Comparison of the host-handling behavior of Eretmocerus mundus on Bemisia tabaci B biotype, Q biotype and Trialeurodes vaporariorum

Host-handling behaviors of Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae) toward first to fourth instar nymphs of the Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) B and Q biotypes and of Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) were compared under laboratory conditions. The host acceptance rates differed among host stages but not among host species or biotypes. In all host species and biotypes, the parasitoids stopped their host-handling behavior before oviposition more often with older hosts. The total host-handling time was longer for the fourth instars than for younger instars, mainly due to the longer oviposition times and probing times. E. mundus showed marking behavior for the B. tabaci B and Q biotypes, but not for T. vaporariorum. In conclusion, E. mundus could parasitize all whitefly biotypes and species used in this study, but both B. tabaci biotypes were more suitable hosts than T. vaporariorum. The younger instars were good oviposition targets in all hosts.     

Host suitability of different instars of the whitefly Bemisia tabaci `biotype Q' for Eretmocerus mundus

Eretmocerus mundus Mercet is a parasitoidof Bemisia tabaci (Genn.) indigenous tothe Mediterranean and is used commercially foraugmentative biological control in Spain andelsewhere. A better understanding of thesuitability of different host instars wouldhelp optimize production and field application.Incidence of parasitism, development time,survivorship and sex ratio were evaluated whendifferent nymphal instars of the sweetpotatowhitefly Bemisia tabaci biotype `Q' wereoffered for parasitization. Experiments wereconducted on sweet pepper at 25 °C, 75%RH and 16:8 (L:D) photoperiod. E. mundusoviposited in all nymphal instars of B.tabaci except the mature 4th instar orpharate adult (previously designated, `pupa').Incidence of parasitism was greatest (33.8± 5.1 parasitized nymphs) and developmenttime shortest (14.1 ± 0.1 d) whenoviposition occurred under 2nd and3rd instar nymphs compared to 1st or4th instars. Survivorship (85%) andoffspring sex ratio (39.8% female) did notdiffer statistically for parasitoids developingin whiteflies that were parasitized asdifferent instars. Although 2nd and3rd instars were clearly the mostfavorable host stage for E. mundus, itscapacity to parasitize and develop on a widerange of host stages is a favorablecharacteristic for both rearing and fieldapplication.     

Variation between laboratory populations in the performance of the parasitoid Encarsia formosa on two host species, Bemisia tabaci and Trialeurodes vaporariorum

We tested the hypothesis that populations of the parthenogenetic parasitic wasp Encarsia formosa Gahan (Hymenoptera: Aphelinidae) differed in their ability to use two different host species, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) and Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae). Of the three wasp populations tested, two populations had been reared for many generations on B. tabaci and one population had been reared for many years on T. vaporariorum. Performance was measured by the number of whitefly nymphs that were successfully parasitized by individual wasps, and performance on either host was measured in separate experiments. There was variation between wasp populations in their performance on the host B. tabaci, with one wasp population reared for many years on this host performing considerably better than the other two populations. There were no significant differences between populations in their use of the preferred host, T. vaporariorum. The experiments were conducted in such a way that we could distinguish heritable differences between populations from environmentally-induced conditioning differences due to the immediate host from which an individual wasp enclosed. In either experiment there were no significant effects of conditioning, although there was a trend within each population for wasps conditioned on T. vaporariorum to have higher performance than those conditioned on B. tabaci. Thirdly, we conducted a selection experiment, initiated with wasps from a single population historically reared on T. vaporariorum, to measure the effect of laboratory rearing on different hosts for 17 generations. We did not see any difference in the performance of wasps on B. tabaci after this period of rearing on either of the two hosts. In summary, populations of E. formosa do differ in their relative performance on B. tabaci. The one population that was tested further did not show any response to selection by rearing, but the ability to respond to selection on performance may not be equal for all populations. The possibility that wasp populations have differential performance on particular hosts may affect the use of this species as a biological control agent.     

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.     

