Bactericera cockerelli
(tomato/potato psyllid)

Bactericera cockerelli is a vector of the plant pathogenic bacterium ‘Candidatus Liberibacter solanacearum’, haplotype A and B, the putative causal agent of zebra chip disease of potato tubers. This insect/pathogen complex is one of the most destructive potato pests in the western hemisphere, and New Zealand, and to a limited extend in Norfolk Island (Australia). It was recognized in the early 1900s that B. cockerelli had the potential to be an invasive and harmful insect, particularly in western United States and Mexico. By the 1920s and 1930s, B. cockerelli had become a serious and destructive pest of potatoes in most of the southwestern United States, giving rise to the description of a new foliar disease that became known as ‘psyllid yellows’. ‘Psyllid yellows’ has not been observed in New Zealand, and the description of the foliar symptoms is very similar to the foliar symptoms of ‘Ca. L. solanacearum’. As it has been suggested, so far, no pathogen or toxin has been associated with ‘psyllid yellows’, leading to the hypothesis that ‘Ca. L. solanacearum’ haplotype A or B has always been present at low, undetectable levels for many years. ‘Ca. L. solanacearum’ haplotypes C and D have been detected, affecting Apiaceae, in seed samples from 1973.

Since the late 2000s, the B. cockerelli/‘Ca. L. solanacearum’ complex has affected other solanaceous crops too, including tomato, pepper, aubergine, tobacco and tamarillo in a number of geographic areas and caused extensive economic losses.

Bactericera cockerelli is native to North America and is also found in Central America. It has invaded New Zealand, where it has caused damage to indoor and outdoor solanaceous crops. B. cockerelli has been placed on the list of quarantine pests in the EPPO region.

Bactericera cockerelli is native to North America and occurs mainly in the Great Plains region of the United States, from Colorado, New Mexico, Arizona and Nevada, north to Utah. More recently, its range has expanded to include Wyoming, Idaho, Montana, California, Oregon, Washington, Alberta and Saskatchewan (Pletsch, 1947; Wallis, 1955; Cranshaw, 1993; Ferguson and Shipp, 2002; Ferguson et al., 2003). This insect pest is common in southern and western Texas and has also been documented in Oklahoma, Kansas, Nebraska, South Dakota, North Dakota, Minnesota and as far west as California and British Columbia. Contrary to reports in the older literature (Pletsch 1947; Wallis 1955; Cranshaw 1993; 2001), the potato psyllid does indeed occur in Washington and Oregon, where it appears to overwinter locally (Jensen, 2012) and usually colonizes potato fields in late June and early July (Munyaneza et al., 2009a; Munyaneza, 2010; 2012; Crosslin et al., 2012a). Murphy et al. (2013) reported B. cockerelli overwintering in the Northwest Pacific (northeast Oregon, southeast Washington state and southwestern Idaho).

Bactericera cockerelli also occurs in Mexico, Guatemala, Honduras, El Salvador, Nicaragua and Ecuador (Pletsch, 1947; Wallis, 1955; Rubio-Covarrubias et al., 2006; Trumble, 2008; 2009; Crosslin et al., 2010; Espinoza, 2010; Munyaneza, 2010; 2012; Rehman et al., 2010; Rubio-Covarrubias et al., 2011; Bextine et al., 2012; 2013a, b; Aguilar et al., 2013a, b; Munyaneza et al., 2013a, b; 2014; Caicedo et al., 2020). There are no early records of B. cockerelli in Central or South America.

Bactericera cockerelli (and ‘Candidatus Liberibacter solanacearum’ haplotype A) is widespread in New Zealand (Teulon et al., 2009) and in Norfolk Island (Australian Government Department of Agriculture, 2015; Thomas et al., 2017). In February 2017, B. cockerelli, but not ‘Ca. L. solanacearum’, was found in Perth (Western Australia) and surroundings on mainland Australia (Department of Agriculture and Food Western Australia, 2017; EPPO, 2017b).

The B. cockerelli/‘Candidatus Liberibacter solanacearum’ complex is a serious and economically important pest of potatoes, tomatoes and other solanaceous crops in the western United States, southern Canada, Mexico, Central America, South America, Australia and New Zealand (EPPO, 2021). Suitable host plants are widespread in almost any part of the world and, given the insect’s current distribution in the Americas, Australia and New Zealand, it is thought that B. cockerelli could establish and overwinter outdoors in a variety of climates, with adults and nymphs able to sustain freezing winter temperatures (Whipple et al., 2012). It could also establish and overwinter under protected conditions in many regions.

