Can natural enemies of current insect pests provide biotic resistance to future pests?

1. Economic pests jeopardize agricultural production worldwide. Classical biological control, comprising the import of exotic natural enemies to control target pest populations, has a successful history in many countries. However, little is known about how these natural enemies contribute to the suppression of pests that are yet to arrive. Biotic resistance theory, though, posits that communities resist species invasions as a result of natural enemies.
2. We assessed the potential of the resident exotic parasitoid wasp fauna in New Zealand (intentionally‐introduced biological control agents and unintentionally‐introduced species) to provide biotic resistance against possible future pests. A dataset was generated containing resident exotic parasitoid species (Ichneumonoidea: Braconidae; Ichneumonidae) in New Zealand, as well as their known global host ranges and the pest status of host species, to infer the potential for biotic resistance.
3. The known exotic ichneumonoid fauna in New Zealand comprises 65 species. These species associate with 107 host species in New Zealand, of which 54 species are pests. However, the current exotic species could potentially suppress 442 pest species not yet occurring in New Zealand.
4. This approach could be used to inform pest management programmes worldwide. Future research should consider how biotic resistance from the established parasitoid fauna can be used to inform specific decisions with respect to classical biological control.

     

A prospective model for the phenology of Microctonus hyperodae (Hymenoptera: Braconidae), a potential biological control agent of argentine stem weevil in New Zealand

A predictive phenological model is described for the parasitoid Microctonus hyperodae, introduced to New Zealand as a potential biological control agent against Argentine stem weevil Listronotus bonariensis. The model is based on development/temperature relationships obtained from experiments on the parasitoid in quarantine prior to its release, allowing early predictions of its phenology in different parts of the target pest's New Zealand range. In particular the model was used to predict the number of parasitoid generations each year, the degree of temporal synchrony between parasitoid adults and the susceptible adult pest stage, the order of parasitism and reproduction in the pest's life cycle as a possible basis for a simplified, discrete host/parasitoid population model, and the likely significance of ecotypic differences in development and diapause characteristics of the parasitoid. These applications demonstrate the potential for simple models to help in climate matching of classical biological control agents and estimation of their interaction with pest dynamics, using data obtainable prior to their introduction and release. In addition the model proved useful as a decision aid during the release programme, by indicating the likely effects of unusual weather and the need or otherwise for further parasitoid releases.     

Long-term Assessment of the Biological Control of Sitona discoideus by Microctonus aethiopoides and Test of a Model

Autumn densities of the pest weevil Sitona discoideus and its braconid parasitoid Microctonus aethiopoides were monitored from 1996 to 1998 on the Canterbury Plains, New Zealand. M. aethiopoides was introduced as a biological control agent in 1982 and first appeared in the study area in 1986. By 1991 around 50% of autumn weevils were parasitized and weevil density had been reduced by 75%. A model for the system at that time suggested that this level of suppression would be sustained. In agreement with the model, the recent survey confirmed that successful biological control had been maintained, with 75% suppression of weevil density but slightly lower rates of parasitism of around 35%. Weevil densities showed a significant trend longitudinally across the area surveyed, increasing from east to west, probably reflecting soil type. Weevil sex ratio was significantly biased towards females, yet the proportion of males that were parasitized was twice that of females. Percent parasitism in autumn related positively to weevil density over time and space. The scale of homogeneity, and by implication effective annual dispersal, is estimated at 12 +/- 4 km radius for weevils.     

Evidence for parasitoid‐induced premature mortality in the Argentine stem weevil

The Argentine stem weevil Listronotus bonariensis Kuschel (Coleoptera: Curculionidae) is an exotic pest of New Zealand ryegrass and the adult‐stage is parasitized by the introduced solitary endoparasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae: Euphorinae). This biological control agent is effective, although, under both laboratory and field conditions, an unexplained source of premature mortality in the weevils is observed after exposure to M. hyperodae. This premature mortality may be affected to varying degrees by the length of time of parasitoid exposure, the physiological conditions of the host, and the host to parasitoid ratios, although it occurs naturally without any physical interruption to the parasitoid ovipositional process. In the present study, the premature mortality reported in earlier studies is confirmed and it is conjectured to be the result of injection of parasitoid venom without an egg. Moreover, the lack of premature mortality resulting from longer exposure periods indicates that there might be a curative effect resulting from subsequent oviposition; the egg reverses the toxic effect induced by the injection of venom only. As discussed, this phenomenon may not be restricted to the L. bonariensis/M. hyperodae system and, accordingly, there are evolutionary, biosecurity and general pest management questions to be considered.     

