Biological control of insect pests in apple orchards in China

Apple is one of the most important fruits in China, and both yield and quality are greatly affected by insect pests. According to surveys, there are more than 200 species of natural enemies in apple orchards. Few, however, have been closely studied. Major natural enemies including parasitoids, predators and pathogens are briefly described in this review, especially focusing on two parasitoids of Trichogramma dendrolimi Matsumura and Aphelinus mali Haldeman, predatory mites and a pathogenic fungus of Beauveria bassiana (Balsamo) Vuillemin as case studies. Augmentation, one important strategy of biological control, supplements the natural control provided by the existing natural enemy community in apple orchards, and greatly increases their efficiency in controlling pests. Conservation biological control is also widely applied in four major apple-producing areas. Based on habitat manipulation, the ground cover planting system helps regulate the microclimate and enhance the biodiversity of apple orchards, effectively conserving the richness and diversity of beneficial insect species. Certain achievements have been made in the main biological control strategies including successful introduction of some exotic natural enemies such as A. mali and Typhlodromus occidentalis Nesbitt, augmentative production and application of biological control agents such as T. dendrolimi, B. bassiana and Bacillus thuringiensis, and further research in conservation of establishing adaptive ground cover planting patterns to local environment. Challenges, however, still exist. Biological control of insect pests in apple orchards is an important part of integrated pest management programs, requiring more research and application in China.     

Impact of invasive apple snails in Hong Kong on wetland macrophytes,nutrients, phytoplankton and filamentous algae

1. Grazing by invasive species can affect many aspects of an aquatic system, but most studies have focused on the direct effects on plants. We conducted mesocosm and laboratory experiments to examine the impact of the invasive apple snail Pomacea canaliculata on macrophytes, filamentous algae, nutrients and phytoplankton. 2. In a freshwater pond, we confined 500 g of Myriophyllum aquaticum or Eichhornia crassipes with 0, 2, 4 or 8 apple snails in 1 m × 1 m × 1 m enclosures for approximately 1 month. Apple snails grazed heavily on both species of macrophytes, with higher overall weight losses at higher snail densities. The damage patterns differed between the two macrophytes. In M. aquaticum, both leaves and stems suffered from substantial herbivory, whereas in E. crassipes, only the roots suffered significant weight reduction. 3. In addition to grazing on macrophytes, apple snails appeared to have controlled the growth of filamentous algae, as these did not develop in the snail treatments. The ability of P. canaliculata to control filamentous algae was supported by a laboratory experiment where the consumption was as high as 0.25 g g⁻¹ snail DW d⁻¹. Because of a lack of native herbivorous snails in the pond, the growth of filamentous algae (mainly Spirogyra sp.) reached 80.3 g m⁻², forming a spongy pond scum in the no‐apple snail control. Together with previous reports that apple snails could eat the juveniles and eggs of other freshwater snails, our results indicated that P. canaliculata could have out‐competed native herbivorous snails from the pond by predation on their juveniles or eggs. Alternatively, P. canaliculata might have out‐competed them by monopolisation of food resources. 4. Nitrogen and phosphorous concentrations remained low throughout both experiments and were not correlated with apple snail density. The treatment effects on chlorophyll a (Chl a) and phytoplankton composition varied in the two experiments. In the M. aquaticum experiment, with increasing snail density, Chl a increased, and the phytoplankton community became dominated by Cryptophyceae. In the E. crassipes experiment, Chl a level was independent of snail density, but with increasing snail density, the phytoplankton community became co‐dominated by Cryptophyceae, Chlorophyceae and Bacillariophyceae. 5. Given the multiple effects of P. canaliculata on wetland biodiversity and function, management strategies should be developed to prevent its further spread. In invaded wetlands, strategies should be developed to eradicate the apple snail and re‐introduce native snails which can control the development of filamentous algae.     