Intrinsic competition between the parasitoids Eretmocerus mundus and Encarsia formosa in Bemisia tabaci

Immature stages of Eretmocerus mundus Mercet and Encarsia formosa Gahan (both Hymenoptera: Aphelinidae) compete in larvae of their host, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Laboratory tests were carried out on excised tree tobacco leaves, exposing B. tabaci nymphs to one of the parasitoid species alone or to both species, one after the other, to obtain multi‐parasitization. Parasitization by E. mundus and E. formosa was allowed on specific host stages in order to obtain interactions between different immature stages of the two parasitoids (eggs, and first, second, and third instars). The outcome from each multi‐parasitization treatment was verified by analysing data on parasitoid adult emergence. Observations under a stereomicroscope and dissections of multi‐parasitized hosts were also performed in order to demonstrate any factors potentially determining the outcome of competition. Eretmocerus mundus clearly prevailed over E. formosa when multi‐parasitism occurred. A higher percentage of adults emerging from multi‐parasitized hosts belonged to this parasitoid species (68.0–88.9% depending on the treatment). The lowest percent emergence by E. mundus (68.0%) and total percent emergence of parasitoid adults (52.2%) were obtained when E. mundus first instars interacted with hosts parasitized by E. formosa third instars. Observations and dissections showed that first‐instar E. mundus induced mortality in E. formosa immatures at penetration into the hosts, although they encountered greater difficulty in exploiting hosts inside which E. formosa had reached the third stage of development. In contrast, development of E. formosa immatures was not immediately inhibited if parasitization took place on hosts inside which E. mundus larvae had already penetrated. In this case, however, E. mundus also prevailed over E. formosa (72.5% of the emerged adults). Implications for the use of these parasitoid species against B. tabaci in biological control programmes are discussed.     

Effects of temperature on the growth and reproduction characteristics of Bemisia tabaci B‐biotype and Trialeurodes vaporariorum

The development period, survival rate, longevity and fecundity of two whiteflies, Bemisia tabaci B‐biotype and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) were compared under different temperature laboratory conditions (15°C, 18°C, 21°C and 24°C). Egg development of B. tabaci B‐biotype was significantly longer compared with that of T. vaporariorum at 15°C, 18°C and 24°C. Significantly longer pseudo‐pupae development and lower survival rate were found in B. tabaci B‐biotype at 15°C compared with those at 18°C, 21°C and 24°C. Significantly higher fecundity was found in B. tabaci B‐biotype at 24°C compared with that at 15°C, 18°C and 21°C. However, the fecundity of T. vaporariorum was significantly lower at 24°C relative to that at 15°C, 18°C and 21°C. Significantly shorter 1st instar larval development was found in T. vaporariorum compared with that of B. tabaci at 15°C and 18°C. Significantly longer 2nd instar larval development was found in B. tabaci and T. vaporariorum at 15°C compared with that at 18°C, 21°C and 24°C. However, significantly shorter 3rd instar larval development was found in T. vaporariorum compared with that of B. tabaci at 15°C, 18°C and 24°C. The adaptive divergence of tolerance to relatively low temperature may be an important factor that results in the interspecific differentiation between the seasonal dynamics of these two whiteflies in China.     

Beauveria bassiana ARP14 a potential entomopathogenic fungus against Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae)

The sweet potato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), and the greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), are important pests of protected crops grown in warm climates. We compared efficacy of a new strain of the entomopathogenic fungus Beauveria bassiana (ARP14) isolated from Riptortus pedestris (Hemiptera: Alydidae) with a commercial strain (GHA) against different life stages of both B. tabaci and T. vaporariorum. Eggs, nymphs, and adults were exposed to 1 × 10⁸ conidia/mL of each strain using the leaf-dipping method. The mycosis rate of B. tabaci eggs (as a proportion) was relatively low (0.13 for B. bassiana ARP14 and 0.10 for B. bassiana GHA), while, for T. vaporariorum eggs, mycosis rate was 0.44 for B. bassiana GHA and 0.27 for B. bassiana ARP14. However, mycosis rate of 1st instars of both whiteflies was much higher than for eggs, for both strains (ARP14 and GHA). The developmental period of B. tabaci eggs exposed to ARP14 was significantly shorter than for either eggs treated with GHA or the control. For 2nd and 4th instar nymphs and adults of both whiteflies there were no differences in mycosis rates between the two B. bassiana strains. These results suggest that, B. bassiana ARP14 could be commercialized as a native biological control agent for control of B. tabaci and T. vaporariorum.     

