Host plants and natural enemies of Bemisia tabaci (Hemiptera: Aleyrodidae) in China

Abstract The sweetpotato whitefly, Bemisia tabaci, has been a destructive pest in China for over the past two decades. It is an extremely polyphagous insect, being recorded feeding on hundreds of host plants around the world. Potential host plants and natural enemies of B. tabaci in the south, southeast, middle, north and northwest of China were investigated during the last decade. In total 361 plant species from 89 families were recorded in our surveys. Plants in the families Compositae, Cruciferae, Cucurbitaceae, Solanaceae and Leguminosae were the preferred host species for B. tabaci, which therefore suffered much damage from this devastating pest due to their high populations. In total, 56 species of parasitoids, 54 species of arthropod predators and seven species of entomopathogenic fungi were recorded in our surveys. Aphelinid parasitoids from Encarsia and Eretmocerus genera, lady beetles and lacewings in Coleoptera and Neuroptera were found to be the dominant arthropod predators of B. tabaci in China. The varieties of host plant, their distribution and the dominant species of natural enemies of B. tabaci in different regions of China are discussed.     

Natural enemy impacts on Bemisia tabaci (MEAM1) dominate plant quality effects in the cotton system

1. Plant quality (bottom‐up effects) and natural enemies (top‐down effects) affect herbivore performance. Furthermore, plant quality can also influence the impact of natural enemies. 2. Lower plant quality through reduced irrigation increased the abundance of the cryptic species from the Bemisia tabaci complex [hereafter B. tabaci Middle East Asia Minor 1 (MEAM1)], but not its natural enemies on cotton. It was therefore predicted that lower plant quality would diminish the impact of natural enemies in regulating this herbivore. 3. Over three cotton seasons, plant quality was manipulated via differential irrigation and natural enemy abundance with insecticides. Life tables were used to evaluate the impact of these factors on mortality of immature B. tabaci (MEAM1) over nine generations. 4. Mortality of B. tabaci (MEAM1) was consistently affected by natural enemies but not by plant quality. This pattern was driven by high levels of sucking predation, which was the primary (key) factor associated with changes in immature mortality across all irrigation and natural enemy treatments. Dislodgement (chewing predation and weather) and parasitism contributed as key factors in some cases. Analyses also showed that elimination of sucking predation and dislodgement would have the greatest effect on overall mortality. 5. The top‐down effects of natural enemies had dominant effects on populations of B. tabaci (MEAM1) relative to the bottom‐up effects of plant quality. Effects were primarily due to native generalist arthropod predators and not more host‐specific aphelinid parasitoids. The findings of this study demonstrate the important role of arthropod predators in population suppression and validate the importance of conservation biological control in this system for effective pest control.     

The status ofBemisia tabaci (Hom.: Aleyrodidae),Trialeurodes vaporariorum (Hom.: Aleyrodidae) and their natural enemies in Crete

The non «B» biotype ofBemisia tabaci (Gennadius) is recorded for the first time in Crete in 1992, in the north east and south east of the island.Trialeurodes vaporariorum (Westwood) is the predominant whitefly on plants in the north and west of the island. Three surveys of Crete were made in 1992 and 1993 for natural enemies ofB. tabaci andT. vaporariorum and resulted in the collection of 4 species ofEncarsia, (plus a number of species that are unidentifiable at this time), anEretmocerus sp. (unidentifiable at this time) and a fungal pathogen,Paecilomyces farinosus (Dickson Ex Fries) Brown &; Smith.Encarsia adrianae was identified fromT. vaporariorum; which constitutes its most westerly distribution point and a new host record respectively.B. tabaci andT. vaporariorum were found on horticultural crops, ornamentals and weeds. Populations of both whitefly species were severely depleted on field hosts throughout the island during the winter of 1992/93. Climatic constraints, competition withT. vaporariorum in otherwise suitable niches, effective natural enemies and an observed low level of polyphagy may explain the present limited distribution of the non «B» biotype ofB. tabaci in Crete.     