Comparison of the predation capacities of two soil-dwelling predatory mites,Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae), on three thrips species

Soil-dwelling predatory mites are natural enemies of various soil pest insects and mites. Both Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) are commercialized natural enemies of thrips, but there is little information on the predation rate of these predatory mites on different thrips species. We compared their predation capacities on three thrips species, Frankliniella occidentalis, F. intonsa, and Thrips palmi, which are major pests of various horticultural plants. The predatory rate of G. aculeifer was higher than that of S. scimitus. Both predator species fed on more T. palmi thrips than F. occidentalis or F. intonsa thrips, which may be attributable to the smaller body size of T. palmi than the other thrips. Predation rates of female adults were 2.6–2.8 times higher than those of deutonymphs in both species. Predation rates were not separated according to the various developmental stages (i.e., second instar larva, pupa, or adult) of thrips; however, deutonymphs fed on fewer adults than larvae or pupae of F. occidentalis. Our results suggest that both G. aculeifer and S. scimitus are active predators that can prey during any of their developmental stages and on any species of thrips tested.     

Population growth and predation interference between two species of predatory phytoseiid mites (Acarina: Phytoseiidae) in interactive systems

Summary Populations of two species of phytoseiid mite predators, Phytoseiulus persimilis Athias-Henriot and Amblyseius degenerans (Berlese), feeding on a tetranychid prey, Tetranychus pacificus McGregor, were allowed to grow separately as well as together on bush lima bean (Phaseolus lunatus Var.) arenas in the laboratory. The population plateau attained by P. persimilis was nearly 5 times higher than that for A. degenerans when each species was on separate leaf arenas. When they were on the same arena, P. persimilis was outcompeted by A. degenerans after about 70 days of population growth. When dispersal to other arenas was necessary for the predators to find prey in another experiment, P. persimilis survived well but not A. degenerans. The mechanisms underlying species displacement were explored further. The differential mortality of immature predators at different developmental stages due to interspecific predation was concluded to be responsible for the population decline of P. persimilis, and the decline of A. degenerans in another experiment was attributed to its sedentary tendency regardless of prey distribution and to the lack of alternative food sources in the system. The implications to biological control of mutual predation between predator species is discussed briefly.     

Impacts of biological control and invasive species on a non-target native Hawaiian insect

The potential for classical biological control to cause unintended harm to native species was evaluated in the case of the endemic Hawaiian koa bug, Coleotichus blackburniae White (Hemiptera: Scutelleridae), and parasitoids introduced to Hawaii for control of an agricultural pest, the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Parasitism of C. blackburniae eggs, nymphs and adults by biocontrol agents was quantified across a wide range of habitats and compared to other sources of mortality. Egg mortality due to the biocontrol agent Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) was low (maximum 26%) and confined to elevations below 500 m on a single host plant. Predation, mainly by alien spiders and ants, was the greatest source of egg mortality (maximum 87%). Parasitism of adult C. blackburniae by the biocontrol agent Trichopoda pilipes (F.) (Diptera: Tachinidae) was near zero at 21 of 24 sites surveyed. Three sites with high bug density had higher levels of T. pilipes parasitism, reaching maxima of 70% among adult female bugs, 100% among males and 50% among fifth instars. Male-biased parasitism indicated that T. pilipes is adapted to using male aggregation pheromone for finding C. blackburniae hosts. The relative impacts of biocontrol agents and other sources of mortality were compared using life tables. Invasive species, particularly generalist egg predators, had the greatest impacts on C. blackburniae populations. Effects of intentionally introduced parasitoids were relatively minor, although the tachinid T. pilipes showed potential for large impacts at individual sites. In retrospect, non-target attacks by biological control agents on C. blackburniae were predictable, but the environmental range and magnitude of impacts would have been difficult to foresee.     

