Accidental introduction of Candidatus Liberibacter europaeus into New Zealand via a weed biocontrol agent from the UK

Authors: FOWLER, SIMON - Manaaki Whenua Landcare Research; LANGE, CLAUDIA - Manaaki Whenua Landcare Research; BEARD, SAM - Queensland University - Australia; CHEESEMAN, DAGMAR - Manaaki Whenua Landcare Research; HOULISTON, GARY - Manaaki Whenua Landcare Research; PAYNTER, QUENTIN - Manaaki Whenua Landcare Research; PETERSON, PAUL - Manaaki Whenua Landcare Research; PITMAN, ANDREW - Queensland University - Australia; SMITH, LINDSAY - Manaaki Whenua Landcare Research; TANNIERES, MELANIE - European Biological Control Laboratory (EBCL); THOMPSON, SARAH - Queensland University - Australia; WINKS, CHRIS - Manaaki Whenua Landcare Research

Submitted to: Biological Control
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/24/2021
Publication Date: 6/26/2021
Citation: Fowler, S.V., Lange, C., Beard, S., Cheeseman, D.F., Houliston, G.J., Paynter, Q., Peterson, P., Pitman, A., Smith, L., Tannieres, M., Thompson, S., Winks, C. 2021. Accidental introduction of Candidatus Liberibacter europaeus into New Zealand via a weed biocontrol agent from the UK. Biological Control. 160(2021) 104697. https://doi.org/10.1016/j.biocontrol.2021.104697.
DOI: https://doi.org/10.1016/j.biocontrol.2021.104697

Interpretive Summary: A biological control programme targeting Scotch broom, a European woody shrub that is a serious invasive weed in New Zealand (NZ), began in 1981. As part of this biocontrol programme, a sap-sucking insect, the broom psyllid (Arytainilla spartiophila), was imported from the UK and released as a biocontrol agent in NZ in 1993. In 2011, a bacterium, Candidatus Liberibacter europaeus (Leu), was detected in Scotch broom plants and broom psyllids at a site in mid-Canterbury, South Island, NZ. Therefore, the aim of this study was to investigate the pathway by which Leu arrived in NZ. To this end, two hypotheses were tested : 1) Leu was imported and released with the broom psyllids from the UK, or 2) Leu was present prior to the introduction of the broom psyllids in NZ. Using molecular tools, Leu was detected in Scotch broom and psyllids from the UK but not in ornamental brooms and other putative host plants in NZ. The NZ surveys also show that Leu absence coincides with broom psyllids absence. In addition, the partial DNA sequences of Leu in Scotch broom and broom psyllids from the UK and NZ are identical. All the results strongly support the hypothesis of the accidental introduction of Leu into NZ via the release of the biocontrol agent. It remains uncertain whether Leu is symptomless in Scotch broom, or pathogenic like several Candidatus Liberibacter spp. that cause destructive plant diseases including citrus greening and potato Zebra chip, and usually vectored by psyllids. Nevertheless, if insect groups known to have the potential to vector plant diseases are to be used in the future as weed biocontrol agents, then either the released insects will have to be confirmed to be free of potential plant pathogens such Ca. Liberibacter spp., or the risks represented by the associated organisms will have to be included in release applications.

Technical Abstract: The bacterium, Candidatus Liberibacter europaeus (Leu) was reported in New Zealand (NZ) in 2011 in Scotch broom, Cytisus scoparius Link, and its biocontrol agent, Arytainilla spartiophila Förster (Hemiptera: Psyllidae). The aim of the study was to investigate the pathway by which Leu arrived in NZ using a retrospective risk assessment of Leu being accidentally imported with the broom psyllids in the 1990s. We developed species-specific primers for Leu detection and carried out end-point and real-time PCR analyses for Leu in potential host plants and broom psyllids throughout NZ to test two hypotheses: 1) Leu was accidentally released in NZ in broom psyllids in 1993; or 2) Leu was present in NZ pre-1993, and maintained in cultivated plants via cuttings/grafting, or in wild Scotch broom populations via shared parasitic plants. There was strong evidence to support the arrival of Leu with broom psyllids in NZ. Firstly, methods used to import broom psyllids from the UK provided a likely pathway for inadvertent release of Leu, which at the time was unknown to science, into NZ. Secondly, Leu in NZ Scotch broom plants was significantly associated with the presence of broom psyllids, with Leu absent from plants at sites without psyllids. In contrast, there was no evidence suggesting Leu was present in NZ before the release of broom psyllids: Leu was not found in ornamental brooms or pears, Pyrus communis L. (a Leu host in Europe), and parasitic plants were too uncommon to maintain Leu in wild Scotch broom. In addition, Leu in UK Scotch broom and broom psyllids has a matching partial 16S sequence to NZ Leu. It remains uncertain whether Leu is pathogenic in Scotch broom, or symptomless as in pears. Unpredictable impacts of Ca. Liberibacter spp. in different plant species probably implies that psyllids considered as future weed biocontrol agents will need to be free of these potential plant pathogens. This accidental introduction of Candidatus Liberibacter europaeus into NZ via a weed biocontrol agent happened because detection methods for unculturable organisms were not developed at the time. Molecular characterisation of insect microbiomes could become an essential procedure for pre-release safety screening of biocontrol agents that are potential vectors of plant pathogens.