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Review

Tomato Potato Psyllid Bactericera cockerelli (Hemiptera: Triozidae) in Australia: Incursion, Potential Impact and Opportunities for Biological Control

by
Shovon Chandra Sarkar
1,*,
Séverin Hatt
2,
Andrew Philips
1,
Mahjuba Akter
1,
Stephen Paul Milroy
1 and
Wei Xu
1,*
1
Food Futures Institute, Murdoch University, Murdoch, WA 6150, Australia
2
Agroecology and Organic Farming, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, 53121 Bonn, Germany
*
Authors to whom correspondence should be addressed.
Insects 2023, 14(3), 263; https://doi.org/10.3390/insects14030263
Submission received: 6 February 2023 / Revised: 26 February 2023 / Accepted: 6 March 2023 / Published: 7 March 2023
(This article belongs to the Section Insect Ecology, Diversity and Conservation)
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Abstract

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Simple Summary

The tomato potato psyllid, Bactericera cockerelli, is an important insect pest of potato, tomato, and other solanaceous crops. B. cockerelli was first detected on mainland Australia in Perth, Western Australia, in early 2017, which poses a major threat to Australian vegetable industries. It damages directly by feeding and indirectly as a vector of Candidatus Liberibacter solanaceaerum (CLso) that causes zebra chip disease in potatoes. Thus far, B. cockerelli has not been reported in other states of Australia. As B. cockerelli has been reported resistant to insecticides in USA and Mexico, biological control with native natural enemies may provide a viable alternative strategy to manage the insect. In this review, we begin with an overview of information on B. cockerelli, its incursion into Australia, and its impact on crops and current management. Opportunities to develop biological control strategies to alleviate the dependence on synthetic insecticides are also considered in this review. Moreover, the potential of existing natural enemies to contribute toward regulating populations of B. cockerelli in the field and the challenges ahead to strengthen the key role they can play through conservation biological control are also discussed.

Abstract

Incursion and establishment of an exotic pest may threaten natural habitats and disrupt ecosystems. On the other hand, resident natural enemies may play an important role in invasive pest control. Bactericera cockerelli, commonly known as the tomato-potato psyllid, is an exotic pest, first detected on mainland Australia in Perth, Western Australia, in early 2017. B. cockerelli causes direct damage to crops by feeding and indirectly by acting as the vector of the pathogen that causes zebra chip disease in potatoes, although the latter is not present in mainland Australia. At present, Australian growers rely on the frequent use of insecticides to control B. cockerelli, which may lead to a series of negative economic and environmental consequences. The incursion of B. cockerelli also provides a unique opportunity to develop a conservation biological control strategy through strategically targeting existing natural enemy communities. In this review, we consider opportunities to develop biological control strategies for B. cockerelli to alleviate the dependence on synthetic insecticides. We highlight the potential of existing natural enemies to contribute toward regulating populations of B. cockerelli in the field and discuss the challenges ahead to strengthen the key role they can play through conservation biological control.

1. Introduction

The tomato potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae), is an invasive polyphagous pest that is spreading globally both naturally and via human activity that damages a wide variety of crops, especially in the Solanaceae [1,2]. In February 2017, B. cockerelli was first detected in mainland Australia in Perth, Western Australia (WA), and since then, its range has expanded rapidly over the southwest of the state [3]. Thus far, B. cockerelli has not been reported in other states of mainland Australia, but if this spread occurs, it may cause substantial disruption to solanaceous crops and huge economic losses in the Australian vegetable industry.
Previously, Butler and Trumble [4] reviewed the biology and ecology of B. cockerelli and presented a set of management strategies to control B. cockerelli and the pathogen it transmits. More recently, Olaniyan et al. [5] updated the current knowledge on B. cockerelli and the control strategies in the context of an imminent risk of invasion in China. Similarly, Vereijssen et al. [6] and Vereijssen [7] did so in the context of New Zealand, where B. cockerelli has become established. In the present review, the current situation of B. cockerelli in Australia is described, and its potential spread across the country is discussed in light of its biological properties and within this country’s ecological context. Finally, the role of native and resident non-native species of natural enemies and host plant species of B. cockerelli for conservation biological control are also discussed.
To date, the application of insecticides has been the main way to control B. cockerelli worldwide; repeated applications are often involved (as reviewed by Butler and Trumble [4]). In the present review, the reliance on chemical control is discussed by highlighting the detrimental ecological effects of insecticide use against B. cockerelli in Australia. As an alternative, opportunities for biological control are presented by reviewing the current challenges for its development and implementation in Australia. Notably, a diversity of potential host plants and natural enemies of B. cockerelli in Australia is identified, and strategies for biological control through habitat management to conserve them in Australian agricultural landscapes are suggested. Our aim is to provide information towards the development of more ecologically based and environmentally friendly strategies for the management of B. cockerelli using existing natural enemies in Australia.

