Target pest: Listronotus bonariensis (Coleoptera: Curculionidae), Argentine stem weevil
Agent introduced: Microctonus hyperodae (Hymenoptera: Braconidae)
1989 and 1990
Goldson et al. (1990), Goldson et al. (1993) - parasitoids were sourced from seven different ecotypes (geographic populations): Ascasubi, Bariloche, General Roca, Mendoza (Argentina), Porto Alegre (Brazil), Colonia, La Serena (Uruguay) and Concepcion (Chile).
Goldson et al. (1990) - adult L. bonariensis were collected from M. hyperodae-parasitised populations in South America (see âImport sourceâ section for location details) between September 1989 and January 1990 and shipped to New Zealand. Specimens were collected from a wide range of habitats within latitudes similar to New Zealand in order to provide as much biotypical material as possible. Habitats varied from subtropical humid to arid subalpine to dryland. A total of 13,447 weevils were imported, which produced 513 M. hyperodae pupae which led to the establishment of 247 pathenogenetic lines (i.e. from 247 individual females). In addition, four apparently impotent males were reared from the imported weevils. Although M. hyperodae has been recorded as being parthenogenetic, such very rare occurrence of males is consistent with species that show obligate thelytoky [the production of females from unfertilised eggs].
Goldson et al. (1993) - initial releases were at 8 sites in three regions of New Zealand: northern/central North Island (Wellsford, Hamilton, Reporoa); Canterbury in central South Island (Lincoln, Hororata); Otago in southern South Island (Sutton, Ophir, Gore). A total of 98,940 parasitised weevils were released (38,880 at North Island sites, 38,920 in Canterbury, 21,140 in Otago) between 1 April and 31 October 1991. Approximately the same number of each ecotype [see 'Import source' section] was released.
McNeill et al. (2002) - excluding the initial releases of 1991, a total of ~660,000 parasitoids were released, of which 613,000 were for commercial contracts. Releases by region (date; number of release sites; total number released): Northland (1997; 2; 11,300), Waikato (1994; 6; 32,700), Bay of Plenty (1996-97; 24; 136,000), East Coast (1993; 3; 13,000), East Coast (1996; 1; 5,000), Hawke's Bay (1995; 2; 9,800), Taranaki (1996-97; 40; 215,000), Manawatu (1994-95; 6; 35,700), Wairarapa (1998; 12; 23,700), Marlborough (1991; 1; 800), Canterbury (1995-96; 23; 172,000), Otago (1992; 1; 6,700). Including the initial releases of 1991, a total of 759,000 M. hyperodae were released. An effort was made to ensure that equal numbers of each ecotype [see 'Import source' section] were included in each release.
Goldson et al. (1993) - the parasitoid was recovered from all three release regions. In the North Island, establishment and build up was very rapid with the first recovery 23 September 1991. First recovery in Canterbury was 8 January 1992, and in Otago 1 October 1992. Relative sparseness of establishment in Otago may have been related to the lower numbers released and cooler conditions.
McNeill et al. (1993) - indications are that M. hyperodae has established in Canterbury and Northland.
Phillips et al. (1994), Goldson et al. (1997) - morphometric analysis of M. hyperodae collected at release sites in Canterbury, Waikato and Auckland (where equal numbers of each ecotype [see âImport sourceâ section] were released) indicate that only two years after the parasitoidâs release âeast of the Andesâ ecotypes (Argentina, Brazil, Uruguay) had established more successfully than âwest of the Andesâ ecotypes (Chile). Laboratory trials have also showed that the Uruguayan ecotype has a 50% higher fecundity than the other ecotypes tested. It has been shown that the New Zealand population of L. bonariensis probably originated in the Uruguayan River Plate area, suggesting that co-evolution may be more critical than climate matching with respect to the success of the various ecotypes released.
Ferguson et al. (1997) - the establishment and dispersal rates of M. hyperodae in the southern South Island (Otago and Southland) are less than those from the Canterbury region north. The parasitoid was released at four sites in Otago and Southland in 1991 and 1992; it has not been recovered from two sites and first recovered after approximately 18 months at the other two sites, at which, by 1996, it had established at levels of up to 15% and spread up to 1 km. In contrast, from Canterbury north, establishment generally occurred with six months of release, with, by 1994, parasitism rates at most sites of 48-84%. In the Waikato, North Island, region, M. hyperodae had dispersed up to 19 km from release sites by 1995, and in Canterbury up to 15 km by 1996. Lower rates of parasitism and slower dispersal in the southern South Island are probably due to lower L. bonariensis population densities, fewer weevil and parasitoid generations per year, and possibly because of ecotypic or genetic differences between the parasitoids and hosts in the southern South Island compared with elsewhere in New Zealand.
