Biological Control 72 (2014) 76–79

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Biological Control

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Perspective

If and when successful classical biological control fails

http://dx.doi.org/10.1016/j.biocontrol.2014.02.0121049-9644/� 2014 Published by Elsevier Inc.

⇑ Corresponding author at: AgResearch Lincoln, Private Bag 4749, Christchurch8140, New Zealand. Fax: +64 3 3218811.

E-mail address: stephen.goldson@agresearch.co.nz (S.L. Goldson).

S.L. Goldson a,b,⇑, S.D. Wratten b, C.M. Ferguson c, P.J. Gerard d, B.I.P. Barratt c, S. Hardwick a, M.R. McNeill a,C.B. Phillips a, A.J. Popay d, J.M. Tylianakis e,f, F. Tomasetto b

a AgResearch Lincoln, Private Bag 4749, Christchurch 8140, New Zealandb Bio-Protection Research Centre, PO Box 85084, Lincoln University, Lincoln 7647, New Zealandc AgResearch Invermay, Private Bag 50034, Mosgiel 9053, New Zealandd AgResearch Ruakura, Private Bag 3123, Hamilton 3240, New Zealande University of Canterbury, School of Biological Sciences, Private Bag 4800, Christchurch 8140, New Zealandf Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, United Kingdom

h i g h l i g h t s

� The reason for persistence ofsuccessful classical biological controlis discussed.� Possible mechanisms for classical

biological control failure areconsidered.� NZ control failure because of host

sexual versus control agent asexualreproduction.� Unique species-depauperate nature

of NZ pastoral ecosystems isdescribed.� Simple ecosystem exaggerates effect

of parasitoid/host reproductivedifferences.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Received 11 October 2013Accepted 20 February 2014Available online 28 February 2014

Keywords:Biological controlEcosystem complexityFailureParasitoidParthenogeneticSpecies diversity

a b s t r a c t

Classical biological control of insects has a long history of success, with high benefit–cost ratios. However,most attempts to introduce a biological control agent have been unsuccessful, largely because the agentdoes not establish in the new environment. This perspectives paper discusses the possibility that evensuccessful biological control may eventually fail, although records show that this is far from a commonevent. A documented example of eventual biological control failure is discussed and the prospect forfuture failures analyzed. Part of this analysis is based on an introduced weevil pest in New Zealandand its successful parasitoid biological control agent. The potential fragility of this host–parasitoid rela-tionship is considered, as well as why it may indeed be starting to show signs of instability; this is par-ticularly from the point of view of New Zealand’s often species-poor agricultural ecosystems.

� 2014 Published by Elsevier Inc.

1. Introduction in a target species’ ecosystem with the objective of permanently

Classical biological control of pest animals, weeds and diseasesinvolves the release of specialist natural enemies of foreign origin

reducing its numbers and impact. Such a control system can beelegant, self-sustaining, non-polluting and inexpensive – when itworks (Gurr and Wratten, 2000). To this might be added: ‘and aslong as it continues to work’. If previously-successful biologicalcontrol starts to fail, the consequences could be enormous, giventhe high benefit-cost ratios of many past successes (Page and Lacey2006; de Clerqet et al., 2011). A wide range of factors point to the

S.L. Goldson et al. / Biological Control 72 (2014) 76–79 77

accelerating need for biological control. Indeed, this requirementcontinues to grow as world trade and speed of transport systemsaccelerate and the need to suppress invasive exotic pest species isgreater than ever (e.g. Goldson 2011). However, there are numerouschallenges including increasing pesticide resistance in many insectspecies, more rigorous environmental scrutiny of existing com-pounds leading to their removal from use, very high pesticide reg-istration costs resulting in fewer successful new molecules comingto market and heightened consumer awareness of residues andenvironmental impacts (Gurr, Wratten and Snyder 2012). Also eco-nomic and practical considerations mean that there is demand forself-sustaining solutions to pest problems, such as classical biolog-ical control, that do not require frequent and expensive manage-ment interventions (e.g. de Schutter, 2010; Wratten et al., 2013).

Declining opportunities for conventional solutions is coincidingwith human population growth and with this, the demand forwhat has been referred to as ‘sustainable intensification’ (e.g. Pret-ty 1997; Godfray et al., 2012). Biological control can contribute tothis requirement, but since 1880, so-called classical biological con-trol of insect pests has remained at a success rate of around 10%(Gurr and Wratten, 2000). If the successful 10% also start to fail,then the consequences would be profound.