2. B. cockerelli as a Crop Pest

B. cockerelli is an economically important agricultural insect pest for a range of crops. Its host range encompasses over 40 species of solanaceous plants and can utilize species from over 20 families [8,9,10,11].
The sum of biological characteristics of B. cockerelli, including its small size (the adult body can vary from 2.5 to 2.75 mm), short developmental times (12–44 days with an average of 15.4 days), high reproductive rate (on average, up to 330 eggs over a female lifetime), flying skill and its superior host acquisition capability contributes to make it an invasive pest [4,9,10,12]. Invasive pests often exhibit high phenotypic plasticity, which makes them difficult to differentiate from native species of the same family at the early stages of development [13,14]. B. cockerelli goes through three stages of development: egg, nymph, and adult. Eggs of B. cockerelli are mainly deposited near the leaf edge and on the lower leaf surface but may be deposited on any part of the plant, although this varies with the host plant [15]. Nymphs of B. cockerelli are usually found in shaded locations (mostly on the lower leaf surfaces) and usually remain sedentary during all five nymphal stages [9]. The adults are pale green in color when they emerge darker in color within 2–3 days and later can become grey or black [16]. Adults have well-developed wings and legs, are good fliers, and jump readily when disturbed [1,17,18]. The optimum temperature for reproduction and development is 24–27 °C, while temperatures above 31 °C may cause death [19,20]. Henne et al. [21] reported that both B. cockerelli nymphs and adults are cold tolerant: nymphs survived at −15 °C for 24 h, and 50% of adults survived at −10 °C for 24 h. However, the development and survival of B. cockerelli are impacted by the identity of the host plant [22].
B. cockerelli can cause severe economic losses by damaging host plants through phloem-feeding and indirectly by acting as a vector of the alphaproteobacterium Candidatus Liberibacter solanacearum (CLso), a bacterial pathogen that can reduce crop yield significantly [5]. In the absence of a pathogen, feeding by B. cockerelli induces a host disorder known as “psyllid yellows” disease. Psyllid yellows are characterized by foliar symptoms, including chlorosis, upward rolling of younger leaves, stunting, and, in severe cases, may result in early plant death [23,24]. For potatoes, tuber development can be greatly affected, resulting in misshapen tubers and abnormal sprouting [24]. Tomatoes also exhibited significant yield reduction because of this disease. Fruit set, size, yield, and quality (including shape and texture) decrease significantly [22,24]. In extreme cases, total yield loss can occur [10,25,26]. Through the transmission of the CLso, B. cockerelli attacks can cause “zebra chip” disease [27,28]. Potatoes affected by zebra chip exhibit symptoms similar to psyllid yellows [28]. The name “zebra chip” comes from the dark lines that appear when infected tubers are fried, which makes fresh and processed potatoes unusable for the market [29].
The zebra chip disorder can spread rapidly within a production region of Solanaceous crops [30,31]. Therefore, the economic impact of zebra chip disease has been severe on the worldwide export business of Solanaceae [32,33]. After the detection of B. cockerelli in WA, the export of all live plant material, not only potato tubers but also all horticultural produce potato tubers market access from WA to other states of Australia was immediately ceased. The movement of material was reinstated on an industry-by-industry basis. To remove the trade barrier on WA potatoes, an extensive surveillance program for CLso detection began in October 2018 with networks of psyllid traps established in various locations where the psyllid had been identified. To date, the CLso pathogen has not been found in WA. However, in 2018, the disease was first reported in Norfolk Island, an external territory of Australia. The disease was in tomato plants with yellowing symptoms [34].