Goldson et al. (1999) â the mean rate of dispersal of M. hyperodae in Canterbury from 1993 to 1995 was 1.9 km per year. This low rate of dispersal is thought to be related to the inhibitory effects of the parasitoid on L. bonariensis flight. Despite this modest dispersal rate, by the winter of 1996, five years after its release, M. hyperodae had spread over an area of 140 square kilometres.
McNeill et al. (2002) - all post-1991 releases established with the exception of one in Wairarapa, one at Mosgiel (Otago) and three in Canterbury. In Canterbury, the parasitoid was re-released on the same or adjacent sites and subsequently established at the three sites. Based on the distribution of releases in New Zealand and the results of surveys it is estimated that M. hyperodae is now very widely distributed in the North Island, with more limited distribution in the South Island.
Impacts on target:
Goldson et al. (1994) - in most places, especially in the north, the parasitoid has established and built up high levels of parasitism (up to 80% by 1994) at release sites with unexpected rapidity (just three years post-release). Preliminary results from both Canterbury and the northern North Island indicate that M. hyperodae parasitism in the 1993-94 season has significantly reduced the damaging larval populations of L. bonariensis in its release areas. There seems little doubt that in many regions in New Zealand the parasitoid will become a major component of Integrated Pest Management systems using resistant grasses.
Goldson et al. (1998) - within four years of release of M. hyperodae, peak parasitism levels of L. bonariensis of >90% were being recorded. A study of L. bonariensis in Canterbury, 1990-1995, showed a growing impact by M. hyperodae from the 1993-94 season onward, with a reduction in the size of the L. bonariensis first summer generation egg and larval peaks coinciding with a build-up of M. hyperodae.
Barker & Addison (2006) - a study in northern New Zealand pastures, 1991-1996, showed 75-90% of overwintering L. bonariensis parasitised by M. hyperodae within three years of the parasitoid establishing at a site. However, asynchrony between emergence of parasitoids and the next generation of adult weevils greatly reduced the influence of M. hyperodae and L. bonariensis populations continued to exhibit marked intergenerational variability in abundance. The asynchrony between parasitoid post-diapause emergence in spring and emergence of L. bonariensis in early summer, along with avoidance behavioral adaptations by adult L. bonariensis to presence of the parasitoid led to short eruptive phases of weevil oviposition during periods when M. hyperodae were less abundant, which may significantly lessen the impact of the parasitoid. Nevertheless, there is evidence for some suppression of weevil abundance in the presence of the parasitoid and it is concluded that M. hyperodae is a useful adjunct to endophyte-conferred host plant resistance in reducing the economic status of L. bonariensis populations in northern New Zealand pastures.
Popay et al. (2011) - given previous evidence that M. hyperodae has reduced the pest status of L. bonariensis, perhaps to occasional outbreaks, it has been unexpected to find evidence from pastures in Waikato and Taranaki over the last 4 years showing that the weevil still causes significant damage at least on occasions. Factors that may be lessening the impact of the parasitoid include asynchronous generations of the parasitoid and its host, host behavioural adaptations, compensatory oviposition and inhibition of flight in parasitised individuals leading to low levels of parasitism in new pastures.
Gerard et al. (2012) - parasitism of L. bonariensis by M. hyperodae between 2006 and 2009 was assessed at the four initial 2006 release sites of Microctonus aethiopoides Irish strain [released against the clover root weevil, Sitona obsoletus] in Waikato, Hawkeâs Bay and Manawatu in the North Island. Parasitism rates were variable and low compared to the rates of parasitism of S. obsoletus by Irish M. aethiopoides. The lowest rates were in 2009 with overall regional means ranging from 5% in Manawatu to 11% in Waikato. With peak end of season M. hyperodae parasitism levels below 50% in the Waikato and Manawatu regions, parasitism levels would have been even lower in summer, and this probably contributed to the major damage levels reported in the North Island during 2006-2011 [see Popay et al. (2011) entry above]. Possible explanations for the low level of M. hyperodae parasitism of L. bonariensis are impacts of the 2008 drought, a response to the presence of Irish M. aethiopoides or simply typical parasitism levels for M. hyperodae in the region.