The literature is rife with references to B. cockerelli hosts from 20 different plant families, which are often merely plants on which adult B. cockerelli have been found but no nymphal development has occurred. This has very likely led to misinformed decision making in countries that led a biosecurity response to the incursion of B. cockerelli (Martin, 2015). B. cockerelli is found primarily on plants within the family Solanaceae. The psyllid feeds, reproduces and develops on a variety of cultivated plant species such as potato (Solanum tuberosum), tomato (Solanum lycopersicum), pepper (Capsicum annuum), eggplant (Solanum melongena), tamarillo (Solanum betaceum [Cyphomandra betacea]) and tobacco (Nicotiana tabacum).

During field surveys, all life stages of the insect have also been found on weedy, non-crop species such as nightshade (Solanum spp.) in the USA and NZ (e.g. Klyver, 1932; Pletsch, 1947; Wallis, 1955; Martin, 2008; Taylor and Berry, 2011; Murphy et al., 2013; Swisher et al., 2013b; Thinakaran et al., 2015a), groundcherry (Physalis spp.) in the USA and Mexico (e.g. Richards and Blood, 1933; Daniels, 1934; Pletsch, 1947; Wallis, 1955; Crespo-Herrera et al., 2012), jimsonweeds (Datura spp.) in the USA and NZ (Klyver, 1931; Wallis, 1955; Vereijssen et al., 2015b), Nicandra spp. in the USA and NZ (Wallis, 1955; Martin, 2008; Vereijssen, J., unpublished data) and Lycium spp. in the USA and NZ (e.g. Richards and Blood, 1933; Romney, 1939; Jensen, 1954; Wallis, 1955; Taylor and Berry, 2011; Vereijssen and Scott, 2013). Some of these weed host plants are also hosts for ‘Candidatus Liberibacter solanacearum’ (Murphy et al., 2014; Vereijssen et al., 2015b). These non-crop plant species are important sources in the landscape for B. cockerelli feeding and breeding when the crops are not in the ground.

Beside solanaceous species, B. cockerelli has been shown to feed, reproduce and develop on Convolvulaceae species, including field bindweed (Convolvulus arvensis) in the USA and NZ (Knowlton and Thomas, 1934; List, 1939; Pletsch, 1947; Wallis, 1955; Kaur et al., 2018a, b; Vereijssen, J., unpublished data), Convolvulus tricolor (Kaur et al., 2018a, b), morning-glory (Ipomoea purpurea) (Knowlton and Thomas, 1934; Wallis, 1955), sweet potato (Ipomoea batatas) in the USA and NZ (Wallis, 1955; Puketapu and Roskruge, 2011) and Ipomoea ternifolia, Ipomoea cordatotriloba, Ipomoea alba and Ipomoea nil in the USA (Kaur et al., 2018a, b).

Genetics

Outbreaks of B. cockerelli in Baja California and coastal California led to the discovery that potato psyllid in those regions is genetically distinct from psyllids in southern Texas and eastern Mexico, which suggests there exists two different potato psyllid biotypes, referred to elsewhere as ‘western’ and ‘central’ biotypes (Liu et al., 2006; Jackson et al., 2009). The western biotype differs from southern Texas populations in several life history traits (Liu and Trumble, 2007). In New Zealand (Thompson et al., 2015), Western Australia (https://news.perth.media/2018/02/02/research-indicates-promising-tpp-control-growers/) and Norfolk Island (Thomas et al., 2017), the western biotype is present.

Following the 2011 reports of zebra chip in Idaho, Oregon and Washington (Crosslin et al., 2012a, b; Munyaneza, 2012), a genetic study by Swisher et al. (2012), using high resolution melting analysis of the mitochondrial Cytochrome C Oxidase subunit I-like gene of B. cockerelli, led to the identification of a third biotype (referred to as ‘northwestern haplotype’), so far known only from the Northwest Pacific. This northwestern potato psyllid biotype is genetically different from the central and western biotypes (Swisher et al., 2012). In addition, a recent study by Swisher et al. (2014) identified a fourth biotype of the psyllid, which appears to be distributed in New Mexico and parts of Colorado and referred to as a ‘southwestern haplotype’. Furthermore, potato psyllids in Mexico, Honduras, El Salvador and Nicaragua were identified as the central haplotype (Swisher et al., 2013a).

Reproductive Biology

In an effort to identify and develop a sex pheromone and other attractants that can be used to develop improved integrated pest management programmes for B. cockerelli, its reproductive biology and the role of chemical signals in sex attraction were studied by Guédot et al. (2010; 2012). It was determined for the first time that the potato psyllid possesses a female-produced pheromone that attracts males (Guédot et al., 2010). Guédot et al. (2012) also showed that adult potato psyllids reach reproductive maturity within 48 h post-eclosion, with females being mature on the day of eclosion and males at 1 day post-eclosion. In addition, oviposition generally began 2 days after mating but was delayed when females mated within 2 days post-eclosion. Seven-day fecundity was lower in ‘Candidatus Liberibacter solanacearum’ infected B. cockerelli than in ‘Ca. L. solanacearum’ free psyllids (Nachappa et al., 2012).