3. Invasiveness and Distribution of B. cockerelli

Over the last two decades, B. cockerelli has received increasing attention and has been recognized as an important pest of solanaceous crops, especially when it was identified as the key vector of CLso [2,35].
In WA, the state Department of Primary Industries and Regional Development (DPIRD) identified B. cockerelli in Perth in February 2017 and found that it was already widespread around the Perth metropolitan area [3]. Olaniyan et al. [5] theorized that B. cockerelli may have arrived in Australia either through legal importation or through the smuggling of infested host plant material. Previously, Biosecurity Australia [36] and Plant Health Australia [37] mentioned that international trade of fresh fruits, potato tubers, nursery stocks, or hitchhiker transportation of psyllids on plant or non-plant materials were possible means of entry to Australia.
In Oceania, B. cockerelli was first found in New Zealand in 2006 [38], and since then, it has established populations all over that country, where it causes extensive damage to crops in the Solanaceae [33]. It is not clear how B. cockerelli arrived in New Zealand. Still, it is believed that, through international trade or through smuggled primary host plant materials, it was introduced from the North American region between 2000 and 2006 [25,32,33,34,39]. After the discovery of B. cockerelli in New Zealand, the Australian government implemented strict measures to prevent the invasion of this pest to Australia [40]. To date, four haplotypes (western, central, northwestern, and southwestern) of B. cockerelli have been identified worldwide. The haplotype found in WA is the western haplotype, previously found in Norfolk Island, New Zealand, Honduras, Guatemala, Mexico, and the western USA [39,41].
Nonetheless, B. cockerelli has so far only been observed in WA in mainland Australia. There are several possible reasons why B. cockerelli has not been discovered in other Australian states so far. The most likely reason is that there is potentially a large host gap between the agricultural areas of WA and those of the other states of Australia. From the edge of the wheat-sheep zone east of Esperance (WA) to the areas west of Ceduna (South Australia) is a distance of some 1000 km. Between is a narrow coastal strip with low rainfall (200–300 mm), strongly seasonal, bordering the desert areas of central Australia. However, the higher rainfall areas where outdoor horticulture is established are much more widely separated than the cereal production areas. Because the potential of Australian native species to host B. cockerelli is poorly known [40], the significance of this geographical separation is unclear. While there is the potential for B. cockerelli to move from WA to the other states via commercial shipments of products, inter-state, and intra-state quarantine regulations are in place. Secondly, the incursion and establishment of B. cockerelli may be hampered because of competition with native psyllid and other insect species. Liu and Trumble [22] observed competition between native and invasive psyllid species in North America. However, there is very little information available about potential interactions of B. cockerelli and Australian native psyllids or other insects that may occupy similar ecological niches.
It should also be recognized that at the early stage of incursion, the density of B. cockerelli will be low, and their smaller size and cryptic behavior create difficulties in identification. Therefore, at the early stage of incursion, B. cockerelli may remain unnoticed in the extensive agricultural landscape of Australia. However, Australia’s eastern and southern states are located in the optimal climate regions for B. cockerelli and thus should be recognized as being at high risk [41].

4. Chemical Control of B. cockerelli and Ecological Effects

Growers have mainly relied on the frequent application of insecticides to control B. cockerelli worldwide, which has also been the basis for managing zebra chips as there is no known treatment available for CLso [42,43].
Insecticides such as cyantraniliprole, spinetoram, oxamyl, imidacloprid, spirotetramat, and tolfenpyrad have been tested under greenhouse conditions against B. cockerelli adults and nymphs in the Columbia Basin [44]. The results showed that spinetoram and high rates of cyantraniliprole had the greatest immediate and residual activity against B. cockerelli adults. Cyantraniliprole and oxamyl were effective against nymphs, with no differences between rates [45]. The effects of different chemical insecticides may vary when applied to different plants or cultivars [46,47].
The management of B. cockerelli is difficult due to their cryptic habits, as the nymph of B. cockerelli usually lives on the lower side of the leaf, which reduces the impact of contact insecticides. Moreover, repeated chemical treatments are frequently necessary to ensure ongoing control of the pest. For example, in Mexico, potato growers have been required to apply up to 30 foliar sprays per season [48]. In New Zealand, a grower can reach nearly fifteen sprays per season [32]. Such high usage of synthetic insecticides can potentially lead to a series of adverse ecological effects, including insecticide resistance in B. cockerelli, residue problems, environmental contamination, toxicity to beneficial and non-target organisms, species displacement, and disruption of biological control [49,50,51,52]. In addition, chemical control of B. cockerelli is costly (around US $700 per hectare) [43,53]. Control measures may seriously erode profit margins when high numbers of applications are needed. Despite this, the reduction of B. cockerelli numbers in potato fields may not decrease CLso infestation [54], and thus saleability of the product is still reduced. Moreover, the application of chemical insecticides can lead to secondary pest outbreaks [55]. For example, pyrethroid insecticides can induce higher oviposition by B. cockerelli females and also flare other pests such as aphids (Hemiptera: Aphididae) and mites (Acari: Tetranychidae) [56].
A study of insecticides, including abamectin, cyantraniliprole, pymetrozine, flonicamid, and spirotetramat on B. cockerelli in WA revealed that abamectin, cyantraniliprole, and spirotetramat effectively suppressed B. cockerelli in pepper, tomato, and potato [3]. Of the feeding deterrents, flonicamid showed some degree of B. cockerelli suppression, while pymetrozine did not provide any suppression of B. cockerelli [3]. These two compounds have also shown limited impact in reports from the USA (Liu and Trumble 2005). To date, there has been no report of insecticide resistance in B. cockerelli in Oceania [5]. In California, Liu and Trumble [22] observed B. cockerelli resistance to imidacloprid (LC50 for 50% of B. cockerelli nymphs). Prager et al. [54] also reported resistance of B. cockerelli to imidacloprid in South Texas (USA). Thus, while there is not yet evidence of insecticide resistance in Australia, in light of the reports from the USA and Mexico [51,57], it can be expected that the B. cockerelli population of Australia and New Zealand will eventually show resistance against chemical insecticides unless resistance management strategies are developed and deployed across industries. However, this relies on (i) the availability and registration of effective insecticides with a range of modes of action and (ii) the level of industry coordination and compliance with resistance management strategies. Resistance has become a major concern, and synthetic insecticides may not be a long-term solution for B. cockerelli management [5].