Goldson, Wratten et al. (2014) - preliminary evidence shows that parasitism of Argentine stem weevil by M. hyperodae has dropped by as much as 50% over the last 10-15 years.
Goldson, Tomasetto & Popay (2014), Goldson et al. (2015) - the reduction in rate of parasitism [see previous entries in this section] is potentially due to host resistance as a result of the parthenogenetic parasitoid not being able to co-evolve, and exacerbated by lack of heterogeneity in NZ pastoral ecosystems and lack of other control agents.
Goldson et al. (2015) - endophytes in host plants are shown not to be the reason for the decline of the biological control of L. bonariensis. Higher autumnal rates of parasitism in tetraploid Lolium multiflorum and tetraploid L. perenne than diploid L. perenne cultivars (the common ryegrass of NZ pastures) may be starting to provide some clues to the mechanisms behind the parastism decline. The absence of observed signs of physiological resistance to the parasitoids (encapsulation of early parasitoid stages) raises the possibility a behavioural shift may have occurred in the weevil to enhance parasitoid evasion, potentially aided by architectural differences between the diploid and tetraploid plants.
Goldson & Tomasetto (2016) - a laboratory study of parasitism rates on tetraploid Italian Lolium multiflorum, diploid L. perenne and diploid hybrid L. perenne x L. multiflorum showed parasitism rates of 75%, 46% and 52% respectively. Similar experiments in the 1990s using the same host plant species gave high parasitism rates, similar to the rate on Italian L. perenne in this study, on all species. The 42% decline in parasitism in the laboratory in the diploid grasses conforms to findings of a similar c. 50% decline in parasitism rates in the field in diploid grasses since the 1990s. In this study there was no difference in parasitism rates with different plant orientation, suggesting the previous contention that the higher levels of parasitism in the tetraploid L. multiflorum could have resulted from a difference in the architecture of the tetraploid versus diploid plants is incorrect. This study supports the contention that if selection pressure has led to an enhancement of some kind of parasitoid-avoiding behaviors amongst L. bonariensis, then such evolution would most likely to have occurred in the country's extensive diploid pastures rather than in the rare tetraploid Italian L. multiflorum pastures.
Pennisi (2017) - at first M. hyperodae was highly effective in New Zealand, killing up to 90% of L. bonariensis. However its effectiveness started to decline after about 7 years, and by 2011 only 5% of weevils were being parasitised in some places. Decline in performance was independent of climate, altitude, farming practices or types of grazer, indicating a change in the weevil itself. Two factors may have favoured the weevil: 1) as an archipelago New Zealand has less biodiversity than continents, and thus fewer generalist natural enemies that could attack the weevil, leaving it freer to evolve countermeasures that might otherwise make it more vulnerable to those enemies, and 2) as the wasp is asexual, it evolves more slowly than the weevil.
Tomasetto, Olaniyan & Goldson (2017) - laboratory studies show significantly lower rates of parasitism in diploid than tetraploid Lolium multiflorum, clear evidence of a ploidy effect on parasitism. Tetraploid L. multiflorum has fewer, more robust and larger tillers than the diploid Lolium spp. so higher parasitism rates may be related to the lack of hiding places for an evasive genetically-driven behaviourally-based resistance by L. bonariensis.
Goldson et al. (2017) - the most significant factor in the loss of efficacy of M. hyperodae against L. bonariensis is likely to be the sexual reproduction of the weevil versus the pathenogenetic reproduction of the parasitoid. In addition, New Zealand's pastoral ecosystems may have contributed to the acquisition of resistance by the weevil, specifically the lack of complexity and thus numbers of parasitoid species, allowing strong selection by M. hyperodae on L. bonariensis in the absence of other interfering or competing species. This effect has probably been heightened by the lack of spatial or temporal refugia for the weevil host.
