Analysis of Foraging Behaviour of the Whitefly Parasitoid Encarsia formosa on a plant: A Simulation Study

The foraging behaviour of Encarsia formosa was analyzed using a stochastic simulation model of the parasitoid's behaviour. Parasitoids were allowed to search during a day on a tomato plant infested with immatures of the greenhouse whitefly, Trialeurodes vaporariorum. The model simulates searching, host selection, host handling and patch leaving behaviour, and the physiological state of the parasitoid. The outputs of the model are the number of visited leaflets and the number of hosts encountered, parasitized or killed by host feeding. The simulation results agreed well with observations of parasitoids foraging on tomato plants. The number of encounters and ovipositions on the plant increased with host density according to a type II functional response. At a clustered host distribution over leaflets and low host densities, the most important parameters affecting the number of ovipositions were the leaf area, the parasitoid's walking speed and walking activity, the probability of oviposition after encountering a host, the initial egg load and the ratio of search times on both leaf sides. At high densities, the maximum egg load and the giving-up time on a leaflet since latest host encounter were the most essential parameters.     

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.     

Egg-limited functional response of Uscana lariophaga, egg parasitoid of bruchid beetle pests in stored cowpea

The functional response of the egg parasitoid Uscana lariophaga Steffan (Hymenoptera: Trichogrammatidae) to eggs of its host Callosobruchus maculatus Fab. (Coleoptera: Bruchidae) was investigated in storage containers filled with a cowpea (Vigna unguiculata Walp.) seed mass. Foraging time was limited to 4 or 24 h. These indirect experiments were supplemented by direct observations of the parasitoid's handling time, egg-laying capacity and initial egg load. The foraging process of U. lariophaga can be divided into two distinct stages: the process leading to detection of host clusters and, after arrival within a host cluster, the response of the parasitoid to the host density within the cluster. The chance that a cluster is found by U. lariophaga appeared independent of the number of host eggs per cluster, but was influenced by the available foraging time. Within a host cluster, U. lariophaga demonstrated a Holling II type functional response. Parasitoids were strongly arrested in host clusters, leading to high levels of parasitism. Direct observations proved that handling time was not a limiting factor, but that U. lariophaga's initial egg load and egg maturation rate limited the plateau level of her functional response. As such, direct observations were essential for a correct interpretation of the mechanisms underlying the shape of the functional response.     

‘Males second’ strategy in the allocation of sexes by the parasitic wasp,Gryon japonicum

Summary Patterns of the sex ratio allocation of Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae), a solitary egg parasitoid of Riptortus clavatus (Thunberg) (Heteroptera: Alydidae), were investigated in the laboratory, and the result was checked against the field data on the sex composition of the parasitoid. When five host eggs were presented simultaneously to each of the females of G. japonicum in a laboratory experiment, they had a strong tendency to lay a male egg in second host egg and female eggs in the others. However, when four host eggs were presented to each female more than 3 h after the completion of oviposition on a host egg, most of the females laid male eggs in the third oviposition, i.e. the second host eggs after the experimental interruption of oviposition. These results indicated that there was a mechanism for G. japonicum to produce a male egg in the second host egg in consecutive ovipositions, and that the mechanism was reset by more than 3 h intervals of oviposition. By this mechanism, G. japonicum is thought to produce the precise sex ratio in response to the size of a host egg batch. Field data on the size of a host egg batch and the sex composition of the parasitoid in a host egg batch supported this view.     

Foraging behaviour of the whitefly parasitoidEncarsia formosa on tomato leaflets

IndividualEncarsia formosa parasitoids were observed continuously until the parasitoids flew away, either on clean tomato leaflets, on leaflets with honeydew, or on leaflets with unparasitized and parasitized whitefly larvae. Encounters with unparasitized and parasitized whitefly larvae, and contact with honeydew arrested the parasitoids on the leaflet. The walking speed increased linearly from 0.179 to 0.529 mm/s between 15 and 25–30°C. The walking activity showed another relationship with temperature: it was below 10% at 15 and 18°C, and increased to about 75% at 20, 25 and 30°C. It was not affected by host encounters or by 1 to 4 ovipositions. The total handling time of hosts was between 1.8–21.8% of the total time on the leaflet. Self-superparasitism was not observed. Conspecific-superparasitism did occur in 14% of the encounters with hosts containing a parasitoid egg, but was not observed anymore when the parasitoid egg had hatched. Experienced parasitoids superparasitized as often as naive females. The foraging behaviour ofE. formosa from landing on a leaf until departure has now been quantified and is discussed.     