5. Prospects for Biological Control Using Existing Natural Enemies in Australia

There appear to be significant opportunities to use natural arthropod enemies for the management of B. cockerelli in Australia as an alternative strategy to insecticide application or as part of an integrated management approach. This may also contribute to the development of resistance management strategies. A number of generalist predator species in Australia may have the potential as biocontrol agents for this new invasive pest (Table 1). Generalist predators are more resilient to pest invasions and have a higher likelihood of being able to utilize a new species as prey; thus, they can often play an important role in developing biological control strategies against new invasive pest species [58,59,60,61,62,63,64,65].
Research over the past two decades has demonstrated the potential of several species to utilize B. cockerelli as prey and, in some cases, has indicated the potential to control populations. Among the Coleoptera, the 11-spotted ladybird beetle, Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and the large spotted ladybird beetle, Harmonia conformis Boisduval (Coleoptera: Coccinellidae) can prey upon all life stages of B. cockerelli, and they were identified by McDonald et al. [110] as potential biocontrol agents for potato in New Zealand. Convergent ladybird beetle Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae) has been reported as a predator of B. cockerelli in California [42]). Laboratory and glasshouse experiments indicated the Southern ladybird beetle, Cleobora mellyi Mulsant (Coleoptera: Coccinellidae), as a potential biocontrol agent for B. cockerelli in New Zealand [111]. This ladybird species, imported to New Zealand from Australia, can consume up to 100 nymphs of B. cockerelli in 24 h [112].
Among the Neuroptera, the brown lacewing Micromus tasmaniae Walker (Neuroptera: Hemerobiidae) can prey upon all life stages of B. cockerelli, and it was identified by MacDonald et al. [110] as a potential biocontrol agent for potato in New Zealand. It is found widely in potato fields in New Zealand and is considered a dominant predator. Importantly, it was observed to attack B. cockerelli early in the potato production cycle [113]. Both M. tasmaniae and Melanostoma fasciatum Macquart (Diptera: Syrphidae) are reported to be able to consume more than 12 nymphs in 24 h [110].
In the Americas, various Hemiptera have been found to manage B.cockerelli. In Mexico, Pineda et al. [114] identified the predatory mirid, Engytatus varians Distant (Hemiptera: Miridae), as a promising biocontrol agent of B. cockerelli on tomatoes. However, E. varians can also damage tomato plants [114]. In Mexico, Perez-Aguilar et al. [115] were able to control B. cockerelli without crop damage on greenhouse tomatoes. When the predatory mirid, Dicyphus hesperus Knight (Hemiptera: Miridae), was evaluated as a biocontrol agent of B. cockerelli and Bemisia tabaci Gennadius (Hemiptera: Aleyrodidaeon) in greenhouse tomatoes, Calvo et al. [116] observed that it could significantly reduce the numbers of both pests. It has been known for some time that the minute pirate bug, Orius tristicolor White (Hemiptera: Anthocoridae), can consume a considerable number of B. cockerelli nymphs and adults in solanaceous crops [4,117]. Similarly, Butler and Trumble [42] confirmed the western big-eyed bug, Geocoris pallens Stål (Hemiptera: Geocoridae), to be a predator of B. cockerelli in potato. This species had been previously noted by Pletsch [23] in the northwestern region of the United States.
In addition to predators, parasitoids might also have potential as biological control agents. Tamarixia triozae Burks (Hymenoptera: Eulophidae), a parasitoid of the Asian citrus psyllid (Diaphorina citri Kuwayama), has between 60% and 80% parasitism rate on B. cockerelli [118]. However, Luna-Cruz et al. [119,120] and Liu et al. [121] reported the high mortality of adult T. triozae due to its susceptibility to insecticides, emphasizing the challenge of combining insecticide usage and biological control in IPM [50,122,123].
Although predators from a range of genera and families are known to attack B. cockerelli, whether measured in the field, glasshouse, or laboratory, substantially more research is needed to establish which species are likely to be viable biological control agents. Key questions relate to the capacity to establish and maintain useful predator populations in the field and the likely choice of prey by polyphagous predators.
Of primary importance will be assessing whether a species can survive and establish useful populations in the crop environment in the geographical location of interest and at the time of year when suppression of the pest population is likely to be needed. This requires autecological data for both the pest and the predator across the likely range of deployment. In Australia, this will be challenging given the diversity of climatic zones and agroecological systems in which solanaceous crops are produced.