Comparison of Searching Behaviour of Two Aphelinid Parasitoids of the Greenhouse Whitefly, Trialeurodes vaporariorum under Summer vs. Winter Conditions in a Temperate Climate

Searching behaviour of two aphelinid parasitoids, Encarsia formosa Gahan and Eretmocerus eremicus Rose and Zolnerowich, was compared in a controlled environment under simulated summer [high light intensity (83 ± 1 W/m²), and 24 ± 1°C] and winter [low light intensity (11 ± 0.5 W/m²), and 20 ± 1°C] greenhouse conditions on tomato leaflets, with and without a single 3rd instar whitefly host, Trialeurodes vaporariorum (Westwood), within a 4-cm tomato leaflet arena. Residence time of both parasitoid species was longer on infested leaflets vs. clean leaflets, and longer under winter than summer conditions. When parasitoids encountered a host on infested leaflets, residence time increased. In all cases, residence time of E. formosa was longer that of E. eremicus. Proportion of time spent searching (i.e. antennating leaf surface while walking or standing still) was longer on clean vs. infested leaflets for both E. formosa and E. eremicus. Walking speed by E. eremicus on clean leaflets was faster than E. formosa under both summer and winter conditions. Host handling time and proportion of host acceptance did not vary among parasitoids. These findings suggest that E. eremicus could be more efficient in host finding on tomato leaflets than E. formosa over all seasons, especially in the winter when natural light is limiting and where daylight temperatures are ≥20°C.     

Host-feeding of three parasitoid species on Bemisia tabaci biotype B and implications for whitefly biological control

Parasitoids in the genera Encarsia and Eretmocerus (Hymenoptera: Aphelinidae) are important biological control agents of whiteflies through their reproductive as well as host‐feeding activities. The feeding capacities of female parasitoids of three species with different reproductive strategies [Encarsia sophia (Girault & Dodd), Encarsia formosa Gahan, and Eretmocerus melanoscutus Zolnerowich & Rose] on their host, sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype B (Homoptera: Aleyrodidae), were evaluated on cabbage in a single‐instar no‐choice experiment in the laboratory and a mixed‐instar choice experiment in the greenhouse. In both single‐ and mixed‐instar experiments, significant differences in host‐feeding capacities were found among the three parasitoid species. Encarsia sophia exhibited superior capacity of host‐feeding compared to E. formosa and E. melanoscutus. In the single‐instar experiment, parasitoids fed more on younger (smaller) hosts than older (larger) hosts. In the mixed‐instar experiments, all three parasitoid species exhibited a clear preference for feeding on older hosts compared to younger hosts. Total number of whitefly nymphs fed on by E. sophia was approximately three times that of the other two parasitoid species. Whitefly mortality accounted for by host‐feeding by E. sophia was up to 59.7%, and, thus, equivalent to parasitization. The significance of host‐feeding of E. sophia for biological control of B. tabaci is discussed.     

B型烟粉虱与温室白粉虱不同虫态的碱性磷酸酶性质比较

为了探明B型烟粉虱Bemisia tabaci B-biotype 和温室白粉虱Trialeurodes vaporariorum体内的碱性磷酸酶(alkaline phosphatase,ALP)在两者竞争替代中所起的作用,以对硝基苯磷酸二钠 (pNPP)为底物,采用个体测定和群体测定的方法,研究比较了2种粉虱不同虫态中该酶的性质。结果表明：2种粉虱的碱性磷酸酶比活力在整个发育历期均逐渐增加,成虫期达到最大。温室白粉虱2至4龄若虫（伪蛹）期的碱性磷酸酶比活力分别是B型烟粉虱对应龄期酶比活力的2.58、2.68和3.14倍; B型烟粉虱雌雄成虫的碱性磷酸酶比活力分别是温室白粉虱雌雄成虫酶比活力的1.24和1.26倍,且2种粉虱雌虫的酶比活力显著大于其雄虫。2种粉虱2龄若虫到成虫的碱性磷酸酶最适pH均为7.8,最适温度均为47℃;在1龄若虫中均未能检测到该酶活性。测定并比较2种粉虱不同虫态碱性磷酸酶动力学特征参数的结果显示,温室白粉虱碱性磷酸酶在3、4龄若虫的亲和力以及在2, 3, 4龄若虫的酶蛋白浓度均显著大于B型烟粉虱的对应值,而在成虫期2种粉虱的亲和力、酶蛋白浓度无差异,B型烟粉虱的活化能显著小于温室白粉虱。据此推测,B型烟粉虱利用碱性磷酸酶在若虫期进行组织骨化和生长发育不如温室白粉虱,但羽化为成虫后利用其进行解毒代谢则可能强于温室白粉虱。     

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.     