Systematic mass rearing and release ofMicroctonus hyperodae (Hym.: Braconidae,Euphorinae), a parasitoid of the argentine stem weevilListronotus bonariensis (Col.: Curculionidae) and records of its establishment in New Zealand

The method whereby equal numbers of seven ecotypes of the parasitoidMicroctonus hyperodae Loan (Hymenoptera: Braconidae, Euphorinae) were reared and released is described along with the reasons for doing so. This was achieved by variably intense rearing effort depending on the number of founder females in that particular ecotype. The parasitoid was released in three regions of New Zealand as a control agent of theListronotus bonariensis Kuschel (Col.: Curculionidae), a severe pest of New Zealand pastures. It was later recovered from all three regions.     

Assessing the non-target impacts of classical biological control agents: is host-testing always necessary?

Release of a biocontrol agent in New Zealand is typically preceded by non-target testing of native or valued species. Nevertheless, if both the target pest and the natural enemy are very different from any native fauna, then there may be no scientific justification for host testing. Gonatocerus ashmeadi (Girault) (Hymenoptera: Mymaridae) is being considered as a biocontrol agent for glassy winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae), should the pest arrive. An assessment of the potential impact of G. ashmeadi on New Zealand’s Cicadellidae and Membracidae, from published literature data, indicates that none of these insects is at risk, as their eggs will not be recognised by the parasitoid because either their size or location places them outside the parasitoid’s search pattern. Consequently, there is no scientific case for any non-target host-testing to be carried out in containment.     

Reproductive characteristics of invasive hyperparasitoid Baeoanusia albifunicle have implications for the biological control of eucalypt pest Paropsis charybdis

Hyperparasitoids can impede the establishment of primary parasitoid biological control agents or limit their control capacity. Although modern quarantine practices generally prevent hyperparasitoids being introduced with biological control agents, introductions can occur via natural pathways or accidentally with incoming passengers and cargo. In New Zealand, Baeoanusia albifunicle Girault is a self-introduced hyperparasitoid of Enoggera nassaui Girault, an intentionally introduced control agent of the eucalypt pest Paropsis charybdis Stål. A self-introduced primary parasitoid, Neopolycystus insectifurax (Girault), also parasitises P. charybdis in New Zealand. We assessed B. albifunicle biology to better understand its potential to disrupt P. charybdis control. It was determined that B. albifunicle is an obligate solitary hyperparasitoid with a longer lifespan, lower fecundity and longer generation time than its host. The hyperparasitoid reduced effective parasitism by E. nassaui to <10% in the lab, indicating it may limit control of the first P. charybdis generation by slowing spring population growth. It was confirmed that N. insectifurax is not hyperparasitised by B. albifunicle and therefore has some potential to substitute for any hyperparasitoid-driven decline in E. nassaui.     

Early impact of endoparasitoid Microctonus hyperodae (Hymenoptera: Braconidae) after its establishment in Listronotus bonariensis (Coleoptera: Curculionidae) populations of northern New Zealand pastures

