Egg Size, Intrinsic Competition, and Lethal Interference in the Parasitoids Encarsia pergandiella and Encarsia formosa

Recent population dynamic theory predicts that disruption of biological control may occur when one parasitoid species' superiority in intrinsic competition is associated with a lower ability to find and exploit hosts (i.e., ability in extrinsic competition). One might expect such a trade-off, for instance, if parasitoids with larger (and fewer) eggs are more likely to prevail in intrinsic competition than species with smaller (and more numerous) eggs. We tested the idea that relative egg size could be used to predict the outcome of intrinsic competition in two closely related endoparasitoids, Encarsia pergandiella Howard and Encarsia formosa Gahan. Contrary to expectation, the parasitoid species with smaller eggs, E. pergandiella, prevailed in intrinsic competition, regardless of the order that hosts were exposed to the two species. In a literature survey, we found four studies of competing pairs of endoparasitoid species for which: (a) egg size estimates were available and (b) one species was consistently superior in intrinsic competition. In three of the four studies, the small-egged species prevailed in intrinsic competition, as we also found. Although E. formosa lost in intrinsic competition, this species negatively affected E. pergandiella's progeny production by host feeding on and killing hosts containing E. pergandiella eggs. E. formosa females also host fed on conspecific-parasitized hosts. As a mechanism of both intra- and interspecific interference competition, host feeding on parasitized hosts contradicts assumptions about the nature of interference competition in existing population dynamics models.     

Secondary host choice by the autoparasitoid Encarsia pergandiella

Autoparasitoids are species of parasitic wasps in the family Aphelinidae which produce females as solitary primary endoparasitoids of homopterans such as whitefly and scale insects (primary hosts), and males as solitary hyperparasitoids. Males generally develop on immature conspecific females or on individuals of other primary parasitoid species (secondary hosts). Encarsia pergandiella is an autoparasitoid that has been introduced to Italy for control of greenhouse whitefly Trialeurodes vaporariorum, in greenhouses and field crops. In this study we examined the secondary host selection behaviour of this species with regard to conspecific females and females of two thelytokous species, E. formosa and E. meritoria. Encarsia formosa has been used successfully for greenhouse whitefly control in Northern Europe, but has not been effective in Southern Italy in winter crops in unheated greenhouses. E. meritoria has recently spread in Italy, and may have potential for biological control of whitefly in the greenhouse environment. In the first experiment, female E. pergandiella were exposed to one of three pair-wise combinations of the three species in petri dish arenas. Parasitism was determined by dissection of the hosts. The number of hosts parasitized by E. pergandiella females did not differ with host species. However, significantly greater numbers of eggs were laid in E. meritoria in both treatments in which it was present; these hosts were more likely to be superparasitized. In a second experiment, observations of females in arenas with equal numbers of all three host species indicated that females encountered and parasitized all host species with approximately equal frequency, although the length of time females spent in the oviposition posture differed with host species.     

The effect of nitrogen fertilizer applied to Euphorbia pulcherrima on the parasitization of Bemisia argentifolii by the parasitoid Encarsia formosa

More wasps of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) were found on fertilized poinsettias, Euphorbia pulcherrima (Willd.) (Euphorbiaceae), than on non-fertilized plants. Parasitization of Bemisia argentifolii Bellows & Perring (Homoptera: Aleyrodidae) by E. formosa was higher on plants treated with calcium nitrate than with ammonium nitrate or on control plants. In a no-choice test, host feeding by E. formosa was higher when hosts were on fertilized plants than when hosts were on control plants. The nitrogen content of whitefly pupae reared on plants treated with ammonium nitrate was higher than those on calcium nitrate-treated plants.Variability in the parasitization of B. argentifolii by E. formosa appears to be due to host plant-mediated differences in the whiteflies. E. formosa may be influenced by the nutritional suitability of the host, which influences whether wasps continue to oviposit, feed, or disperse.     