Intraguild interactions between the predator Macrolophus pygmaeus and the parasitoid Eretmocerus mundus,natural enemies of Bemisia tabaci

The native parasitoid Eretmocerus mundus Mercet and the predator Macrolophus pygmaeus Rambur are widely used to control Bemisia tabaci (Gennadius) in Mediterranean tomato greenhouses. An optimal biological control strategy for B. tabaci should take into account intraguild interactions between these natural enemies. In this study, predator's prey preferences and prey consumption were studied when offered different parasitoid and whitefly stages. The effect of the host plant on the adults of both natural enemies was also examined. M. pygmaeus preferred to consume B. tabaci over E. mundus when immature stages and adults of B. tabaci and E. mundus were offered. They consumed a larger amount of healthy B. tabaci nymphs and adults than of parasitised nymphs or E. mundus adults. The predator M. pygmaeus interfered with the reproduction of E. mundus females on cotton but not on tomato. However, B. tabaci nymphal mortality on tomato associated with parasitoid host feeding was also lower when the adult parasitoids coexisted with the predators. The joint release of M. pygmaeus and E. mundus adults did not increase the control of the whitefly B. tabaci.     

The Role of Natural Enemy Foraging Guilds in Controlling Cereal Aphids in Michigan Wheat

Insect natural enemies (predators and parasitoids) provide important ecosystem services by suppressing populations of insect pests in many agricultural crops. However, the role of natural enemies against cereal aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. The objectives of this research were to characterize the natural enemy community in wheat fields and evaluate the role of different natural enemy foraging guilds (foliar-foraging versus ground-dwelling predators) in regulating cereal aphid population growth. We investigated these objectives during the spring and summer of 2012 and 2013 in four winter wheat fields on the Michigan State University campus farm in East Lansing, Michigan. We monitored and measured the impact of natural enemies by experimentally excluding or allowing their access to wheat plants infested with Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae). Our results indicate that the natural enemy community in the wheat fields consisted mostly of foliar-foraging and ground-dwelling predators with relatively few parasitoids. In combination, these natural enemy groups were very effective at reducing cereal aphid populations. We also investigated the role of each natural enemy foraging guild (foliar-foraging versus ground-dwelling predators) independently. Overall, our results suggest that, in combination, natural enemies can almost completely halt early-season aphid population increase. Independently, ground-dwelling predators were more effective at suppressing cereal aphid populations than foliar-foraging predators under the conditions we studied. Our results differ from studies in Europe and the US Great Plains where foliar foraging predators and parasitoids are frequently more important cereal aphid natural enemies.     

Intraguild predation by the generalist predator Orius majusculus on the parasitoid Encarsia formosa

Intraguild predation of Orius majusculus (Reuter) (Heteroptera: Anthocoridae) on Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae), both natural enemies of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), was studied under laboratory conditions. The experiments quantified prey consumption by 5th instar nymphs and adults of O. majusculus offered unparasitised 3rd, early 4th or 4th instar B. tabaci nymphs or parasitised nymphs containing 2nd or 3rd larval instar or pupal parasitoids. In addition, prey preference of the two stages of O. majusculus for parasitised or unparasitised whitefly nymphs was studied using nine different prey combinations. Both predator stages readily preyed upon on both unparasitised and parasitised B. tabaci. In no-choice experiments, predation on 3rd instar E. formosa by adult predators was the highest, while predator nymphs preyed most on unparasitised 3rd instar B. tabaci and 2nd instar parasitoids. Predation of predator stages was lowest on 4th instar B. tabaci and E. formosa pupae. In all prey combinations, both stages of O. majusculus showed a significant preference for parasitised over unparasitised whitefly nymphs except for the combination of 5th instars of O. majusculus with early 4th instar whiteflies and E. formosa pupae. The results indicate that intraguild interactions between O. majusculus and E. formosa may have negative effects on biological control of B. tabaci.     

