Plant-mediated interactions: Considerations for agent selection in weed biological control programs

Plant-mediated indirect interactions among herbivores (arthropods and pathogens) are common and extensively reported in the ecological literature. However, they are not well-documented with respect to weed biological control. Such interactions between biological control agents can have net positive or negative impacts on total weed suppression depending on the strength of the interaction(s), the relative importance of the agent indirectly impacted, and the combined weed suppression that results. A better understanding of plant-mediated interactions may improve decision-making about which agents to introduce in classical biological control programs for greatest impact on invasive weeds. This paper reviews the subject, including examples from the biological control literature; outlines the need for research on indirect effects of herbivores on other herbivores; discusses how such knowledge may strengthen classical biological control programs for invasive weeds; and provides recommendations for the kind of studies that should be done and how information about plant-mediated interactions could be integrated into agent evaluation protocols, to assist in decision-making about agents for importation and release.     

The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent

Melaleuca quinquenervia (Cav) S.T. Blake (broadleaf paperbark) is an Australian tree that has become a serious weed in many places around the world. Two insects Oxyops vitiosa (the melaleuca weevil), and Boreioglycaspis melaleucae (the melaleuca psyllid), which were introduced to Florida as part of a biological control programme, have been very effective in reducing survival and reproduction of this weed. There are two terpene chemotypes of M. quinquenervia; one rich in the sesquiterpene E-nerolidol whereas the other is rich in viridiflorol. Viridiflorol is a strong feeding deterrent for the melaleuca weevil and retards larval development. The larvae therefore avoid the viridiflorol-rich chemotype, in contrast, female melaleuca psyllids prefer to oviposit on these leaves. To identify the molecular basis of these preferences, we isolated and characterised two terpene synthases from the viridiflorol-rich chemotype, both of which utilise farnesyl pyrophosphate and have the same product profile. Chemotypic variation in terpenes in M. quinquenervia is under strong genetic control and the reproductive potential of each chemotype is limited by a different insect. These insects could, therefore, be selective agents for the maintenance of chemotypic variation in M. quinquenervia.     

Opportunities for biological weed control in Europe

The development and application of biological weed control offer greatopportunities not only for farmers, nature conservationists and othervegetation managers but also for institutions and companies that wish tosell plant protection services and products, and for the general publicthat demands safe food and a visually attractive and diverseenvironment. Despite the obvious opportunities for biological weedcontrol, few control agents are actually being used in Europe. Potentialagent organisms have features that make them particularly strong anduseful for biological control, but they also have weaknesses. Weaknessesinclude a too narrow or too wide host specificity, lack of virulence, orsensitivity to unfavourable environmental conditions.Developing specific knowledge on the interaction between weeds andpotential biological control agents, as well as expertise to increasethe effect of control agents and so achieve sufficient weed control in acost-effective manner, should have the highest priority in researchprogrammes. From 1994 to 2000 most ongoing research on biological weedcontrol in Europe was combined in a cooperative programme. This COSTAction concentrated on the interactions between five target crop weedsand their antagonists (pathogens and insects), on furthercharacterisation of the specific blems and potential control agents andon the most suitable biological control approach.The next major challenge will be to apply the findings provided byCOST-816 to the development of practical control solutions. The leadingobjective of a new concerted research programme with European dimensionswill be to stabilise or even promote biodiversity in the most importantEuropean ecosystems by integrating biological weed control in themanagement of these systems.     

Nutrient composition of soil and plants may predict the distribution and abundance of specialist insect herbivores: implications for agent selection in weed biological control

Abstract  Refining the process of selecting specialist herbivores that are used as biological control agents to maximise effects on the targets can diminish the risk to non-target species. While biotic factors (e.g. plant demography and agent–host interactions) have been explored for clues to improve the way we make agent selection decisions, recent ecological research indicates that abiotic factors related to the habitat (e.g. plant and soil nutrient composition, and soil characteristics) are important predictors of insect herbivore community composition. In this paper we explore the relevance of plant nutrient composition to aid in selecting agents for the invasive Eurasian perennial Euphorbia esula (leafy spurge) in Illinois, USA. We propose that an approach that compares such abiotic factors across the native and invaded ranges of plants in conjunction with the community composition of specialist herbivores in the native range may yield valuable clues in selecting agents that are most likely to establish and regulate populations of the target weed.     

