Biocontrol introduction
Target pest: Sitona obsoletus (Coleoptera: Curculionidae) = Sitona lepidus, clover root weevil
Agent introduced: Microctonus aethiopoides Irish biotype (Hymenoptera: Braconidae)
Imported:
2000
Import source:
Ireland
Import notes:
Goldson et al. (2001) - in the European summer of 2000, approximately 8,500 Sitona lepidus [subsequently reclassified as S. obsoletus] were collected from 15 locations in 11 European countries, and parasitoids reared out and identified, initially in Montpellier, France, and later at North Wyke, Devon, England. All ecotypes of M. aethiopoides were found to develop readily in S. obsoletus and between September and November 2000 four shipments, totalling 1,599 parasitised weevils, were sent from North Wyke to New Zealand containment for culturing and analysis. These yielded 267 M. aethiopoides pupae, from which 204 adults were reared. By November 2000, six ‘ecotypes’ of M. aethiopoides had been established in containment at Lincoln, Canterbury. These were from (with the numbers in brackets indicating the number of parental pairs each population could be traced back to by May 2001) Aberystwyth (Wales) (2), Athenry (Ireland) (1), Heggenes (Norway) (3), Mikkeli (Finland) (1), Montpellier (France) (2) and North Wyke (England) (3). In addition, ‘hybrids’ were established from North Wyke/Brasov (Romania) (2), Mikkeli/Pordenone (Italy) (2), Mikkeli/Wigtown (Scotland) (1) and Montpellier/Nancy (France) (3).
[See Goldson et al. (2003) and Goldson et al. (2005) in the 'General comments' section relating to the selection of the Irish strain for release.]
McNeill et al. (2006) – the pathenogenetic Irish strain of M. aethiopoides (all other European strains collected [see Goldson et al. (2001) above] reproduced sexually) was selected as a potential candidate for introduction to New Zealand [for the rationale, see Goldson et al. (2003) and Goldson et al. (2005) in the 'General comments' section]. Between 12 July 2000 and 1 April 2004, five collection trips were made with a total of 11,257 S. obsoletus collected from nine locations throughout Ireland and Northern Ireland. Of these, 10,055 were imported into quarantine in New Zealand. Levels of parasitism were very low (with the highest from any one collection site being approximately 7%); a total of 79 pupae were recovered, from which 52 female M. aethiopoides emerged. Individual parasitoids have been maintained as separate lines and are still being reared in 2006. Quarantine-based parasitism of S. obsoletus by Irish M. aethiopoides over more than 20 parasitoid generations has averaged 25% (range 0-95%).
Gerard et al. (2011) - four lines of Irish M. aethiopoides were used in the releases, each descendant of parthenogenetic females collected in Northern Ireland.
Released:
2006
Release details:
Gerard et al. (2007), Gerard et al. (2011) - initial releases, consisting of parasitised weevils, were carried out at four North Island sites in 2006: 5,500 at Springdale, Waikato (5 January), 4,250 at Patoka, Hawke's Bay (26 January), 3,700 at Fielding, Manawatu (14 February) and 3,550 at Bulls, Manawatu (14 February).
Phillips et al. (2007) - between Aug 2006 and Mar 2007 the first South Island releases (a total of 4,276 parasitoid-exposed weevils) were made in the Rai Valley (Blenheim) and Richmond (Nelson).
Gerard et al. (2010) - in addition to the releases reported by Gerard et al. (2007) (see above), 22 medium-releases (1,000-2,500 parasitised weevils) between 2006 and 2010 and 2,073 mini-releases (10 parasitised weevils) to individual farmers between 2007 and 2010 were made throughout the North Island.
Phillips et al. (2010) - releases at Upper Takaka (Tasman) April 2009, Rotherham (North Canterbury) May 2009/January 2010 and Rakaia Island (Canterbury) May 2010.
Ferguson et al. (2012) - by 2012 the parasitoid had been released at 27 South Island locations.
Basse et al. (2015) - nearly a million M. aethiopoides were released 2013-2015 in Otago and Southland, the majority of these in Southland in the first half of 2015.
Hardwick et al. (2016) - between late summer 2014 and winter 2015 approximately 1.1 million parasitised weevils were released at approximately 6,000 sites in Southland, Otago and South Canterbury.
Establishment:
Gerard et al. (2007) - parasitism of S. obsoletus in June 2006 was recorded as Waikato 33%, Hawkes Bay 13%, Manawatu 13% at Fielding and 20% at Bulls.