Butler and Trumble [42] have questioned whether biological control is feasible given the high reproductive rate of B. cockerelli. This will depend not only on the voracity of the predator but also on the timing of its release relative to the likely development of the B. cockerelli population and on the predator’s own reproduction rate [110]. In New Zealand, modeling capacity has been developed to predict the timing of likely B. cockerelli pressure based on the temperature conditions at the beginning of the season [124]. Whether this can be usefully adapted to Australian production systems will depend on the size of overwintering pest populations, their likely movement into crops, and the applicability of the model assumptions to Australian production environments.
The capacity of the predator population to remain in the system after release, particularly after B. cockerelli numbers have been suppressed, will influence release strategies. If the predator population declines too far, it may not have the capacity to respond to a new influx of the pest, and populations may need to be supplemented. Here again, polyphagous predators may present an advantage given their ability to utilize a range of food sources. If alternative food sources are present when the target pest declines, it will increase the likelihood of the predator remaining in the location. The possibility of conservation biological control to assist with maintaining predators in the environment will be discussed in the next section.
The species presented in Table 1 are already resident in Australian agroecosystems. This reflects their capacity to establish and maintain populations in the environment and makes them logical choices for evaluation. However, whether the population size is large enough or can build up quickly enough to provide a meaningful impact on B. cockerelli pest populations needs to be evaluated and appropriate intervention thresholds established. An interesting aspect in this regard will be the effect of utilizing B. cockerelli as a major food source (in contrast to established food sources) on the life expectancy and reproductive rate of the predator.
In many situations [125,126,127], perhaps more likely in field-grown crops than in the greenhouse, questions of prey choice and prey switching may also be significant. If alternative food sources are present, is the predator likely to utilize B. cockerelli, the alternative food source, or both? Calvo et al. [116] observed that D. hesperus established, reproduced, and significantly controlled two major Solanaceae pests, B. tabaci and B. cockerelli at the same time in the greenhouse. It is possible that this may be influenced by the previous feeding experience of the predator, whether this was under conditions of artificial rearing or in the field. That is, is it possible that a predator will adapt more quickly to the utilization of B. cockerelli if the species was part of its diet in the past?
There has been a recent trend towards using multiple natural enemies for the management of B. cockerelli to get more stability in pest control. de Lourdes Ramírez-Ahuja et al. [128] observed that the simultaneous release of the parasitoid T. triozae and the predatory mirid D. hesperus have an additive effect on the reduction of B. cockerelli populations. Entomopathogenic fungus Beauveria bassiana and the parasitoid T. triozae have also displayed potential for wide applications for controlling B. cockerelli worldwide [118,121,129], and Tamayo-Mejía et al. [130] suggested their combined application for biological control of B. cockerelli. However, the sub-lethal effects of B. bassiana on T. triozae would reduce their efficiency in B. cockerelli control [130,131]. These undesirable effects can possibly be minimized by the synchronized application of the two agents [131]. Additionally, resource competition might occur between predator species when they compete for the same prey [132,133,134]. Therefore, careful planning and management are required for combinations of biocontrol agents to control B. cockerelli.
From our preliminary field survey, laboratory, and glasshouse study (unpublished data), Australian native and non-native resident predators can play an important role in the biocontrol of B. cockerelli. Ladybird beetles (H. conformis, Cheilomenes sexmaculata Fabricius (Coleoptera: Coccinellidae), Coccinella transversalis Fabricius (Coleoptera: Coccinellidae) and Hippodamia variegata Goeze (Coleoptera: Coccinellidae)) and lacewings (Mallada sp. Schneider (Neuroptera: Chrysopidae) and M. tasmaniae) have been observed feeding on B. cockerelli in capsicum fields (Figure 1). Further, non-native resident species H. variegata and native species C. transversalis ladybird beetles successfully survived and suppressed B. cockerelli populations in the laboratory and in cage experiments using glasshouse-grown tomato plants [135,136]. Suppression by the ladybird beetles resulted in a positive influence on plant chlorophyll content and biomass.

