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.     

Exploring the foraging environment of a natural enemy of Callosobruchus maculatus: Spatial egg distribution in stored cowpea

Knowledge of the spatial distribution of stored product insects may reduce the dependency on chemicals for control of these insects. Biological control, for instance, could be improved based on such knowledge. In this paper we describe the three-dimensional spatial oviposition pattern of Callosobruchus maculatus in stored cowpea. Individual C. maculatus females oviposited in clusters of 70±15 (SD) eggs. These clusters were variable in shape. In any cluster 90 to 95% of the eggs fitted into a volume of 19.1±3.5 cm³. The egg density was highest (0.6 eggs bean^–1) at the center of a cluster and decreased towards the periphery. A statistically significant relationship existed between the number of eggs n in a cluster and the cluster volume, V(cm³): V=11.5+0.11n. We also investigated the spatial egg distribution of beetles which emerged from egg clusters such as those produced by individual females. Their oviposition was not confined to one specific area but was scattered throughout the bean mass. A point pattern analysis showed that the density of the `parent' cluster had no effect on the spatial egg pattern. These results give insight into the foraging environment which the egg parasitoid Uscana lariophaga, a promising candidate for biological control of C. maculatus, is facing. We argue that the probability p of encountering at least one other bean with eggs after a parasitization is a function of the number n of beans that are visited: p=1–0.42 (0.37)^(n–1).     

Uscana lariophaga, West-African egg parasitoid of the cowpea bruchid beetleCallosobruchus maculatus: photoperiod, parasitization and eclosion interactions

The diurnal pattern of parasitization and eclosion of the trichogrammatidUscana lariophaga Steffan, egg parasitoid of the cowpea bruchidCallosobruchus maculatus (Fabricius) was studied for L12:D12 photoperiods. The wasp parasitized eggs throughout each 24-h period with about 70% of the parasitization taking place during the first 12 h regardless whether it was the photophase or the scotophase. More female progeny was produced when the first 12-h period was photophase instead of scotophase. Eclosion of wasps took place over a period of 4 days and occurred during the second half of the scotophase and the first half of the photophase. The number of wasps eclosed during the photophase was similar to that eclosed during the scotophase. Average development time was 8.9 days at 30°C. Male development was completed 6 to 8 h before the females, hence a higher percentage of females emerged in the later eclosion peaks. During scotophases more females eclosed than during photophases. Although the results indicate that the wasp is able to perform under dark storage conditions the effect of permanent low light intensity remains to be studied.     

Effect of host quality of Callosobruchus maculatus (Coleoptera: Bruchidae) on performance of the egg parasitoid Uscana lariophaga (Hymenoptera: Trichogrammatidae)

Development and reproductive success of the solitary egg parasitoid Uscana lariophaga Steffan were examined after development in eggs of the bruchid storage pest Callosobruchus maculatus Fabricius reared at either low or high densities on cowpea seeds and laid at day 1 and 4 of maternal life. Both bruchid larval competition and maternal age negatively affected egg size, but the latter more than the former. Uscana lariophaga reared in small hosts developed slower, were smaller and produced fewer eggs compared to parasitoids reared in large hosts. Fecundity of the parasitoid was heavily influenced by host egg size. This was reflected in the values for the intrinsic rate of increase of U. lariophaga, which differed for wasps that developed in host eggs laid by bruchid females of different age. Wasps allocated marginally more female offspring to larger hosts.     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non-significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.     

Density dependence of Anaphes sordidatus (Hymenoptera: Mymaridae) parasitism on eggs of Listronotus oregonensis (Coleoptera: Curculionidae)

Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) oviposits in carrot leaves and the larvae feed in carrot roots. Its eggs are parasitized by Anaphes sordidatus (Girault) (Hymenoptera: Mymaridae) throughout its oviposition period. This parasitoid is the major biotic mortality factor for L. oregonensis. Parasitism by A. sordidatus was studied for three years in sequentially sown plots of carrots, Daucus carota var. sativa. Over the scason, significantly fewer L. oregonensis eggs were oviposited in later sown carrots than in earlier sown carrots because oviposition started later in late sown plots of carrots. A positive temporal density-dependent relationship was observed each year between parasitism rates and host densities. This positive density dependence occurred in early and mid-summer for earlysown carrots where host density reached 1–2 host eggs per plant but disappeared in late summer when host density decreased while parasitism remained high. Latesown carrots had low host egg density (0.2 host egg per plant) and contributed little to the total number of eggs. In these late sown plots, parasitism increased rapidly to over 80% but no density dependence was observed. Spatially, few statistically significant regressions were found but all indicated a positive spatial density-dependence. Most non-significant regressions occurred because the range of egg density was too small between plots for a given date.     

