Development rate,number of mature oocytes at emergence and adult size ofEncarsia tricolor at constant and variable temperatures

The duration of the development of the aphelinidEncarsia tricolor Föerster (a parasitoid of the aleyrodidTrialeurodes vaporariorum (Westwood), adult size and number of mature oocytes at emergence were determined under constant and variable temperature regimes. Females developed successfully from 14 to 32°C, but a 100% of pupal mortality was observed at 34°C. Males developed successfully from 16 to 28°C and they developed faster than females. Female and male, egg to adult development at constant temperatures ranged from 51.1 (14°C) to 14.3 (28°C) days and from 32.6 (16°C) to 11.8 (28°C) days, respectively. Predictions of the rate of development at variable temperatures were more accurate when made from 2nd and 3rd degree polynomials than from linear regressions. The number of mature oocytes at emergence ranged from 0.1 (30°C) to 2.2 (20°C). FemaleE. tricolor attained the greatest size at 20–24°C. The comparison with literature data shows thatE. tricolor develops faster thanT. vaporariorum at temperatures above 15°C.     

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.     

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 laying and host stage preference at constant temperatures inEncarsia tricolor [Hym.: Aphelinidae]

Encarsia tricolor Foërster is a facultative autoparasitoid that develops on the important pestTrialeurodes vaporariorum (Westwood) in outdoor crop conditions, which makes this aphelinid species promising for biological control programs in regions where field and protected crops coexist. In this paper we report the results obtained in the study of daily and totalE. tricolor egg laying and of adult female preference for different host stages in which to lay eggs at constant temperatures in the range 10 to 32 °C. Only whitefly nymphs were present in the searching arena (tomato leaflets). The mean number of eggs laid per female in one day ranged from 4.0 (10 °C and 32 °C) to 15.2 (24 °C). The mean total number of eggs increased with temperature from 10 to 28 °C, reaching a maximum of 123 eggs per female at 28 °C, and decreased sharply from 28 to 32 °C. The relation between the intrinsic rate of increase (r_m) and temperature in the range 10 to 28 °C followed a straight line whose equation was r_m=?0.076+0.011*T (R²=0.99). The r_m ofE. tricolor was greater than the r_m ofT. vaporariorum when temperature was higher than 9.2 °C. The preference for any particular host instar in which to lay eggs was not always significant. However, N4 was the host instar preferred whenever preference was statistically significant.     

Host age and host selection byTrichogramma nubilale

Selection byTrichogramma nubilale (Ertle & Davis) for different aged egg masses ofOstrinia nubilalis (Hübner) was examined by separating components of parasitism. FemaleT. nubilale were exposed to egg masses of 2 different ages (freshly laid egg masses versus 1, 2, 3 or 4 day old egg masses), and the age of the initial egg mass inspected, number and percent of eggs and egg masses parasitized, and the emergence rate of pharate parasitoids was recorded. When there was a large difference in age between young and old egg masses, ♀♀ inspected initially more young egg masses (>2 days difference), parasitized a greater percent of young egg masses (>2 days difference), and parasitized more eggs/parasitized egg mass in young egg masses (>3 days difference) than old egg masses. Females did not discriminate between host age when hosts were similar in age. Successful emergence of parasitoids was greater from younger eggs than older eggs, although emergence was better from one-day-old eggs than from fresh eggs. These results imply that when the hosts were sufficiently different in age, ♀♀ were attracted to younger egg masses more than older egg masses, and they tended to remain ovipositing for longer periods of time on younger egg masses than older egg masses. Moreover, ♀♀ appeared to prefer to oviposit in hosts in which their young are more likely to complete development.      

Artificial diets for rearing the coconut hispine beetle,Brontispa longissima (Coleoptera: Chrysomelidae), and their suitability to two specialist parasitoids

The coconut hispine beetle, Brontispa longissima (Gestro), is a serious invasive pest that infests young unopened fronds of coconut palms (Cocos nucifera L.) in Southeast Asia. We previously developed the first artificial diet for rearing B. longissima larvae, which contained a leaf powder of young coconut fronds. Because the fronds are required for healthy growth of coconut palms, it is necessary to reduce their use for rearing the beetles. In this study, we tested two new artificial diets for the beetle larvae, which contained the leaf powders of mature coconut leaves or orchard grass (Dactylis glomerata L.). Brontispa longissima successfully developed from hatching to adulthood on both the mature coconut leaf diet and orchard grass diet. The beetles reared on the mature coconut leaf diet and orchard grass diet developed faster than those reared on the young coconut leaf diet. Fecundity and egg hatchability of beetles did not differ among the three diet treatments. We then examined the suitability of beetle larvae or pupae reared on each diet as hosts for two specialist endoparasitoids, Asecodes hispinarum Boucek and Tetrastichus brontispae Ferriere. The survival rate from oviposition to adult emergence for A. hispinarum was 43.8% in hosts reared on a young coconut leaf diet, 77.1% on a mature coconut leaf diet, and 85.7% on an orchard grass diet. For T. brontispae, the survival rate was 70.0% in hosts reared on the young coconut leaf diet, 38.1% on the mature coconut leaf diet, and 66.7% on the orchard grass diet. Our results indicate these artificial diets can be useful for rearing B. longissima and its two parasitoids, helping to reduce the costs of mass rearing these insects.     