6. Conservation of B. cockerelli Natural Enemies in Agricultural Landscapes

Conservation biological control is the practice of preserving the habitat surrounding fields to allow the natural enemies of pests to maintain a constant presence in the ecosystem, thus allowing faster colonization of the crops [137]. Faster colonization, in turn, would lead to greater and more timely control of pests. While a diversity of potential B. cockerelli predators and parasitoids has been identified (Table 1; see also the previous section), we have conducted a field survey to identify the effective natural enemies of B. cockerelli occurring in the environment in Western Australia (unpublished data). To our knowledge, habitat management to enhance biological control against this pest has not been evaluated either in Australia or elsewhere.
Research into conservation biological control of other pests in Australia and into ecological services more generally may guide research aiming at testing habitat management strategies for the control of B. cockerelli. Some previous results may prove directly applicable, such as information on population dynamics or movement of generalist predators in the environment where these species have also been identified as predators of B. cockerelli. In Australia, non-crop habitats such as native forests and remnant woodlands are known to host predators, and parasitoids of crop pests benefit from woody shelterbelts and windbreak hedgerows, as well as remnant native grasslands (reviewed by Gagic et al. [138]). Whenever possible in Australia, native plant species should be chosen when designing and implementing semi-natural habitats since it has been shown that native species host more natural enemies and fewer pests in comparison to exotic plant species [139].
The proportion of native vegetation and its fragmentation and spatial distribution varies dramatically across the agricultural areas of WA (https://dwer.wa.gov.au/ (accessed on 1 May 2022)). In the central wheat belt particularly, the proportion of native vegetation is low, and the remnants are fragmented. By contrast, in the higher rainfall zones south of Perth, that is, west of approximately 116°30′ E, there are more extensive areas of forest and reserve (Geographical Information Services 2016). It is in the higher rainfall areas of WA that B. cockerelli is currently found and where the main crop hosts, potato, tomato, capsicum, and eggplant, are produced. In some cases, tomato and potato crops are grown adjacent to forests or remnant native vegetation. The value of this contact needs to be assessed in terms of the colonization of crops by predators. However, it should also be noted that WA has a very high diversity of native species of Solanaceae. The capacity of these species to host B. cockerelli has not been explored. Thus, proximity to native vegetation may present risks and benefits that must be evaluated.
Flower-rich semi-natural habitats have also been explored to bolster populations of beneficial species. Sowing strips of buckwheat (Fagopyrum esculentum Moench, Polygonaceae) and coriander (Coriandrum sativum L. Apiaceae) is possible adjacent to fields of Solanaceae [140,141,142]. These flowers are known to be visited by several natural enemies (Coccinellidae, Chrysopidae, Syrphidae, parasitoids) of B. cockerelli and enhance fitness by providing alternative foods [143,144]. Crops of species such as lucerne (Medicago sativa L., Fabaceae) in spring and sorghum (Sorghum bicolor L. Moench, Poaceae) in summer, can host a high abundance of generalist predators, including Coccinella spp., Nabis spp., and Micromus spp. [145]. In their review, Rizvi et al. [146] highlighted the potential role of sorghum (Sorghum bicolor L. Moench, Poaceae) as a banker plant sown at the border of capsicum fields and indicated that the technique is now being trialed by growers in WA.
Successful experiences of habitat management conducted outside Australia enhancing natural enemies of B. cockerelli could also contribute to the development of effective conservation biological control against this pest. Many of the B. cockerelli natural enemies present in Australia (Table 1) depend on nectar and pollen for surviving and reproduce, i.e., adult Syrphidae, Eulophidae, Encyrtidae [118,147], and adult Coccinellidae, Chrysoperla spp. and Orius spp. are mixed feeders [148,149]. Notably, flower-rich habitats could use multi-species and functional mixtures to attract and support a diversity of natural enemies throughout the season [150]. In Switzerland, for instance, wildflower strips composed of a mixture of annual forb species significantly enhanced the abundance of adult lacewings and eggs and the richness of predatory hoverflies in adjacent potato crops [151]. In China, annual wildflower strips sown outside but along greenhouses enhanced the abundance of Orius sp. and lacewings in eggplants (Solanum melongena L., Solanaceae) cultivated indoors [152]. In the USA, hedgerows composed of native shrubs and bordered by native grasses enhanced the abundance of predatory ladybird beetles, including Hippodamia spp., in adjacent tomato fields [153].
The management of native vegetation, the utilization of existing crops in the landscape as hosts, and the introduction of planted strips of ‘banker plants’ all present possibilities for enhancing the biological control of B. cockerelli. However, their benefit and strategies for their implementation will need to be considered across the diversity of the Australian production environments and systems. Where these approaches contribute to enhancing populations of generalist predators, it is possible that they may enhance the management of a range of pest species and so have a wider benefit.