Effects of macrophytes on feeding and life-history traits of the invasive apple snail Pomacea canaliculata

1. Biological invasions have become a serious threat to ecosystems worldwide. Various factors can contribute to the success of biological invasion. We examined how different macrophyte food affected feeding and life‐history traits of the invasive herbivorous snail Pomacea canaliculata, and whether differences in snail life‐history traits could explain its successful infestation of agricultural and non‐agricultural wetlands in Asia. 2. We tested five cultivated and five wild semi‐aquatic macrophytes. Snail daily feeding rate varied substantially with plant species, ranging from 1.3% to 22% of its body mass. Snails fed with four (Amaranthus gangeticus, Apium graveolens dulce, Ipomoea aquatica and Nasturtium officinale) of the five cultivated macrophyte species exhibited high survivorship, fast growth and high fecundity. Snails fed with Colocasia esculenta, however, grew poorly, did not reproduce and eventually died. 3. Of the five wild species (Eichhornia crassipes, Ludwigia adscendens, Murdannia nudiflora, Myriophyllum aquaticum and Polygonum hydropiper), M. nudiflora supported a high snail survival, but snails had slower growth and lower fecundity than those reared on the four palatable cultivated species. Snails fed with L. adscendens grew substantially slower than those fed with M. nudiflora, and produced only a small clutch of eggs. Snails fed with E. crassipes, M. aquaticum and P. hydropiper had very low survivorship, grew very little and did not reproduce. 4. We determined six plant properties and their correlation with the feeding, growth and reproduction of the apple snails. Cultivated macrophytes in general had a higher nutritional value and lower physical and chemical defences. Phenolic content was negatively correlated with snail feeding rate, while plant nitrogen and phosphorus contents were positively correlated with snail egg production and growth, respectively. 5. These results indicate that, due to their higher nutritional value and lower chemical and physical defences, cultivated macrophytes are in general desirable for the apple snail which may partly explain its successful invasion into wet agricultural areas in Asia. This snail may also selectively graze poorly defended wild macrophytes in non‐agricultural wetlands, leading to changes in floral diversity and wetland functioning. Management of this and other apple snails with similar life‐history traits should thus focus on the prevention of their further spread.     

Experimental predation studies of malacophagous larvae of Sepedon fuscipennis (Diptera: Sciomyzidae) and aquatic snails

Experimental studies were conducted under both laboratory and field conditions to determine the effects of prey density, three levels of prey aggregation, water depth, and predator density on the number of snails killed per larva of Sepedon fuscipennis. Of these factors, predation rates were most influenced by prey density and water depth. The number of small (2–4.5 mm) Lymnaea palustris killed per larva of S. fuscipennis increased at a decreasing rate as prey density increased under shallow water conditions. Larvae killed a mean of 14 snails at a prey density of 200/m², while an average of 24 snails were killed per larva of S. fuscipennis at a prey density of 4000/m². This functional response to prey density was largely confined to third-instar larvae, and as water depth was increased the response was not apparent.A field study in which larval densities of S. fuscipennis were manipulated showed that the population density of smaller individuals of L. palustris (< 4.5 mm) was reduced when predator density was increased. Populations of Physa integra, Gyraulus parvus, and larger L. palustris were not significantly reduced by the malacophagous larvae at the levels tested.     

Leech predation on juvenile freshwater snails: effects of size,species and substrate

Summary The leechGlossiphonia complanata does not appear to have substantial impact on snail populations, but this may be due to most studies focusing on adult snails rather than juvenile snails. In this study I investigated how predation rates ofG. complanata feeding on newly-hatched and juvenile snails was affected by snail species, snail size, snail density and substrate, in a laboratory experiment. Number of snails eaten increased with increasing density resulting in a type II functional response curve. Predation rates were higher when leeches were feeding onLymnaea emarginata than onPhysa gyrina, whereas there was no significant difference in predation rates when they were feeding onL. emarginata andHelisoma anceps. Sandy substrates and greater snail size resulted in decreased predation rates. Sand reduced movement speed ofG. complanata, which probably reduced encounter rates. Thus, there was a comparatively large effect of leech predation on newly-hatched snails, due to a high probability of encounter and high predation rates, but spatial and temporal refuges probably reduce the importance of leech predation as a structuring force in freshwater snail assemblages.     