Phillips et al. (2007) - by May 2007, two months post-release, 7-14% of clover root weevils at Richmond and Rai Valley were parasitised, indicating the parasitoid was likely to establish.
Gerard et al. (2010) - of the 15 pre-2009 mini-releases only two appear unsuccessful. 2009/2010 data from Hawkes Bay, Taranaki and Waikato showed the parasitoid can disperse naturally at over 15km/year.
Phillips et al. (2010) - in April 2010, 5% parasitism was recorded at Rotherham, indicating establishment.
Gerard et al. (2011) - Irish M. aethiopoides was detected at all four initial release sites (in Waikato, Hawke’s Bay and Manawatu) by the fourth month following release in 2006 and increases in parasitism was rapid, peaking between 15% and 31% in the first winter and between 69% and 88% in the following winter (2007). In Hawke’s Bay, parasitism was detected 1.7 km from the release site in winter 2007, 17 km in summer 2008, and 65 km to the south in 2009, suggesting a dispersal rate of 15-20 km per year.
Ferguson et al. (2012) - by the summer of 2011-12 the parasitoid was probably distributed throughout the North Island. In the South Island the parasitoid has been recovered from 111 sites.
Hardwick et al. (2016) - following the 2014-15 releases in Southland, Otago and South Canterbury, the parasitoid rapidly established at all 50 monitored release sites and dispersed from them. The biocontrol agent now occurs at all locations in New Zealand where clover root weevil is present.
Impacts on target:
Gerard et al. (2007) - by April 2007 60% of S. obsoletus in release paddocks in Waikato were parasitised, 70% in Hawkes Bay and 55% at Fielding.
Phillips et al. (2010) - 50% parasitism at Richmond, 75% at Rai Valley. The rapid establishment of the parasitoid in Marlborough and Nelson appears to be reducing clover root weevil damage.
Gerard et al. (2011) - within three years at the Hawke’s Bay 2006 release site, M. aethiopoides appears to be suppressing S. obsoletus populations and has dispersed naturally over 60 km.
Gerard et al. (2012) – parasitism of S. obsoletus by Irish M. aethiopoides at the four initial release sites [see the Gerard et al. (2007), Gerard et al. (2011) entry in ‘Release details’ section] increased from an overall 15% in the year of release in 2006 to 75% in 2010.
Ferguson et al. (2012) - in the South Island the rate of parasitism has varied over time and by site. Maximum recorded rates per site were: Lincoln, Canterbury 70%; Invermay Agricultural Centre, Taieri Plain, Otago ~70%; Taieri Plain Site #2 10%; Mataura, Southland 24%; Woodlaw, Southland 50%.
Basse et al. (2015) - since release M. aethiopoides has achieved parasitism rates exceeding 70%. The estimated economic benefits of biocontrol of clover root weevil in Southland in 2015 are $14.78/ha/year ($2.3 million in total) on dairy farms and $6.86/ha/year ($4.7 million in total) on sheep and beef farms. These are comparable to previous estimates of the benefit of biocontrol of clover root weevil over all of New Zealand, which have ranged from $5.93/ha/year ($80M/year) to $18.55/ha/year ($150.2M/year).
Hardwick et al. (2016) - observations following the 2014-2015 releases in Southland, Otago and South Canterbury suggest that winter parasitism of clover root weevil reaches its expected maximum of 75-95% about 18-24 months after release, which is consistent with previous results. Such parasitism levels cause adult weevil densities to decline.
Ferguson et al. (2018) - a cost-benefit analysis of S. obsoletus and its biocontrol undertaken in 2016 estimated the total benefit of M. aethiopoides Irish biotype to New Zealand would be $156.5 million p.a. from 2018 onwards.
Gerard et al. (2021) - population studies on the Irish strain of M. aethiopoides and S. obsoletus were carried out in the Waikato region of the North Island from 2011 to 2015. Very low parasitism and parasitoid larval densities from November to January indicates that the absence of S. obsoletus adults during spring (September to November) causes near extinction of M. aethiopoides populations each year. Fortunately, with overlapping summer and autumn S. obsoletus generations, M. aethiopoides has a constant supply of hosts when its generation time is shortest and by autumn the parasitoid reaches levels that give good control in second generation weevils. The ability to recover from extremely low levels each spring allows M. aethiopoides parasitism levels and larval populations to follow the host populations in a typical predator-prey relationship. The parasitoid population levels were able to increase rapidly in response to a minor outbreak of clover root weevil over summer 2011-12 in this study.