The biology of Puccinia chondrillina a potential biological control agent of skeleton weed

During investigations on the parasites of Chondrillajuncea in the Mediterranean region, the rust, Puccinia chondrillina, was found to be one of the most damaging. This macrocyclic and autoecious rust which is specific to the genus Chondrilla, remains active throughout the year and attacks all stages and all parts of the plant. In the Mediterranean region the rust appears to multiply solely by the uredo-stages and the teleutospores produced at the end of the summer have no obvious role in the life-cycle of the fungus. The uredospores germinated at temperatures of 0–36 °C and were used for inoculation of Chondrilla seedlings in the greenhouse. The rust occurs from the cold continental climates of southern Siberia to the hot, Mediterranean ones of Portugal and North Africa. In many situations the rust has been found to play an important role in the reduction of C. juncea populations. Young seedlings were highly susceptible to attack and were often destroyed. Older rusted plants gave many fewer viable seeds than healthy plants and were also often unable to produce new rosettes from their roots.     

Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control programme

The Florida Everglades have been invaded by an exotic weed fern, Lygodium microphyllum. Across its native distribution in the Old World tropics from Africa to Australasia it was found to have multiple location-specific haplotypes. Within this distribution, the climbing fern is attacked by a phytophagous mite, Floracarus perrepae, also with multiple haplotypes. The genetic relationship between mite and fern haplotypes was matched by an overarching geographical relationship between the two. Further, mites that occur in the same location as a particular fern haplotype were better able to utilize the fern than mites from more distant locations. From a biological control context, we are able to show that the weed fern in the Everglades most likely originated in northern Queensland, Australia/Papua New Guinea and that the mite from northern Queensland offers the greatest prospect for control.     

A strategy for evaluating the safety of organisms for biological weed control

A strategy for establishing the specificity and safety of an organism as a biological weed control agent is described. A critical first step is to expose to its attack a small group of plants very closely related and exhibiting morphological and biochemical similarities to the weed. To prevent an erroneous negative result tests are also made on selected cultivated plants, including those closely related to the weed, those of which the associated insects and fungi are little known, those that have evolved apart from or been little exposed to the agent, those attacked by closely related organisms and those already recorded as hosts. The circumstances under which the strategy might fail to indicate safety are discussed, i.e. polyphagous organisms attacking plants irregularly distributed throughout many families, organisms highly specific to two alternate hosts, and those attacking two or three phylogenetically widely separated plant groups. The additional crop plant testing, included in the overall strategy to deal with such possible failures, is discussed. It is shown that the strategy would have included Sesamum tndicum in the list of plants challenged by the bug Teleonemia scrupulosa in biological testing for control of Lantana camara, thereby forewarning of the attack that was subsequently observed in Africa.     

Chemotype variation of the weed Melaleuca quinquenervia influences the biomass and fecundity of the biological control agent Oxyops vitiosa

Host plant nutritional and non-nutritional variability can have a significant effect on herbivore populations by influencing survival, larval performance, and fecundity. The effect of chemical and physical variation of the leaves of two chemotypes of the weed Melaleuca quinquenervia was determined on the biomass and fecundity of the biological control agent Oxyops vitiosa (Coleoptera: Curculionidae). M. quinquenervia chemotypes were distinguished by the principal terpenoids E-nerolidol and viridiflorol using gas chromatography and mass spectroscopy. Not only were the terpenoid profiles of the two chemotypes different but the viridiflorol leaves had greater toughness (1.2-fold) and reduced nitrogen (0.7-fold). When the larvae and adults were fed leaves of the E-nerolidol chemotype increased adult biomass (1.1-fold) and fecundity were found (2.6- to 4.5-fold) compared with those fed leaves of the viridiflorol chemotype. Regardless of the larval diet, when adults were fed the E-nerolidol chemotype leaves they had greater egg production compared with those adults fed the viridiflorol leaves. Moreover, adult pre-oviposition period was extended (1.5-fold) when individuals were fed the viridiflorol leaves compared with those fed the E-nerolidol leaves. By rearing the O. vitiosa weevil on the more nutritious chemotype plants these results assisted in the mass production and establishment of the M. quinquenervia biological control agent.     

Predictable risk to native plants in weed biological control

Data on field host use of 112 insects, 3 fungi, 1 mite, and 1 nematode established for biological control of weeds in Hawaii, the continental United States, and the Caribbean indicate that the risk to native flora can be judged reliably before introduction. Virtually all risk is borne by native plant species that are closely related to target weeds. Fifteen species of insects introduced for biological control use 41 native plant species; 36 of which are congeneric with target weeds, while 4 others belong to two closely allied genera. Only 1 of 117 established biological organisms uses a native plant unrelated to the target weed. Thus the elements of protection for the native flora are the selection of weed targets that have few or no native congeners and the introduction of biological control organisms with suitably narrow diets.     

