Complex interactions among fish, snails and macrophytes: implications for biological control of an invasive snail

The golden apple snail (Pomacea canaliculata), a native of freshwater wetlands of South America, has invaded many Asian countries and grazed heavily in agricultural and wild areas. Common carp (Cyprinus carpio) has been proposed as a biological control agent against this snail, but little is known about its impact on non-target aquatic plants and animals. In a 8-week enclosure experiment, we quantified the impact of common carp on three species of aquatic macrophytes and nine species of snails, including the apple snail, in a shallow pond. The results showed that the apple snail or carp alone significantly reduced the plant biomass, although the apple snail had a stronger overall herbivorous effect than the carp. The carp completely removed juvenile apple snails, but had only a weak predatory effect on larger apple snails and no effect on the adults’ oviposition frequency. Furthermore, the carp significantly reduced the populations of most species of other snails that occurred naturally in the pond. Our results thus indicate that common carp can be an effective biological control agent against the invasive apple snail, but caution should be taken about its potential to reduce wetland floral and faunal diversity.     

Evolution in invasive plants: implications for biological control

Evidence is increasing that invasive plants can undergo rapid adaptive evolution during the process of range expansion. Here, we argue that evolutionary change during invasions will also affect plant-antagonist interactions and, thus, will have important implications for biological control programmes targeted at invasive plants. We explore how altered selection in the new range might influence the evolution of plant defence (resistance and tolerance) and life history. The degree to which such evolutionary processes might affect biological control efficacy is largely unexplored. We hope that, by testing the hypotheses that we propose here, a closer link can be established between biological control and evolutionary biology, to the benefit of both disciplines.     

Riverine macrophytes control seasonal nutrient uptake via both physical and biological pathways

1. In low-gradient, macrophyte-rich rivers, we expect that the significant change in macrophyte biomass among seasons will strongly influence both biological activity and hydraulic conditions resulting in significant effects on nutrient dynamics. Understanding seasonal variation will improve modelling of nutrient transport in river networks, including annual estimations of export, which could optimise decision-making and management outcomes.
2. We explored the relationships among seasonal differences in reach-scale nutrient uptake, macrophyte abundance, solute transport and transient storage in the River Gudenå (Denmark), a large macrophyte-rich river. We used the minimal pulse addition technique to measure uptake of ammonium, nitrate, soluble reactive phosphorus, as well as reach-scale metabolism, and surface transient storage in spring, summer, and autumn.
3. We found that riverine uptake changed among seasons and was linked to macrophyte biomass via both biological activity, reflected in reach-scale metabolism, and through physical processes, as solute transport was influenced by longitudinal dispersion. In this macrophyte-rich river, seasonal changes in macrophyte biomass affected contact time between the water and biota, which influenced ammonium and soluble reactive phosphorus uptake. Using stoichiometric scaling of reach-scale metabolism, we found that seasonal variation also influenced the relative contributions of autotrophic and heterotrophic biota in assimilatory uptake.
4. In summary, riverine nutrient uptake was not static, highlighting the importance of seasonality, with significant implications for modelling of nutrient export in river networks. Moreover, current management strategies that remove macrophyte biomass (i.e. weed cutting and dredging) will short-circuit the positive effects of enhanced nutrient uptake resulting from abundant macrophytes in rivers.

     

Flooding compromises compensatory capacity of an invasive plant: implications for biological control

Plant compensatory growth is proposed to be insidious to biological control and known to vary under different environmental conditions. However, the effects of microsite conditions on compensation capacity and its indirect impacts on biological control of plant invaders have received little attention. Alligator weed, Alternanthera phioxeroides, is an invasive plant worldwide, growing in both aquatic and terrestrial habitats that are often affected by flooding. Biological control insects have been successful in suppressing the plant in many aquatic habitats but have failed in terrestrial habitats. To evaluate the impact of flooding on compensation capacity, we conducted common garden and greenhouse experiments in which plants were grown under different moisture conditions (aquatic versus terrestrial). Our results show that plants were able to fully recover from continued herbivory in the terrestrial habitat, but failed in the aquatic habitat, indicating a flooding-regulated plant compensatory capacity. Also, the grazed plants increased below-ground growth and reproductive root bud formation in the terrestrial habitat, but there was no such difference in the aquatic habitat. Our findings suggest that the differing plant compensatory capacity, affected by flooding, may explain the different biological control efficacy of alligator weed in aquatic and terrestrial habitats. Understanding mechanisms in plant invader compensation in different microsite conditions is important for improving management efficiency.     

