A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.     

Nematophagous fungi: prospective biological control agents of animal parasitic nematodes?

The rapidly escalating problem of anthelmintic resistance and the increasing concerns of chemical residues in livestock products and the environment pose serious threats to the future of chemotherapeutic control o f animal parasitic nematodes. One possible non-chemotherapeutic approach is biological control using nemotophagous fungi. Although Gr?nvold and colleagues recently described their experiments with two nematode-destroying fungi, Arthrobotrys and Duddingtonia, this alternate control option has received relatively little research attention. Here, Peter Waller broadens the discussion to consider the fundamental problems and prospects of this non-chemotheropeutic control strategy.     

Is Puccinia xanthii a suitable biological control agent of Ambrosia artemisiifolia?

Common ragweed, Ambrosia artemisiifolia, is a highly allergenic North American plant that has become invasive in some parts of Europe, Asia and Australia following its introduction to many places in the world. Some earlier works suggested that a microcyclic autoecious rust fungus, Puccinia xanthii, known to infect A. artemisiifolia in the USA only, can be considered as a potential classical biocontrol agent (BCA) of this noxious weed in Europe and elsewhere. However, an extensive field survey did not reveal the presence of either P. xanthii or any other rusts on common ragweed in 14 US states and two Canadian provinces in 2002 and 2003. Moreover, P. xanthii infecting A. artemisiifolia has never been recorded in Canada, although it is known to occur on A. trifida and Xanthium spp. there. Nevertheless, herbarium specimens collected between 1855 and 1963 in five states of the USA confirmed the presence of P. xanthii on A. artemisiifolia. It is concluded that currently P. xanthii cannot be regarded as a promising BCA of A. artemisiifolia, although it did occur on common ragweed at least a few decades ago in the USA and some forms of this rust species have already been evaluated as effective BCAs of Xanthium in Australia.     

Accumulation,degradation and biological effects of lindane on Scenedesmus obliquus (Turp.) Kütz

A study was made of accumulation, degradation and biological effects of lindane (r-BHC) on Scenedesmus obliquus (Turp.) Kütz. The work was conducted in a sewage reservoir in Han-Ku, Tianjin. Experimental results show that at 0.1–10 mgl⁻¹ concentration of lindane, the growth, chlorophyll and carotene content in S. obliquus do not differ much from the control. At concentrations of 50–100 mgl⁻¹, however, growth is inhibited, and chlorophyll and carotene content is low. From the beginning of the experiment until the fifth day, growth rate and pigment content increase constantly. On the seventh day, they start to decrease. Spectrographic analysis shows that pigment content decreases, but pigment structure is not changed even at high concentration of lindane. At 1–10 mgl⁻¹ of lindane, amino acids remain unchanged, with the exception of aspartine, arginine, methionine and phenylalanine. Scenedesmus obliquus (Turp.) Kütz possesses a certain accumulating capacity for r-BHC, which is higher at 1 mgl⁻¹ than at 10 mgl⁻¹. Accumulation is enhanced with time and is better under turbulent conditions. Gas chromatograms show that after treatment for 24 h, there are two more peaks at retention time 1′32″ and 1′53″, respectively, suggesting that a certain degree of lindane degradation occurs. The nature of these degradation products awaits further study. As a conclusion S. obliquus (Turp.) Kütz holds promise in the treatment of lindane-containing wastewaters in the range of 1–10 mgl⁻¹.     

Genetic control and racial variation of β-glucosidase isozymes in maize (Zea mays L.)

-Glucosidase (-D-glucoside glucohydrolase, E.C. 3.2.1.21, -Glu) isozyme variants were studied in a large number of inbred lines, crosses, and races of maize (Zea mays L.). The pattern of Mendelian inheritance demonstrated for -GLU variants indicated that they are under nuclear gene control. Twenty-two allelic forms at a single locus were identified in the materials studied by starch gel electrophoresis. Genetic data indicate that -GLU in maize is functionally a dimer. Variation of -GLU isozymes in 51 racial collections of maize from Mexico showed little correlation with morphological or geographical data. In 39 collections from Central America, variation patterns appeared to have some association with altitude.This work was supported in part by NIH Research Grant GM 11546.Paper No. 5040 of the Journal Series of the North Carolina Agricultural Experiment Station, Raleigh, North Carolina.     