Gerard & Hiszczyńska-Sawicka (2022) - laboratory trials feeding M. aethiopoides adults with guttation fluid (xylem sap exuded from leaves through special structures known as hydathodes) from ryegrasses infected with either of three Epichloe festucae var. lolii endophyte strains (which produce alkaloids that protect the grass against grazing by mammals and insects) showed no detrimental effect of the guttation fluid on longevity. Instead, fluid from plants infected with the AR37 strain endophyte increased M. aethiopoides adult longevity and may contribute to its efficacy as a biocontrol agent in autumn in ryegrass-dominant pastures lacking other available food sources.
Inwood et al. (2023) - while the introduction of M. aethiopoides Irish strain has led to the suppression of S. obsoletus in New Zealand, this biocontrol is likely to fail in the future given the experience with Microctonus hyperodae. The latter was released in New Zealand as a biocontrol of Listronotus bonariensis (Argentine stem weevil); it was initially successful, but its effectiveness is now declining. The asexual reproduction of M. hyperodae is likely to have contributed to this decline [see the M. hyperodae introduction record]. Like M. hyperodae, M. aethiopoides Irish strain reproduces asexually. However, genome assemblies show that core meiosis genes are conserved in both species, suggesting the potential for sexual reproduction. These findings will be invaluable for future work investigating genomic factors that influence success or failure of Microctonus-based biocontrol in New Zealand, and have potential to be exploited in attempt to increase its effectiveness.
Impacts on non-targets:
Goldson et al. (2005) - host range testing for M. aethiopoides European biotype was carried out in quarantine in New Zealand with strains from Wales, Ireland and Romania [see ‘Import notes’ section]. However, the Irish strain, found to be parthenogenetic, was used predominantly in the testing. Potential non-target host weevils tested were five native species in tribes closely related to the tribe to which S. obsoletus belongs and four introduced species released in New Zealand as weed biocontrol agents. European M. aethiopoides was able to develop in the native weevils Irenimus aequalis, Nicaeana cervina, Catoptes cuspidatus, Protolobus porculus and Steriphus variabilis with parasitism rates of 13, 28, 2, 7 and 8%, respectively. These levels were significantly less than those in the corresponding S. obsoletus controls (69%). These results suggest that in the field I. aequalis and N. cervina could probably support successive generations of European M. aethiopoides while C. cuspidatus is very unlikely to. Protobolus porculus and S. variabilis may support some parasitoid development but this is unlikely to be at a level that would significantly affect the host population densities. Of the introduced weevils tested low levels of development were found in the nodding thistle biocontrol agent Rhinocyllus conicus (1%), and the gorse biocontrol agent Exapion ulicis (7%). In comparison, development levels of M. aethiopoides Morrocan biotype (released in New Zealand as a biocontrol of Sitona discoideus) in these two hosts in this study were 23% and 12% respectively. Rhinocyllus conicus, but not E. ulicis, is known to be attacked in the field in New Zealand by Moroccan M. aethiopoides. These results suggest neither of these biocontrol agents are likely to be field hosts for European M. aethiopoides. In conclusion, this study indicates that while European M. aethiopoides is capable of successfully parasitising non-target species, rates of parasitism were less than its Moroccan counterpart and it is likely to have fewer hosts [see Barratt et al. (1997) information in the Microctonus aethiopoides Moroccan biotype entry]; therefore, should the parthenogenetic biotype from Ireland be released in New Zealand its ecological impacts are likely to be less severe than those already imparted by the Moroccan M. aethiopoides.
Gerard et al. (2012) - Irish M. aethiopoides can use Listronotus bonariensis [the introduced pest Argentine stem weevil] as an alternative host, but to date only very low levels of Irish M. aethiopoides have been detected in field-collected L. bonariensis. DNA sequencing has shown that around 7% of parasitoid larvae in L. bonariensis collected in 2009 and 2010 from the four original 2006 Irish M. aethiopoides release sites [see the Gerard et al. (2007), Gerard et al. (2011) entry in ‘Release details’ section] were Irish M. aethiopoides, the rest being M. hyperodae [the parasitoid released against L. bonariensis].