Tomasetto, Tylianakis et al. (2017) - 21 years of field data from 196 sites across New Zealand show that M. hyperodae was initially nationally successful (up to 90% parasitism) but that parasitism rates then declined by 44% (leading to pasture damage of c. $160 million per annum). At all locations, regardless of abiotic factors and numbers released, the decline began 7 years (14 host generations) after parasitoid release and reached a plateau at present-day rates after 12 years. Field trials, supporting previous laboratory trials, showed parasitism was lower in plots of Lolium perenne than plots of L. multiflorum, indicating that resistance to parasitism is host plant dependent. Results suggest that low plant and enemy biodiversity in intensive large-scale agriculture may have facilitated the evolution of host resistance by L. bonariensis.
Tomasetto, Cianciullo et al. (2018) - 25 years of field-sampling data from three distinct ecoregions shows a one year time-lag in decline of parasitism rates between Waikato and Canterbury, indicating resistance evolved a year earlier in Waikato due to the accelerated life-history in that region. Thus adaptation leading to resistance might have similarly occurred in different parts of the country indicating that the genetic variation needed for the acquisition of resistance was equally present everywhere.
Tomasetto, Casanovas et al. (2018) - data from 1993 and 2018 were analysed to determine if the functional response (the consumer behaviour response to prey density) of M. hyperodae to L. bonarensis in two of the most common New Zealand pasture grasses (Lolium multiflorum and L. perenne) reflects observed differences in field parasitism and whether this functional response has changed over time. A Type I functional response was found in L. multiflorum in both years, but the slope of the relationship declined over time, suggesting a decline in searching efficiency in L. multiflorum since 1993. There was no evidence for any type of functional response in L. perenne; this coincides with lower parasitism rates found on this host plant than in L. multiflorum, both in the field and laboratory. These results support the hypothesis that parasitism decline could be the result of evolution of resistance based on enhanced evasive behaviour by L. bonariensis.
Shields (2019), Shields, Wratten, Phillips et al. (2022), Shields, Wratten, van Koten et al. (2022) - laboratory trials showed that L. bonariensis parasitoid-avoidance behaviour in the form of reduced feeding and on-plant presence differed depending on the host plant. Weevils on a diploid hybrid (diploid Lolium perenne x diploid L. multiflorum) had the most consistent reduced feeding and plant abandonment responses to M. hyperodae, those on diploid L. perenne had similar responses but these were delayed, while those on tetraploid L. multiflorum showed a reduced feeding response but no plant abandonment. These results reflect recent L. bonariensis field parasitism rates that are low on diploid host plants (including diploid L. multiflorum) compared to those in the 1990s, but which have not declined in tetraploid L. multiflorum, and may explain the behavioural mechanisms behind the decline. As well as lack of evolved behaviour on tetraploid L. multiflorum, a possible explanation for the weevilâs observed behaviour of remaining on the plant and continuing to feed in the presence of M. hyperodae is that tetraploidy enhances characteristics favourable to the weevil, such as higher nitrogen content. Behavioural responses to M. hyperodae in these trials also differed between L. bonariensis regional populations, reflecting current parasitism rates and history. Those from the Waikato region, where the greatest parasitism decline has occurred (from approximately 70% 1994-2000 to approximately 14% 2011-2014 at Ruakura), had the strongest behavioural responses. Those from Canterbury and Auckland where there has been a medium decline in parasitism (e.g. approximately 62% 1994-2000 to 32% 2011-2019 at Lincoln, Canterbury) showed delayed feeding reduction and plant abandonment responses, while those from Otago where parasitism rates have always been low (approximately 8% with no significant difference between the 1994-2000 and 2011-2019 periods at Mosgiel) exhibited a minimal behavioural response. The extent of parasitism decline at a given location was directly related to the accumulated degree-days above the parasitoidâs development temperature threshold, in turn, taken to be indicative of parasitoid activity and selection pressure. Weevils from the warmer northern region showed higher rates of parasitoid avoidance than those from the cooler south. The findings in this work strongly suggest that L. bonariensis behavioural responses are the mechanism behind the proposed evolution of resistance [see entries above in this section] causing the parasitism decline.
Harrop et al. (2020) - empirical modelling of the L. bonariensis-M. hyperodae interaction has indicated that resistance is inevitable when hosts have more genetic variation than their predators. Genome-wide DNA sequencing of L. bonariensis collected from 10 sites across New Zealand showed high heterozygosity and a high proportion of unstructured variation across populations (in contrast to earlier reports of low genetic diversity, based on traditional molecular markers), consistent with large effective population size and gene flow between populations. This implies that L. bonariensis has been able to evolve more rapidly than M. hyperodae, which reproduces asexually.