Infection of tomato by Tomato Yellow Leaf Curl Virus alters the foraging behavior and parasitism of the parasitoid Encarsia formosa on Bemisia tabaci

Encarsia formosa Gahan is a solitary endoparasitoid that is commercially reared and released for augmentative biological control of whiteflies including Bemisia tabaci (Gennadius). Bemisia tabaci biotypes B and Q are two most invasive species that greatly reduce crop yields in China by feeding on plant sap and by transmitting Tomato Yellow Leaf Curl Virus (TYLCV). The effects of TYLCV infection of tomato on E. formosa foraging on B. tabaci B and Q are unknown. In Y-tube olfactometer assays in the present study, E. formosa significantly preferred TYLCV-infected tomato plants over TYLCV-free plants. The wasp females also significantly preferred TYLCV-infected tomato plants infested with 3rd-instar nymphs of B. tabaci biotype Q over TYLCV-free plants with biotype Q nymphs. However, no significant differences were observed when B. tabaci biotype B was infested on tomato plants. The oviposition bioassays confirmed that TYLCV infection on tomato plants resulted in the recruitment of parasitoids. These results indicate that TYLCV-infection of tomato increase the foraging of E. formosa on B. tabaci, as differs on the B and Q biotypes.     

Can the Understory Affect the Hymenoptera Parasitoids in a Eucalyptus Plantation?

The understory in forest plantations can increase richness and diversity of natural enemies due to greater plant species richness. The objective of this study was to test the hypothesis that the presence of the understory and climatic season in the region (wet or dry) can increase the richness and abundance of Hymenoptera parasitoids in Eucalyptus plantations, in the municipality of Belo Oriente, Minas Gerais State, Brazil. In each eucalyptus cultivation (five areas of cultivation) ten Malaise traps were installed, five with the understory and five without it. A total of 9,639 individuals from 30 families of the Hymenoptera parasitoids were collected, with Mymaridae, Scelionidae, Encyrtidae and Braconidae being the most collected ones with 4,934, 1,212, 619 and 612 individuals, respectively. The eucalyptus stands with and without the understory showed percentage of individuals 45.65% and 54.35% collected, respectively. The understory did not represent a positive effect on the overall abundance of the individuals Hymenoptera in the E. grandis stands, but rather exerted a positive effect on the specific families of the parasitoids of this order.     

Species distribution models for natural enemies of monarch butterfly (<Emphasis Type="Italic">Danaus plexippus</Emphasis>) larvae and pupae: distribution patterns and implications for conservation

Prey populations can be strongly influenced by predators and parasitoids, and migratory prey whose distributions vary geographically throughout their breeding seasons encounter different combinations of predators and parasitoids throughout their range. North American monarch butterflies (Danaus plexippus) are susceptible to a wide variety of natural enemies, but the distribution of these natural enemies has not been quantified. We developed ecological niche models using environmental data to identify areas with suitable abiotic conditions for eight known natural enemies of monarchs, including six predators: Arilus cristatus, Harmonia axyridis, Monomorium minimum, Podisus maculiventris, Polistes spp., and Solenopsis geminata; and two parasitoids: Lespesia archippivora and Pteromalus cassotis. We combined correlated suitable areas for individual predators and parasitoids to identify regions with the most predator and parasitoid species potential. The Gulf Coast, West Coast, Florida, and parts of the eastern United States are predicted to have the most natural enemy species. We suggest that future research should assess monarch mortality rates in these areas, and that monarch conservation strategies consider pressure from natural enemies.     