Efficacy of multiple biocontrol agents against the sweet potato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on tomato

Abstract: Biological control provides an environmentally harmonious and potentially stable management tactic to combat noxious pests such as Bemisia tabaci, notorious for its resistance to synthetic pesticides. Bioassays conducted under control chamber conditions integrating applications of the parasitoid Encarsia formosa, reared for 20 years on Trialeurodes vaporariorum, and the fungus Verticillium lecanii on the third‐fourth instar nymphs of B. tabaci on tomato, showed a comparable effect between the parasitoid‐fungus combined treatment and the fungus treatment alone (70.7% vs. 70.4%). Analysis of our results indicates antagonism between the two biocontrol agents related to the parasitoids’ ability to discriminate between infected and healthy B. tabaci nymphs. The parasitoid treatment alone produced 36.3% mortality, with no mortality in the distilled water controls. The behavioural performance of the parasitoid could have either genetic or environmental causes. Bioassays studying the feeding habit of the imported mirid predator Macrolophus caliginosus (adults) and the indigenous mirid Camptotylus reuteri (nymphs and adults) on eggs, or early second instar nymphs of B. tabaci, and choice preference tests indicated a significant difference in feeding between M. caliginosus and C. reuteri. There was no significant difference in percentage feeding of M. caliginosus on eggs (2.2%) or second instar nymphs (8.0%). There was a significant difference in feeding of M. caliginosus adults (18.6%) when offered eggs and second instars in the same arena compared with eggs or second instars offered separately. These results could be attributed to the biological behaviour of the predator having a type III functional response. Studies with the local C. reuteri species showed no significant difference in adult and nymphal consumption on second instars of B. tabaci compared with nymphs on eggs. However, C. reuteri adults fed less on eggs compared with nymphs. This local predatory species appears to be more efficient than M. caliginosus in feeding on particular stages of B. tabaci without depending on prey density. This is further supported by the low consumption of both adults and nymphs in the choice test (4% and 2.3%, respectively) compared with M. caliginosus adults (18.6%).     

Egg allocation of the autoparasitoid encarsia tricolor at different relative densities of the primary host (Trialeurodes vaporariorum) and two secondary hosts (Encarsia formosa and E. tricolor)

Parasitism, offspring sex ratio and superparasitism of the facultative autoparasitoid Encarsia tricolor Foërster (Hymenoptera: Aphelinidae) when given access to arenae with different proportions of the primary host (Trialeurodes vaporariorum (Westwood)) and two species of secondary hosts (E. tricolor and Encarsia formosa Gahan) were studied.Parasitism and offspring sex ratio were not affected by female age in the range 3–10 days old. When the secondary hosts were young E. tricolor pupae, eggs were mostly laid on primary hosts, so the offspring sex ratio was more female-biased than expected, and secondary hosts were not superparasitized at all. When the secondary hosts were fully grown E. formosa larvae, superparasitism was small and offspring sex ratio was more male-biased than expected. E. tricolor females were able to discriminate between hosts previously parasitized by themselves and non-parasitized hosts.     

Identification,comparison, and functional analysis of salivary phenol‐oxidizing enzymes in Bemisia tabaci B and Trialeurodes vaporariorum

The differences in the ability of the invading whitefly, Bemisia tabaci (Gennadius) (commonly known as biotype B and hereafter as B) and Trialeurodes vaporariorum (Westwood) (both Hemiptera: Aleyrodidae) to utilize salivary phenol‐oxidizing enzymes – polyphenol oxidase (PPO) and peroxidase (POD) to detoxify plant defensive phenolic compounds were explored. Polyphenol oxidase and POD were found in the saliva of both B and T. vaporariorum. For tomato colonies, the PPO and POD activities in the watery saliva of B were 2.27‐ and 1.34‐fold higher than those of T. vaporariorum. The PPO activities against specific phenolic compounds commonly found in plants were compared. The activities of those from B were significantly greater than those from T. vaporariorum. We also measured PPO activity in both species after they had fed on plants that were undamaged or had been previously damaged with either a plant pathogen [Phytophthora infestans (Mont.) de Bary (Peronosporales)] infection, mechanical damage, B infestation, or exogenous salicylic acid. For B, PPO activities in watery saliva increased 229, 184, 152, and 139% in response to the four treatments, whereas those of T. vaporariorum only increased 133, 119, 113, and 103%, respectively. Biotype B infestation significantly increased the total phenolic content of tomato leaves. Meanwhile, feeding on tomato infestation with B had no significant effect on the survival rate of B, but decreased the survival rate of T. vaporariorum significantly. These results suggest that B has stronger ability utilizing PPO to detoxify high concentrations of phenolics than T. vaporariorum, and this contributes to a significant advantage for B to hold high fitness on plants with induced resistance. Possible roles of salivary PPO in the competition between B and T. vaporariorum are discussed.     