Impact of the egg parasitoid Uscana lariophaga and the larval-pupal parasitoid Dinarmus basalis on Callosobruchus maculatus populations and cowpea losses

In West Africa, Uscana lariophaga Steffan (Hymenoptera: Trichogrammatidae) and Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) parasitize the eggs and larvae, respectively, of Callosobruchus maculatus Fab. (Coleoptera: Bruchidae), an important pest of stored cowpea. The impact of the parasitoids on pest populations was evaluated in clay pots similar to the ones used in traditional storage in Niger. At the beginning of the storage period, cowpeas were infested with one density of C. maculatus and with either one or both of the parasitoid species. If the parasitoids we inoculated as single species in stores, both D. basalis and U. lariophaga significantly suppressed the bruchid population, but the former did so more effectively than the latter. A combination of D. basalis and U. lariophaga resulted in the same suppression of bruchid populations as when D. basalis was the only parasitoid. Fifteen weeks after storage, the parasitoids reduced the number of grains damaged significantly by 38–56%. The effect of inoculating single or multiple parasitoid species on C. maculatus populations in an augmentation strategy is discussed.     

Functional response of Trichogramma chilonis to Galleria mellonella and Chilo sacchariphagus eggs

A biological control programme using inundative releases of Trichogramma chilonis Ischii (Hymenoptera: Trichogrammatidae) reared on Galleria mellonella L. (Lepidoptera: Pyralidae) is currently underway to reduce infestations of Chilo sacchariphagus Bojer (Lepidoptera: Crambidae) in sugarcane, Saccharum spp., on Réunion Island. To assess the potential of the parasitoid as an inundative biocontrol agent, the functional response of three T. chilonis strains was tested with G. mellonella and one strain with C. sacchariphagus host eggs in glass tubes in the laboratory. The shape of the functional response (type II or III) was determined using logistic regression, and attack coefficients and handling times (T_h) were determined using non‐linear least‐square regression. The behaviour of all three strains with G. mellonella host eggs corresponded to a type III response. The St Benoît T. chilonis strain had a significantly shorter estimate of T_h than the St Pierre strain (P<0.05) and may, therefore, be more appropriate as a biocontrol agent. The functional response with C. sacchariphagus host eggs was a type II with the St Benoît T. chilonis strain. More T. chilonis wasps developed per host egg from the larger C. sacchariphagus host eggs (2.9) relative to G. mellonella (1.1). Superparasitism at low host egg densities was, therefore, likely to have been less frequent with C. sacchariphagus. Black eggs were chosen as an estimate of number of eggs parasitized, although they represent the number of eggs where parasitism led to complete pupal development. The low rate of detected parasitism at low host densities with G. mellonella eggs may be due to incomplete pupal development due to superparasitism rather than lack of parasitism, thus explaining the type III functional response.     

Side-effects of cowpea treatment with botanical insecticides on two parasitoids of Callosobruchus maculatus

Studies on the protective effect of botanical products against pest insects have infrequently been extended to side‐effects on natural enemies. Indirect effects of botanicals on the storability of seeds could occur through their possible negative impact on biological control agents. Four plant powders and six plant oils with a known effect on the cowpea beetle Callosobruchus maculatus (Fabr.) (Coleoptera: Bruchidae) were investigated for their effect on the beetles’ egg parasitoid Uscana lariophaga (Steffan) (Hymenoptera: Trichogrammatidae) and the larval parasitoid Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae). All treatments caused a decrease in parasitisation by U. lariophaga, and developing parasitoids of this species were affected by powders of Nicotiana tabacum (L.) and Tephrosia vogelii (Hook. f). In a two‐choice situation using a linear olfactometer, U. lariophaga was repelled by most of the oils. In a no‐choice situation, parasitisation by D. basalis was hampered by treatment with plant powders, but eggs that were laid developed normally. In a Y‐tube olfactometer, this parasitoid did not discriminate between odours of untreated and plant‐powder‐treated beans. The powders of N. tabacum and T. vogelii had stronger negative effects on the two parasitoids than the powders of Azadirachta indica (Juss.) or Blumea aurita (DC). In samples collected from untreated traditional storage facilities, subsequently treated with plant powders in the laboratory, none of the treatments could prevent the increase in beetle numbers. At 24 days after treatment, most beetles had emerged from beans treated with powders of N. tabacum and T. vogelii. Parasitoids were affected by the botanical insecticides tested here, but the powders of A. indica and B. aurita may be compatible with biological control by D. basalis.     