Patch Time Allocation by the Parasitoid <Emphasis Type="Italic">Diadegma semiclausum</Emphasis> (Hymenoptera: Ichneumonidae). II. Effects of Host Density and Distribution

This study investigated the effects of host density and distribution on the patch-leaving behavior of Diadegma semiclausum (Hymenoptera: Ichneumonidae), a solitary endoparasitoid of larval Plutella xylostella (Lepidoptera: Plutellidae). Individual female wasps were released onto an experimental plant infested with host larvae at different densities and distributions, and were allowed to freely leave for an alternative host plant placed upwind of the experimental plant in a wind tunnel. The influence of host density and distribution, as well as within-patch foraging experience, on the parasitoids patch-leaving tendency was analyzed by means of the proportional hazards model. This study aimed to test the predictions of a number of patch-leaving models, including the Marginal Value Theorem, rules of thumb, and incremental or countdown mechanisms. The parasitoids patch-leaving tendency decreased with increased host density, more clustered host distribution, and unsuccessful host encounter as a result of host defense, but increased with successful oviposition. None of the simple rules of thumb such as fixed time, fixed number of hosts parasitized, or fixed giving-up time was employed by this parasitoid. The results agreed with the general predictions of the Marginal Value Theorem that patch residence time and numbers of ovipositions by the parasitoid increased with increasing host density. The decreasing influence of oviposition on the parasitoids patch-leaving tendency, regardless of host density or distribution, was consistent with the prediction of a countdown mechanism.     

The pancreatic islets of the teleost Scorpaena scropha

Summary The principal pancreatic islets of the teleost Scorpaena scropha are found ultrastructurally to contain four different kinds of parenchymal cells, viz. ₁-(= D), ₂-, -and agranular cells. The -cells show considerable variations in the shape of the secretory granules. A peculiar feature is that many of these granules are composed of fibrillar subunits, often in parallel arrangement. All -granules are surrounded by membranes and between the membrane and the granule core there is a moderately wide electron lucent space. The electron density of the cytoplasm in the -cells varies somewhat. The ₂-cells possess typical secretory granules with an electron dense core and a closely applied membrane. The secretory granules in the ₁-cells show also a closely applied membrane but a less dense core. Also in the -cells the electron opacity of the cytoplasm varies. The agranular cells are mainly characterized by low cytoplasmic electron density, narrow cisterns of endoplasmic reticulum and sometimes a laminated Golgi complex. Small immature secretory granules are occasionally seen in the cytoplasm of these cells. The significance of the fibrillar -granules remains obscure.This work was supported by grants from the Nordic Insulin Fund, the Town of Umeå, the Swedish Medical Research Council (Project No. B69-12X-718-04A), and by a postdoctoral fellowship from the United States Public Health Service.     

Influence of initial egg density and host size on the development of the gregarious parasitoid <Emphasis Type="Italic">Bracon hebetor</Emphasis> on three different host species

Bracon hebetor (Say) (Hymenoptera : Braconidae) is a gregarious parasitoid that attacks a variety of important lepidopterous pests of stored product and in the field. In this study the effect of host species, size and larval competition on parasitoid size, survival and development were investigated. In laboratory studies, wasp eggs at a range of densities, were placed on larvae of different weight of three Lepidoptera host species namely Adoxophyes orana (Fischer von Röslerstamm, Tortricidae), Plodia interpunctella (Hubner, Pyralidae) and, Lobesia botrana(Dennis & Schiffermueller, Tortricidae). On A. orana survival of immature parasitoids was very low at all densities and different host weights. On L. botrana survival progressively reduced as egg density increased at both host weights examined for this host. Survival on P. interpunctella was significantly affected by egg density but not by host weight. Initial egg density had a significant effect on the size of emerging adults from each rearing host. Smaller adult parasitoids emerged as egg density per larva increased. Larval host weight of P. interpunctella and A. orana had a significant effect on the size of emerging adult parasitoids mainly at the higher egg densities used in these experiments. The above results of host quality on fitness of parasitoid are discussed.     