In spite of this low rate, successful classical biological controlmay to date have appeared to be a ‘magic bullet’ because it can de-liver long-term outcomes. However, there is some evidence thatresistance could arise. For example, Henter and Via (1995a) foundsignificant variation in susceptibility to a parasitic wasp Aphidiuservi in Haliday Acyrthosiphon pisum (Harris) clones collected froma single population. The wasps oviposited in aphids from bothresistant and susceptible lines, but the eggs failed to develop inthe resistant hosts indicating that this aphid population had thepotential to evolve resistance. However, field-collected material ta-ken in early and late summer, covering several generations, re-vealed no response to selection by the wasps. The authorsspeculated that amongst other things, this could have been causedby fitness costs associated with resistance or interference causedby other control systems. Similarly, Kraaijeveld and Godfray(1997) working on Asobara tabida (Nees) parasitism of Drosophilamelanogaster Meigen found that the extent to which the latterwas selected to invest in defenses against pathogens and parasitesdepended on the advantages that ensue should infection/parasit-ism occur, but also on the costs of maintaining defenses in the ab-sence of such potential selection pressures. Also there is thesuggestion of evolution of resistance whereby the host Hypera pos-tica (Gyllenhaul) has apparently exhibited an increase in theencapsulation rate of the parasitoid Bathyplectes curculionis (Thom-son) (Berberet et al., 2003). More broadly, Hufbauer and Roderick(2005) have analyzed in some detail, the implications of microevo-lution in biological control.

In spite of such indications, there are indeed remarkably few,maybe only one, published examples of successful classical biolog-ical control clearly failing through the onset of resistance in theprey/host. Indeed, often where successful classical biological con-trol has not persisted, this has turned out to be in conjunction withchanged management practices such as altered pesticidal regimes,or changed genetic composition of the control agents through re-leases of additional strains etc. The former appears to be the casewith the biological control of the walnut aphid (Chromaphisjuglandicola Kaltenbach) by Trioxys pallidus Haliday (Aphididae) inCalifornia (N. Mills, UC Berkeley; pers. comm.). This process maynow be occurring in New Zealand with the accelerating use ofbroad-spectrum pesticides against the recently-colonized toma-to–potato psyllid (Bactericera cockerelli Sulc.) on solanaceous crops.It appears that the only definitive example of the evolution of prey/host resistance is from Canada. Here, the larch sawfly, Pristiphoraerichsonii Hartig (Hymenoptera: Tenthredinidae), was controlled

for 27 years by the ichneumonid wasp, Mesoleius tenthredinus Mor-ley before failing through widespread host encapsulation of theparasitoid’s eggs (Ives and Muldrew 1984; Dahlsten and Mills1999). A Bavarian strain of M. tenthredinis was later found thatcould overcome the immune response of P. erichsonii, and crossesbetween the Bavarian and Canadian strains also inherited this abil-ity (Turnock et al., 1976). Related to this, Turnock and Muldrew(1971) suggested that the likelihood that resistance of this typewill develop can be reduced by providing more than one effectivecontrol agent, and recent experimental results have supported this(Kraaijeveld et al., 2012).

Overall, such complexity and infrequency of the occurrence ofbiological control resistance is in marked contrast to the extent,rapidity and unequivocal nature of the appearance of resistanceto pesticides and transgenic pest-resistant crops (e.g. Tabashniket al., 2013). There has been some discussion as to why classicalcontrol should be so robust (e.g. Holt and Hochberg 1997). Basedon the work of such contributors as Henter and Via (1995a) andKraaijeveld and Godfray (1997), there are indications of a seriesof factors that are thought to contribute to biological control stabil-ity. A probable important factor is that biocontrol control agentscan co-evolve with a pest and thereby counteract resistance devel-oping in the latter (Henter and Via, 1995a,b). Should a pest developresistance in this way, it may incur metabolic or other costs (e.g. areduction in fecundity) as a consequence (Kraaijeveld and Godfray,1997). There could also be mechanisms that stabilize susceptibilitythrough the provision of either spatial (e.g. Hanski, 1981) or tem-poral refugia (e.g. Godfray, Hassell and Holt, 1994). Low distur-bance regimes can also preserve biological control effectiveness(e.g. Jonsson et al., 2012). Related to this, diverse agro-ecosystemsmay stabilize biological control, as they often comprise a widerange of natural-enemy guilds that contribute to pest suppression(Tylianakis and Romo, 2010).