Trichogramma platneri (Hym.: Trichogrammatidae): Host choices between viable and nonviable codling moth,Cydia pomonella,and three-lined leafroller,Pandemis limitata (Lep.: Tortricidae) eggs

In laboratory host-preference studies,Trichogramma platneri Nagarkatti (Hym.: Trichogrammatidae) females, reared on viable codling moth,Cydia pomonella (L.) (Lep.: Tortricidae) eggs, parasitized significantly more viable than nonviable codling moth eggs produced by cobalt 60 irradiated adults. This ovipositional preference was maintained when competition increased per host egg. Similarly, one, three and fiveT. platneri females consistently oviposited more eggs into viable versus nonviable host eggs. A single femaleT. platneri parasitized a similar number of viableC. pomonella and three-lined leafroller,Pandemis limitata (Robinson) (Lep.: Tortricidae) eggs. However, as the number of females per host eggs increased, a significantly larger number of codling moth versus leafroller eggs were parasitized. One, three and fiveTrichogramma females parasitized significantly moreP. limitata versus nonviableC. pomonella eggs. NonviableC. pomonella eggs deflated to less than 25% of their original volume in four and ten days when held under dry and humid conditions respectively. The blackened prepupal stage of the parasitoid generally occurred in the nonviableC. pomonella eggs four days post-parasitization whereas the parasitized viable eggs blackened zero to one day earlier. Incubation under dry or humid conditions did not appear to influence the number of parasitized eggs that were able to blacken and show evidence of parasitism. Summerland Research Centre Contribution No. 938.     

Inoculative releases of Trichogramma ostriniae for suppression of Ostrinia nubilalis (European corn borer) in sweet corn: field biology and population dynamics

The effectiveness of inoculative releases of Trichogramma ostriniae Pang and Chen for suppression of Ostrinia nubilalis (Hübner) in sweet corn was assessed. Early-season, low-density (75,000 females ha⁻¹) releases were made, and establishment, levels of parasitism and sex ratios of emerging T. ostriniae quantified. T. ostriniae established effectively for each season that they were released, but appeared to be unable to overwinter. Parasitism levels tracked egg mass numbers closely, and T. ostriniae persisted in fields even where insecticides were applied. Parasitism by indigenous Trichogramma species was 3%. Field populations of T. ostriniae were distinctly female biased (78%), with males produced in the majority of broods. Numbers of males did not increase linearly with number of O. nubilalis eggs parasitized, but appeared to remain constant above an egg mass size of about 20 eggs. A Type-I functional response to increasing egg and egg mass density was found under field conditions, where the proportion of egg masses parasitized remained constant with increasing egg mass density. A relatively consistent percentage of eggs per egg mass was parasitized, with a linear increase in number of eggs parasitized with increasing number of eggs per egg mass. These results show that T. ostriniae established viable reproductive populations in sweet corn following inoculative release, with the potential to contribute to reduced dependence on insecticides for the control of O. nubilalis in an integrated pest management program.     

Population growth rate of the parasitic rotifer Proales gigantea,and susceptibility to parasitization in the snail Lymnaea acuminata at different stages of embryonic development

Developing eggs of the host snail Lymnaea acuminata were experimentally parasitized with the parasitic rotifer Proales gigantea to study the population growth rate of the parasite within the snail egg capsule and the susceptibility of the host eggs at different stages of embryonic development. The population growth rate of P. gigantea was 0.46 ± 0.07 individual^–1 day^–1 at the ambient temperature of 18–22 °C. Snail eggs were most susceptible to rotifer attack during the initial stages of development, becoming progressively more resistant after the hippo stage. Yet, regardless of the stage of development, the host embryo was doomed to die without hatching even if one individual rotifer gained entry inside the egg capsule. The presence of P. gigantea within the parasitized egg capsules or in the mucilage had no effect on the developmental rates and hatching success of non-parasitized eggs within the same egg mass.     