Adaptive significance of egg size plasticity in response to temperature in the migrant skipper, Parnara guttata guttata (Lepidoptera: Hesperiidae)

Females of the migrant skipper, Parnara guttata guttata, that are reared under lower temperatures lay smaller eggs. The adaptive significance of egg size plasticity in response to temperature is unknown in this species. We suggest, based on the following experimental results, that P. g. guttata uses temperature as an indirect cue to predict the host condition (leaf toughness) of the next generation. First, larvae were reared under the typical conditions of temperature and photoperiod experienced during the immature stages in the first, second, and overwintering (third) generations (LD 16:8 at 25°C, LD 14:10 at 25°C and LD 14:10 at 20°C). Females reared under LD14:10 at 20°C produced more, smaller eggs than those reared under LD14:10 and LD16:8 at 25°C. Secondly, survival rates of first instar larvae derived from females reared under the three photoperiod/temperature treatments were measured on young soft rice leaves (soft), or tough, old rice leaves (tough). Survival rates of hatchlings reared on soft and tough leaves did not differ when females were reared under LD16:8 and LD14:10 at 25°C. However, hatchling survival was significantly higher on soft than on tough leaves when females were reared under LD14:10 at 20°C. Thirdly, we found that egg size plasticity in response to temperature in P. g. guttata may be a threshold response. Temperatures below 20°C experienced during the immature stages may be effective for production of smaller and more eggs in the overwintering generation of P. g. guttata.     

Foraging Behavior of the Parasitoid Encarsia formosa on Gerbera jamesonii Leaves

Insight into the foraging behavior of the parasitoid Encarsia formosa Gahan for whitefly hosts was gained by continuous observation of individual parasitoids on leaves of the ornamental plant Gerbera jamesonii, until females left the leaf. Comparison of the parasitoid behavior on three cultivars gave similar results. Mean searching time on uninfested G. jamesonii leaves of three cultivars was 1 h 30 min and the mean percentage of walking activity of the total observation time on those cultivars was 61%. Both parameters were not influenced by different leaf structures of Gerbera cultivars. Encounters with hosts arrested the parasitoids on the leaves. The walking activity and the percentage of host encounters that resulted in an oviposition decreased with decreasing egg load of the parasitoid. In comparison with tomato, where biological control of whiteflies is successful, only minor differences in the foraging behavior occur, except for the residence time of females, which was about three to four times longer on G. jamesonii leaves, but these leaves are about seven times larger than tomato leaves. The facts that (1) the foraging behavior of E. formosa on G. jamesonii is independant of the cultivar and (2) the foraging behavior is, in many aspects, similar to that on tomato suggest that biological control of whitefly on this ornamental plant is a potential option.     

Aspects of life-table studies and functional response of Lysiphlebia mirzai

The fecundity, reproductive rate, and survival of Lysiphlebia mirzai parasitising third instar nymphs of the cereal aphid Rhopalosiphum maidis were measured at six different host densities under constant laboratory conditions. The survival rate (l_x) of the female parasitoids was unaffected by host density, with an average adult life-span of 5–6 days at all densities. The age-specific fecundity rate (m_x) was host density-dependent. The value of m_x decreased rapidly from the first day of parasitisation. The number of hosts available determined the maximum possible number of mummies. At 200 hosts available per day, the average fecundity was 184.6 mummies/female; the maximum number of mummies yielded by any female was 200. The relationship between host density and the number of aphids parasitised per female was linear at 50 aphids/cage/day, but at higher host densities (100 aphids/cage/day) a significant curvilinear regression was observed. The intrinsic rate of natural increase (r_m) increased with increasing host density. Maximum value of r_m (0.262) was obtained at a host density of 200. The response of r_m to changes in host density and parasitoid sex ratio is shown. A typical type II functional response was observed for L. mirzai. The curve was described by a logistic curve, N_p=200/[1+exp(5.65–1.60 ln N_o)]. The search rate of the parasitoid was inverse host density-dependent. No significant variation in the sex ratio of F₁ offspring was observed at different initial host densities. Sex ratio values exceeded 0.5 at all host densities. The results evaluated the reproductive potential of L. mirzai as a promising biological control agent.     

Effects of diet on longevity and fecundity of the spined stilt bug, Jalysus wickhami

We evaluated the suitability of selected food items for the adult spined stilt bug, Jalysus wickhami Van Duzee (Hemiptera: Berytidae), by providing one of seven diet treatments: (1) prepupae of the parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae), on a leaf of tobacco (Nicotiana tabacum L., NC 2326) (Solanaceae); (2) C. congregata prepupae alone (i.e., no tobacco leaf); (3) eggs of the parasitoid's host, Manduca sexta (L.) (Lepidoptera: Sphingidae), on a tobacco leaf; (4) M. sexta eggs alone; (5) tobacco aphids, Myzus nicotianae Blackman (Homoptera: Aphididae), on a tobacco leaf; (6) a tobacco leaf alone; and (7) no prey and no tobacco. A tobacco leaf was necessary for the long-term survival of stilt bugs, but prey source did not affect longevity. Regardless of the prey type, stilt bugs with access to a tobacco leaf lived 21–23 days, while stilt bugs without access to tobacco lived less than 12 days. Animal prey provided a protein source required for egg deposition in J. wickhami, and prey species differed in their relative nutritive values. Female stilt bugs that fed on M. sexta eggs or on C. congregata prepupae were significantly more fecund (102 and 106 nymphs per female, respectively) than females that fed on tobacco aphids (24 nymphs per female). Results suggest that stilt bugs may feed on tobacco aphids and C. congregata prepupae when other prey are unavailable.     