Spontaneous Gac mutants of Pseudomonas biological control strains: cheaters or mutualists?

Bacteria rely on a range of extracellular metabolites to suppress competitors, gain access to resources, and exploit plant or animal hosts. The GacS/GacA two-component regulatory system positively controls the expression of many of these beneficial external products in pseudomonad bacteria. Natural populations often contain variants with defective Gac systems that do not produce most external products. These mutants benefit from a decreased metabolic load but do not appear to displace the wild type in nature. How could natural selection maintain the wild type in the presence of a mutant with enhanced growth? One hypothesis is that Gac mutants are "cheaters" that do not contribute to the public good, favored within groups but selected against between groups, as groups containing more mutants lose access to ecologically important external products. An alternative hypothesis is that Gac mutants have a mutualistic interaction with the wild type, so that each variant benefits by the presence of the other. In the biocontrol bacterium Pseudomonas chlororaphis strain 30-84, Gac mutants do not produce phenazines, which suppress competitor growth and are critical for biofilm formation. Here, we test the predictions of these alternative hypotheses by quantifying interactions between the wild type and the phenazine- and biofilm-deficient Gac mutant within growing biofilms. We find evidence that the wild type and Gac mutants interact mutualistically in the biofilm context, whereas a phenazine-defective structural mutant does not. Our results suggest that the persistence of alternative Gac phenotypes may be due to the stabilizing role of local mutualistic interactions.     

Sequential control of phytochrome-mediated synthesis de novo of β-amylase in the cotyledons of mustard (Sinapis alba L.) seedlings

In the cotyledons of mustard (Sinapis alba L.) seedlings irradiated from the time of sowing with continuous red light, the photoreversibility of the phytochrome-mediated increase in -amylase activity (EC 3.2.1.2) is lost 36 h after sowing (coupling point). However, the induced increase of -amylase activity cannot be detected before 46 h after sowing (starting point). Density labeling with deuterium oxide shows that the increase of enzyme activity in light and darkness coincides precisely with the synthesis of -amylase protein. Thus, phytochrome mediates an increase of -amylase synthesis de novo. Since there is no turnover detectable by density labeling, it is concluded that -amylase of mustard cotyledons is a physiologically stable enzyme (half-life >5 d). The 10-h time gap between loss of photoreversibility and onset of light-induced -amylase synthesis points to a relatively stable regulatory element within the signal chain (transmitter) which links -amylase synthesis to the primary action of phytochrome. A 12-h lag between the cessation of phytochrome action and the cessation of induced -amylase synthesis indicates a limited lifetime of the transmitter (about 12 h). The effect of this result on the interpretation of the coupling point is discussed.Abbreviations P_r, P_fr red and far-red absorbing forms of phytochrome     

Can cruciferous agroecosystems grown under variable conditions influence biological control of Plutella xylostella (Lepidoptera: Plutellidae)?

Determining the most efficacious method for the release of parasitoids is challenging, depending on the crop area to be covered and the environmental conditions created by the agroecosystem. Release of the parasitoid Oomyzus sokolowskii (Kurdjumov) and the effect of crucifers cropping systems were investigated in relation to diamondback moth (DBM), Plutella xylostella (L.) control. First, we investigated the dispersal ability of O. sokolowskii. Kale plants were infested with 20, 25, 30 and 35 DBM larvae each, at distances of 0, 8, 16, and 24 m, from a central release point in the field. Second, the effect of a multiple host plant system composed of cabbage, broccoli and Napa cabbage on the parasitism capacity of O. sokolowskii was investigated. Lastly, the parasitism capacity of O. sokolowskii and the colonization rate of DBM were investigated comparing cropping systems composed of either a monoculture of cabbage, or three different intercropping systems: cabbage and green onion, cabbage and cilantro, and cabbage, green onion and cilantro. For all experiments, selected plants were infested with sentinel DBM larvae and caged with mesh that allowed parasitoids to search inside the cages while reducing the impact of opportunists on DBM larvae. Results showed that parasitoids were able to disperse and parasitize P. xylostella at similar rates throughout a field of kale up to 24 m from the release point. Intercropping of cabbages with other crop plants did not negatively affect parasitism rates of O. sokolowskii, which makes it promising for DBM biological control; however it did not interfere with cabbage colonization by DBM.     