Evidence now suggests that at least some of these drivers ofbiological control stability could well break down. A case studyin this context is New Zealand’s pastoral ecosystem. This currentlysupports high biological control efficacy of several introduced wee-vil pests (e.g. Barlow and Goldson, 1993; Barker and Addison 2006;Gerard et al., 2011). However, as discussed below, there may nowbe some reason to look again at the durability of such success, de-spite the history of biological control persistence – see earlier. Thisconcern is based on the relatively low alpha diversity of inverte-brates in New Zealand’s intensive pastoral ecosystem comparedwith native grassland systems. The former are effectively incom-plete ‘transplants’ of the biodiversity found in the northern hemi-sphere origin of New Zealand’s pasture plants (ryegrass and whiteclover) with relatively few New Zealand native herbivorous arthro-pod species persisting in that environment. Thus, while New Zea-land’s farmland may superficially appear to be similar to largepastoral ‘monocultures’ elsewhere e.g. forb-rich European mead-ows, the latter include far more native and endemic biodiversity,suggesting greater ecological stability and a larger community ofbiological control agents. This contrasts with New Zealand pasturewhich probably has weaker food-web assemblages (sensu Bersieret al., 2002) than in many other regions. These circumstances sug-gest that in the case of parasitoid-based systems at least, shouldclassical biological control programs begin to weaken throughthe acquisition of, for example, immune-based pest resistance,then the ‘background biological control’ may not be powerful en-ough to ameliorate the potential consequences.

Exotic pest populations in New Zealand’s grasslands often buildup to very high and damaging densities (e.g. Barker et al., 1989;Goldson et al., 1998; Gerard et al., 2009), probably because of thehomogeneity of the pasture ecosystem and absence of species-richguilds, discussed above (Goldson et al., 1997). Release from naturalenemies in a new range is well known from the invasion literature

78 S.L. Goldson et al. / Biological Control 72 (2014) 76–79

to facilitate exotic species establishment (e.g. Hong and Stiling2006). Given that, the objective of biological control is to increasethe contribution made to top-down control by enemies such asparasitoids (Stiling and Cornelissen 2005). If classical biologicalcontrol introductions are carried out carefully, fourth-trophic levelhyperparasitoids should not be introduced along with the selectedagent. However, the margin for colonization gained through theabsence of enemies can come with the negative influence of theintroduced species having to consume novel host/prey resourcesto which it is not adapted. Where there are not suitable existingflora or fauna in the receiving area this in turn can impose con-straints on success (Parker et al., 2006). Yet in a biological controlcontext, such conditions often no longer apply; rather, exotic con-sumers have frequently co-evolved with their resource (e.g. intro-duced parasitoids attacking an invasive pest). In effect, suchcontrol agents lack their native suite of enemies, so they receivethe benefit of a new host-rich environment, minus the cost. How-ever, when the pest and its biocontrol agents are both accidentallyintroduced, fourth trophic-level agents often accompany the spe-cies in the third trophic level. This is demonstrated by recent workby and Varennes et al. (in press).

2. A New Zealand case study

The general observations on the persistence of biological control,given above, are well exemplified by two exotic weevil species inNew Zealand, the Argentine stem weevil Listronotus bonariensis(Kuschel) (ASW) and the clover root weevil Sitona lepidus Gyllenhal(CRW). ASW arrived in New Zealand in about 1910 and CRW arrivedaround 1990. Due to their ability to reach very high densities (e.g.Barker et al., 1989; Gerard et al., 2011), they are both able to causevery severe damage to New Zealand’s large areas of improvedryegrass/clover pasture (e.g. Prestidge et al., 1991; Barlow andGoldson, 2002). Fortunately, extremely effective biological controloccurred via two introduced braconid endoparasitoid speciesbelonging to the genus Microctonus Wesmael. These were Microct-onus hyperodae Loan released against ASW in 1991 (Goldsonet al., 1993), and Microctonus aethiopoides Loan released againstCRW in 2006 (Gerard et al., 2006). Parasitism rates by both thesewasp species reached up to 90% shortly after release (Goldsonet al., 1998; Barker et al., 2006; Gerard et al.,. 2011). These rates(e.g. Loan and Lloyd, 1974; Goldson et al., 1990, 2001) and the hostweevil population densities (e.g. Goldson et al., 1990, 2001, unpub-lished data) were much higher than those observed in their centersof origin. In effect, the population dynamics found in New Zealandpastures have probably never occurred in the species’ history. Thisis almost certainly the reason why in New Zealand, observed relictbehaviors in exotic pest species appear to confer no adaptive valuewhatsoever. A good example of this is the continuation of relictdiapause in ASW (Goldson and Emberson, 1980).