Effects of Palpita unionalis and Galleria mellonella larval densities on functional response,egg dispersion and progeny sex ratio of Habrobracon hebetor

To assess the potential of the hymenopteran ectoparasitoid, Habrobracon hebetor Say as a biological control agent, we evaluated its response to different larval densities of two pyralid hosts, Palpita unionalis Hbn. and Galleria mellonella L. The former host is a serious pest of olive trees, whereas the latter is used as a factitious host in parasitoid mass rearing. In order to study the functional response of the parasitoid, five host densities (1, 2, 3, 5, 7) of either late instar larva per Petri dish were used. The shape of the functional response curve was determined using logistic regression and could be described as a type II response for both hosts, characterised by a monotonic decelerating increase in the number of hosts attacked with increasing host density. Female parasitoids allocated more eggs to the first larva attacked than all the remaining larvae. Aggregated dispersion patterns for parasitoid egg distribution at different host densities were estimated using the Green index. Multiple visits and ovipositions by females did not significantly affect the total number of progeny produced or their sex ratio. This study has generated novel information on egg laying, egg distribution and sex ratio of H. hebetor when reared on G. mellonella and has the potential to be used in the development of sustainable biological control programmes aimed at P. unionalis in olive orchards.     

Can there be an escalating arms race without coevolution? Implications from a host-parasitoid simulation

Summary Under a restricted set of conditions, predator-prey or parasite-host systems may exhibit an escalating arms race over several generations that is not coevolutionary. Preconditions for such a process include high correlation between prey/host quality and defensive capability, and phenotypic plasticity in predator/parasite-counter defenses that responds to quality. We present simulation models based on the parasitoid waspEurytoma gigantea, which lays its egg in the goldenrod gall induced by the flyEurosta solidaginis. For the parasitoid to successfully lay an egg, the gall walls must be thinner than the parasitoid's ovipositor is long. Wall thickness is highly correlated with gall size, so probability of successful attack declines with gall size. However, since the parasitoid eats the gall tissue, individuals developing in small galls have little food and mature with shorter ovipositors than those which develop in large galls. The simulation showed that the population mean parasitoid size is set by mean gall size. Since small galls are more frequently parasitized, there is a selection pressure on the gallmaker to induce larger galls. But, an additional simulation showed that since parasitoid ovipositor length depends on gall size, an evolutionary increase in gall size will also result in a non-evolutionary increase in parasitoid body size and ovipositor length over several generations.     

The Escherichia coli cell division proteins FtsY, FtsE and FtsX are inner membrane-associated

Summary The cell division genes ftsY, ftsE and ftsX form an operon mapping at 76 min on the Escherichia coli chromosome. The protein products of these genes have been indentified previously. We have studied the cellular location of the radiolabelled Fts proteins using maxicells and standard fractionation procedures. Previous protein sequence homologies suggested an inner membrane location for FtsE. We have confirmed this predicted location and have shown that FtsY and FtsX are also inner membrane-associated. These results are igreement with the hypothesis that FtsE may act at the inner membrane, in a septalsome complex, by coupling ATP hydrolysis to the process of bacterial cell division.     

Bionomics ofTrioxys indicus [Hym.: Aphidiidae], a parasitoid ofAphis craccivora [Hem.: Aphididae]: 31. Effect of host haemolymph on the numerical response of the parasitoid

The influence of kairomones on the numerical response of the parasitoidTrioxys indicus against its hostAphis craccivora at its varying density was studied. The kairomones (applied as aqueous extract of the host) significantly enhanced the rate of parasitisation and multiplication and the area of discovery of the parasitoid and also the K-values of mortality of the host at all parasitoid densities introduced (1, 2, 4, 8, 12 and 16 parasitoids) into troughs having about 200 hosts. The sex-ratio of F₁ offspring decreased at lower parasitoid densities and remained more or less unchanged at higher parasitoid densities after the application of kairomones. The present findings indicate that if kairomones are applied properly, the number of hosts destroyed by a stimulated parasitoid will be about 200, twice the number reported earlier, thus fewer parasitoids will be needed to regulate an estimated population of the hosts.      