The passionvine mealybug,Planococcus minor (Maskell) (Hemiptera: Pseudococcidae), and its natural enemies in the cocoa agroecosystem in Trinidad

Planococcus minor (Maskell) is native to South Asia, but it is also present in several Neotropical locations including the island of Trinidad in the southern Caribbean. The mealybug poses a serious threat to uninfested countries in this region as well as the mainland U.S. As part of an effort to gather much needed information on P. minor, 33 cocoa (Theobroma cacao L.) field sites on the island were surveyed in 2006 with a view to assess the occurrence and pest status of the mealybug. P. minor was identified from 20 field sites, indicating that it was well distributed across the island on this crop, which appeared to be a reliable indicator host plant. Infestation levels were generally low and populations were sparsely distributed across the field sites categorized into three habitat types. The following year, nine field sites were surveyed for natural enemies of P. minor using laboratory-infested potatoes in sentinel traps. Species from four insect orders and six families were collected and identified. The major predators belonged to the families Cecidomyiidae and Coccinellidae. Two primary parasitoids, Leptomastix dactylopii Howard (Encyrtidae) and Coccidoxenoides perminutus (Girault) (=Pauridia peregrina Timberlake, =Coccidoxenoides peregrinus (Timberlake)) (Encyrtidae), were reared from different mealybug stages, along with several hyperparasitoids. The primary parasitoids were probably introduced fortuitously. These diverse natural enemies were recovered throughout the sampling period from the different habitat types. The identification of key natural enemies associated with P. minor has important implications for the implementation of biological control in newly infested areas.     

Performance of Bemisia tabaci (Genn.) Biotype B (Hemiptera: Aleyrodidae) on Weeds

Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae) is regarded as a pest with a large number of hosts, including crops and weeds. The performance of this whitefly on seven weeds was evaluated in order to identify the most suitable host. The following weeds that are very common in intense agricultural areas in the state of São Paulo, Brazil, were selected for this study: spurge (Euphorbia heterophylla), beggarticks (Bidens pilosa), red tasselflower (Emilia sonchifolia), small-flower galinsoga (Galinsoga parviflora), pigweed (Amaranthus viridis), black nightshade (Solanum americanum), and morning glory (Ipomoea sp.). In free-choice tests, adult preference and oviposition were greatest on spurge. In contrast, morning glory was the least attractive and least oviposited plant. In assays carried out for egg–adult development, egg viability was greater than 87% over all weeds, whereas nymph viability ranged from 74 to 97%. The developmental period from egg to adult ranged from 26.7 to 49.1 days among the hosts under study. The lowest nymph density rate was observed for beggarticks and morning glory. Cluster analysis resulted in a single group formed by spurge, indicating its superiority as a host for B. tabaci biotype B. Even though the parameters evaluated indicate that spurge is the most suitable host among the weeds, all the others allow the reproduction of B. tabaci biotype B. For this reason, they should be observed during cropping and the intercrop period in areas infested by this whitefly.     

Natural enemies of the pumpkin caterpillarDiaphania indica [Lepidoptera: Pyralidae] in Tamil Nadu

The survey for the natural enemies associated with the pumpkin caterpillar,Diaphania indica revealed the presence of 20 species of parasitoids, predators and pathogens. Of these, 16 were parasitoids belonging to the familiesBraconidae, Ichneumonidae, Bethylidae, Elasmidae andChalcididae. Except for 3 species the remaining parasitoids were new records forD. indica. The predators recorded were ants and spiders. A microsporidia also was recorded for the first time onD. indica.      

Detection of Bemisia tabaci remains in predator guts using a sequence-characterized amplified region marker

Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) B biotype is an invasive species (biotype) in China. In order to understand the role that native natural enemies might play in its control, techniques were developed for detecting B. tabaci DNA within the gut of predators. A species-specific DNA fragment, ca. 350 bp, was identified by random amplified polymorphic DNA analysis. This fragment was absent in other closely related or co-occurring prey species, cotton, and other select predator species. After cloning and sequencing the fragment, one pair of sequence-characterized amplified region (SCAR) primers was developed, which amplified a single band of 240 bp. Specificity tests performed with the primers showed the presence of the 240-bp band for B. tabaci in all developmental stages and both sexes, in adult Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) fed on B. tabaci nymphs in the laboratory, and in predators collected in cotton fields. Following consumption of a single red-eyed B. tabaci nymph, prey DNA was detectable in 100% of P. japonica at t = 0, decreasing to 20% after 12 h of digestion, and no B. tabaci DNA detected at t = 24 h. In total, we analyzed the gut contents of 185 field-collected predators, representing four different orders. All nine field-collected predator species (namely, P. japonica, Harmonia axyridis, Scymnus hoffmanni, Coccinella septempunctata, Orius sauteri, Chrysopa pallens, Chrysopa formosa, Erigonnidium graminicolum, and Neoscona doenitzi) contained DNA from B. tabaci and are assumed predators of this pest insect. Overall, the B. tabaci was eaten by more than 50% of field-collected predator individuals, including larvae of the coccinellids (P. japonica and H. axyridis) and lacewings (C. pallens and C. formosa) and adults of O. sauteri and the spiders (E. graminicolum and N. doenitzi). There was a trend of a higher percentage of larval than adult coccinellids and lacewings that preyed on B. tabaci in the field. This study provides a framework for the future use of molecular gut content analysis in arthropod conservation ecology and food web research, with considerable potential for quantifying threats to invasive or endemic pest species in China and elsewhere.     

Response of Bemisia tabaci Genn. (Hemiptera: Aleyrodidae) Biotype B to Genotypes of Pepper Capsicum annuum (Solanales: Solanaceae)

Bemisia tabaci Genn. biotype B is a widely distributed plant pest that represents one of the major constraints for horticultural crop production. The purpose of the present work was to evaluate the oviposition preference, survivorship, and development of B. tabaci biotype B on semi-cultivated genotypes of Capsicum annuum from southeast Mexico. In free-choice experiments to evaluate the oviposition preference, lower number of eggs laid by B. tabaci biotype B was observed in the genotypes Maax and Xcat´ik relative to that in the commercial genotype Parado. Egg hatchability was significantly lower in Pico Paloma, Bolita, Blanco, Chawa, Payaso, and Xcat´ik than in the rest of the genotypes, including the commercial genotype Jalapeño. Likewise, survivorship of nymphs was significantly lower in Pico Paloma, Bolita, and Blanco than in the remaining genotypes. Nymph developmental time and the period of development from egg to adult were the shortest in Amaxito. Therefore, sources of resistance to B. tabaci biotype B by antibiosis (accumulation of plant defense compounds) might be found in the semi-cultivated genotypes Pico Paloma, Bolita, and Blanco.     

Predators,parasitoids and pathogens of ticks: A review

Research conducted on natural enemies of ticks, namely predators, parasitoids and pathogens, is reviewed. Predators include ants, birds, rodents, lizards, shrews, spiders and domestic chickens. All the known parasitoids are hymenopteran wasps belonging to the genera Ixodiphagus and Hunterellus. The work so far done on bacteria, fungi, viruses and rickettsiae which are pathogenic to ticks is reviewed, both with regard to experimental infections and natural infections. The possibilities of using natural enemies as biological control agents of ticks are discussed.     

Fitness of Encarsia sophia (Hymenoptera: Aphelinidae) parasitizing Trialeurodes vaporariorum and Bemisia tabaci (Hemiptera: Aleyrodidae)

Abstract Fitness and efficacy of Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae) as a biological control agent was compared on two species of whitefly (Hemiptera: Aleyrodidae) hosts, the relatively smaller sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype ‘B’, and the larger greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Significant differences were observed on green bean (Phaseolus vulgaris L.) in the laboratory at 27 ± 2°C, 55%± 5% RH, and a photoperiod of 14: 10 h (L: D). Adult parasitoids emerging from T. vaporariorum were larger than those emerging from B. tabaci, and almost all biological parameters of E. sophia parasitizing the larger host species were superior except for the developmental times of the parasitoids that were similar when parasitizing the two host species. Furthermore, parasitoids emerging from T. vaporariorum parasitized more of these hosts than did parasitoids emerging from B. tabaci. We conclude that E. sophia reared from larger hosts had better fitness than from smaller hosts. Those from either host also preferred the larger host for oviposition but were just as effective on smaller hosts. Therefore, larger hosts tended to produce better parasitoids than smaller hosts.     