3. Discussion

As mentioned above, the literature supports the idea that spa-tial heterogeneity can lead to the retention of biological control-susceptible genes within the host species (Vermeij, 1985). Simi-larly, Holt and Hochberg (1997) commented on the importanceof spatial structure, where a colonizing-extinction cycles occuracross patches of various sizes and distances apart. There arenumerous mathematical models and experiments describing suchprocesses that are beyond the scope of this contribution (e.g.Levins 1968, 1969; Hanski 1981; Tscharntke et al., 2005). Furtherto this, heterogeneity can provide refugia for populations withresistant genes to various selection pressures, and this in turn allowspopulations to persist. Thus, with regard to the discussion to date

about the relative dearth of references to evolved resistance inclassical biological control hosts, a major consideration is that ingeneral, such analyzes have been based on those reasonably di-verse, patchy and evolved ecosystems often observed in parts ofthe world beyond New Zealand.

The New Zealand pasture environment therefore provides aninteresting contrast to what is found elsewhere. It has features thatmay allow the testing of some of the existing ideas around whyresistance to biological control should occur so rarely. Indeed, itcan be hypothesized that ASW and CRW resistance to biologicalcontrol in New Zealand pastoral ecosystems is much more likelyto occur than elsewhere, despite the factors listed above that arethought to prevent it. Firstly, co-evolution with the pest is mostunlikely if the introduced parasitoids are parthenogenetic, as isthe case for both M. hyperodae and M. aethiopoides (Irish strain). In-deed, allozyme data indicate M. hyperodae probably reproduces byameiotic thelytoky (i.e., apomixis), so mother and offspring arenearly always genetically identical (Iline and Phillips 2004) withthe only possible sources of new M. hyperodae variation beingmutation and, perhaps, hybridization. While attempts were madeto deliberately introduce some variability within M. hyperodaethrough the selection of presumed separate geographical popula-tions (Goldson et al., 1993; Phillips et al., 2008), their adaptive po-tential is still very likely to be minimal compared to that of ASW.Conversely, the weevil hosts undergo sexual recombination of al-leles, even though the population shows little apparent regionalgenetic variation (e.g. Williams et al., 1994). Secondly, New Zea-land’s pastoral ecosystem is anything but heterogeneous eitheron a small or large scale and this indicates a likely scarcity of refu-gia in which genetic susceptibility to control agents can be con-served. This means that parasitoids with a high attack rate (sensuNicholson, 1933) are likely to encounter most if not all hosts,thereby increasing the likelihood of the occurrence of pest resis-tance, because of the weak or absent ‘metacommunity’ (Leiboldet al., 2004; Urban et al., 2008). Finally, those data that do existin the literature suggest that resistance to parasitoid biologicalcontrol agents is most likely when a pest is suppressed by a singleagent (e.g. Turnock and Muldrew, 1971; Kraaijeveld et al., 2012);again, this is precisely the situation with the CRW and ASWsystems.

The thinking behind this contribution has arisen because there isnow preliminary evidence that shows that in New Zealand the ratesof parasitism of ASW have dropped by as much as 50% over the last10–15 years. While it is too early for consternation, there is clearreason for further analysis of both the indicative data themselvesand the environment in which broad-acre biological classical con-trol operates in New Zealand. If the apparent loss of control contin-ues or worsens, the question is therefore, irrespective of themechanism, does this fit with one or more of the theoretical consid-erations developed above? If it does, then it could indicate that thevery thing that has led to such outstanding biological control suc-cesses, highly invasible species-depauperate and uniform ecosys-tems, could become the ultimate cause of their failure.

Acknowledgments

The authors gratefully acknowledge the valuable editorialcomments by the Rt Hon Simon Upton (OECD Paris) andAssociate Professor Hazel Chapman (University of Canterbury,New Zealand). We are also grateful to the following colleaguesfor their help in developing the arguments in this paper: ProfMark Hoddle, University of California, Riverside, USA; Prof NickMills, University of California, Berkeley, USA; Prof Roy Van Drie-sche, University of Maryland, USA; Dr Rachel McFadyen, CSIRO,Australia.

S.L. Goldson et al. / Biological Control 72 (2014) 76–79 79

Funding for this work has been contributed by the New ZealandMinistry for Ministry for Business, Innovation and Employment(MBIE) (LINX0802) (SDW) and its precursors (SLG and others).JMT is funded by a Rutherford Discovery Fellowship administeredby the Royal Society of New Zealand.

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