Optimum psyllid development occurs at approximately 27°C, whereas oviposition, hatching and survival are reduced at 32°C and cease at 35°C (List, 1939; Pletsch, 1947; Wallis, 1955; Abdullah, 2008; Yang and Liu, 2009; Yang et al., 2010a). Total development time was not affected by infection with ‘Ca. L. solanacearum’ (Nachappa et al., 2012), and may be affected by host plant (Yang and Liu, 2009). A single generation may be completed in 3 to 5 weeks, depending on temperature. The number of generations varies considerably among the geographic regions, usually ranging from three to seven. However, once psyllids colonize an area, prolonged oviposition causes the generations to overlap, making it difficult to distinguish between generations (Pletsch, 1947; Wallis, 1955; Munyaneza et al., 2009a). Both adults and nymphs are very cold tolerant, with nymphs surviving temporary exposure to temperatures of -15°C and 50% of adults surviving exposure to -10°C for over 24 h (Henne et al., 2010a; Whipple et al., 2012).

Physiology and Phenology

Longevity

Longevity of B. cockerelli is on average 16-18 days under field conditions (Yang et al., 2013). Longevity is affected by their ‘Ca. L. solanacearum’ status (Nachappa et al., 2012).

Associations

‘Candidatus Carsonella ruddii’, the obligate and primary endosymbiont of psyllids, has been confirmed in B. cockerelli (Nachappa et al., 2011; Hail et al., 2012). Besides ‘Ca. L. solanacearum’, several other secondary endosymbionts associated with the potato psyllid have recently been reported, including the bacteria Wolbachia, Acinetobacter, Methylibium, Rhizobium, Gordonia, Mycobacterium and Xanthomonas (Nachappa et al., 2011; Hail et al., 2012; Arp et al., 2014). Little information is available on the interactions and symbiont relationship between these microorganisms and the potato psyllid.

Environmental Requirements

Weather is an important element governing the biology of B. cockerelli and its damage potential; B. cockerelli seems to be adapted for warm, but not hot, temperatures. Cool weather, or at least the absence of elevated temperatures, has been associated with outbreaks of this insect (Pletsch, 1947; Wallis, 1955; Capinera, 2001; Cranshaw, 2001).

Bactericera cockerelli is attacked by a number of naturally occurring natural enemies in the different geographic areas, including chrysopid larvae, coccinellids, geocorids, anthocorids, mirids, nabids, syrphid larvae and the parasitoids Tamarixia triozae (Hymenoptera: Eulophidae) and Metaphycus psyllidis (Hymenoptera: Encyrtidae), but little is known about their effects on psyllid populations in the field (Pletsch, 1947; Wallis, 1955; Cranshaw, 1993; Al-Jabr, 1999; Butler et al., 2010; Walker et al., 2011a; Butler and Trumble, 2012; Liu et al., 2012; MacDonald et al., 2016). T. triozae was approved for release from containment in New Zealand and subsequently released in several regions (EPA, 2016; Barnes, 2017). It has established self-sustaining populations (HortiDaily, 2020). In addition, several entomopathogenic fungi, including Beauveria bassiana, Metarhizium anisopliae, Lecanicillium muscarium and Isaria fumosorosea [Cordyceps fumosorosea], have been determined to be effective natural enemies of B. cockerelli, causing psyllid mortality up to 99 and 88% under laboratory and field/greenhouse conditions, respectively (Lacey et al., 2009; 2011; Mauchline and Stannard, 2013).

General

• Research model

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Control

Management of B. cockerelli in the USA and New Zealand has been reviewed and discussed by Munyaneza (2012), Munyaneza and Henne (2012), Butler and Trumble (2012) and Vereijssen (2020).

Monitoring B. cockerelli is essential for its effective management. Early season management of this insect is crucial to minimize damage and psyllid reproduction in the field. The adult populations are commonly sampled using sweep nets or vacuum devices, but egg and nymphal sampling requires visual examination of foliage. The adults can also be sampled with yellow water-pan traps or yellow sticky traps. Typically, in the USA, psyllid populations are highest at field edges initially, but, if not controlled, the insects will eventually spread throughout the crop (Butler and Trumble, 2012; Workneh et al., 2012). In New Zealand, this edge effect is less pronounced, possibly because there is more vegetation, as opposed to barren earth, surrounding the crops (Vereijssen, J., unpublished data).