The South American curculionid Listronotus bonariensis (Kuschel) is an important pest of pastures in New Zealand. Population census data were gathered for L. bonariensis in northern New Zealand pastures during 1980-1983 in the absence of parasitism and again in 1991-1996 after the introduction and establishment of the braconid parasitoid Microctonus hyperodae Loan as a biological control agent. M. hyperodae achieved high rates of parasitism, with 75-90% of overwintering L. bonariensis parasitized within 3 yr of the parasitoid establishing at a site. Multistratum analysis of variance (ANOVA), with allowance for variation in host plant resource (numbers of Neotyphodium-free grass tillers), indicated reduction in the abundance of L. bonariensis life stages in the early part of life cycle. Although providing evidence for suppression of L. bonariensis, these analyses indicated the regulatory role of M. hyperodae was weak because L. bonariensis populations continued to exhibit marked intergenerational variability in abundance. Analyses of life tables indicated larval + pupal survival contributed most to intergenerational changes in abundance, irrespective of presence or absence of M. hyperodae. However, the density dependence of the stage survivals was modified in the presence of the parasitoid, with loss of density-dependent mortality in overwintering adults and increased density dependence in population natality. Regression analyses indicated dual contribution of parasitism and host plant resource to regulation of population natality and population trend in L. bonariensis. We conclude that M. hyperodae is a useful adjunct to host plant resistance in reducing the economic status of L. bonariensis populations in northern New Zealand pastures.     

The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data

1. A simple, intuitive argument and the tenets of the biological control literature both suggest that, in general, parasitoids with a greater fecundity will provide better control of their hosts, and will thus be better biological control agents. 2. A model of host-parasitoid dynamics, based on the standard Thompson–Nicholson–Bailey approach and incorporating the effects of parasitoid fecundity-limitation and host density-dependence, also indicates that as parasitoid fecundity decreases so does local stability and the degree of host suppression. 3. A taxonomically diverse data set obtained from the biological control record failed to support this theoretical prediction, but at the same time indicated a strong effect of host taxon on the outcome of biological control. 4. The hypothesis that the fecundity of parasitoids is correlated positively with their ability to suppress host populations is supported by data exclusively from the host order Lepidoptera. 5. Possible explanations for the divergence between the fecundity-limitation hypothesis and the complete data set include: the ability of parasitoids to provide long-term control of pests without the presence of a stable host–parasitoid equilibrium; differences between the concepts of successful control in theory and practice; evolutionary trade-offs between fecundity and other parasitoid life-history features, such as search efficiency, leading to better pest control by parasitoids with low fecundity; and differing windows of vulnerability to parasitoid attack between host taxa.     

Host specificity testing and suitability of the parasitoidMicroctonus hyperodae (Hym.: Braconidae,Euphorinae) as a biological control agent ofListronotus bonariensis (Col.: Curculionidae) in New Zealand

The behaviour of the parasitoidMicroctonus hyperodae Loan was studied under quarantine conditions to determine its likely host range in New Zealand. The species was imported from South America as a potential biological control agent of Argentine stem weevil,Listronotus bonariensis (Kuschel). The study involved systematic evaluation of the parasitoid's behaviour when exposed to 24 non-host weevil species; all but three of these were native to New Zealand. Of those tested, four were found to sustain someM. hyperodae development. However, further examination showed that in all but one species,Irenimus aequalis (Broun), parasitoid development was impeded, with up to 50% of the larvae becoming encapsulated. Overall, those weevil species that were attacked produced only 19% of the parasitoids derived fromL. bonariensis controls. As an adjunct to this quarantine study, a review of the habitats of the native weevil and target pest populations indicated that refugia would probably exist for native alpine species. I. aequalis was not considered to be threatened byM. hyperodae as this weevil has benefited from the advent of European agricultural systems to the extent that it is now recognised as a minor pest. In view of its relatively oligophagous behaviour, the parasitoid was recommended as suitable for release.      

Distribution, prevalence and host associations of Hymenoptera parasitic on Calliphoridae occurring in flystrike in New Zealand

Abstract. Between 1920 and 1930, four species of parasitoid Hymenoptera (Tachinaephagus zealandicus, Alysia manducator, Nasonia vitripennis and Brachymeria ucalegon) were imported to New Zealand as an aid in the control of the blowflies causing myiasis in sheep (flystrike). Their long-term effects have never been investigated and the extent to which they were successful in establishing and enlarging their ranges has been given scant regard over the last 60 years. A long-term epidemiological study of flystrike in New Zealand between 1986 and 1996 obtained 4061 samples of blowfly larvae from flystruck sheep and carrion and overall 1.1% of these larval samples (most from the North Island) were found to be parasitized. Tachinaephagus zealandicus and A. manducator were present in field strikes, together with the endemic Aphaereta aotea recently found to be a parasite of calliphorids. The endemic species Phaenocarpa antipoda was found in association with carrion but not flystrike. Neither N.vitripennis nor B.ucalegon were isolated from larvae in field strikes, the former because it parasitizes only pupae and the latter may be extinct as it has not been sighted since its introduction in 1919.
It is concluded that if parasitoid wasps are able to locate and parasitize blowfly larvae on struck sheep, then their parasitism rate on more accessible larvae on carcases may be correspondingly greater. For this reason their scope for use in integrated management of flystrike could be increased by culturing and field release.     

