the population of the San José scale by more than 60% (Table 2). According to Khan [105], the release of 35 individuals of Chilocorus infernalis Mulsant per plant significantly reduced C. perniciosa infestation. As reported by Mesbah et al. [92], mineral oils may cause adverse effects on nontarget parasitoids. The latter authors reported that mineral oils (mostly Marsona oil®, Moxy oil® and CAPL-2) exhibited higher toxicity (16–30% mortality) against the San José scale parasitoid Aphytis diaspidis Howard.
Table
Table 2. Predators and parasitoids recorded from C. perniciosa based on literature data.
Table 2. Predators and parasitoids recorded from C. perniciosa based on literature data.
SpeciesTaxonomyReferences
PredatorsChilocerus infernalis Mulsant 1853
syn Chilocorus bijugus, Mulsant 1856		Coleoptera, Coccinellidae[59,105,106,107,108,109,110]
Chilocerus bipustulatus (Linnaeus, 1758)Coleoptera, Coccinellidae[15,103,104,111]
Chilocerus renipustulatus
(L.G. Scriba, 1791)		Coleoptera, Coccinellidae[104,111]
Coccinella septempunctata (Linnaeus, 1758)Coleoptera, Coccinellidae[109,110]
Exochomus quadripustulatus (Linnaeus, 1758)Coleoptera, Coccinellidae[104]
Lindorus lophantae (Blaisdell, 1892) Coleoptera, Coccinellidae[103]
Sticholotis marginalis, Kapur, 1956Coleoptera, Coccinellidae[109,110]
Pharoscymnus fleksibilis (Mulsant, 1853) Coleoptera, Coccinellidae[109,110]
Oenopia sauzeti
Mulsant, 1866		Coleoptera, Coccinellidae[110,112]
Platynaspis saundersi (Crotch, 1874)Coleoptera, Coccinellidae[112]
Cybocephalus fodori Endrody-Younga, 1965Coleoptera, Cybocephalidae[15,103]
ParasitoidsAphytis spp.Hymenoptera
Chalcidoidea
Aphelinidae		[103]
Aphytis sp proclia group WalkerHymenoptera
Chalcidoidea
Aphelinidae		[109,110,111]
Aphytis diaspidis (Howard, 1881)Hymenoptera
Chalcidoidea
Aphelinidae		[104,113]
Aphytis maculicornis Masi, 1911Hymenoptera
Chalcidoidea
Aphelinidae		[111]
Aphytis mytilaspidis
(Le Baron, 1870)		Hymenoptera
Chalcidoidea
Aphelinidae		[103,111]
Azotus perspeciosus Girault,1916Hymenoptera
Chalcidoidea
Aphelinidae		[109,110]
Azotus kashmirensis Narayanan, 1961 *Hymenoptera
Chalcidoidea
Aphelinidae		[35,110]
Encarsia perniciosi (Tower, 1913) syn. Prospaltella perniciosiHymenoptera
Chalcidoidea
Aphelinidae		[104,109,110,111,113]
Hispaniella lauri Mercet, 1911Hymenoptera
Chalcidoidea
Aphelinidae		[114]
Marietta carnesi (Howard, 1910) *Hymenoptera
Chalcidoidea
Aphelinidae		[35]
Teleterebratus perversus
Compere & Zinna, 1955		Hymenoptera
Chalcidoidea
Encyrtidae		[108]
Holcotorax spp.Hymenoptera
Chalcidoidea
Encyrtidae		[104]
Sympiesis spp.Hymenoptera
Chalcidoidea
Eulophidae		[104]
Apantheles sspHymenoptera
Braconidae		[104]
* hyperparasitoid.
Microorganisms such as entomopathogenic fungi, bacteria, viruses and nematodes also reduce the number of insects. This particularly applies to entomopathogenic fungi. They occupy an important position among all biocontrol agents because of their route of pathogenicity, broad host range and ability to control, e.g., sap-sucking pests. It is important to emphasise the minimal negative effect of entomopathogenic fungi on nontarget organisms, for which reason they offer a safer alternative in IPM [115,116]. Buhroo [117] and Buhroo et al. [22] tested fungal pathogens against crawlers and nymphs of C. perniciosa. Three fungal species, Beauveria bassiana (Bals.), Lecanicillium lucanii (Zimmermann) Zare & Gams and Metarhizium anisopliae (Metschin.) showed the highest efficacy against the SJS. High mortality (>75%) was determined at a concentration of 15 × 105 conidia/mL on day 30 after treatment (10 days after the emergence of the first crawlers). M. anisopliae showed slightly lower efficacy against the SJS. However, entomopathogenic fungi should be used when complete eradication of the pest is not required, and some crop damage is acceptable. Therefore, entomopathogenic fungi should be applied in combination with other methods if the pest must be completely eliminated.
The San José scale has been traditionally controlled by pesticides and dormant oils; there are some additional biological methods used in the control of this insect pest. Its sex-pheromone is known and has been in use for decades as a tool for monitoring C. perniciosa. However, increased pressure of SJS during recent years is providing a reason to look at new way of using pheromone for reducing this pest abundance. A new management strategy is mating disruption (MD) as a method for their control. MD is based on the release of synthetic sex pheromones, aiming to interrupt mate-finding communication and prevent mating in the target pest [68,84]. Males of San José scale are weak flyers; they only fly for a very short distance, while females are wingless, and this feature makes this species a very good species for testing pheromone-mediated mating disruption as an alternative strategy to insecticides [84]. Mating disruption has been commercially developed and applied against the vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae) and the California red scale A. aurantii. Critical factors affecting MD effectiveness are pest density and effective disruption late in the season. According to literature data [68,69] MD applied to scale insect pests is more effective in small plots and compatible with biological control and integrated management programs. However, there are no commercially registered San José scale disruption products; research on this is still ongoing. The key factors for its commercial application are technological advances in pheromone synthesis and pheromone formulations. According to research conducted by Maas [69], Franco et al. [68] and Gut [84] in recent years, the potential for mating disruption as a pest control of San José scale seems high.