Paynter et al. (2022) - a retrospective study compiled previously published laboratory host testing records for M. aethiopoides, Irish strain in New Zealand and field host records in New Zealand for those hosts parasitised in the laboratory. In addition, targeted field surveys (focusing on weevils that supported some parasitoid development during host specificity testing but had not previously been confirmed as field hosts) were carried out. Hosts for which rates of field parasitism of more than 10% have been recorded were classified as “major field hosts”. Rates below 10% (considered a conservative threshold) are unlikely to have significant population level impacts on the hosts. Laboratory parasitism has been recorded in six of nine species tested against M. aethiopoides, Irish strain. Of those six species, two non-target “major field hosts” - the natives Chalepistes aequalis (previously lrenimus aequalis) and Nicaeana cervina - and one other non-target field host - the introduced Listronotus bonariensis (the pest Argentine stem weevil) - are recorded.
General comments:
Goldson et al. (2003) - hybridisation trials between a European strain of M. aethiopoides (a parasitoid of S. obsoletus) and a Moroccan strain (widespread in New Zealand and an effective biocontrol of lucerne weevil, Sitona discoideus, but ineffective against S. obsoletus) showed that while these strains have notable host differences they are not reproductively isolated. Results showed a progressive decline in efficacy between the initial crossing of European females with Moroccan males and ensuing strain hybrids. Therefore, a strain introduced into New Zealand to control S. obsoletus could cross with the Moroccan strain, significantly reducing effectiveness of M. aethiopoides against both S. obsoletus and S. discoideus.
Goldson et al. (2005) - fortunately, the population imported from Ireland [see Goldson et al. (2001) in ‘Import notes’ section] has been found to be parthenogenetic, so this variant offers promise as a biocontrol agent for S. obsoletus [avoiding the possibility of hybridisation with the Moroccan biotype of M. aethiopoides released against Sitona obsoletus - see Goldson et al. (2003) above].
Gerard et al. (2006) – under New Zealand’s Hazardous Substances and New Organisms (HSNO) Act 1996 a number of criteria define a ‘new organism’, the most relevant being an “An organism belonging to a species that was not present in New Zealand immediately before 29 July 1998”. Importing and/or releasing a new organism requires HSNO Act approval following a risk assessment by the Environmental Protection Agency (EPA). With the Moroccan biotype of M. aethiopoides already established in New Zealand, there was no need to obtain a HSNO Act approval to release the Irish strain. However, concerns about possible hybridisation between biotypes and known differences in host range suggested that a cautious approach should be taken, and at AgResearch’s request, in December 2004 the Minister for the Environment prescribed M. aethiopoides to be a ‘risk species’. As a result all strains, with the exception of the Moroccan biotype, are considered to be ‘new organisms’ and as such require a HSNO Act approval. [See ‘EPA approvals’ section below.]
EPA Applications:
EPA (2005d) - 23 May 2005: application by AgResearch Ltd to release from containment an Irish strain of the insect Microctonus aethiopoides Loan (Hymenoptera: Braconidae) for biological control of the clover root weevil Sitona lepidus Gyllenhal (Coleoptera: Curculionidae) [subsequently reclassified as Sitona obsoletus], a major pest of clovers. EPA Application # NOR05001, approved with controls 8 Nov 2005.
References
Basse B, Phillips CB, Hardwick S and Kean JM (2015). Economic benefits of biological control of Sitona obsoletus (clover root weevil) in Southland pasture. New Zealand Plant Protection 68: 218-226
EPA (2005d). Application to EPA (NOR05001) to release from containment an Irish strain of the insect Microctonus aethiopoides Loan (Hymenoptera: Braconidae) for biological control of the clover root weevil Sitona lepidus Gyllenhal (Coleoptera: Curculionidae), a major pest of clovers. Environmental Protection Authority website https://www.epa.govt.nz/database-search/hsno-application-register/view/NOR05001
Ferguson CM, Barratt BIP, Bell N, Goldson SL, Hardwick S, Jackson M, Jackson TA, Phillips CB, Popay AJ, Rennie G, Sinclair S, Townsend R, Wilson M (2018). Quantifying the economic cost of invertebrate pests to New Zealand's pastoral industry. New Zealand Journal of Agricultural Research https://doi.org/10.1080/00288233.2018.1478860
Ferguson CM, McNeill MR, Phillips CB, Hardwick S, Barton DM and Kean JM. (2012). Status of clover root weevil and its biocontrol agent in the South Island after six years. Proceedings of the New Zealand Grassland Association 74: 171-176
Gerard P, Vasse M, Wilson D (2012). Abundance and parasitism of clover root weevil (Sitona Lepidus) and Argentine stem weevil (Listronotus bonariensis) in pastures. New Zealand Plant Protection 65: 180-185 https://journal.nzpps.org/index.php/nzpp/article/view/5391
Gerard P, Wilson D, Upsdell M (2021). Contrasting host: parasitoid synchrony drives differing levels of biocontrol by two introduced Microctonus spp. in northern New Zealand pastures. BioControl 66: 727-737 https://doi.org/10.1007/s10526-021-10104-8
Gerard PG, McNeill MR, Barratt BIP, Whiteman SA (2006). Rationale for release of the Irish strain of Microctonus aethiopoides for biocontrol of clover root weevil. New Zealand Plant Protection 59: 285–289 https://doi.org/10.30843/nzpp.2006.59.4471
Gerard PJ, Eden TM, Hardwick S, Mercer CM, Slay MWA and Wilson DJ. (2007). Initial establishment of the Irish Strain of Microctonus aethiopoides in New Zealand. New Zealand Plant Protection 60: 203-208.
