Niche modification and stability of competitive systems. II. Persistence of interspecific competitive systems with parasitoid wasps

Effects of niche shift in ecological time scale on the population dynamics of competing species were studied in the experimental populations of two parasitoid wasp species, Anisopteromalus calandrae and Heterospilus prosopidis (both are solitary parasites), on a host, the azuki bean weevil, Callosobruchus chinensis. Four resource conditions were set up with combination of kind of bean (azuki or black eye), and host distribution (uniform or clumped). In each resource condition, four developmental stages of hosts were provided as a resource spectrum for parasitoid wasps. Population dynamics of the two wasp populations were investigated in each resource condition in Multi-Generation Competitive Systems (MGCS), in which fresh hosts of four developmental stages were periodically introduced and were parasitized competitively by the two wasp species. Competitive coexistence of both wasps occurred in the azuki-clumped condition, where the peaks of the resource utilization curves separated in the two species; pupae in A. calandrae and the early or late fourth instar in H. prosopidis, A. calandrae was eliminated in the azuki-uniform condition and H. prosopidis went extinct in two black eye conditions irrespective of host distributions. The degrees of overlap of the resource utilization patterns of the two wasp species during population dynamics were not significantly different among resource conditions irrespective of the results of coexistence or extinction. Even in the azuki-clumped condition, however, extinction of A. calandrae was observed when resource partitioning could not be realized with only the late fourth instar larvae available to wasps. Further analytical experiments showed that parasitizing ability of A. calandrae increased with host density per bean with azuki beans, but A. calandrae could express higher parasitizing ability with black eye beans than H. prosopidis irrespective of host density per bean. The flexibility in parasitizing ability by A. calandrae for various host stages under different resource conditions was thought to be the major factor in determining the competitive coexistence or the extinction of either species under different resource conditions. The present experiments also suggested that different second-best host stages between competitors could be a major contributing factor to competitive coexistence.     

Population fluctuation and persistence of one-host–two-parasitoid systems depending on resource distribution: from parasitizing behavior to population dynamics

Population dynamics and variability were examined in one-host–two-parasitoid experimental systems with different resource distributions: resource-clumped and resource-sparse conditions. The system consists of a seed beetle host, Callosobruchus chinensis, and two parasitoid wasps, Anisopteromalus calandrae (Pteromalidae) and Heterospilus prosopidis (Braconidae). In the resource-clumped condition, suitable hosts for parasitism (the late fourth-instar larvae and pupae) were clumped in 1 large resource patch, but they were scattered evenly among 16 small patches in the resource-sparse condition. Population censuses were conducted at 10-day intervals in long-term cultures, renewing 10 g of azuki beans (Vigna angularis). In both resource conditions, the first period was a single-species system of C. chinensis only, and A. calandrae was added in the second period. The one-host–one-parasitoid system with C. chinensis and A. calandrae showed stable population dynamics with small fluctuations. After addition of H. prosopidis in the third period, two of three replicates persisted to day 800 in each resource condition, although one replicate in each went to extinction at an immediate outbreak of the H. prosopidis population after the introduction. Population variabilities of C. chinensis and H. prosopidis were significantly higher and the mean population size of A. calandrae was significantly smaller in the resource-sparse condition than that in the resource-clumped one. A short-term experiment on parasitism efficiencies revealed that H. prosopidis parasitized significantly more at a low host density in the resource-sparse condition than in the resource-clumped one. Mutual interference of H. prosopidis was weak enough at low parasitoid densities but became abruptly stronger with high densities. Providing fresh hosts in a mixture of already parasitized ones, host-searching behaviors of a parasitoid were recorded by video for 3 h and were compared between the two wasp species. H. prosopidis could parasitize fresh hosts more efficiently than A. calandrae through frequent long-distance walks (walking to distant beans at one bout or outside a clump of beans with hosts and back soon on a distant bean of the clump) after reencounters with parasitized hosts. Considering all the experimental results, populations were judged to be more fragile and more likely to go to extinction in the resource-sparse condition than in the resource-clumped one. A higher attacking efficiency of H. prosopidis destabilized population dynamics more in the resource-sparse condition. Received: December 23, 1998 / Accepted: January 20, 1999     

Genetic variation can promote system persistence in an experimental host-parasitoid system

We tested experimentally the effects of genetic variation in host population on the host-parasitoid system persistence. The experimental systems consisted of one parasitoid wasp species (Heterospilus prosopidis), one bean weevil species (Callosobruchus chinensis), and one bean species, of which only the host species (bean weevil) was genetically manipulated. As control treatments with low genetic heterogeneity in the host population, we used two bean weevil strains (Kyoto and Niigata strains) which have several contrasting ecological traits. For the high genetic heterogeneity treatment, hybrid bean weevils which were generated by crossbreeding the strains Kyoto and Niigata were used. In the multiple-generation experiments, all three treatments had different patterns of extinction. The control treatment with the Niigata strain was very prone to system extinction, whereas the treatment with hybrids showed coexistence of constituent species in almost all replicates and also showed stabilized population dynamics. The other control treatment, using the Kyoto strain, showed intermediate proneness. To interpret the results of multiple-generation experiments, we conducted several short-term experiments. The different persistence patterns between the two control treatments were explained by the shapes of the host-finding abilities of wasps and the growth rate of the bean weevils. The mean values of many ecological traits of hybrid lines were not different from those of the Kyoto strain, but their variability increased. These outcomes corresponded well to the prediction of models by Doebeli [J Theor Biol (1997) 188:109–120]. We discuss the mechanisms in which the variability in host species population was effective for the prolonged system persistence.     