Effects of pond size and consequent predator density on two species of tadpoles

Experimental ponds were used as a model system of habitat patches to study the effect of habitat size on the relative growth performance of tadpoles of Bufo americanus and Pseudacris triseriata, and on colonization by predatory insects. Three pond depths and surface areas were habitat size treatments in a replicated, factorial experiment. Tadpoles of both species were astablished together at a single density and ponds were left open to natural colonization by aquatic insects. Pond area had a significant effect on the multivariate response of P. triseriata larval period, survival, and metamorphic mass. P. triseriata survived better relative to B. americanus in larger ponds. However, increasing pond area led to greater incidence of predacious beetle larvae (Dytiscus, Coleoptera: Dytiscidae). Dytiscus larvae had a significant negative effect on the survival of P. triseriata and led to reduced P. triseriata survival relative to B. americanus in colonized ponds. The results suggest that habitat size can influence community structure by altering the distribution of predation among habitat patches.     

Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions

Following the rapid spread of soybean aphid, Aphis glycines in North America in the early 2000’s, biological control was identified as a cost-effective approach for management of this invasive pest. Two parasitoid species, Binodoxys communis and Aphidius colemani, were considered as potential candidates for classical and inundative biological control, respectively. The objectives of the present study were to determine the overwintering capacity of B. communis under climatic conditions prevailing in northeastern North America, and to measure parasitism and dispersal capacity of A. colemani when released in soybean fields. Field and laboratory assessments showed that the Chinese strain of B. communis, Harbin 2002, has a very poor capacity to enter into diapause (<0.8%), and thus to establish in North America. We suggest that this strain has gradually lost its ability to enter diapause during the extended periods of quarantine and laboratory confinement, during which it was continuously exposed to non-diapause rearing conditions. A. colemani did not show strong potential to control A. glycines. Following the release of approximately 8400 females in experimental plots, only 113 mummies were recovered within a radius of 60 m from the release point. Although both parasitoids were promising in controlled environments, the B. communis Harbin 2002 strain and the A. colemani commercial strain did not show strong potential to control A. glycines populations in soybean fields.     

Biological control of parthenium (Parthenium hysterophorus): the Australian experience

ABSTRACT

Parthenium is a Weed of National Significance in Australia. Biological control of parthenium in Australia commenced in 1977 and since then nine insect species and two rust fungi have been introduced and established. Seven of them are widespread, however the time taken for field establishment varied widely between various agents, ranging from one to 15 years. Among them, the stem-galling Epiblema moth, the stem-boring Listronotus weevil, the seed-feeding Smicronyx weevil and the root-feeding Carmenta moth occur in all parthenium-infested areas at high population densities. The leaf-feeding Zygogramma beetle occurs only in central and southern Queensland, and not in northern Queensland. The parthenium summer rust occurs seasonally in central and northern Queensland, while the parthenium winter rust is more widespread in southern Queensland than in central Queensland, but does not occur in north Queensland. The sap-feeding Stobaera planthopper and the leaf-mining Bucculatrix moth established and are widespread, but their damage levels remain very low. The stem-galling Conotrachelus weevil and the stem-boring Platphalonidia moth are believed to be established, but at very low abundance. Biological control has resulted in significant reductions in the abundance and impact of parthenium in Australia. As a result, the area infested with parthenium in central Queensland has declined since the mid-1990s. Due to the absence of many of the effective agents in southern and south-eastern Queensland, agents from central Queensland are being redistributed there. Additionally, based on Australian success, many of these agents have also been introduced into other countries around the world.     