The functional response of Uscana lariophaga under different egg distributions of its host Callosobruchus maculatus

The functional response of the egg parasitoid Uscana lariophaga Steffan (Hymenoptera: Trichogrammatidae) was tested under three different host distributions (even, clumped and random) within clusters of Callosobruchus maculatus Fab. (Coleoptera: Bruchidae) eggs. A Holling Type II functional response was found for all three distributions. Over low host densities, less than 50% of the host clusters was parasitized. At low host densities, U. lariophaga females parasitized significantly fewer eggs in random egg clusters with many beans than in clusters with fewer beans and an even or clumped egg distribution. At higher egg densities, plateau levels of maximum number of hosts parasitized were the same for all three egg distributions. Uscana lariophaga appears to be adapted to search for even or clustered egg distributions, as can be found in the field and under storage conditions.     

Cloning of Candida pelliculosa beta-glucosidase gene and its expression in Saccharomyces cerevisiae

Summary Candida pelliculosa var. acetaetherius is a strain of yeast which can utilize cellobiose as the carbon source. From a gene library prepared from this yeast, the -glucosidase gene has been cloned in a S. cerevisiae host using a chromogenic substrate, 5-bromo-4-chloro-3-indolyl--glucoside as an indicator. It was proved by Southern analysis that the DNA fragment carrying the -glucosidase gene originated from C. pelliculosa. -Glucosidase produced by S. cerevisiae transformants was secreted into the periplasmic space. In Candida, -glucosidase was not induced by cellobiose but was derepressed by lowering the concentration of glucose. The regulation of -glucosidase synthesis in S. cerevisiae carrying the cloned -glucosidase was not clear compared with that in Candida, however, the enzyme activity in low glucose medium (0.05%) was reproducibly higher than in high glucose medium (2%). We have found the sequence that controls the expression of the -glucosidase gene negatively in S. cerevisiae.     

Influence of host behavior and host size on the success of oviposition ofCotesia urabae andDolichogenidea eucalypti (Hymenoptera: Braconidae)

Behavioral interactions among Cotesia urabaeAustin and Allen, Dolichogenidea eucalyptiAustin and Allen (Hymenoptera: Braconidae), and their host Uraba lugensWalker, the gum leaf skeletonizer (Lepidoptera: Noctuidae), were observed at three host sizes over a 20-min period. These sizes were first instar (small, gregarious), fourth-fifth instar (mid, gregarious), sixth-seventh instar (large, solitary) larvae. Unlike C. urabae, D. eucalyptiused its legs to hold small larvae before ovipositor insertion. D. eucalyptialso visited patches of small larvae more frequently, proceeded less often through patches of mid larvae, and made significantly fewer ovipositions in mid and large larvae. Small larvae responded to both parasitoids by dispersing outward, while mid larvae responded to parasitoids by moving inward to form a denser group. Larvae reared or thrashed after each parasitoid visit, especially mid larvae, and some continued to do so for up to 2h after parasitoid departure. Mid and large larvae occasionally injured parasitoids by biting their appendages. By rearing or thrashing immediately prior to an encounter with a parasitoid, mid and large larvae decreased the likelihood of being parasitized by up to 50%.     

Influence of Host Pheromone on Egg Parasitism by Scelionid Wasps: Comparison of Phoretic and Nonphoretic Parasitoids

The kairomonal activity of the attractant pheromone for the spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae), was investigated by exposing fresh pentatomid egg masses in field traps with or without synthetic pheromone. Predominantly two parasitoids were recovered from exposed eggs of P. maculiventris and Euschistus obscurus: Telenomus podisi Ashmead (a generalist pentatomid egg parasitoid) and Telenomus calvus Johnson (a phoretic specialist on Podisus eggs) (Hymenoptera: Scelionidae). The incidences of T. podisi from P. maculiventris and E. obscurus eggs placed in pheromone-baited and nonbaited traps were not significantly different, suggesting that this oophagous wasp does not use the spined soldier bug attractant pheromone as a kairomone. However, T. calvus was reared almost exclusively from egg masses of P. maculiventris placed inside pheromone-baited traps. These results suggest that T. calvus females orient to volatile chemicals emitted by spined soldier bug males as a searching strategy to find areas likely to contain host eggs, in addition to the previously discovered strategy of using the pheromone to guide their phoretic behavior. The data also indicate that T. calvus can distinguish between the egg masses of these pentatomid hosts at close range.