Biological control: implications of the analogy between the trophic interactions of insect pest-parasitoid and snail-trematode systems

An analogy between the tropic interactions of insect pest-hymenopterous parasitoid and snail-larval trematode systems is proposed. The goal of most agricultural pest management programs is increase in production of a plant crop, the deleterious agent is an herbivorous insect pest, the controlling agent, a parasitoid. Other parasitoid species may or may not have a significant effect on the control of the host by the key mortality factor.In snail—schistosome systems the goal is reduction of worm burdens in human populations, removed in space and time from the snail-sporocyst interaction; the deleterious agent is the schistosome, trophically equivalent to the hymenopterous parasitoid. Therefore, control may be achieved through competitive displacement of the schistosomes by other larval trematodes having superior intrinsic competitive abilities and better searching efficiencies at low host densities.Hyperparasites, sciomyzid Diptera and Daubaylia may also play a role in this view of schistosomiasis control. The Hassell-Varley parasite quest theory is applied to larval trematodes. The inversely proportional relationship between the area of discovery and miracidial density when logarithmically transformed is further evidence for the dynamic similarity of snail-trematode and insect-parasitoid systems.Other applications of the generally accepted principles of insect pest biological control to a medically important trematode indicate that (1) schistosome population control, not eradication, is the appropriate goal of public health programs, (2) the criteria for implementation and success of such programs must be in terms of the relationship between medical injury and the frequency distribution of worms in humans, and (3) a good biological control agent is likely to have a high searching efficiency at low host densities, kill more than one snail host, be highly host specific, be scarce when successful, reside in regions were schistosomiasis is negligible as a medical problem.     

Development of teratocytes associated with Microctonus aethiopoides Loan (Hymenoptera: Braconidae) in natural and novel host species

A laboratory study investigated development of teratocytes derived from the parasitoid Microctonus aethiopoides Loan in the natural host, Sitona discoideus Gyllenhal, and in three novel hosts, the introduced weed biological control agent Rhinocyllus conicus (Froehlich), and two New Zealand native species Nicaeana cervina Broun and Irenimus stolidus Broun. Weevils were exposed to parasitoids and then examined 6, 10 and 15 days post-parasitism for parasitoid stage and size, and teratocyte number and size. In all hosts, teratocyte numbers decreased and size increased as parasitoid development progressed, although 6 days after parasitism, fewer, larger teratocytes were found in I. stolidus than S. discoideus or N. cervina. In weevils containing second-third instar parasitoid larvae, the most permissive hosts, S. discoideus and N. cervina contained more teratocytes than the least permissive hosts I. stolidus and R. conicus. Host gender influenced some aspects of parasitoid and teratocyte development. Total teratocyte volume was greater in female than male S. discoideus at all sampling times, and at 10 days post-parasitism in N. cervina. A possible relationship between host suitability and teratocyte development is discussed.     

Parasitism of the lucerne pest Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) and non-target weevils by Microctonus aethiopoides Loan (Hymenoptera: Braconidae) in south-eastern Australia, with an assessment of the taxonomic affinities of non-target hosts of M. aethiopoides recorded from Australia and New Zealand