The effects of temperature and host density on the development and survival of Copidosoma koehleri

Developmental rates for Copidosoma koehleri Blanchard (Hymenoptera: Encyrtidae) and its host, Phthorimaea operculella (Zeller), were determined at 10, 15, 23, 27, 29, 32, 34 and 35°C from host egg to adult. The developmental rates determined for both species showed good fit to mathematical models of insect development. At 15°C mean emergence of adult C. koehleri was 15 days after P. operculella adults emerged. At 29°C mean emergence of C. koehleri was only 5 days after that of P. operculella. P. operculella developed at 35°C, but parasitized larvae, and therefore C. koehleri, did not tolerate temperatures above 32°C. In the presence of C. koehleri, host survival was low (3%) at low host egg densities, but greater (20%) at higher host densities. Parasitized larvae of P. operculella were less able to compete for food resources, as measured by adult emergence.     

The impact of the egg parasitoid Uscana lariophaga on Callosobruchus maculatus populations and the damage to cowpea in a traditional storage system

In West Africa, Uscana lariophaga (Hymenoptera: Trichogrammatidae) parasitizes the eggs of Callosobruchus maculatus (Coleoptera: Bruchidae), an important pest of stored cowpea. The impact of the egg parasitoid on pest populations was evaluated in clay pots used in traditional storage in Niger. At the beginning of the storage period cowpeas were infested with different densities of larval instars and adults of C. maculatus and inoculated with one density of U. lariophaga. The higher the initial densities of C. maculatus, the better the egg parasitoid was able to establish itself and to control the population of C. maculatus, limiting the damage to cowpea. After three months of storage, the egg parasitoid significantly reduced the number of C. maculatus adults by 68 at the lowest and 86 percent at the highest initial density of the beetle; the percentage of damaged beans was reduced by 13 and 19% respectively.     

Host-searching behavior ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae): Superparasitism

The foraging behavior ofVenturia canescens, a solitary endoparasitoid of lepidopteran larvae, was investigated in the laboratory. FemaleVenturia canescens with a larger number of mature eggs to lay were found to have higher levels of superparasitism (measured as numbers of eggs laid per parasitized host). Increased parasitoid density was found to result in reduced levels of superparasitism by host-deprived (i.e.,undepleted) wasps. Females which had been allowed access to hosts before the experiment (depleted wasps) laid fewer eggs per parasitized host than undepleted wasps, although there was no significant difference in the levels of superparasitism among the depletion periods of 1, 2, 5, and 7 h. It was also found that an egg which was encountered less than 15 min after oviposition was much less likely to be avoided than one which was encountered after more than 15 min had elapsed.     

Uscana lariophaga, egg parasitoid of bruchid beetle storage pests of cowpea in West Africa: the effect of temperature and humidity

The stored-product bruchid pests,Callosobruchus maculatus (Fabricius) andBruchidius atrolineatus (Pic) cause considerable production losses in cowpea in West Africa.Uscana lariophage Steffan parasitizes the eggs of the bruchids both in the field and in storage. As chemical control of bruchids in traditional granaries is not appropriate for poor farmers, enhancement of the efficacy of the parasitoid by environmental manipulation has been investigated. The effect of temperature on the capacity ofU. lariophaga to parasitize eggs has been studied at eleven constant and three fluctuating temperatures within the range 10 to 45°C. Longevity of the female wasp decreased with increasing temperature. The rate of development increased linearly at temperatures from 17.5 to 35°C, but decreased from 35 to 40°C. Mortality of the developing wasp remained below 20% from 20 to 37.5°C, but outside this range, mortality reached 100% at 15 at 42.5°C. Most parasitization occurred at temperatures of 25 and 30°C. Sex ratio (percentage females) increased with temperature in the high temperature range. The intrinsic rate of increase (r_m) forU. lariophaga was highest in the temperature range from 30 to 37.5°C and was higher than that ofC. maculatus at all temperatures. While the r_m value ofC. maculatus did not vary much at temperatures from 25 to 35°C, the r_m value of the wasp doubled. Relative humidity did not effect longevity, egg-laying capacity, mortality, development time and sex ratio of the wasps withC. maculatus as host. However, withB. atrolineatus as the host, development time and mortality increased at lower relative humidity levels. The results indicate that temperature is the major regulating factor on the parasitoid. As the type of storage structure and its location (sun or shade) affects the temperature inside the store, ways are being investigated of manipulating the storage environment through temperature regulation to increase the impact of the parasitoid.     