Effects of global environmental changes on parasitoid–host food webs and biological control

Global environmental changes threaten biodiversity and the interactions between species, and food-web approaches are being used increasingly to measure their community-wide impacts. Here we review how parasitoid–host food webs affect biological control, and how their structure responds to environmental change. We find that land-use intensification tends to produce webs with low complexity and uneven interaction strengths. Dispersal, spatial arrangement of habitats, the species pool and community differences across habitats have all been found to determine how webs respond to landscape structure, though clear effects of landscape complexity on web structure remain elusive. The invasibility of web structures and response of food webs to invasion have been the subject of theoretical and empirical work respectively, and nutrient enrichment has been widely studied in the food-web literature, potentially driving dynamic instability and altering biomass ratios of different trophic levels. Combined with food-web changes observed under climate change, these responses of food webs could signal changes to biological control, though there have been surprisingly few studies linking food-web structure to pest control, and these have produced mixed results. However, there is strong potential for food-web approaches to add value to biological control research, as parasitoid–host webs have been used to predict indirect effects among hosts that share enemies, to study non-target effects of biological control agents and to quantify the use of alternative prey resources by enemies. Future work is needed to link food-web interactions with evolutionary responses to the environment and predator–prey interactions, while incorporating recent advances in predator biodiversity research. This holistic understanding of agroecosystem responses and functioning, made possible by food-web approaches, may hold the key to better management of biological control in changing environments.     

What makes a successful biocontrol agent? A meta-analysis of biological control agent performance

We qualitatively reviewed the biocontrol literature in two major journals, Biological Control and Environmental Entomology, over the past 10 years by scoring 878 studies into 11 biocontrol-oriented questions. Quantitative meta-analyses were then used on data from 145 studies to examine the effects of different types of biocontrol agents (parasitoids, predators, and pathogens) on several attributes of weed and pest populations. Results for our qualitative review showed that most biocontrol studies were focused on lepidopteran pests, and that parasitoids were the most common biocontrol agents used. Our quantitative review showed that, for weeds, biocontrol agents significantly reduced weed biomass (−82.0%), flower (−98.9%), and seed production (−89.4%). For pests, our quantitative review showed that biocontrol agents significantly reduced pest abundance by 130% compared to control groups, increased parasitism (+139.0%) and increased overall pest mortality (+159.0%) compared to targets not exposed to biocontrol agents. Effects on pest mortality tended to be stronger for parasitoids than predators, although reductions caused in pest abundance were much stronger when predators were used as biocontrol agents. Addition of two or more biocontrol agents increased mortality by 12.97% and decreased pest abundance by 27.17% compared to single releases. Separate sets of meta-analyses demonstrated that the negative impacts of biocontrol on non-target species were much smaller than those for target species, although adverse effects of biocontrol on non-target organisms are based on small sample sizes and should be interpreted with caution. Our results also showed that biocontrol efficacy tended to be higher when agents were generalists than when they were specialists. Large fail–safe numbers found for most of the estimated effects indicate the robustness of the results found for the efficacy of biological control programs.     

Dynamical behaviour of biological regulatory networks—II. Immunity control in bacteriophage lambda

A number of bacterial and viral genes take part in the decision between lysis and lysogenization in temperate bacteriophages. In the lambda case, at least five viral genes (cI, cro, cII, N and cIII) and several bacterial genes are involved. Several attempts have been made to model this complex regulatory network. Our approach is based on a logical method described in the first paper of the series which formalizes the interactions between the elements of a regulatory network in terms of discrete variables, functions and parameters. In this paper two models are described and discussed, the first (two-variable model) focused on cI and cro interactions, the second (four-variable model) considering, in addition, genes cII and N. The treatment presented emphasizes the roles of positive and negative feedback loops and their interactions in the development of the phage. The role of the loops between cI and cro, and of cI on itself (which both have to be positive loops) was discovered earlier; this group's contribution to this aspect mainly deals with the possibility of treating these loops as parts of a more extended network. In contrast, the role of the negative loop of cro on itself had apparently remained unexplained. We realized that this loop buffers the expression of genes cro itself, cII, O and P against the inflation due to the rapid replication of the phage. More generally negative auto-control of a gene appears an efficient way to render its expression insensitive (or less sensitive) to gene dosage, whereas a simple negative control would not provide this result.     