7. Conclusions

B. cockerelli is spreading internationally. It poses a threat to the production of globally important Solanaceous crops both directly and as a vector for CLso. The use of chemical insecticides has already caused problems through the development of insecticide resistance in the psyllid and through the disruption of its natural enemies. Research, development, and implementation of biological control against B. cockerelli present an important alternative approach to control that may also contribute to the development of resistance management strategies or be incorporated as a possible component of Integrated Pest Management approaches.
The diversity of generalist natural enemies of B. cockerelli that are already present in Australia is promising. This shifts the emphasis for future research away from identifying potential predators and towards quantifying their benefit within Australian agroecological systems. Questions of population dynamics within these systems and the influence of the prey species on the development and reproduction of the predators are of primary importance. These factors are likely to vary substantially across the continent. A major variable will be the influence of surrounding vegetation on both the pest and predator species.

Author Contributions

Conceptualization, S.C.S.; writing—original draft preparation, S.C.S., S.H., S.P.M., and W.X.; writing—review and editing, S.C.S., S.H., A.P., M.A., S.P.M. and W.X. All authors have read and agreed to the published version of the manuscript.

Funding

S.C.S. was supported through the “Research Training Program (RTP)” scholarship and Murdoch International Postgraduate Scholarship (MIPS)” by Murdoch University. W.X. is funded by an Australian Research Council Discovery Early Career Researcher Award (DECRA) (DE160100382). S.H. is funded by the European Union’s Horizon 2020 programme “Nurturing excellence by means of cross-border and cross-sector mobility” (MarieSklodowska—Curie Individual Fellowship, Grant agreement ID: 891566). This research is also funded by the Agricultural Produce Commission (APC P2123 197POT and APC P2123 197VEG) of WA, Australia.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The new data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Insects 14 00263 g001 550
Figure 1. Coccinella transversalis larvae praying on Bactericera cockerelli nymphs on capsicum in the field.
Figure 1. Coccinella transversalis larvae praying on Bactericera cockerelli nymphs on capsicum in the field.
Insects 14 00263 g001
Table
Table 1. Natural enemies that occur in Australia and that have been identified in other countries as preying upon or parasitizing Bactericera cockerelli.
Table 1. Natural enemies that occur in Australia and that have been identified in other countries as preying upon or parasitizing Bactericera cockerelli.
ClassOrderFamilySpeciesDistribution in AustraliaReferences
ArachnidaAcariAnystidaeAnystis baccarum LinnéNSW, QLD, SA, TAS, VICHolm and Wallace [66]
PhytoseiidaePhytoseiinaeNSW, NT, QLD, SA, TAS, VIC, WAWalter and Beard [67]; Beard [68]
AraneaeAraneideaCyclosa sp.; Nesoscona sp.All statesWhyte and Anderson [69]
DictynidaeIxeuticus candidus KochAll statesNew [70]
LinyphiidaeLaetesia raveni
Hormiga and Scharff		NSW, QLD, SAHormiga and Scharff [71]
MiturgidaeCheiracanthium spp.All statesRaven [72]; Hogg et al. [73]