Analysis of the genetic diversity of Bemisia tabaci populations in Shanxi province, China☆

Five different primer combinations were used for the analysis of 152 B biotype Bemisia tabaci (Gennadius) individuals and five Trialeurodes vaporairiorum individuals collected from 19 counties and seven host plants in Shanxi province in China, respectively. The main objective of the present study was to use AFLP markers to determine the genetic diversity of B. tabaci populations collected from Shanxi Province. The use of these primer combinations allowed the identification of 127 polymorphic bands (52.26%) from 60 to 500 bp. The average number of polymorphic bands per primer was 25.4 while the range for the five primers was 20–32. The average degree of heterozygosity was 0.251, while the range for the five primers was 0.204–0.289. The results suggested definite genetic diversity among different B. tabaci populations. Cluster analysis showed that B. tabaci populations were firstly scattered to three genetic groups according to the regions, then every genetic group was scattered to several subgroups according to the host plants, which revealed the genetic variability of B biotype B. tabaci populations has been not only among different regions, but also among different host plants in Shanxi Province.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

Post-release evaluation of biological control of Bemisia tabaci biotype “B” in the USA and the development of predictive tools to guide introductions for other countries

Climatic matching and pre-release performance evaluation were useful predictors of parasitoid establishment in a retrospective analysis of a classical biological control program against Bemisia tabaci biotype “B” in the USA. Laboratory evaluation of 19 imported and two indigenous parasitoid species in quarantine on B. tabaci showed that the Old World Eretmocerus spp, had the highest attack rate. The climate matching program CLIMEX was used to analyze the establishment patterns of five Old World Eretmocerus spp. introduced to the Western USA. The top matches ±10% for the climate of the area of introduction and origin of the introduced parasitoids always included the species that established. The Old World Eretmocerus spp. came from regions characterized by many separate biotypes of B. tabaci other than “B,” but are considered specialists of the B. tabaci complex as compared to the indigenous North American oligophagous Eretmocerus spp. This narrower host range and high attack rate combined with climatic adaptation may account for their establishment in the USA. A set of predictive tools and guidelines were used to select the best candidate for importation and possible release into Australia that has been recently invaded by the “B” biotype. The establishment patterns of the introduced Eretmocerus spp. and a comparison of climates of their respective locations in the USA were compared with the affected area in Australia. The best climatic match was the Lower Rio Grande Valley of Texas suggesting its dominant parasitoid, E. hayati ex. Pakistan be considered as the first candidate for evaluation as a biological control agent.     

Identification of biotypes and secondary endosymbionts of Bemisia tabaci in Korea and relationships with the occurrence of TYLCV disease

Bemisia tabaci is a species complex that consists of at least 24 genetically diverse biotypes. Here, we determined the biotypes of 27 populations collected in 17 different regions of Korea. Nucleotide sequence comparisons of cytochrome oxidase showed that 26 populations were Q biotype and that one population, the Goyang population, was B biotype. Further subgroup analysis of the Q biotype showed that all populations belonged to the Q1 subgroup, which originates from Western Mediterranean countries. Five endosymbiotic bacteria from various B. tabaci populations were analyzed by comparing rDNA sequences. Hamiltonella was detected in all the populations tested regardless of biotype. Cardinium was detected in all Q biotype populations but not in the B biotype population, while Rickettsia was detected in the B biotype population but not in Q biotype populations. Arsenophonus and Wolbachia were detected in 35% and 58% of Q biotype populations, respectively, but not in the B biotype population. Our results show that the endosymbiont profile is strongly associated with each biotype and with subgroups of the Q biotype. Survey of TYLCV disease from 2008 to 2010 indicated that this disease is widely spread in Korea. This study suggests that the rapid spread of TYLCV may be associated with endosymbiont infection, particularly Hamiltonella infection of B. tabaci.