Banker plants promote functional biodiversity and decrease populations of the cabbage whitefly Aleyrodes proletella

In this study, potential banker plant systems against the cabbage whitefly Aleyrodes proletella Linnaeus (Hemiptera: Aleyrodidae) were developed under controlled conditions. The two most promising banker plant systems, that is, the parasitoid Encarsia tricolor Förster (Hymenoptera: Aphelinidae) either with Aleyrodes lonicerae Walker on European columbine (columbine system) or with Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae) on Hokkaido squash (pumpkin system), were further evaluated in the field. Although the pumpkin system produced three times more parasitoids than the columbine system, both banker plants led to an 1.5-fold increase in A. proletella parasitism rates. However, only the pumpkin system increased the abundance of syrphid larvae on cabbage by 61.5% and reduced A. proletella populations on average by 4.4%–25.8% depending on the respective assessment date. In conclusion, the pumpkin system revealed to be a promising (supplementary) control measure against A. proletella. Options for further improvement and standardization of the pumpkin system as well as a potential implementation in cabbage production are discussed.     

Overwintering of reproductively mature females of a pro‐ovigenic parasitic wasp,Leptopilina heterotoma (Hymenoptera: Figitidae)

Leptopilina heterotoma is a Drosophila parasitoid mainly occurring in temperate regions, and females of this species are pro‐ovigenic (i.e. all or nearly all of their lifetime eggs are already mature at emergence). Here I investigated how L. heterotoma overwinters in Sapporo, Japan, a cool temperate region, by outdoor and laboratory experiments. Females of this species had mature eggs at emergence as expected, and they did not resorb eggs even if they were exposed to cold or starvation. Nevertheless, females were able to overwinter, and post‐overwintering females retained parasitization capacity. In this species, thus, adult overwintering is not associated with reproductive diapause. However, females grown in late autumn or at low temperatures (e.g. 5°C) had a fewer number of mature eggs and higher winter survival. At low temperatures, female larvae could save energy by reducing egg production and allocate the saved energy to expenditure for overwintering. In contrast to females, males and pre‐adult individuals were not able to overwinter.     

Life history traits of adults and embryos of the Antarctic midge Belgica antarctica

Although larvae of the Antarctic midge, Belgica antarctica, live for more than 2 years, the adult and embryonic stages are brief and are less well known than the larvae. In this report, we provide additional details of these understudied life stages with laboratory observation on adult emergence, longevity, preoviposition period and embryonic development. Male adults emerged slightly earlier than females, and they also lived longer. More than a half (57 %) of the adults that emerged in the laboratory were males. Females produced only a single egg mass and died within a day after oviposition. Embryonic development required 16 days at 4 °C, and prior to hatching, the pharate larvae perform a distinct sequence of behaviors that include drinking and peristaltic movement. We also discuss points that need to be resolved for laboratory propagation of this species.     

Leaf age and life history variables of a leafminer: the case of Liriomyza trifolii on potato leaves

Field observations and laboratory experiments have demonstrated that infestation by the serpentine leaf miner, Liriomyza trifolii Burgess (Diptera: Agromyzidae), begins in the lower leaves of the potato plant, and proceeds through the middle leaves to those of the upper canopy. In choice and no‐choice experiments, mated adult L. trifolii females were given access for 48 h to potato plants, and caged on differently aged leaves. The extent of their feeding and oviposition on the 5–7 leaflets of the upper, middle, and lower leaves were recorded. The life history variables of the next generation were estimated: percentage egg hatch, number of mines formed, larval survival, number of pupae formed, size and weight of pupae, percentage pupation, number of adults formed, percentage emergence, size and weight of adults, sex ratio, adult longevity, and their reproductive performance. The results showed that L. trifolii females laid fewer eggs on the upper leaves, which were poor hosts for larvae. However, a comparison of oviposition behavior between the middle and lower leaves showed that the data did not fit the oviposition preference–offspring performance hypothesis, which postulates that females preferentially oviposit on hosts on which larvae perform best. Females exhibited a preference for the larger, older, lower leaves, although the middle leaves were superior for the growth and development of the young stages. It is hypothesized that adult ovipositional preference for the older, larger, and thicker leaves of the lower foliage may be influenced by factors other than resource quality for larvae.     