Host selection by the autoparasitoid Encarsia pergandiella on primary (Bemisia tabaci) and secondary (Eretmocerus mundus) hosts

In autoparasitoids, females are generally primary endoparasitoids of Hemiptera, while males are hyperparasitoids developing in or on conspecific females or other primary parasitoids. Female‐host acceptance can be influenced by extrinsic and/or intrinsic factors. In this paper, we are concerned with intrinsic factors such as nutritional status, mating status, etc. We observed the behavior of Encarsia pergandiella Howard (Hymenoptera: Aphelinidae) females when parasitizing primary (3rd instar larvae of Bemisia tabaci Gennadius [Homoptera: Aleyrodidae]) and secondary hosts (3rd instar larvae and pupae of Eretmocerus mundus Mercet [Hymenoptera: Aphelinidae]) for a period of 1 h. Females had different reproductive (virgin or mated younger) and physiological (fed elder or mated elder) status. Virgin females killed a large number of secondary hosts while investing a long time per host. However, they did not feed upon them. Mated females killed a lower number of secondary hosts and host feeding was observed in both consuming primary and secondary hosts. It was common to observe host examining females of all physiological statues tested repeatedly stinging the same hosts when parasitizing, killing or rejecting them. Fed elder females parasitized more B. tabaci larvae than E. mundus larvae or pupae, while investing less time on the primary host than on the secondary host. They also parasitized more B. tabaci larvae than mated elder females, while investing less time per host. The access of females to honey allowed them to lay more eggs.     

Comparison of Foraging Behavior, Interspecific Host Discrimination, and Competition of Encarsia formosa and Amitus fuscipennis

The foraging behavior of Amitus fuscipennis MacGown & Nebeker and Encarsia formosa Gahan was studied on tomato leaflets with 20 Trialeurodes vaporariorum (Westwood) larvae in the first or third stage. Ten of the whitefly larvae were previously parasitized and contained a conspecific or a heterospecific parasitoid egg or larva. The host type (host stage and/or previous parasitization) did not influence the foraging behavior of either parasitoid species. The residence time on these tomato leaflets was about 0.9 h for A. fuscipennis and 1.9 h for E. formosa. Amitus fuscipennis hardly stood still and fed little, while E. formosa showed extensive standing still and feeding. As a result, the time walking while drumming was similar for both parasitoid species. The numbers of host encounters and ovipositions per leaflet were similar for both parasitoid species. However, the residence time of A. fuscipennis was half as long as that of E. formosa so the rate of encounters and ovipositions was higher for A. fuscipennis. Amitus fuscipennis is more efficient in finding and parasitizing hosts under these conditions. The walking activity and host acceptance of the synovigenic E. formosa diminished with the number of ovipositions, but not those of the proovigenic A. fuscipennis. Encarsia formosa is egg limited, while A. fuscipennis is time limited because of its short life span and high egg load. Both parasitoid species discriminated well between unparasitized larvae and self-parasitized larvae, but discriminated poorly those larvae parasitized by a conspecific and did not discriminate larvae parasitized by a heterospecific. Self-superparasitism, conspecific superparasitism, and multiparasitism were observed for both parasitoid species. Superparasitism always resulted in the emergence of one parasitoid and multiparasitism resulted in a higher emergence of one parasitoid of the species that had parasitized first. The data suggest that A. fuscipennis is a good candidate for use in biological control of high-density spots of T. vaporariorum when we consider its high encounter and oviposition rate.     

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.     

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.     

Poinsettia (Euphorbia pulcherrima Willd Ex Koltz) Cultivar-Mediated Differences in Performance of Five Natural Enemies of Bemisia argentifolii Bellows and Perring, n. sp. (Homoptera: Aleyrodidae)