OxyopidaeOxyopes spp.All statesVink and Sirvid [74]; Baehr et al. [75]
SalticidaeHabronattus spp.All statesRichardson et al. [76]
TheridiidaeTheridion sp.All statesFramenau [77]
ThomisidaeThomisidae spp.All statesSzymkowiak [78]
InsectaColeopteraCoccinellidaeCleobora mellyi Mulsant; Hippodamia variegata Goeze; Coccinella transversalis
Fabricius, etc.		All statesPope [79]; Lipiski [80]; Franzmann [81]; Slipinski [82]; Li et al. [83]
MelyridaePhycosecis litoralis PascoeAll statesBeutel and Pollock [84]
StaphylinidaePlatystethus sp.All statesChandler [85]
DermapteraForficulidaeForficula auricularia
L.		NSW, QLD, SABinns et al. [86]
DipteraDolichopodidaeAsyndetus Loew; Chrysotus spp. Medetera spp. BickelAll statesBickel [87,88,89]
SyrphidaeAllograpta Osten Sacken; Sphaerophoria spp.; Melanostoma sp.All statesMengual and Thompson [90]; Robertson et al. [91]; Finch and Cook [92]
HemipteraAnthocoridaeOrius Wolff; O. gracilis sp. n.NSW, NT, QLD, WAPostle et al. [93]
BerytidaeRhyparochrominae spp.; Berytinus spp.NSW, QLD, SA, TASSlater and Woodward [94]; Wheeler and Schaefer [95]
NabidaeNabis kinbergii ReuterAll statesMa et al.l. [96]
GeocoridaeGermalus Stål; Stylogeocoris MontandonNT, QLD, SA, VICMalipatil and Blackett [97]
MiridaeCreontiades Distant; Engytatus passionarius sp. nov.All statesMalipatil and Cassis [98]; Minghetti et al. [99]
PentatomidaeOechalia schellenbergii GuérinAll statesSands and Coombs [100]
ReduviidaeEmesopsis spp.All statesTatarnic et al. [101]
HymenopteraEncyrtidaeBaeoanusia xanthopleuron sp. n.; Avetianella coombsi sp. n.NSW, QLD, SA, VICSchmidt and Noyes [102]
EulophidaeTamarixia spp.NSWZuparko et al. [103]
FormicidaeLinepithema humile MayrNSW, QLD, SA, TAS, VIC, WAWalters and Mackay [104]
NeuropteraChrysopidaeChrysoperla spp.; Mallada signatus Schneider; Lauraya retivenosa sp.n.NSW, QLD, SA, TAS, VIC, WASmithers [105]; Winterton [106]
HemerobiidaeMicromus tasmaniae WalkerACT, NSW, QLD, SA, TAS, VIC, WANew [107,108]
ThysanopteraAeolothripidaeCranothrips Bagnall; Cycadothrips MoundTAS, VICMound and Marullo [109]
States of Australia: Australian Capital Territory (ACT), New South Wales (NSW), Queensland (QLD), Northern Territory (NT), Western Australia (WA), South Australia (SA), Victoria (VIC), and Tasmania (TAS). Distribution area data collected from ‘Atlas living of Australia (www.ala.org.au).’
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Sarkar, S.C.; Hatt, S.; Philips, A.; Akter, M.; Milroy, S.P.; Xu, W. Tomato Potato Psyllid Bactericera cockerelli (Hemiptera: Triozidae) in Australia: Incursion, Potential Impact and Opportunities for Biological Control. Insects 2023, 14, 263. https://doi.org/10.3390/insects14030263

AMA Style

Sarkar SC, Hatt S, Philips A, Akter M, Milroy SP, Xu W. Tomato Potato Psyllid Bactericera cockerelli (Hemiptera: Triozidae) in Australia: Incursion, Potential Impact and Opportunities for Biological Control. Insects. 2023; 14(3):263. https://doi.org/10.3390/insects14030263

Chicago/Turabian Style

Sarkar, Shovon Chandra, Séverin Hatt, Andrew Philips, Mahjuba Akter, Stephen Paul Milroy, and Wei Xu. 2023. "Tomato Potato Psyllid Bactericera cockerelli (Hemiptera: Triozidae) in Australia: Incursion, Potential Impact and Opportunities for Biological Control" Insects 14, no. 3: 263. https://doi.org/10.3390/insects14030263

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