Abstract  The braconid parasitoid Microctonus aethiopoides Loan has been released in Australia and New Zealand for biological control of the lucerne pest Sitona discoideus Gyllenhal. In New Zealand, the parasitoid attacks a number of endemic weevil species. A survey of Curculionoidea found in and near lucerne in south-eastern Australia was carried out to investigate whether similar non-target parasitism was occurring, and to relate this to levels of parasitism found in the target host, S. discoideus . Some of the original M. aethiopoides release sites were particularly targeted in the survey of 25 sites in Victoria, New South Wales and South Australia. Almost 2500 weevils were collected, of which over 90% were S. discoideus , with the remaining 197 other weevils comprising 29 species found at 15 of the 25 sites. Parasitism of S. discoideus by M. aethiopoides occurred at 12 lucerne sites, with levels ranging from 0 to 25%. A single incidence of parasitism of a species of an Australian native weevil Prosayleus sp. by M. aethiopoides was recorded. No parasitism of any other weevil species was observed. The taxonomic affinities between Sitona and native Australian and New Zealand weevils are discussed, concluding that non-target host range in M. aethiopoides may be determined more by ecological factors than by taxonomic affinities among its hosts.     

Invertebrate predation of 15N-marked prey in semi-field wheat enclosures

One of the most famous examples of successful, classical biological control in Japan is the introduction of the parasitoids Coccobius fulvus and Aphytis yanonensis against the citrus pest arrowhead scale Unaspis yanonensis. Together, they comprise a host‐parasitoid system that has been demonstrated to be stable. To test the conventional theory that successful biological control of pests occurs through the establishment of a low stable equilibrium, brought about by the density‐dependent responses of natural enemies to the pest species, sampling was carried out at five sites in the field during 2000 and 2001 to examine the relationship between the rate of parasitism by C. fulvus and the density of its host. The data were analysed using three statistical techniques at nine spatial scales. Contrary to conventional theoretical predictions, each method of analysis detected very little density‐dependence at any spatial level in this study. Parasitoid aggregations independent of host density were not sufficient to stabilise host–parasitoid interactions. Our results suggest that neither spatial density‐dependent nor density‐independent parasitism is necessary for successful biological control, or for the stability of the host–parasitoid system. We propose an alternative mechanism: a spatial refuge induced by parasitoid introduction may stabilise a system.     

Allozyme markers to help define the South American origins of Microctonus hyperodae (Hymenoptera: Braconidae) established in New Zealand for biological control of Argentine stem weevil

The thelytokous parasitoid, Microctonus hyperodae Loan, was collected from eight South American locations and introduced to New Zealand in 1991 for biological control of Argentine stem weevil, Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Parasitoids from each population were released in equal numbers at each New Zealand site to give them the same opportunities to establish. Population markers have been sought to identify the South American geographic populations that have become most successful in New Zealand. These would assist in determining the importance of concepts such as climate matching and host-parasitoid coevolution to the establishment of natural enemies in new regions for biological control. Vertical polyacrylamide electrophoresis was used to survey 16 enzymes and ten calcium binding proteins, and this paper reports variation at three putative loci. Malate dehydrogenase, a dihydrolipoamide dehydrogenase isozyme and a calcium binding protein exhibited clear genetic variation, each with two alleles. All M. hyperodae isofemale lines from east of the Andes mountains shared one genotype, all but one from west of the Andes shared another, while a population from within the Andes contained both genotypes. This variation was highly congruent with previously described morphometric variation. At two loci, the maintenance of heterozygotes, and the absence of homozygotes, within isofemale lines suggested M. hyperodae thelytoky is apomictic.     

Host preferences ofTrichogrammatoidea bactrae fumata (Hym.: Trichogrammatidae) an egg parasitoid of leafrollers (Lep.: Tortricidae)

Trichogrammatoidea bactrae fumata Nagaraja is a naturally occurring egg parasitoid of some leafrollers in New Zealand kiwifruit orchards. The parasitoid showed a distinct preference for younger host-eggs ofEpiphyas postvittana, in which it achieved a higher rate of successful development. Such a preference is not as apparent withCtenopseustis obliquana. Host-species preference experiments found that the parasitoid rarely attackedPlanotortrix octo, and successful wasp emergence from parasitised eggs of this host was low.Epiphyas postvittana was the preferred host whenT. bactrae fumata was reared on this species. When reared onC. obliquana, the parasitoid showed no preference forE. postvittana orC. obliquana.     