Laboratory evaluations of five natural enemies of the silverleaf whitefly, Bemisia argentifolii Bellows and Perring, n. sp., were conducted to determine their potential as biological control agents in greenhouse poinsettia ranges. Adult longevity, prey consumption or host feeding and parasitism rates, and parasitoid emergence were measured for one predator, Delphastus pusillus LeConte, and four parasitoids, Encarsia formosa Gahan, Encarsia luteola Howard, Encarsia pergandiella Howard, and Encarsia transvena (Timberlake), as possible indicators of efficacy. Characterization of each parameter was performed on two poinsettia cultivars: the first, ′Annette Hegg Brilliant Diamond,′ has trichome densities on the leaf undersurfaces approximately 15% less than the trichome densities on the leaf undersurfaces of the second cultivar, ′Lilo.′ Adult longevity varied significantly between natural enemies (ranging from an average high of 85.2 days for female D. pusillus feeding on B. argentifolii nymphs to an average low of 2.8 days for the Canada colony of E. formosa), but not between cultivar. Prey consumption and oviposition by D. pusillus varied between prey type (nymphs consumed > eggs consumed) and poinsettia cultivar (′Annette Hegg Brilliant Diamond′ > ′Lilo′). Host feeding, parasitism and total number of B. argentifolii nymphs killed varied significantly among Encarsia spp., but no single wasp performed better than the rest across all three parameters. Host feeding, parasitism, and total number of nymphs killed were greater on ′Annette Hegg Brilliant Diamond′ than on ′Lilo′ and this difference was consistent among the four parasitoid species. Among parasitoid species differences in percentage emergence were consistent between the two poinsettia cultivars with emergence from parasitized nymphs on ′Lilo′ being greater than emergence on ′Annette Hegg Brilliant Diamond.′ Results from these evaluations suggest that the probability of achieving successful augmentative biological central will be greater on poinsettia cultivars with fewer trichomes. In addition, achieving biological control is likely to be difficult with releases of E. transvena, but a greater chance for success may be possible through releases of D. pusillus when whitefly densities are high or through releases of E. formosa (Beltsville colony) or mated E. pergandiella independent of whitefly densities.     

Hyperparasitism behaviour of the autoparasitoid <Emphasis Type="Italic">Encarsia tricolor</Emphasis> on two secondary host species

Hyperparasitism by virgin female Encarsia tricolor was studied by direct observation of its behaviour when contacting two secondary host species (Encarsia formosa and E. tricolor) at different host stages (first and second larval stage, third larval stage, and pupal stage). The searching and hyperparasitism behavioural sequence of E. tricolor was independent of the host stage of the whitefly (Aleyrodes proletella), and was similar to several related primary parasitoid species. In experiments with equal numbers of secondary hosts, encounter frequencies were equal for both secondary host species in all developmental stages observed. However, rates of hyperparastism were different according to host stage and host species. Hosts in the late larval stages were most preferred for hyperparasitization and the heterospecific E. formosa was more preferred as a secondary host than the conspecific, E. tricolor, in particular from the prepupal stage onwards. The window of vulnerability, i.e., the duration of the period in which a secondary host is susceptible to hyperparasitism, was largely determined by the occurrence and rate of melanization after the onset of pupation. The duration of a successful hyperparasitization event was longer than one that failed. Superparasitism occurred only once in all cases. The potential effect of autoparasitoids on biological control programs and the consequences for selection and release of an effective, yet ecologically safe agent are discussed. Handling editor: Torsten Meiners.     

Temperature dependent functional response ofEncarsia formosa parasitizing the Poinsettia-strain of the cotton whitefly,bemisia tabaci, on Poinsettia

The control efficiency and performance ofEncarsia formosa Gahan (Hymenoptera: Aphelinidae) as influenced by the density of its host, the Poinsettia-strain ofBemisia tabaci Gennadius (Homoptera: Aleyrodidae), were investigated by laboratory experiments on Poinsettia (Euphorbia pulcherrrima Willd.).E. formosa showed a Type II functional response to fourth instar larvae ofB. tabaci, the response plateau increasing with temperature. A response model for randomly searching parasitoids incorporating temperature-dependent handling time and temperature-independent search rate was in accordance with the results, and gave an estimated search rate of 0.033 leaf·hour⁻¹ and handling times of 1.54, 2.86 and 20.1 h at 28°C, 22°C and 16°C, respectively. From the latter, the maximum number of hosts that can be parasitized at the three temperatures are 10.4, 5.6 and 0.8 larvae per day (provided the light period is 16 h). The number of hosts with ovipositor punctures was higher than the number of parasitized hosts, especially at 22°C and 28°C, implying thatE. formosa refrains from laying eggs in some of the hosts examined with the ovipositor. About 31% of the punctured larvae did not contain any eggs. Superparasitism occured during the experiment presumably originating from young, inexperienced parasitoids. Individual larvae were occasionally punctured several times, also by non-superparasitizingE. formosa. The resulting distribution of ovipositior holes was random, indicating thatE. formosa on the basis of antennal testing is unable to determine if a larva has previously been examined with the ovipositor. Almost fifty percent of the punctures were not followed by egg-depositions. Besides parasitizationE. formosa used hosts as food source. The number of hostfed larvae was independent of density, but varied with temperature being highest at 28°C (0.12 hostfed larvae per parasitoid per day).