Chromosome‐level genome assembly of the greenhouse whitefly (Trialeurodes vaporariorum Westwood)

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is an agricultural pest of global importance. Here we report a 787‐Mb high‐quality draft genome sequence of T. vaporariorum assembled from PacBio long reads and Hi‐C chromatin interaction maps, which has scaffold and contig N50 lengths of 70 Mb and 500 kb, respectively, and contains 18,275 protein‐coding genes. About 98.8% of the assembled contigs were placed onto the 11 T. vaporariorum chromosomes. Comparative genomic analysis reveals significantly expanded gene families such as aspartyl proteases in T. vaporariorum compared to Bemisia tabaci Mediterranean (MED) and Middle East‐Asia Minor 1 (MEAM1). Furthermore, the cytochrome CYP6 subfamily shows significant expansion in T. vaporariorum and several genes in this subfamily display developmental stage‐specific expression patterns. The high‐quality T. vaporariorum genome provides a valuable resource for research in a broad range of areas such as fundamental molecular ecology, insect–plant/insect–microorganism or virus interactions and pest resistance management.     

New records of entomopathogenic fungi infecting Bemisia tabaci and Trialeurodes vaporariorum, pests of horticultural crops, in Argentina

The whiteflies Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) are major crop pests throughout the world. Although extensive research about biological control of whitefly by parasitoids and predators has been conducted, also entomopathogenic fungi can be considered as potential biological control agents. Surveys for entomopathogenic fungi were carried out in organic and conventional horticultural crops in greenhouses and open fields in Buenos Aires and Corrientes provinces, Argentina. These surveys resulted in the recovery and isolation of the following fungi from whiteflies: Lecanicillium lecanii (Zimmerm.) Zare & W. Gams, L. muscarium (Petch) Zare & W. Gams, L. longisporum (Petch) Zare & W. Gams, Isaria fumosorosea Wize and I. javanica (Frieder. & Bally) Samson & Hywel-Jones. Pathogenicity tests were conducted against T. vaporariorum nymphs using a conidial suspension (1 × 10⁷ conidia/ml) of the fungi. A mortality rate between 26.6% and 76.6% was obtained at 7 days post-infection. These are the first records of natural infections in the southernmost region of the South American continent of L. lecanii, L. muscarium, L. longisporum and Isaria javanica (Ascomycota: Hypocreales) on T. vaporariorum and also the first report of I. fumosorosea on B. tabaci.     

Developmental rates of two congeneric parasitoids,Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), utilizing different egg provisioning strategies

Endoparasitic Hymenoptera vary in the extent to which they provision their eggs and thus in the degree to which they appear to rely on their hosts for resources during embryonic development. In this study, developmental rates were examined in two congeneric parasitoid species, Encarsia formosa and E. pergandiella, that provision their eggs to different degrees. E. formosa eggs are much larger than E. pergandiella eggs. E. formosa eggs hatch significantly earlier than the eggs of E. pergandiella when deposited in 1st or 4th instar nymphs of a common whitefly host, Bemisia tabaci. Both species hatch earlier in 4th instar nymphs, but the delay in hatching in hosts parasitized as 1st instars is much greater in E. pergandiella. While E. formosa develops more rapidly to the 1st larval instar, E. pergandiella emerge as adults significantly earlier, though smaller, than E. formosa adults regardless of the host instar parasitized. These findings show that the extent of provisioning in the eggs of these wasps does not strictly determine their order of progression through different stages of development.     