Fungal associations in Asphondylia (Diptera: Cecidomyiidae) galls from Australia and South Africa: implications for biological control of invasive acacias

Gall-forming Asphondylia are well represented on Australian Acacia and have potential for biological control where Australian acacias cause ecological or economic harm, particularly South Africa. Asphondylia in Australia and South Africa are associated with communities of fungi in their galls. In Australia, Botryosphaeria dothidea (as its Dichomera synanamorph) is the most abundant and sometimes the only fungus present and is implicated as the primary species forming a mutualistic relationship with Asphondylia. In the combined analysis of ITS and elongation factor 1-α sequence data, isolates of B. dothidea from Australia and South Africa form distinct sub-clades. Female Asphondylia carry B. dothidea (as Dichomera conidia) in mycangia located posterior to sternite 7. While conidia are always present on field-collected specimens, laboratory-reared females rarely carry conidia. The mechanism and location of spore collection remains unresolved, but needs to be understood if Asphondylia species are to be utilised for biological control of invasive Australian acacias. As B. dothidea is a polyphagous plant pathogen capable of infecting crops of economic importance, including Acacia plantations, the introduction of novel strains of B. dothidea associated with biological control of acacia is undesirable, however endemic forms of the fungus could possibly be exploited by introduced Asphondylia.     

No evidence for evolutionarily decreased tolerance and increased fitness in invasive Chromolaena odorata: implications for invasiveness and biological control

Tolerance, the degree to which plant fitness is affected by herbivory, is associated with invasiveness and biological control of introduced plant species. It is important to know the evolutionary changes in tolerance of invasive species after introduction in order to understand the mechanisms of biological invasions and assess the feasibility of biological control. While many studies have explored the evolutionary changes in resistance of invasive species, little has been done to address tolerance. We hypothesized that compared with plants from native populations, plants from invasive populations may increase growth and decrease tolerance to herbivory in response to enemy release in introduced ranges. To test this hypothesis, we compared the differences in growth and tolerance to simulated herbivory between plants from invasive and native populations of Chromolaena odorata, a noxious invader of the tropics and subtropics, at two nutrient levels. Surprisingly, flower number, total biomass (except at high nutrient), and relative increase in height were not significantly different between ranges. Also, plants from invasive populations did not decrease tolerance to herbivory at both nutrient levels. The invader from both ranges compensated fully in reproduction after 50?% of total leaf area had been damaged, and achieved substantial regrowth after complete shoot damage. This strong tolerance to damage was associated with increased resource allocation to reproductive structures and with mobilization of storage reserves in roots. The innately strong tolerance may facilitate invasion success of C. odorata and decrease the efficacy of leaf-feeding biocontrol agents. Our study highlights the need for further research on biogeographical differences in tolerance and their role in the invasiveness of exotic plants and biological control.     

Intraguild interactions between two biological control agents in citrus fruit: implications for biological control of medfly

The parasitoid wasp Spalangia cameroni and the predatory beetle Pseudoophonus rufipes have long been studied for use as biological control agents against the Mediterranean fruit fly Ceratitis capitata, particularly in citrus fruit orchards. Nevertheless, these two species of natural enemies, when competing for a common resource, may experience intraguild predation (IGP) interactions. These possible interactions, affecting parasitism and predation, have been evaluated in the present work, under laboratory conditions, through potential changes in functional response. Regarding host/prey density, both natural enemies, when acting alone, showed a type II functional response. Nevertheless, due to IGP, S. cameroni, in the presence of P. rufipes, showed a higher fertility rate and a type III functional response. The parasitism behaviour of S. cameroni was affected by the presence of the predator, reducing the host handling time. Conversely, the parasitism rate of S. cameroni did not vary in the presence of P. rufipes but the degree of superparasitism decreased and led to an increased fertility rate and an increasingly female‐biased sex ratio. Meanwhile, the predatory efficiency of P. rufipes was not affected by the presence of S. cameroni but discrimination between parasitised and unparasitised pupae of C. capitata, with a preference for the latter, was reported for this predator species. Our results suggest that in biological control programmes, the use of only one of these species is recommended at low infestation levels, whilst at high densities of the pest, the combination of both natural enemies seems to be the most appropriate strategy.     

Multi-generational effects of simulated herbivory and habitat types on the invasive weed Alternanthera philoxeroides: implications for biological control

Long-term pre-release evaluations of how invasive plants respond to herbivory in introduced ranges can help identify the most effective biological control agents. However, most evaluations have been conducted within only one generation of introduced invasive species. This study tested effects across seven generations of simulated herbivory (i.e., defoliation) and habitat types on the invasive weed Alternanthera philoxeroides. We found total biomass of A. philoxeroides was decreased by defoliation during the first three generations when grown in a simulated aquatic habitat, but was decreased by defoliation only in the first generation when grown in a simulated terrestrial habitat. Defoliation significantly decreased stem diameter and collenchyma thickness and increased cortex thickness and total phenol production in A. philoxeroides grown in a simulated terrestrial or aquatic habitat during the first generation, but showed little effect during the following six successive generations. The associations between stem anatomical structural parameters and biomass significantly differed between non-defoliation and defoliation treatments in the simulated aquatic habitat, but not in the simulated terrestrial habitat. Our results suggest simulated herbivory exerted successful biological control on A. philoxeroides during the first generation in a simulated terrestrial habitat and the first three generations in a simulated aquatic habitat, but failed to restrain the vegetative offspring of A. philoxeroides. This failure of long-term biological control on A. philoxeroides might be caused by changes in the stem anatomical structure and compensatory growth. Our study highlights the need for long-term pre-release evaluation when testing the efficiency of biological control agents.