Examination of sex attractants for monitoring weed biological control agents in Hawaii

The identification of sex attractants was undertaken for potential use in the study of two biological control agents against Rubus spp. in Hawaii. Attractants for Croesia zimmermani (Lepidoptera: Tortricidae) and Schreckensteinia festaliella (Lepidoptera: Heliodinidae) were developed by field screening a variety of putative lures in sticky traps, based on attractants for congeneric species. Croesia zimmermani was most attracted to E11-tetradecen-1-ol and E11-tetradecenal, while S. festaliella was attracted to (10,12)-(E,E)-hexadecadienal alone. Development of monitoring systems based on sex attractants can enable better evaluation of biocontrol programmes, and provide cost-effective information on presence/absence, density, phenology, synchrony with the host, dispersal rate and other useful parameters.     

The biology and host specificity of the onion weed rust, Puccinia barbeyi, a potentially useful agent for biological control in Australia

Onion weed, Asphodelus fistulosus L., (Liliaceae) a weed of Mediterranean and Middle Eastern origin is widespread in southern Australia where it invades pastures making them unsuitable for grazing. A program of research is underway to discover natural enemies of this plant and to study their possible role in the biological control of onion weed. A rust fungus Puccinia barbeyi (Roum.) Magnus has been found to severely attack A. fistulosus . Observations on the biology of the rust confirmed that it is monoecious and microcyclic and multiplied essentially by aecial and telial stages, although occasionally urediniospores also appeared among teliospores. Several members of the Liliaceae exposed to the aeciospores of the rust remained unattacked indicating that it is most probably specific to Asphodelus spp. and thus its potential for the biological control of A. fistulosus in Australia should be studied further.     

Refining the conditions for sympatric ecological speciation

Can speciation occur in a single population when different types of resources are available, in the absence of any geographical isolation, or any spatial or temporal variation in selection? The controversial topics of sympatric speciation and ecological speciation have already stimulated many theoretical studies, most of them agreeing on the fact that mechanisms generating disruptive selection, some level of assortment, and enough heterogeneity in the available resources, are critical for sympatric speciation to occur. Few studies, however, have combined the three factors and investigated their interactions. In this article, I analytically derive conditions for sympatric speciation in a general model where the distribution of resources can be uni‐ or bimodal, and where a parameter controls the range of resources that an individual can exploit. This approach bridges the gap between models of a unimodal continuum of resources and Levene‐type models with discrete resources. I then test these conditions against simulation results from a recently published article (Thibert‐Plante & Hendry, 2011, J. Evol. Biol. 24 : 2186–2196) and confirm that sympatric ecological speciation is favoured when (i) selection is disruptive (i.e. individuals with an intermediate trait are at a local fitness minimum), (ii) resources are differentiated enough and (iii) mating is assortative. I also discuss the role of mating preference functions and the need (or lack thereof) for bimodality in resource distributions for diversification.     

Host specificity ofDisonycha argentinensis [Col.: Chrysomelidae], an agent for the biological control ofalternanthera philoxeroides (Alligator weed) in Australia

The biology and host specificity of a South American flea beetle,Disonycha argentinensis Jacoby was investigated in quarantine facilities in Australia. Damage from feeding by larvae and adults ofD. argentinensis onAlternanthera philoxeroides (Mart.) Griseb (alligator weed) indicated that it might be a useful biological control agent for the plant when growing in terrestrial situations. Complete development of the immature stages took place only onAlternanthera philoxeroides. Adults produced a few feeding scars onBeta vulgaris L. (beetroot) andAmaranthus spinosus L. (spiny amaranth) but failed to oviposit. Host specificity studies indicated that establishment of this beetle in Australia would be without significant risk to nontarget plant species.D. argentinensis was first released in Australia in 1980.     

Sex ratio effects on copulation,fecundity and progeny fitness for Agasicles hygrophila,a biological control agent of alligator weed

Determining the best ratio of females to males of an insect's natural enemy is important for maximising population increase and promoting population establishment of a natural enemy. In this study, copulation behaviour, fecundity, progeny fitness and rate of population increase for the flea beetle, Agasicles hygrophila Selman & Vogt (Coleoptera: Chrysomelidae), were compared at different female percentage treatments (i.e., 80%, 66.7%, 50%, 33.3% and 20% females). The results showed that the copulation frequency and duration in males decreased, whereas those in females increased as the number of males increased. At 20%, 33.3% and 66.7% females, the rates of population increase were 3.4-, 2.17- and 0.79-fold higher than that at 50% females. Females at 20% and 33.3% were found to be optimal for mass rearing of the beetle.     