Intraspecific nest parasitism in the grey starling (Sturnus cineraceus)

We studied intraspecific nest parasitism in the grey starling (Sturnus cineraceus) in 1992 and 1993. We used three criteria to detect nest parasitism: (i) the appearance of more than one egg per day while the host was laying; (ii) the appearance of extra eggs after the host completed its clutch; and (iii) the appearance of eggs which were of a different shape, size and color to other eggs in the clutch. There were 290 nests (157 nests in 1992; 133 nests in 1993) in which the clutch was completed early (clutches initiated before May 10). Twenty-nine (1992) and 32 (1993) nests contained at least one parasitic egg. Parasitic eggs hatched if they were laid during the laying period and early in the incubation period of their host, and a few of them fledged. Fledging success of parasitic eggs was not different from that of eggs in non-parasitized nests if parasitic eggs were laid during the host's laying period. However, fledging success of all parasitic eggs was fewer than that of eggs in non-parasitized nests. By comparison, fledging success of parasitized nests was not a great as that of non-parasitized nests.     

Egg-laying experience and acceptance of parasitized hosts by the parasitoid,Leptopilina heterotoma (Hymenoptera: Eucoilidae)

The influence of egg-laying experience on the response of females of the eucoilid parasitoid,Leptopilina heterotoma, to parasitized and unparasitizedDrosophila melanogaster host larvae was examined under more controlled conditions than those used in past studies. In laboratory assays, we precisely manipulated both the number of eggs laid by females and the kind of larvae (parasitized versus unparasitized) in which the eggs were laid. We found that the tendency to avoid laying eggs in parasitized hosts depended markedly on whether or not eggs had been laid previously, but depended little on whether those eggs had been laid in parasitized or unparasitized hosts. The observed effect of general egg-laying experience on avoidance of parasitized hosts may reflect responses to either changes in the wasp's internal state (perhaps, changes in egg load) or changes in the wasp's neural representation of the external environment (such as those presumed to occur during learning). In light of these results, we offer a tentative reinterpretation of several earlier studies.     

Contrasting scales of oviposition and parasitism in praying mantids

We report on spatial patterns of parasitism of oothecae (egg cases) of praying mantises (Stagmomantis limbata) by torymid wasps, Podagrion spp. Using collections of mapped mantid oothecae from Riparian sites in the Sonoran desert and Grassland sites in the Chiricahua Mountains (both in Arizona, USA), we characterized the spatial distributions of oothecae and parasitism. The likelihood of an egg case suffering some parasitism was higher at Grassland sites, which had high oothecal densities, than at low-density Riparian sites. However, experimental isolation of Grassland oothecae to densities comparable to Riparian sites reduced parasitism rates. At Riparian sites, parasitized oothecae exhibited on average the same extent of parasitism as parasitized oothecae at high densities but with much greater variation. Indeed, large fractions of Riparian oothecae suffered both severe (>50%) and light (<20%) parasitism, whereas most parasitized Grassland oothecae suffered intermediate levels of parasitism. Analysis of first nearest neighbor distances indicated that the parasite load of an ootheca did not depend on its immediate isolation. However, extending the analysis to include subsequent nearest neighbors (using a technique from spatial statistics called the R(K) function), we found that even though oothecae of S. limbata were spatially clustered, some oothecae in a (statistically defined) cluster escaped parasitism when overall oothecal densities were low. This pattern suggests that when oothecae are sparsely distributed, Podagrion wasps exploit only a fraction of the oothecae available locally, even though the oothecae are strongly aggregated relative to their overall density. We suggest this lack of congruency in the scales of oothecal deposition and parasitism at low densities (which is absent when oothecae are at high densities) may be explained in part by behavioral aspects of the parasite's reproduction, including increased host fidelity by relatively sedentary female parasites. Received: June 13, 2000 / Accepted: October 16, 2000     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non‐significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.