Gerard et al. (2021) - overwintering M. hyperodae parasitism rates exceeded 75% within three years of release but have tracked downwards since then and notable weevil damage has been evident in susceptible pastures, with developing host resistance hypothesised as a cause [see earlier entries in this section]. Population studies on M. hyperodae and L. bonariensis carried out in the Waikato region of the North Island 2011-2015 and compared to data collected in Waikato 1991-1996 soon after the parasitoidâs release suggest other contributing factors. This study shows that, although M. hyperodae has been a successful biocontrol of L. bonariensis, its efficacy in the Waikato region is hampered severely by asynchrony with its host. The large differences between 1990s and current levels of parasitism by M. hyperodae in overwintering Waikato L. bonariensis populations are most likely due to the combination of high levels of endophyte-conferred pest-resistant grass in the pastures suppressing the second weevil generation (late-summer/early-autumn) at the time of peak parasitoid activity and the occurrence of a third generation of adult weevils (peaking in mid-winter) after most parasitoid adult activity has ceased, the former factor enhanced by, and the latter caused by, a warming climate and hot dry summers. This does not preclude the possibility that there has been a genetic shift in L. bonariensis to avoid parasitism (the resistance hypothesis). The study has shown that M. hyperodae has remarkable persistence: it prevails despite very low host populations and inhospitable Waikato pastures to recover to close to 1990sâ parasitism levels each spring.
Goldson et al. (2022) - sampling of L. bonariensis and M. hyperodae in the Canterbury region of the South Island between 11 January 2017 and 4 April 2018 showed that the G-vac (suction) field collection technique leads on average to a 26% over-estimation of M. hyperodae parasitism rates compared to those found using turf flotation. This result has implications for the interpretation of long-term studies, with the G-vac method typically used post-2000 and turf flotation pre-2000. After approximately 50 weevil generations since M. hyperodae was first released in 1992, recent sampling has shown an approximate reduction in parasitism of 57% and 30% at Ruakura (Waikato, North Island) and Lincoln (Canterbury, South Island), respectively. Therefore, correcting for the 26% over-estimation of parasitism rates, indications are that the actual declines in parasitism have been approximately 60% at Ruakura and 36% at Lincoln, respectively, further highlighting the loss of parasitoid efficacy since the early-1990s.
Inwood, Harrop et al. (2023) - modelling has shown that the failing control of L. bonariensis by M. hyperodae is contributed to by the parthenogenetic nature of M. hyperodae reproduction [see entries above in this section]. RNA sequencing suggests M. hyperodae parthenogenesis involves meiosis and that the potential for sexual reproduction may have been retained. Upregulation of genes involved in endoreduplication provides a potential mechanism for the restoration of diploidy in eggs after meiosis. Alternatively, if sexually reproducing M. hyperodae could be identified in their home range (and the production of four impotent males during the importation and rearing of this parasitoid [see Goldson et al. (1990) entry in âImport notesâ section] indicates this species has the potential to reproduce sexually in its home range), their introduction to New Zealand would be more beneficial than an additional release of asexual M. hyperodae as it would increase genetic diversity while also allowing the biocontrol agent to evolve alongside its host.
Inwood, Skelly et al. (2023) - a genome assembly for M. hyperodae shows that core meiosis genes are conserved, consistent with previous work suggesting the potential for sexual reproduction in this species [see Inwood, Harrop et al. (2023) entry above]. A novel virus, provisionally named Microctonus hyperodae flamentous virus (MhFV), is also identified, and may contribute to premature mortality of L. bonariensis. These findings are invaluable for ongoing investigation of the M. hyperodae biocontrol decline and have potential to be exploited in attempt to increase the effectiveness of M. hyperodae biocontrol.
Impacts on non-targets:
Goldson et al. (1992) - host range testing was carried out in quarantine in New Zealand on 24 non-target weevil species, all but three being New Zealand natives. (Native species of a similar size to L. bonariensis and in the same subfamily, (Brachycerinae) were primarily targeted.) Results showed that four native species - Irenimus aequalis, Irenimus sp. 3, Catoptes robustus and Nicaeana cinerea - were able to sustain development of M. hyperodae. However, these weevil species produced, on average, only 19% of the parasitoids derived from L. bonariensis controls, and, with the exception of L. aequalis, the affected species caused considerable levels of M. hyperodae encapsulation/emaciation and substantial reductions in the development rates of any surviving larvae. It is concluded that only L. aequalis is likely to be able to maintain significant M. hyperodae development; in addition, in the field alpine refugia probably exist for the other three species attacked. From a conservation perspective, I. aequalis is unlikely to be threatened by M. hyperodae as it has invaded agricultural systems to the degree it is considered a minor pest.