Coexistence of multiple parasitoids on a single host due to differences in parasitoid phenology

There are many well-documented cases in which multiple parasitoids can coexist on a single host species. We examine a theoretical framework to assess whether parasitoid coexistence can be explained through differences in timing of parasitoid oviposition and parasitoid emergence. This study explicitly includes the phenology of host and parasitoid development and explores how this mechanism affects the population dynamics. Coexistence of the host with two parasitoids requires a balance between parasitoid fecundity and survival and occurs most readily if one parasitoid attacks earlier but emerges later than the other parasitoid. The host density can either be decreased or increased when a second coexisting parasitoid is introduced into the system. However, there always exists a single parasitoid type that is most effective at depressing the host density, although this type may not be successful due to parasitoid competition. The coexistence of multiple parasitoids also affects the population dynamics. For instance, population oscillations can be removed by the introduction of a second parasitoid. In general, subtle differences in parasitoid phenology can give rise to different outcomes in a host–multi-parasitoid system, and this may offer some insight into why establishing criteria for the ‘ideal’ biological control agent has been so challenging.     

Argentine stem weevil ( Listronotus bonariensis, Coleoptera: Curculionidae) population dynamics in Canterbury, New Zealand dryland pasture

The Argentine stem weevil (Listronotus bonariensis) was an economically important pest in New Zealand pastures until the release of the parasitoid Microctonus hyperodae. This contribution uses historical data to investigate the regulation of the pest populations prior to, and somewhat during, the establishment of this parasitoid in dryland Canterbury, New Zealand. Thus, a significant goal of this study is to provide an L. bonariensis population dynamics baseline for any future work that aims to analyse the full effects of M. hyperodae on the weevil, now that equilibrium with the weevil host has been reached.The population dynamics of L. bonariensis, based on a life-table approach, were investigated using data collected regularly for eight years from populations in Canterbury, New Zealand. The key factor affecting end-of-season L. bonariensis density was found to be variation in second generation fourth instar prepupal and pupal mortality. This may have been caused by arrested development and ongoing mortality resulting from the onset of cooler autumnal conditions.A compensatory response was found in recruitment to the second summer weevil generation, whereby the realised fecundity of the emergent first summer generation of weevils was found to be negatively related to the density of adult weevils per ryegrass tiller. This is the first time that this has been found via long-term population analysis of L. bonariensis, although indications of this have been found elsewhere in caging, pot and small plot experiments.In this study, the effect of the parasitoid biocontrol agent Microctonus hyperodae on L. bonariensis population dynamics was unclear, as the analysis covered a period when the parasitoid Microctonus hyperodae was introduced and still establishing. It does, however, raise important questions for future analysis in terms of the interaction between parasitism and unrealised fecundity.The results in this contribution also highlighted regional differences. Overwintering mortality of adult weevils in Canterbury was constant between years, whilst earlier studies in the North Island Waikato region indicated this mortality was density dependent. In addition, the availability of tillers in endophyte-free ryegrass pastures in Canterbury had no influence on egg and early-instar larval survival, which contrasts with the finding from endophytic Waikato pastures.     

A European pest to control a new zealand weed: investigating the safety of heather beetle, Lochmaea suturalis (Coleoptera: Chrysomelidae) for biological control of heather, Calluna vulgaris

Heather, Calluna vulgaris (L.) Hull, is a serious invasive weed in the central North Island of New Zealand, especially in Tongariro National Park, a World Heritage Area. Heather beetle, Lochmaea suturalis (Thomson), is a foliage-feeding pest of Calluna in Europe, that was selected as the most promising biological control agent for introduction into New Zealand, because it causes high levels of damage to Calluna in Europe. Host-range tests indicated that L. suturalis poses a negligible threat to native New Zealand plants. Cultivars of Calluna grown as ornamentals are suitable food plants, but are unlikely to be severely affected because L. suturalis requires a damp understorey of moss or litter for successful oviposition and pupation, which is rarely present in gardens. However, mosses and litter occurring under Calluna stands in Tongariro National Park are suitable substrates for eggs and pupae. Lochmaea suturalis released in New Zealand has been freed of parasitoids and a microsporidian disease that attack the beetles in Europe.