Gerard PJ, Hiszczyńska-Sawicka E (2022). Impact of guttation fluid from perennial ryegrass infected with different strains of Epichloe festucae var. lolii endophyte on Microctonus aethiopoides adult longevity. New Zealand Plant Protection 75: 50-56 https://journal.nzpps.org/index.php/nzpp/article/view/11756/11611
Gerard PJ, Wilson DJ and Eden TM. (2010). Clover root weevil biocontrol distribution in the North Island - release tactics and outcomes. Proceedings of the New Zealand Grasslands Association 72: 85-89
Gerard PJ, Wilson DJ, Eden TM (2011). Field release, establishment and initial dispersal of Irish Microctonus aethiopoides in Sitona lepidus populations in northern New Zealand pastures. BioControl 56: 861-870
Goldson SL, McNeill MR, Proffitt JR (2003). Negative effects of strain hybridisation on the biocontrol agent Microctonus aethiopoides. New Zealand Plant Protection 56: 138-142 https://journal.nzpps.org/index.php/nzpp/article/view/6055/5883
Goldson SL, McNeill MR, Proffitt JR, Barratt BIP (2005). Host specificity testing and suitability of a European biotype of the braconid parasitoid Microctonus aethiopoides as a biological control agent against Sitona Lepidus (Coleoptera: Curculionidae) in New Zealand. Biocontrol Science and Technology 15(8): 791-813 https://doi.org/10.1080/09583150500136444
Goldson SL, Phillips CB, McNeill MR, Proffitt JR and Cane RP (2001). Importation to New Zealand Quarantine of a candidate biological control agent of clover root weevil. New Zealand Plant Protection 54: 147-151 https://journal.nzpps.org/index.php/nzpp/article/view/3756/3584
Hardwick S, Ferguson CM, McCauley P, Nichol W, Kyte R, Barton DM, McNeill MR, Philip BA and Phillips CB. (2016). Response to clover root weevil outbreaks in South Canterbury, Otago andSouthland; the agricultural sector and government working together. Journal of New Zealand Grasslands 78: 117-122
Inwood SN, Skelly J, Guhlin JG, Harrop TWR, Goldson SL, Dearden PK (2023). Chromosome-level genome assemblies of two parasitoid biocontrol wasps reveal the parthenogenesis mechanism and an associated novel virus. BMC Genomics 24, Article number: 440 https://doi.org/10.1186/s12864-023-09538-4
McNeill MR, Proffitt JR, Gerard PJ, Goldson SL (2006). Collections of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) from Ireland. New Zealand Plant Protection 59: 290-296 https://journal.nzpps.org/index.php/nzpp/article/view/4475/4303
Paynter Q, Barton DM, Ferguson CM, Barratt BIP (2022). Relative risk scores generated from laboratory specificity tests predict non-target impacts of Microctonus spp. parasitoids in the field. Biological Control, Volume 170, July 2022, 104927 https://doi.org/10.1016/j.biocontrol.2022.104927
Phillips CB, McNeill MR, Hardwick S, Ferguson CM and Kean JM (2010). South Island distributions of clover root weevil and its biocontrol agent. Proceedings of the New Zealand Grassland Association 72: 227-232
Phillips CB, McNeill MR, Hardwick S, Vink CJ, Kean, JK, Bewsell D, Ferguson CM, Winder LM, Iline II, Barron MC and Stuart B (2007). Clover root weevil in the South Island: detection, response and current distribution. New Zealand Plant Protection 60: 209-216