     

Cross-correlation analysis of invasive mango mealybug and its associated natural enemies in relation to meteorological factors: implications for biological control

Damage caused by invasive downey snow line mealybug, Rastrococcus iceryoides Green (Hemiptera: Pseudococcidae) has been reported to vary between 30% to complete crop loss where no control measure is applied. The current studies seek to determine factors influencing R. iceryoides population outbreaks, parasitoid – host and predator–prey relationships as well as predict optimal management strategies through weather modelling over a period of 28 months from 2008 to 2010 in Tanzania. The highest incidence of R. iceryoides was recorded during the dry season coinciding with the major mango fruiting season. The relationship between R. iceryoides and the parasitoid was positive but not significant, which implies the influence on outbreaks was negligible probably due to low percent parasitism (<12%). However, the predator abundance was directly and significantly related to that of R. iceryoides. Average temperature, average relative humidity, rainfall, and R. iceryoides abundance were autocorrelated to each other. Cross-correlation coef?cients vary significantly from ?0.286 to 0.589 for the pair-variable between R. iceryoides, temperature, relative humidity, rainfall, parasitism and predators. Our findings showed that temperature was the key climatic variable that significantly influenced R. iceryoides outbreaks while rainfall was significantly negatively associated with the pest. Time series analyses show R. iceryoides population increased 4 months after an increase in average temperature in all the sites, 11 months after rainfall and 11 months after relative humidity in Kibaha and Dar es Salaam, respectively. Our findings revealed that R. iceryoides is an excellent target for classical biological control. Thus, the importation of promising co-evolved parasitoid specific to R. iceryoides from the aboriginal home is crucial in formulating an efficient and sustainable management approaches against the invasive mealybug pest in mango agro-ecosystems.     

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.     

Web-site selection strategies of linyphiid spiders in alfalfa: implications for biological control

Site-specific foraging can enhance the ability of generalist predators to provide effective and sustainable levels of pest control in agroecosystems. This can result from increased growth rates, higher population densities, and improved capture frequencies of pests at high prey density microsites. We tested the hypothesis that linyphiid spiders would exhibit microhabitat-specific web-site selection strategies in alfalfa. This was predicted to result in high prey densities at web-sites compared to paired non-web-sites through direct, or indirect, selection of prey-rich habitats. A total of 22,242 potential prey items were collected from mini-sticky traps located at 896 microsites. Web-centered mini-sticky traps on the ground, representative of Erigone autumnalis Emerton (Araneae: Linyphiidae) webs, captured similar numbers of potential prey as paired non-web-centered traps nearby. However, aerial sticky traps at web-sites of Bathyphantes pallidus (Banks) (Araneae: Linyphiidae) contained significantly more Diptera and Empoasca fabae (Harris) (Homoptera: Cicadellidae) than paired non-web-centered sticky-traps. Prey activity-densities also varied between web-sites of E. autumnalis and B. pallidus. Diptera were dominant at aerial microsites of B. pallidus whilst Collembola were abundant on ground-based traps of E. autumnalis. These results suggest that in alfalfa, the pressure for selecting prey-rich web-sites by erigonine spiders is low, but B. pallidus exhibits a selective web-location strategy targeted towards high quality dipteran prey. These sites also captured large numbers of E. fabae, a major pest of alfalfa, thus implicating aerial-based linyphiines as valuable predators in biological control.     

Models for integrated pest control and their biological implications

Successful integrated pest management (IPM) control programmes depend on many factors which include host-parasitoid ratios, starting densities, timings of parasitoid releases, dosages and timings of insecticide applications and levels of host-feeding and parasitism. Mathematical models can help us to clarify and predict the effects of such factors on the stability of host-parasitoid systems, which we illustrate here by extending the classical continuous and discrete host-parasitoid models to include an IPM control programme. The results indicate that one of three control methods can maintain the host level below the economic threshold (ET) in relation to different ET levels, initial densities of host and parasitoid populations and host-parasitoid ratios. The effects of host intrinsic growth rate and parasitoid searching efficiency on host mean outbreak period can be calculated numerically from the models presented. The instantaneous pest killing rate of an insecticide application is also estimated from the models. The results imply that the modelling methods described can help in the design of appropriate control strategies and assist management decision-making. The results also indicate that a high initial density of parasitoids (such as in inundative releases) and high parasitoid inter-generational survival rates will lead to more frequent host outbreaks and, therefore, greater economic damage. The biological implications of this counter intuitive result are discussed.     