Barrett et al. (1997) - laboratory host range tests were carried out to investigate potential non-target hosts of M. hyperodae and surveys conducted to investigate non-target parasitism by this parasitoid in the field. In the laboratory, M. hyperodae was exposed to 11 potential non-target host species, including seven native species. The parasitoid oviposited in five of the native species (Nicaeana cervina, Irenimus aemulator, I. aequalis, I. egens and I.stolidus) and completed development in all of these except N. cervina. However, prepupal emergence from the native species was only 14% of that from the target species L. bonariensis. In the field, M. hyperodae was recovered from two non-target species: the native I. aequalis and a recent accidental introduction, Sitona lepidus [now S. obsoletus - the pest clover root weevil]. Both records were from Waikato, and in both instances, only a single parasitised host has been detected to date. Irenimus aequalis was predicted as a potential field host in pre-release host range testing (Goldson et al. 1992 - see above); the conclusion from that testing that M. hyperodae was likely to have a narrow host range in the field is supported by this study.
Ferguson et al. (1997) - a study between January 1993 and January 1997 at two release sites in Otago at which M. hyperdoae established showed no parasitism of the 10 species of non-target weevils collected, despite these being common, supporting the contention that this parasitoid has a narrow host range and indicating that it has not switched to non-target weevils to bridge periods of target host scarcity.
Barratt et al. (2000) - pasture surveys at three sites in Otago, three in Canterbury and one in Waikato between September 1993 and October 1998 found M. hyperodae parastising native weevils at only two sites: a single individual of I. aequalis at the Hamilton (Waikato) site [as reported by Barratt et al. (1997) - see above] and a very low incidence of parasitism of Steriphus variabilis at the Springston (Canterbury) site.
Barratt (2004) - in laboratory host range testing in addition to that reported by Barratt et al. (1997) [see above], M. hyperodae was found to parasitise the native weevil Catoptes robustus. No field non-target hosts are reported in addition to a single parasitised individual of Ireniumus aequalis and Sitona obsoletus and a small number of Steriphus variablis [see above entries].
Paynter et al. (2022) - a retrospective study compiled previously published laboratory host testing records for M. hyperodae 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 could be considered âmajor field hostsâ. Rates below 10% (considered a conservative threshold) are unlikely to have significant population level impacts on the hosts. Laboratory parasitism has been recorded in 10 of 15 species tested against M. hyperodae. Of those 10 species none have been recorded as âmajor field hosts and four have been recorded with field parasitism at rates of <10% - the natives Chalepistes aequalis (previously lrenimus aequalis), C. egens (I. egens) and C. stolidus (I. stolidus) and the introduced Sitona obsoletus (the pest clover root weevil).
Barker GM, Addison PJ. (2006). Early impact of endoparasitoid Microctonus hyperodae (Hymenoptera: Braconidae) after its establishment in Listronotus bonariensis (Coleoptera: Curculionidae) populations of northern New Zealand pastures. Journal of Economic Entomology 99 (2): 273-287
Barratt BIP (2004). Microctonus parasitoids and New Zealand weevils: Comparing laboratory estimates of host ranges to realized host ranges. Assessing Host Ranges of Parasitoids and Predators used for Biological Control; A guide to Best Practice. Van Driesche, R.G. and Reardon, R. (Ed.s) Forest Health Technology Enterprise Team - Morgantown, West Virginia. September 2004. 243p.