Prerelease efficacy test of the psyllid,Arytinnis hakani,a prospective biological control agent of the invasive weed Genista monspessulana

In weed biological control, conducting a prerelease efficacy test can help ascertain if prospective biological control agents will be capable of controlling the target plant. Currently, the phloem-feeding psyllid, Arytinnis hakani, is being evaluated as a prospective agent for the exotic invasive weed, Genista monspessulana, in the USA. Small potted plants were exposed to 0, 4, 8, 12 or 16 A. hakani second-instar nymphs which were allowed to develop on the plants for six weeks in an incubator at 18°C. Increasing A. hakani densities had a significant negative impact on the number of leaflets grown, per cent change in plant height and the final number of leaflets per centimeter of plant height. Increase in plant height and the number of leaflets relative to uninfested plants were reduced by 16 and 29%, respectively, at the highest infestation levels. Psyllids did not increase leaf senescence. One of the 10 plants that was exposed to 16 psyllids died, whereas none of the others died. Weekly nymphal mortality was 10–18% at the lowest density (four psyllids), but was at least 40% at the three highest densities. Although dead nymphs were replaced weekly, insect mortality may have reduced impact on the plants, especially at the higher densities. This insect is multivoltine, so prolongation of the infestation period may have a greater impact on the plant.     

Constraints in weed biological control: contrasting responses by implementing nations

The compilation of papers in this Special Issue (SI) derives from a Symposium at the 25th International Congress of Entomology, in 2016, entitled “Rise or demise? A global outlook on the future of classical biological weed control”. In the SI-opening-paper, a summary of the 5th edition of the world catalogue of weed biocontrol agents and their target weeds provides a comprehensive international perspective. Weed biocontrol implementation is beleaguered by perceptions of risk and restrictive regulatory procedures, notably in the USA, and less so in Canada. Thus, most of the papers in this SI comprise accounts of innovative responses to these challenges from scientists in the USA. Political and funding issues have inhibited weed biocontrol in Australia over the past decade, but there appears to be a gradual reversal of this trend in recent years. In contrast, in New Zealand and in South Africa, the practice is flourishing, and there are significant recent initiatives in Europe. Overall, the contributions in the SI suggest an optimistic prognosis for weed biological control.     

Phytophagous insects found onSalsola in Turkey during exploration for biological weed control agents for California

A total of 50 species of phytophagous insects were collected from Russian thistle (Salsola iberica Sennen & Pau),S. kali L.,S. tragus L., and their apparent hybrids in Turkey during June and July, 1970. These collections contained many new host-plant and locality records forSalsola insects. Among the natural enemies detected and thought to warrant further consideration as agents worth importing for the biological control of Russian thistle in California were:Piesma salsolae (Becker) (Hemiptera-Heteroptera: Piesmatidae); Coleophora klimenoschiella Toll (Lepidoptera: Coleophoridae); an unidentified species ofPhycitidae (Lepidoptera), and an undeterminedLixus sp. (Coleoptera: Curculionidae). Coleophora parthenica Meyrick, scheduled for initial release in California for the biological control of Russian thistle in early-1973, also is reported for the first time from Turkey.     

Seed preferences by rodents in the agri‐environment and implications for biological weed control

Post‐dispersal seed predation and endozoochorous seed dispersal are two antagonistic processes in relation to plant recruitment, but rely on similar preconditions such as feeding behavior of seed consumers and seed traits. In agricultural landscapes, rodents are considered important seed predators, thereby potentially providing regulating ecosystem services in terms of biological weed control. However, their potential to disperse seeds endozoochorously is largely unknown. We exposed seeds of arable plant species with different seed traits (seed weight, nutrient content) and different Red List status in an experimental rye field and assessed seed removal by rodents. In a complementary laboratory experiment, consumption rates, feeding preferences, and potential endozoochory by two vole species (Microtus arvalis and Myodes glareolus) were tested. Seed consumption by rodents after 24 h was 35% in the field and 90% in the laboratory. Both vole species preferred nutrient‐rich over nutrient‐poor seeds and M. glareolus further preferred light over heavy seeds and seeds of common over those of endangered plants. Endozoochory by voles could be neglected for all tested plant species as no seeds germinated, and only few intact seeds could be retrieved from feces. Synthesis and applications. Our results suggest that voles can provide regulating services in agricultural landscapes by depleting the seed shadow of weeds, rather than facilitating plant recruitment by endozoochory. In the laboratory, endangered arable plants were less preferred by voles than noxious weeds, and thus, our results provide implications for seed choice in restoration approaches. However, other factors such as seed and predator densities need to be taken into account to reliably predict the impact of rodents on the seed fate of arable plants.