Bactericera cockerelli management is currently dominated by insecticide applications (Goolsby et al., 2007; Berry et al., 2009; Gharalari et al., 2009; Butler et al., 2011; Guenthner et al., 2012; Vereijssen et al., 2018; Vereijssen, 2020), but psyllids in general have been shown to develop insecticide resistance due to the high fecundity and short generation times (McMullen and Jong, 1971). Therefore, alternative strategies should be considered to limit the impact of the potato psyllid and its associated pathogen. Even with conventional insecticides, B. cockerelli tends to be difficult to manage. It has been determined that ‘Candidatus Liberibacter solanacearum’ is transmitted to potato very rapidly by the potato psyllid, and that a single psyllid per plant can successfully transmit this bacterium to potato in as little as 6 h, ultimately causing zebra chip (Buchman et al., 2011a, b). This represents a substantial challenge for growers in controlling the potato psyllid and preventing pathogen transmission. Just a few infective psyllids feeding on potato for a short period could result in substantial spread of the disease within a potato field or region (Henne et al., 2010b; Cameron et al., 2013). Most importantly, conventional insecticides may have limited direct disease control, as they may not kill the potato psyllid quick enough to prevent transmission of ‘Ca. L. solanacearum’, although they may be useful for reducing the overall population of psyllids.

The most valuable and effective strategy to manage zebra chip would likely be those that exclude the insect vector, such as mechanical barriers. Merfield et al. (2015a, b) trialled mesh covers to protect potato crops from B. cockerelli in New Zealand. Despite issues with aphids building up under the covers (Merfield 2017a, b; Merfield et al., 2019) and more research is needed, the mesh covers are used by organic and home gardeners.

Another tactic to reduce zebra chip is to discourage vector feeding, such as the use of plants that are resistant to psyllid feeding or less preferred by the psyllid. Unfortunately, no resistant or tolerant potato variety is commercially available yet, but research is promising (Rashidi et al., 2017; Rubio-Covarrubias et al., 2017; Anderson et al., 2018). However, some conventional and biorational pesticides, including plant and mineral oils and kaolin, have shown some substantial deterrence and repellency to potato psyllid feeding and oviposition in laboratory and field trials (Gharalari et al., 2009; Yang et al., 2010b; Butler et al., 2011; Peng et al., 2011; Walker et al., 2011; Barnes et al., 2013; 2014) and could be useful tools in integrated pest management programmes to manage zebra chip and B. cockerelli (Wright et al., 2017).

Several predators and two parasitoids of B. cockerelli are known, though there is little documentation of their effectiveness. In some areas such as southern Texas, early planted potato crops are more susceptible to psyllid injury than crops planted mid- to late season (Munyaneza et al., 2012). This is in contrast to New Zealand, where early planted potato crops in Pukekohe can be grown without insecticide use because of the biological control agents keeping the low numbers of B. cockerelli under control (Walker et al., 2012).

A review and information on synthetic insecticides used to control B. cockerelli is provided by Munyaneza (2012), Munyaneza and Henne (2012), Butler and Trumble (2012) and Vereijssen et al. (2018). Application of synthetic pesticides should be informed by proper monitoring (field inspections). Good insecticide coverage or translaminar activity is important because psyllids are commonly found on the underside of the leaves. Also, the different life stages require use of specific insecticides as it has been shown that chemicals controlling adults do not necessarily control nymphs or eggs. Because several generations often overlap, caution should be taken when selecting and applying insecticides targeted against the potato psyllid in relation to which life stages are present in the crop and timing of insecticide applications.

Reduced susceptibility to imidacloprid has been found in B. cockerelli populations in capsicum in California (Liu and Trumble, 2007) and in potato in Texas (Prager et al., 2013). Good insecticide resistance management with rotating modes of action is required in psyllid management programmes.

At least four haplotypes of B. cockerelli have so far been identified (Swisher et al., 2012; Swishet et al., 2014) and more may be discovered. Although these psyllid haplotypes have been shown to be different genetically, little is known of their differences in biological traits. This information is essential, especially for pest management purposes. In addition, information on overwintering of B. cockerelli, particularly in the regions with temperate climate (Jensen, 2012; Murphy et al., 2013), is lacking. Furthermore, accurate information on long distance movement and dispersal of B. cockerelli is crucial for predicting temporal and spatial colonization of field crops by this insect. Therefore, it is imperative that studies are conducted to further clarify the biology, ecology, movement and dispersal of B. cockerelli, in order to develop effective management strategies for this insect pest.

04/10/2014 Updated by:

Joseph E Munyaneza, USDA-ARS, USA

19/11/12 Original text by:

Joseph E Munyaneza, USDA-ARS, USA