Barratt BIP, Evans AA, Ferguson CM, Barker G, McNeill MR, Phillips CB (1997). Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and M. hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Environmental Entomology 26: 694-702 https://doi.org/10.1093/ee/26.3.694
Barratt BIP, Evans AA, Ferguson CM, McNeill MR, Addison P (2000). Phenology of native weevils (Coleoptera: Curculionidae) in New Zealand pastures and parasitism by the introduced braconid, Microctonus aethiopoides Loan (Hymenoptera: Braconidae). NZ Journal of Zoology 27: 93â110 https://www.tandfonline.com/doi/pdf/10.1080/03014223.2000.9518215
Cameron PJ, Hill RL, Bain J, Thomas WP (1989). A Review of Biological Control of Invertebrate Pests and Weeds in New Zealand 1874-1987. Technical Communication No 10. CAB International Institute of Biological Control. DSIR Entomology Division. 424p.
Ferguson CM, Evans AA, Barratt BIP, Phillips CB (1997). Establishment and dispersal of Microctonus hyperodae Loan (Hymenoptera: Braconidae) in Otago and Southland. Proceedings of the New Zealand Plant Protection Conference 50: 41-46 https://journal.nzpps.org/index.php/pnzppc/article/view/11274/11124
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
Goldson SL, Barker GM, Barratt BIP, Barlow ND (1994). Progress in the biological control of Argentine stem weevil and comment on its potential. Proceedings of the New Zealand Grassland Association 46: 39-42 https://www.nzgajournal.org.nz/index.php/ProNZGA/article/view/2131/1759
Goldson SL, McNeill MR, Banaa M, Olaniyan O, Popay AJ, Barratt BIP, van Koten C (2022). Implications of sampling bias and population behaviour in the study of parasitoid-based biocontrol of Listronotus bonariensis in New Zealandâs exotic pasture ecosystems. New Zealand Journal of Agricultural Research 66(4): 374-388 (2023). Published online 13 Jun 2022.
Goldson SL, McNeill MR, Phillips CB, Proffitt JR (1992). Host specificity testing and suitability of the parasitoid Microctonus hyperodae (Hym.: Braconidae, Euphorinae) as a biological control agent of Listronotus bonariensis (Col.: Curculionidae) in New Zealand. Entomophaga 37(3): 483â498 https://doi.org/10.1007/BF02373121
Goldson SL, McNeill MR, Proffitt JR, Barker GM, Addison PJ, Barratt BIP, Ferguson CM (1993). Systematic mass rearing and release of Microctonus hyperodae (Hym.: Braconidae, Euphorinae), a parasitoid of the Argentine stem weevil Listronotus bonariensis (Col.: Curculionidae), and records of its establishment in New Zealand. Entomophaga 38(4): 527-536
Goldson SL, McNeill MR, Stufkens MW, Proffitt JR, Pottinger PR, Farrell JA (1990). Importation and quarantine of Microctonus hyperodae, a South American parasitoid of Argentine stem weevil. Proceedings of the New Zealand Weed and Pest Control Conference 43: 334-338 https://journal.nzpps.org/index.php/pnzwpcc/article/view/10904/10736
Goldson SL, Phillips CB, McNeill MR, Barlow ND (1997). The potential of parasitoid strains in biological control: observations to date on Microctonus spp. intraspecific variation in New Zealand. Agriculture, Ecosystems and Environment 64: 115-124 https://doi.org/10.1016/S0167-8809(97)00029-7
Goldson SL, Proffitt JR, Baird DB. (1998). The bionomics of Listronotus bonariensis (Coleoptera: Curculionidae) in Canterbury, New Zealand. Bulletin of Entomological Research 88, 415-423
Goldson SL, Proffitt JR, McNeill MR, Baird DB (1999). Linear patterns of dispersal and build up of the parasitoid Microctonus hyperodae (Hymenoptera: Braconidae) in Canterbury, New Zealand. Bulletin of Entomological Research 89(4): 347â353
Goldson SL, Tomasetto F and Popay AJ (2014). Biological control against invasive species in simplified ecosystems: its triumphs and emerging threats. Current opinion in insect science 5: 50-56
Goldson SL, Tomasetto F and Popay AJ (2015). Effect of Epichoe endophyte strains in Lolium spp. cultivars on Argentine stem weevil parastism by Microctonus hyperodae. New Zealand Plant Protection 68: 204-211