The potency of lemon (Citrus limon L.) essential oil to control some fungal diseases of grapevine wood

This study aimed to evaluate the in vitro antifungal activity (AA) of the essential oil (EO) of lemon (Citrus limon L.) against three pathogenic fungi attacking grapevine wood. The composition of the EO was also studied. Ten volatile components were identified by gas chromatography–mass spectrometry. The results showed that the EO consists of volatile components where monoterpene hydrocarbons are the most abundant ones. Four major components were identified, which represent 99.9% of the total EO (limonene, neral, ß-pinene, and ?-terpinene). The AA of the EO was evaluated against three pathogenic fungi attacking grapevine wood (Eutypa sp., Botryosphaeria dothidea, and Fomitiporia mediterranea). The results showed that the EO exerts AA against all tested fungi and significantly inhibits their growth. Eutypa sp. is the most sensitive fungus. These results show, for the first time, a new use for the EO of lemon (C. limon L.) to control fungal diseases of grapevine wood.     

Impact of soil salinity on the plant-growth – promoting and biological control abilities of root associated bacteria

The effectiveness of plant growth – promoting bacteria is variable under different biotic and abiotic conditions. Abiotic factors may negatively affect the beneficial properties and efficiency of the introduced PGPR inoculants. The aim of this study was to evaluate the effect of plant growth – promoting rhizobacteria on plant growth and on the control of foot and root rot of tomatoes caused by Fusarium solani under different soil salinity conditions. Among the five tested strains, only Pseudomonas chlororaphis TSAU13, and Pseudomonas extremorientalis TSAU20 were able to stimulate plant growth and act as biological controls of foot and root rot disease of tomato. The soil salinity did not negatively affect the beneficial impacts of these strains, as they were able to colonize and survive on the roots of tomato plants under both saline and non-saline soil conditions. The improved plant height and fruit yield of tomato was also observed for plants inoculated with P. extremorientalis TSAU20. Our results indicated that, saline condition is not crucial factor in obtaining good performance with respect to the plant growth stimulating and biocontrol abilities of PGPR strains. The bacterial inoculant also enhanced antioxidant enzymes activities thereby preventing ROS induced oxidative damage in plants, and the proline concentrations in plant tissue that play an important role in plant stress tolerance.     

Temperature and the biology and predation of Ilione albiseta (Diptera: Sciomyzidae) — Potential biological control agent of liver fluke

The effect of temperature on predation by Ilione albiseta (Diptera: Sciomyzidae) on Lymnaea peregra was investigated at 14°, 17°, 20°, 23° and 26°C. The mean dry weight of snail tissue (Lymnaea peregra) attacked and consumed per day by first and second instar I. albiseta larvae was highest at 20°C while for third instar and total larval duration period it was greatest at 23°C. The mean number of snails killed per day during the third instar was also highest at 23°C. The total amount of snail tissue consumed by I. albiseta larvae increased significantly from first to second instar and from second to third instar at each constant temperature. Mean survival period of unfed first instar larvae decreased from 28.4 days at 14°C to 11 days at 26°C and the mean length of the second instar cephalopharyngeal skeleton decreased with increasing temperatures. As temperature increased the rate of consumption of oxygen (dissolved in water) by first and third instar larvae rose.     

Increasing floral diversity for selective enhancement of biological control agents: A double-edged sward?