Age‐related changes in the development of oocytes and testicular follicles after emergence in Stavsolus japonicus (Plecoptera)

Abstract Female stoneflies oviposit several times during the adult stage of their life cycle. The number of eggs within the deposited egg masses decreases at successive ovipositions. To clarify the reason for this decrease and to determine the conditions of testicular follicles, the patterns of development of oocytes and testicular follicles on different days after emergence are investigated in the systellognathan species Stavsolus japonicus (Okamoto) (Perlodidae). The size of the mature oocytes in the ovariole peaks a few weeks after emergence but decreases to the lowest level by 35 days after emergence. Several maturing oocytes can be observed in the ovarioles of individuals a few weeks after emergence but only one mature oocyte is observed at 35 days after emergence. The decreased number of eggs laid per mass by older individuals may therefore be due to the lower maturation of all the ovarioles.     

The parasite-host relationship betweenEncarsia formosa (Hymenoptera: Aphelinidae) andTrialeurodes vaporariorum (Homoptera: Aleyrodidae) I. Host finding by the parasite

Analysis of the searching behaviour ofEncarsia formosa showed that this parasite was not able to locate its individual hosts (Trialeurodes vaporariorum) from a certain distance. In addition, quantitative data on sizes and numbers of hosts of each stage present on the leaf parts under observation, and the number of contacts the wasp made with these showed that the host-searching behaviour ofE. formosa on a leaf is random. Since, moreover, the distribution of the hosts over the leaf is random too, the number of hosts parasitized per unit of time is entirely dependent on the walking speed of the parasite and the number and sizes of the hosts present.     

Egg maturation dynamics of the parasitoid Microplitis rufiventris: starvation speeds maturation in early life

The number of mature eggs carried by a female parasitoid at any given moment (egg load) is a fitness‐related parameter affecting reproductive potential and impacting upon host population dynamics. Microplitis rufiventris Kokujev (Hymenoptera: Braconidae) is a solitary koinobiont endoparasitoid wasp of several noctuid pests, including Spodoptera littoralis. The number of mature eggs carried by females at emergence is approximately 50. The rate of egg maturation is strongly affected both by feeding status and access to host larvae. In early adult life, egg maturation rates are lower for 6–72 h in fed wasps compared with food‐deprived wasps. When given access to hosts, honey‐fed wasps live for approximately 9 days with high lifetime fecundity (226 eggs). By contrast to early adult life, the total realized fecundity is positively affected by feeding status, where water‐fed and starved females have 140 and 107 eggs, respectively. Egg resorption is most pronounced in the later life of females. The results suggest, in addition to confirming the effect of honey‐feeding on total fecundity, that fecundity of starved wasps includes rapid egg maturation early in life, which potentially could improve the performance of the parasitoid as a biological control agent.     

Host selection and sex ratio in a heteronomous hyperparasitoid

Abstract.

• 1 Encarsia tricolor Förster is a heteronomous hyperparasitoid: females develop as primary endoparasitoids of Homoptera, whereas males develop hyperparasitically in primary endoparasitoids, including conspecific females.
• 2 When offered pupae of Encarsia inaron (Walker) or conspecific pupae, E.tricolor showed a distinct preference to exploit E.inaron for male production.
• 3 Parasitoids were given the opportunity to gain different types of ovipositional experience on male and female hosts and were then offered patches containing mixtures of male and female hosts in various ratios. The mean sex ratio which they laid was not dependent on the relative availability of each type of host, whereas prior ovipositional experience had a significant effect.
• 4 Adaptive reasons for the observed oviposition strategies are suggested.

     

Does superparasitism improve host suitability for parasitoid development? A case study in the Microplitis rufiventris-Spodoptera littoralis system

Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. Recent studies have shown that allocation of additional eggs to an already parasitized host may be beneficial under certain conditions. In the present work, mortality of Microplitis rufiventris wasps was significantly influenced by both host instar of Spodoptera littoralis larvae at parasitism and level of parasitism. In single parasitization, all host instars (first through sixth) were not equally suitable. Percentage of emergence success of wasp larvae was very high in parasitized first through third (highly suitable hosts), fell to 60% in the fourth instar (moderate suitable) and sharply decreased in the penultimate (5th) instars (marginally suitable). Singly parasitized sixth (last) instar hosts produced no wasp larvae (entirely unsuitable), pupated and eclosed to apparently normal adult moths. The scenario was different under superparasitism, whereas supernumerary individuals in the highly suitable hosts were almost always killed as first instars, superparasitization in unsuitable hosts (4th through 6th) had significant increase in number of emergence success of wasp larvae. Also, significantly greater number of parasitoid larvae successfully developed in unsuitable hosts containing three wasp eggs than counterparts containing two wasp eggs. Moreover, the development of surplus wasp larvae was siblicidal in earlier instars and nonsiblicidal gregarious one in the penultimate and last “sixth” instars. It is suggested that the optimal way for M. rufiventris to deal with high quality hosts (early instars) is to lay a single egg, while the optimal way to deal with low quality hosts (late instars) might be to superparasitize these hosts.     