Tea: Biological control of insect and mite pests in China

Tea is one of the most economically important crops in China. To secure its production and quality, biological control measures within the context of integrated pest management (IPM) has been widely popularized in China. IMP programs also provide better control of arthropod pests on tea with less chemical insecticide usage and minimal impact on the environment. More than 1100 species of natural enemies including about 80 species of viruses, 40 species of fungi, 240 species of parasitoids and 600 species of predators, as well as several species of bacteria have been recorded in tea ecosystems in China. Biological and ecological characteristics of some dominant natural enemies have been well documented. Several viral, bacterial, and fungal insecticides have been commercially utilized at large scale in China. Progress in biological control methods in conjunction with other pest control approaches for tea insect pest management is reviewed in this article. Knowledge gaps and future directions for tea pest management are also discussed.     

Biological control of marine invasive species: cautionary tales and land-based lessons

Biological control (biocontrol) has successfully regulated pest populations in terrestrial agroecosystems, but it has also caused negative unintended consequences for native species. Marine biologists and resource managers have recently published a growing number of proposals to include biocontrol in integrated pest management programs in oceans, seas and estuaries. Here, I review six ecologically and taxonomically diverse case studies of marine biocontrol programs at various stages of planning and implementation. Proposals include viral or microbial control of harmful algal blooms, predatory control of the ctenophore Mnemiopsis leidyi in the Black Sea, parasitic regulation of the European green crab Carcinus maenas, castration by ciliates of the seastar Asterias amurensis in Australia, herbivory of the toxic green alga Caulerpa taxifolia in the Mediterranean by sacoglossan sea slugs, and insect biocontrol by the planthopper Prokelesia marginata to ameliorate ecological impacts of the saltmarsh cordgrass Spartina alterniflora. Where data exist, I evaluate these examples in terms of lessons marine invasion biologists can glean from the rich history of terrestrial biocontrol, and explicitly contrast agroecosystems with invaded marine habitats. Host specificity cannot be guaranteed in the marine biocontrol proposals examined. Feasible alternatives to classical biocontrol in the marine realm should be emphasized, including more investment in invasion prevention tools, early detection and eradication while invasions are small, and increased attention to native natural enemies to control exotic pests. Biocontrol in marine habitats is risky: it poses many more uncertainties and has a much sparser history than its counterpart on land.     

Feeding behavior of black carp Mylopharyngodon piceus (Pisces: Cyprinidae) on fry of other fish species and trematode transmitting snail species

Fish raised in aquaculture ponds may get infected with fishborne zoonotic trematodes (FZT) during the nursing stage. Freshwater snails serve as intermediate hosts for FZT and we wanted to explore the possibility of controlling snails by stocking nursery ponds with a few juvenile specimens of the mollusc-eating fish, black carp (Mylopharyngodon piceus). Obviously, the risk that black carp might also prey on the juvenile fishes in nursery ponds should first be assessed. Laboratory trials showed that all size classes of juvenile black carp consumed fry of common carp (Cyprinus carpio) even when offered snails as food; the odds of survival of fry from tanks with medium sized and large black carp was 5.6% and 39.9%, respectively of that of fry in tanks with small sized black carp. Since the large black carp also consumed fewer snails than medium sized fish, we believe that large specimens were stressed in the experimental aquaria. Under semi-field conditions, presence of the black carp had no effect on survival of fry of Oreochromis niloticus and C. carpio both in the absence and presence of snails as alternative food. The black carp consumed most snails offered with the exception of some of the large snails. We conclude that under field conditions, predation by black carp on fish fry is minimal and field trials in nursery ponds are warranted. Due to the risks that black carp pose to native imperiled snails and other molluscs, trials should be restricted to ponds within the fish’s native or existing range.     

Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation

The combined release of species of generalist predators can enhance multiple pest control when the predators feed on different prey, but, in theory, predators may be excluded through predation on each other. This study evaluated the co-occurrence of the generalist predators Macrolophus pygmaeus Rambur and Orius laevigatus (Fieber) and their control of two pests in a sweet pepper crop. Both predators consume pollen and nectar in sweet pepper flowers, prey on thrips and aphids, and O. laevigatus is an intraguild predator of M. pygmaeus. Observations in a commercial sweet pepper crop in a greenhouse with low densities of pests showed that the two predator species coexisted for 8 months. Moreover, their distributions in flowers suggested that they were neither attracted to each other, nor avoided or excluded each other. A greenhouse experiment showed that the predators together clearly controlled thrips and aphids better than each of them separately. Thrips control was significantly better in the presence of O. laevigatus and aphid control was significantly better in the presence of M. pygmaeus. Hence, combined inoculative releases of M. pygmaeus and O. laevigatus seem to be a good solution for controlling both thrips and aphids in greenhouse-grown sweet pepper. The predators are able to persist in one crop for a sufficiently long period and they complement each other in the control of both pests. This study also provides further evidence that intraguild predation does not necessarily have negative effects on biological control.     

Reprint of: Biological control of rice insect pests in China

Rice is one of the most important food crops in the world. China has the second largest area of the rice growing in the world and the highest yield of rice produced. Infestation by insect pests, especially rice planthoppers, stem borers and leaf folders, is always a serious challenge to rice production in China. Current methods for controlling insect pests in China mainly include good farming practices, biological control, breeding and growing resistant varieties, and the use of chemical insecticides. However, for farmers, the favorite method for insect pest control is still the application of chemical insecticide, which not only causes severe environmental pollution and the resurgence of herbivores but also reduces populations of the natural enemies of herbivores. To control insect pests safely, effectively and sustainably, strategies encouraging biological control are currently demanded. Here we review the progress that has been made in the development and implementation of biological controls for rice in China since the 1970s. Such progress includes the species identification of the natural enemies of rice insect pests, the characterization of their biology, and the integration of biological controls in integrated pest management. To develop effective ecological engineering programs whose aim is to implement conservation biological controls, further research, including the evaluation of the roles of plants in non-crop habitats in conservation biological controls, volatiles in enhancing efficiency of natural enemies and natural enemies in manipulating insect pests, and education to increase farmers’ knowledge of biological controls, is proposed.     

棉田捕食性瓢虫控害功能的分析

在系统调查棉田捕食性飘虫种数量动态的基础上,应用生态能学的方法,分析并比较了不同插种期、套间作等农业措施对棉田捕食性飘虫控害虫功能的影响。结果表明,不同类型棉田飘虫对害虫的摄入量为26．45－70kJ.m^-2,分别占整个捕食性在天敌摄入量的28．30％－47．88％,是棉田捕食性天敌的优势种类;不同类型棉田飘虫对棉蚜的控害系数为5．07％－12．85％,并随着棉花播种期的推后和间套作呈现出下降趋势,它们在棉田生态系统害虫生态调控中发挥着重要作用。     

Viral biocontrol of invasive vertebrates: Lessons from the past applied to cyprinid herpesvirus-3 and carp (Cyprinus carpio) control in Australia

This paper reviews successful and, briefly, unsuccessful viral biocontrol programs for invasive vertebrate pests to provide lessons for future programs, especially the potential use of cyprinid herpesvirus-3 to control carp in Australia. There have only been three major programs where viral pathogens have been used successfully against invasive vertebrate pests. Myxoma and rabbit hemorrhagic disease viruses were used to control rabbits in Australia, and feline panleukopenia virus helped eliminate cats from sub-Antarctic Marion Island. These programs have shown us that successful viral biocontrol programs for invasive species must include: a thorough understanding of the biology of the target species, and of the viral epidemiology; an integrated pest management program involving both the virus and other control methods; and, a post-release assessment of the ecological benefits of the program. The most important practical lessons identified in this review are: the greatest impact of viruses as biocontrol agents is in the first years following release; unsuspected cross-reactive viruses may confer protection on the target species; and, there may be age- or temperature-related resistance to the virus in the target species.