5. Concluding Remarks and Perspectives

The problems associated with SJS control are influenced by changes in plant protection programmes applied in Europe and worldwide, which recommend limiting the use of chemical plant protection products to the minimum necessary. Currently recommended insecticides are highly selective for the pest; hence, growers require a sustainable chemical control strategy for C. perniciosa based on accurate data of its biology and behaviour. The best strategy for managing San José scale is to prevent serious infestations, and the most optimal cultural control is to prune out infested branches. This reduces the number of scales and opens up tree canopies, allowing better spray penetration. It is therefore necessary to develop and promote precise SJS monitoring systems using new technologies. Further research is required on new solutions of using products based on biologically active substances and environmentally friendly pest management tactics for mating disruption based on the release of synthetic sex pheromones.

Author Contributions

Conceptualization, K.G. and K.K.; methodology, K.G., I.K., K.K. and E.G.-D.; formal analysis, K.G.; investigation, K.K.; resources, E.G.-D. and I.K.; writing—original draft preparation, K.G., I.K., K.K. and E.G.-D.; writing—review and editing, I.K.; supervision, K.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of Life Sciences in Lublin, grant number OKK/S/44, in 2019–2022.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All the required data relevant to the presented study are included in the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Timing of San José scale 1st-generation events based on degree-day accumulations.
Table 1. Timing of San José scale 1st-generation events based on degree-day accumulations.
Biofix (DD)Emergence of 1st-Generation Crawlers (DD)Developmental Threshold (°C)Accumulating DD Start DateCountryReference
FirstPeak
94–140 360 510/55010.01 March USA (NY)[55]
116 326
(210 after biofix);		- 10.01 MarchPortugal[26]
275 405 after biofix600–700 after biofix10.51 January/1 MarchUSA [14]
Mid–late April (196 after biofix)(41–43 days after biofix)10.5After biofixNorthern Greece[55]
285534- 10.51 March India (Kashmir)[59]
84 286–294 -10.61 March USA (Tennessee)[31]
135324
(189 after biofix)		-10.6-Czech Republic[29]
Biofix—first male catch from overwintering generation; DD—degree day.
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Golan, K.; Kot, I.; Kmieć, K.; Górska-Drabik, E. Approaches to Integrated Pest Management in Orchards: Comstockaspis perniciosa (Comstock) Case Study. Agriculture 2023, 13, 131. https://doi.org/10.3390/agriculture13010131

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Golan K, Kot I, Kmieć K, Górska-Drabik E. Approaches to Integrated Pest Management in Orchards: Comstockaspis perniciosa (Comstock) Case Study. Agriculture. 2023; 13(1):131. https://doi.org/10.3390/agriculture13010131

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Golan, Katarzyna, Izabela Kot, Katarzyna Kmieć, and Edyta Górska-Drabik. 2023. "Approaches to Integrated Pest Management in Orchards: Comstockaspis perniciosa (Comstock) Case Study" Agriculture 13, no. 1: 131. https://doi.org/10.3390/agriculture13010131

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Golan, K., Kot, I., Kmieć, K., & Górska-Drabik, E. (2023). Approaches to Integrated Pest Management in Orchards: Comstockaspis perniciosa (Comstock) Case Study. Agriculture, 13(1), 131. https://doi.org/10.3390/agriculture13010131

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