Additional notes on Anisopteromalus sp. (Hymenoptera: Pteromalidae), the sibling species of a parasitic wasp of stored‐product pests,Anisopteromalus calandrae (Howard): A new alternative host,an eye color mutant and DNA barcodes

A parasitic wasp of stored‐product pests, Anisopteromalus calandrae (Howard), is known to have a sibling species with a different chromosome number. Here, we report establishment and characterization of an eye color mutant in this sibling species. The phenotype of the mutant is red eye in adults, and crossing experiments revealed that the mutant phenotype is recessive to wild type (brown eye color). We also report DNA barcode sequences (a partial sequence of mitochondrial cytochrome‐c oxidase subunit I) of A. calandrae and the sibling species to enable accurate identification of these morphologically similar species. Analyses of our laboratory strains showed that 12.6% of the analyzed sequences (82 of 652 bp) differed between the two species. Finally, we note that the seed beetle Callosobruchus chinensis (Linné) (family Bruchidae), host of our laboratory strains of the sibling species, is a new record of alternative host at the family‐level for the wasp (known hosts: Anobiidae (natural host) and Curculionidae (alternative host)).     

Some like it hot,some not: influence of extreme temperatures on Lariophagus distinguendus and Anisopteromalus calandrae

The parasitic wasp species Lariophagus distinguendus (Förster) (Hymenoptera: Pteromalidae) and Anisopteromalus calandrae (Howard) (Pteromalidae) are used for inoculation biological control of the granary weevil Sitophilus granarius (L.) (Coleoptera: Curculionidae) in grain stores in Europe. To assess their suitability for biological control under extreme temperatures in winter and summer, we studied the influence of temperatures on their parasitization behaviour under natural fluctuating temperature conditions in the field and under constant temperature conditions in the laboratory. At low temperatures (≤20°C), L. distinguendus showed a higher parasitization rate than A. calandrae. At high temperatures (≥25°C), A. calandrae performed better than L. distinguendus that was negatively affected already at temperatures above 30°C. These findings suggest a temperature‐dependent release of either L. distinguendus or A. calandrae to allow a more efficient application of the wasps in biological control.     

The effects of spatial and temporal environmental heterogeneities on persistence in a laboratory experimental community

Among many stabilizing factors for community dynamics, spatial and temporal heterogeneities have been widely considered in recent years as two of the most important properties. However, the difference between the two types of heterogeneities have not been studied, except for Clark and Yoshimura (1993). We evaluated experimentally the effect of temporal and spatial heterogeneities on the persistence of a biological community. The experimental communities consisted of one parasitic wasp species, one bean weevil species, and two kinds of bean. Temporal and spatial heterogeneities of experimental communities were generated by kinds and timing of bean supply. Of all the experimental communities, the most persistent community was a temporally and spatially homogeneous community with Red Kidney bean as primary resource. Compared to spatially heterogeneous communities, temporally heterogeneous communities were more persistent. These results were easily explained by considering the attack rate of parasitic wasps and the difference between arithmetic and geometric means. In order to discuss the relative importance of environmental heterogeneity and the mode of biological interaction on community persistence, we have to measure the degree of environmental heterogeneity as the rate of change of the strength of interspecific interactions.     

Intraspecific interference between native parasitoids modified by a non-native parasitoid and its consequence on population dynamics

1. The number of natural enemies that should be introduced to control a pest is a controversial subject in biocontrol. A previous semi-mechanistic model parameterised using a laboratory system consisting of two parasitoid wasps, Anisopteromalus calandrae and Heterospilus prosopidis, parasitising a pest beetle, Callosobruchus chinensis, indicated that the introduction of the non-native parasitoid H. prosopidis decreases the level of intraspecific interference between native A. calandrae females. The model also suggested that this decrease was the main factor destabilising the population dynamics of the host–parasitoid system, resulting in chaos. 2. To test this population-level decrease and host density independence in the interference of A. calandrae, we observed individual behaviours to quantify the level of intraspecific interference between two A. calandrae females in the presence or absence of H. prosopidis at two different host densities. 3. When H. prosopidis was present, the number of direct antagonistic interference events between A. calandrae females, sting duration, host feeding events (but not stinging events), and patch residence time were reduced. However, the presence of H. prosopidis decreased the patch residence time and the proportion of hosts parasitised by A. calandrae only when the host density was low. 4. The reduction in intraspecific interference between A. calandrae females by H. prosopidis and its host density independence support the population-level prediction, whereas the observed reduction in host-feeding behaviours in A. calandrae by H. prosopidis was not predicted. Overall pest control by the native parasitoid was unaffected by the non-native parasitoid as host density increased.     