Compatibility among entomopathogenic hyphocreales and two beneficial insects used to control Trialeurodes vaporariorum (Hemiptera: Aleurodidae) in Mediterranean greenhouses

The effect of the combined use of Encarsia formosa or Macrolophus caliginosus and one of three marketed mycoinsecticides, Mycotal® (Leucanicillium muscarium-based), Naturalis-L™ (Beauveria bassiana-based) and PreFeRal® (Isaria fumosorosea-based), on the control of the whitefly, Trialeurodes vaporariorum, was studied under laboratory and greenhouse conditions. The results of both types of tests, the bioassays and the greenhouse trials, for all combinations of E. Formosa with each of the three mycoinsecticides showed that the total mortality of larval populations of T. vaporariorum was not affected. The mortality of T. vaporariorum larvae treated in the second instar revealed the capacity for both B. bassiana- and L. muscarium-based formulations and E. formosa to kill the host either separately or in association. Because of its higher pathogenic activity (under our test conditions), L. muscarium provoked a large proportion of mycoses in larvae exposed to parasitization. In contrast, the efficacy of parasitization was higher in larvae treated with B. bassiana and exposed to E. formosa because of a lower pathogenic activity of the fungus. Bioassays carried out with third-instar larvae of T. vaporariorum showed a low susceptibility to both tested fungi. Consequently, mortalities recorded in larvae subjected to the combined treatments by consecutive exposures or at 2-4 days post-parasitization were mainly caused by the development of the parasitoid. Greenhouse trials showed that fungus-induced mortality of T. vaporariorum in plants treated with L. muscarium, I. fumosorosea, and B. Bassiana was significant compare to control. L. muscarium, B. bassiana and I. fumosorosea killed young whitefly larvae and limited parasitization to 10% or less. Second-instar larvae of M. caliginosus were not susceptible to L. muscarium and B. bassiana formulations with any mode of contamination: direct spraying of larvae, spraying on the foliar substrate or by contaminated T. vaporariorum prey. In greenhouse trials, M. caliginosus populations treated with fungi were not significantly affected compared to controls.     

Genetic diversity and geographic distribution of Bemisia tabaci and Trialeurodes vaporariorum in Costa Rica

The tobacco whitefly Bemisia tabaci (Gennadius) cryptic species complex and of the greenhouse whitefly Trialeurodes vaporariorum (Westwood) are extensively reported as destructive pests in vegetable crops worldwide. A survey was conducted in 2011 and 2012 to determine the occurrence and genetic diversity present in the populations of these whiteflies in the major vegetable production areas of Costa Rica. Insect samples were collected from sweet pepper (Capsicum annuum L.), tomato (Solanum lycopersicum L.), common bean (Phaseolus vulgaris L.) and weeds present in commercial crops either in open field or greenhouse conditions. PCR‐RFLP analysis of mitochondrial cytochrome c oxidase subunit 1 gene (mtCOI) sequences of 621 whitefly individuals confirmed the presence of the Mediterranean (MED) type of the B. tabaci and of T. vaporariorum in most sampled regions. Also, individuals of the Middle East‐Asia Minor 1 (MEAM1) type of the B. tabaci were observed in low numbers. Contingency analyses based on type of crop, geographical region, whitefly species, year of collection and production system confirmed that T. vaporariorum was the most frequent species in vegetable production areas in Costa Rica, both in greenhouses and in open fields. B. tabaci MED is likely spreading to new areas of the country, whereas B. tabaci MEAM1 was mostly absent or rarely found. Comparisons of mtCOI sequences from B. tabaci individuals revealed the presence of four B. tabaci sequence haplotypes (named MED‐i, MED‐ii, MEAM1‐i, MEAM1‐xviii) in Costa Rica, three of them identical to B. tabaci haplotypes previously reported in the Western Hemisphere and other parts of the world. Analysis of sequences of T. vaporariorum individuals revealed a more complex population with the presence of 11 haplotypes, two of which were identical to T. vaporariorum sequences reported from other countries.     

Effects of host stage on the development of the facultative autoparasitoid Encarsia tricolor (Hymenoptera: Aphelinidae)

Encarsia tricolor is a facultative autoparasitoid of the glasshouse whitefly, Trialeurodes vaporariorum, with a potential in biological control. The rate of development, number of mature oocytes at emergence, number of ovarioles and size of the emerged adults were studied. Five nymphal instars (N1, N2, N3, N4, and pharate adult) of T. vaporariorum were used as hosts for the females. Female larvae and pupae of E. tricolor and Encarsia formosa were used as hosts for the males. Females developed faster when the egg was laid on N3 (18.0 days from egg to adult) and slower on N1 (22.3 days). Females were bigger when developing from N1 and N3 than from N4 and pharate adult. On emergence the mean number of mature oocytes was always small (0.8–2.6). Males developed faster and were smaller than females, and developed faster and were larger on larvae of E. formosa.