Parasitism and dispersal potential of Sirex noctilio: implications for biological control

1 Sirex noctilio F. (Hymenoptera: Siricidae) is a wood‐boring wasp that attacks many pine species, including commercial trees planted throughout the world. Management of its populations is largely based on biological control using the nematode Beddingia siricidicola. Adult females are sterilized by the nematode, but are free to move and attack new trees, promoting nematode dispersal. Although generally successful, wasp management through nematode introductions has sometimes been inadequate. 2 We evaluated the effect of parasitism by B. siricidicola on flight performance of woodwasps under laboratory conditions. Using flight mills, we recorded a total of 46 flight trials over 23 h, obtained from infected and control (uninfected) females. 3 Although all wasps lost weight during flight, parasitized females were significantly smaller and suffered larger weight losses than uninfected females. In addition, total flight distance and velocity were lower in parasitized females. 4 Because nematode infection transmission relies on healthy wasps attacking trees previously visited by nematode‐bearing females, differential dispersal capacity could limit biological control success.     

Patterns of parasitoid host utilization and development across a range of temperatures: implications for biological control of an invasive forest pest

Although climate change frequently has been linked to observed shifts in the distributions or phenologies of species, little is known about the potential effects of varying temperatures on parasitoids and their relationships with hosts. Using the egg parasitoid Oobius agrili (Hymenoptera: Encyrtidae) we examined host utilization patterns of this species across a range of temperatures (20–35 °C) to explore how changing climate could affect the interaction with its host—the emerald ash borer (EAB) (Coleoptera: Buprestidae), a serious invasive forest pest that has killed tens of millions of ash (Fraxinus spp.) trees in North America. Results from our study showed that the window of host susceptibility to O. agrili parasitism declined significantly from 14.8 to 2.6 days in an inverse second-order relationship with increasing exposure temperatures from 20 to 35 °C. In contrast, parasitoid host attack rate changed in a bell-shaped second-order relationship—i.e., increased with temperatures from 20 to 25 °C, but decreased at about the same rate when temperatures increased from 30 to 35 °C. This range of temperatures also significantly affected the development and mortality of immature parasitoids with 35 °C resulting in 100 % mortality. There was little mortality (0–4.5 %) and no significant differences in the percentage (20.9–34.9 %) of immature O. agrili that entered diapause (as mature larvae) at 20, 25, and 30 °C. However, there were significant differences in the time event of adult wasp emergence within this temperature range. The median time for 50 % of immature O. agrili emerging as adults at 20, 25, and 30 °C were 38, 18, and 17 days after parental wasp oviposition, respectively. Together these findings indicate that the non-linear and unequal temperature effects on these host utilization parameters are likely to result in differential host parasitism rates, and thus could reduce the efficacy of this parasitoid in suppressing host populations due to climate change (global warming and extreme heat).     

The potential for biological control of invasive alien aquatic weeds in Europe: a review

A retrospective analysis shows that invasive, alien, free-floating and emergent aquatic weeds in Europe are good targets for classical biological control, and that genus-specific chrysomelid and curculionid beetles offer the most potential. Ludwigia spp., Azolla filiculoides, Lemna minuta, Crassula helmsii and Hydrocotyle ranunculoides should be prioritised as targets. Fungal pathogens have been under-utilised as classical agents but, whilst they may have some potential against free-floating weeds, they appear to be poor candidates against submerged species, although the suitability of arthropod agents against these difficult targets still merits investigation. The use of indigenous pathogens as inundative agents (mycoherbicides) shows some promise.     

Extreme winter aggregation of invasive rainbow trout in small tributaries: implications for effective control

Because of their high economic and recreational value, salmonids have been extensively introduced worldwide and are responsible for significant impacts on native ecosystems. However, effective methods for controlling or eradicating introduced populations of salmonids are still limited, particularly in large river systems. Here, we demonstrated that invasive rainbow trout Oncorhynchus mykiss immigrated to and extremely aggregated in small tributaries during the winter, which can be utilized for effective population control. Seasonal census was conducted in 10 small tributaries of the Otofuke River in the Tokachi River basin, central Hokkaido, Japan. Winter abundance was 8–125 times higher than summer abundance in four of the tributaries where water velocities were low. Relatively large individuals (200–350 mm) aggregated in several pools at an unusually high density (>2–3 individuals/m² or 170–440 individuals per pool). Females were common in the small tributaries in the winter, but not in the summer. Therefore, removal of invasive rainbow trout may be best practised in such small tributaries during early winter. Because many stream fishes overwinter in specific, often limited, habitats, more attention should be paid to such winter habits in the effective management of non-native fish species.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.