Floral resource subsidies can have differential effects on insect herbivores compared with the herbivores’ natural enemies. While the nectar of many plant species enhances parasitoid fitness, it may also increase damage by herbivores. This may occur as a result of enhanced herbivore fitness or by enhancing fourth-trophic-level processes, possibly disrupting a trophic cascade as a result. The responses of different arthropod guilds to different floral resource subsidies were compared using Plutella xylostella (Hyponomeutidae), its parasitoid Diadegma semiclausum (Ichneumonidae) and data from two other published herbivore–parasitoid systems. These were Dolichogenidea tasmanica (Braconidae) and its host Epiphyas postvittana, and Copidosoma koehleri (Encyrtidae) and its host Phthorimaea operculella. The parasitoids and hosts in the three systems exhibited differential responses to the nectar sources. The differential response was not explained by morphology, demonstrating that physical access to nectaries alone does not determine the potential of flowers as a food source. For some flowering plants, enhancement of herbivore and parasitoid fitness occurred. Other flowering plants, such as buckwheat and phacelia, conferred a selective enhancement on parasitoids by increasing only their fitness. More effective conservation biocontrol may be achieved by the provision of selective floral resources. Attempts to ‘engineer’ agroecosystems to enhance biological control require an extensive knowledge of the ecology of the herbivore, its enemies and their interactions with potential resource subsidies.     

Are indigenous strains of Trichogramma sp. (Hym., Trichogrammatidae) better candidates for biological control of lepidopterous pests of the olive tree?

Strains of the egg parasitoid, Trichogramma, indigenous in olive groves in the Mediterranean region (T. bourarachae Pintureau & Babault, T. cacoeciae Marchal, T. cordubensis Vargas & Cabello, T. euproctidis Girault, T. nerudai Pintureau & Gerding, T. oleae Voegelé & Pointel) as well as commercially available strains (T. brassicae Bezdenko, T. cacoeciae, T. evanescens Westwood), were assessed in laboratory and semi-field experiments for their attributes as biological control agents for use against lepidopterous olive pests like the olive moth (Prays oleae Bern.) and the jasmine moth (Palpita unionalis Hübn.). In a choice test, an Egyptian strain of T. cordubensis parasitized significantly more olive and jasmine moth eggs than those of the rearing host Sitotroga cerealella Olivier. This strain was also most efficient in finding eggs of the target pests on olive foliage and on potted olive trees. Survival and fecundity of a Tunisian strain of T. bourarachae was not affected when exposed to hot (35°C) and arid (< 40% relative humidity) conditions in comparison to the mild standard of 25°C and 70% relative humidity. It was concluded that indigenous strains collected from olive groves were more effective against the target pests and more tolerant to arid conditions than commercially available parasitoid species, indicating that biological control agents should preferably be isolated from the relevant pest/crop system.     

Does experimental evolution produce better biological control agents? A critical review of the evidence

Biological control of crop pests is considered a good alternative or complement to the use of pesticides. However, legislation restricts the importation of natural enemies of pests. A potential way to circumvent this limitation is by using experimental evolution and/or artificial selection to improve native biological control agents. Here, we review studies that have used these methodologies and evaluate their success. Experimental evolution or artificial selection has been used on a wide range of traits, with most focusing on improving the performance of natural enemies in ecologically relevant environments, such as in the presence of pesticides or at different temperatures. Although most studies were poorly replicated, the selected traits generally improved following the selection process. However, correlated responses (often in the form of trade‐offs) with other traits of interest were common. We suggest that the selection procedure can be improved by increasing replication and performing experimental evolution under more semi‐natural environments, to ensure that the most useful traits are being selected.     

Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control

A seminal paper by Howarth (Proc Hawaii Entomol Soc 24:239–244, 1983) entitled “Classical biological control: Panacea or Pandora’s Box” ignited a sometimes acrimonious debate over the relative safety of introductions for classical biological control. Extolled for years as environmentally benign, the litany of negative non-target effects profiled by Howarth heightened awareness of this issue. Several factors have muddied this debate including the conflation of frequency of effects with their strength, grouping the effects of disparate biological control agents together, and the lack of quantitative data on either side of the argument. Here, I examine the potential for non-target effects among insect parasitoids, the most common group used for biological control of arthropods. In response to calls for better quantitative studies, I highlight three different techniques, quantitative food webs, life table analysis, and experimental populations, respectively, to quantitatively assess or reassess non-target effects in different systems. I also explore three methodological approaches employed to ascertain the strength of competitive interactions between native and introduced parasitoids, a potential non-target effect that has received little attention in the literature. These types of studies may greatly increase our understanding of the nature of non-target interactions with introduced parasitoids and bring more rigor to a debate often dominated by rhetoric.