Influence of host age and host deprivation on longevity, egg load dynamics and oviposition rate in Microplitis rufiventris

Adult size, longevity, egg load dynamics and oviposition ofMicroplitis rufiventris Kok. which began their development in the first, second, third （preferred hosts） or fourth （non-preferred hosts） instar larvae of Spodoptera littoralis （Boisd.） were studied. The parasitoid size was largely determined by the initial host size at parasitism. Non-ovipositing females derived from older hosts lived for longer periods than those derived from younger ones. However, the ovipositing females, irrespective of their size, lived for almost the same periods. At emergence, the oviducts of adult females contain a significant amount of mature eggs available for oviposition for a few hours on eclosion day. Egg load increases during the early phase of adult life. The amount of additional mature eggs and rate of egg maturation per hour was greater for wasps derived from preferred hosts compared with those in females derived from non-preferred hosts. The pattern of egg production in M. rufiventris females depended on the availability of hosts for parasitization. Host-deprived females depleted the egg complement with aging; the longer the host deprivation, the lower the oviduct egg load. Marked reduction in both realized or potential fecundity of host-deprived females was observed following host availability. Host privation for more than 3 days induced a marked deficit fecundity pattern through the female＇ s life. The realized fecundity was determined by the interaction among host availability, the number of eggs that are matured over the female＇ s life span, oviposition rate and host size from which the female was derived. These results suggest that： （i） M. rufiventris wasp is a weak synovigenic species; （ii） the maturation of additional eggs is inhibited once the maximum oviduct egg load is reached; （iii） the egg load of the newly emerged female is significantly less than the realized fecundity; and （iv） because M. rufiventris females oviposit fewer eggs when they begin depleting their egg supply at 3 days, augmentative releases will require release immediately following emergence to ensure the highest parasitization rate in the field.     

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.     

Gonotrophic and embryonic development of the Palaearctic screwworm fly Wohlfahrtia magnifies

Abstract. Gonotrophic and embryonic development of Wohlfahrtia magnifica were studied on pupae and adults reared in the laboratory. Gonotrophic development in screwworm begins 8 days after pupation in yellow eye pharate adults. The adult female emerges with its oocytes at stage 3 and requires only 2 days for complete oogenesis and 5 days for complete embryogenesis. Mating occurs 2–5 days after adult emergence, starting the embryonic development. Each female produces an average of 76.8 active larvae which can produce a traumatic lesion in their hosts. When food sources were regularly supplied, synchronization of gonotrophic stages can be observed. These stages together with the embryonic ones are described.     

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.     

Asymmetric effects of adult nutrition on reproductive success of male and female Diaeretiella rapae (Hymenoptera: Aphidiidae)

The role of diet supplements (honey, water or no supplements) on egg maturation, oviposition strategy and longevity of the parasitic wasp Diaeretiella rapae McIntosh (Hymenoptera: Aphidiidae) is investigated. Parasitoids feed as larvae on hosts to acquire nutrition for growth and development, and further gain additional resources during their adult stage by feeding on either host or nonhost resources. The additional resources acquired by adults can help them to increase their reproductive activity or life expectancy, or both. Diaeretiella rapae females emerge with some developed eggs and no additional resources are required for egg maturation or successful oviposition. Females are able to oviposit and produce viable offspring immediately after emergence, and the number of eggs left in the ovaries of females decreases with subsequent oviposition, suggesting that ovigeny index of D. rapae is inclined towards pro‐ovigenic status. When unmated males and females are offered honey solution, females are attracted to it, whereas males display courtship and make mating attempts but then feed on honey after mating. The oviposition efficiency of female D. rapae increases by 30% when they feed on honey compared with when starved. Honey‐fed D. rapae adults live significantly longer (almost twice as long) than starved adults. Honey‐fed females deprived of hosts live longer than those offered hosts regularly. The positive effects of honey‐feeding on longevity are greater in females than in males. Taken together, the results of the present study suggest that the provision of additional resources to adult D. rapae parasitoids could enhance their life expectancy and parasitism efficiency in biological control programmes.