Goldson SL, Tomasetto F, Jacobs JME, Barratt BIP, Wratten SD, Emberson RM, Tylianakis J (2017). Rapid biocontrol evolution in New Zealand's species-sparse pasturelands. Proceedings of the 5th International Symposium on Biological Control of Arthropods, Langkawi, Malaysia, September 11-15, 2017: 32-34 https://www.cabi.org/cabebooks/FullTextPDF/2017/20173267440.pdf
Goldson SL, Wratten SD, Ferguson CM, Gerard PJ, Barratt BIP, Hardwick S, McNeill MR, Phillips CB, Popay AJ, Tylianakis JM and Tomasetto F. (2014). If and when successful classical biological control fails. Biological Control 72: 76-79
Harrop TWR, Le Lec MF, Jauregui R, Taylor SE, Inwood SN, van Stijn T, Henry H, Skelly J, Ganesh S, Ashby RL, Jacobs JME, Goldson SL, Dearden PK. (2020). Genetic diversity in invasive populations of Argentine stem weevil associated with adaptation to biocontrol. Insects 2020, 11(7), 441
Inwood SN, Harrop TWR, Dearden PK (2023). The venom composition and parthenogenesis mechanism of the parasitoid wasp Microctonus hyperodae, a declining biocontrol agent. Insect Biochemistry and Molecular Biology 153, Article Number 103897 https://doi.org/10.1016/j.ibmb.2022.103897
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, Addison PJ, Proffitt JR, Phillips CB, Goldson SL. (2002). Microctonus hyperodae: a summary of releases and distribution in New Zealand pasture. New Zealand Plant Protection 55: 272-279
McNeill MR, Phillips CB, Goldson SL (1993). Diagnostic characteristics and biology of three Microctonus spp. (Hymenoptera: Braconidae, Euphorinae) parasitoids of weevils (Coleoptera: Curculionidae) in New Zealand pasture and lucerne. New Zealand Entomologist 16(1): 39-44 https://doi.org/10.1080/00779962.1993.9722648
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
Pennisi E (2017). In a first, natural selection defeats a biocontrol insect Science 356 (6338): 570
Phillips CB, Baird DB, Goldson SL (1994). The South American origins of New Zealand Microctonus hyperodae parasitoids as indicated by morphometric analysis. Proceedings of the New Zealand Plant Protection Conference 47: 220-226 https://journal.nzpps.org/index.php/pnzppc/article/view/11100/10950
Popay AJ, McNeill MR, Goldson SL, Ferguson CM. (2011). The current status of Argentine stem weevil (Listronotus bonariensis) as a pest in the North Island of New Zealand. New Zealand Plant Protection 64: 55-62
Shields MW (2019). Host-parasitoid avoidance behaviour in the context of contemporary evolution in insect classical biological control: A thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy at Lincoln University. Doctoral dissertation, Lincoln University https://researcharchive.lincoln.ac.nz/bitstream/handle/10182/11016/Shields_%20PhD.pdf?sequence=4&isAllowed=n
Shields MW, Wratten SD, Phillips CB, Van Koten C, Goldson SL (2022). Plant-mediated behavioural avoidance of a weevil towards its biological control agent. Frontiers in Plant Science 13:923237
Shields MW, Wratten SD, van Koten C, Phillips CB, Gerard PJ, Goldson SL (2022). Behaviour drives contemporary evolution in a failing insect-parasitoid importation biological control programme. Frontiers in Ecology and Evolution 10, Article Number 923248 https://doi.org/10.3389/fevo.2022.923248
Tomasetto F, Casanovas P, Brandt SN, Goldson SL (2018). Biological control success of a pasture pest: has its parasitoid lost its functional mojo? Frontiers in Ecology and Evolution, Volume 6, Article 215 https://www.frontiersin.org/articles/10.3389/fevo.2018.00215/full
Tomasetto F, Cianciullo S, Reale M, Attorre F, Olaniyan O, Goldson SL. (2018). Breakdown in classical biological control of Argentine stem weevil: a matter of time. BioControl (2018) https://doi.org/10.1007/s10526-018-9878-4
Tomasetto F, Olaniyan O, Goldson SL. (2017). Ploidy in Lolium spp. cultivars affects Argentine stem weevil parasitism by Microctonus hyperodae. New Zealand Plant Protection 70: 326 (Poster abstract) http://journal.nzpps.org/index.php/nzpp/article/view/98
Tomasetto F, Tylianakis JM, Reale M, Wratten SD, Goldson SL. (2017). Intensified agriculture favors evolved resistance to biological control. Proc Natl Acad Sci USA 114 (15): 3885-3890 https://doi.org/10.1073/pnas.1618416114