Sex allocation of three solitary ectoparasitic wasp species on bean weevil larvae: Sex ratio change with host quality and local mate competition

Sex ratio manipulation by ovipositing females was surveyed in 3 solitary ectoparastic wasp species,Dinarmus basalis (Pteromalidae),Anisopteromalus calanrae (Pteromalidae), andHeterospilus prosopidis (Braconidae), that parasitize azuki bean weevil (Callosobruchus chinensis (L) (Coleoptera: Buruchidae)) larvae within azuki beans (Vigna angularis). Variables were local mate competition (LMC) and host quality (HQ). We used host age as a measure of host quality (from 9-to 16-day-old hosts), changed the number of ovipositing females to control the level of local mate competition (1 female and 10 females), and examined oviposition patterns of the wasps. The offspring sex ratios (proportion of females) of the 3 wasp species respond qualitatively same to HQ and LMC. The common qualitative tendency among the 3 species is an increase of sex ratios increase with host age. In the process of changing the sex ratio (9–13-day-old) 3 wasp species respond only to HQ. In the hosts that end development in size (14–16-day-old) wasps respond to LMC. The response of sex ratio change to LMC in the old host ageclasses are different among the 3 species. In the situation that there exists LMC (10 females) sex ratios are the same among the 3 wasps. However, the sex ratios in no LMC (single female) are heterogeneous among the 3 wasps.     

Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis (Fahraeus) (Coleoptera: Bruchidae)

Mating behavior and the male's contribution to female fecundity were studied in the bean weevil Bruchidius dorsalis (Fahraeus) (Coleoptera: Bruchidae) in comparison with two other species, Callosobruchus chinensis (which infests stored beans) and Kytorhinus sharpianus (which feeds on wild legumes). Only females of B. dorsalis showed multiple mating and characteristic precopulatory behavior that appeared to solicit the male's nutritious secretion. In contrast, all females of the other two species did not copulate multiply and did not show such precopulatory behavior. In B. dorsalis, the decrement of male body weight just after copulation indicated that seminal fluid weighing as much as approximately 7% of the male's body weight was transferred to the female. Fecundity was more than eight times higher in females that had copulated ten times than in females that had copulated only once, indicating that males paid most of the nutritional cost of egg production. These facts suggest that the sex role is reversed in B. dorsalis. Received: May 22, 1998 / Accepted: July 19, 1999     

Regulation of Progeny Sex by Anisopteromalus calandrae (Hymenoptera: Pteromalidae) in Relation to Host Preference,Host Vulnerability and Host Size

Regulation of progeny sex by Anisopteromalus calandrae (Howard) in relation to host preference, host vulnerability and host size was studied with two host species, Sitophilus oryzae (L.) and Callosobruchus chinensis L. A. calandrae preferred S. oryzae to C. chinensis (preference index = 0.87). The progeny sex ratio (females/total) was significantly higher on C. chinensis, the less preferred host, than on S. oryzae regardless of the instar age of the two host species. A. calandrae could locate only a few young larvae of C. chinensis (≤third instar), which could be apparently due to the low vulnerability of the young larvae locating deeper in the adzuki bean kernels. The larval instar age of Sitophilus oryzae affect the progeny sex ratio of A. calandrae, but that of Callosobruchus chinensis did not except invulnerable ones. The progeny sex ratio of A. calandrae produced from C. chinensis, ranged from 0.66±0.05 to 0.82±0.02. The invulnerability of the young larval instar of C. chinensis and regulation of the progeny sex ratio by A. calandrae based on host size in a manner of absolute rule could explain the higher sex ratio on the young larval instar of C. chinensis, less preferred and less vulnerable host, than the old larval instar of S. oryzae, highly preferred host. The differences in host vulnerability could be another factor for A. calandrae assigning progeny sex ratio.     

Strategic ejaculation and level of polyandry in <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis> (Coleoptera: Bruchidae)

Variation in the level of polyandry of females produces a difference in the risk of sperm competition among males. As a consequence, investment in ejaculate expenditure by males should vary. We compared the number of sperm ejaculated by males into the female reproductive organ of six strains of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae), when males were reared at different larval densities in a bean. A significant positive correlation was found between the remating frequency of females and the ratio of the ejaculate sizes of high-density and low-density males as a measure of the response to the risk of sperm competition among males. The measure was estimated by dividing the number of sperm ejaculated by males reared at high larval density in a bean with the number of sperm ejaculated by males reared alone. The number of sperm transferred by a male to a female was not correlated with the duration of copulation. The results suggest an evolutionary relationship between ejaculatory expenditure and the level of polyandry in C. chinensis.     

Utilization of an unpredictable food source by Melanterius ventralis, a seed-feeding biological control agent of Acacia longifolia in South Africa

A seed-feeding weevil, Melanterius ventralis (Coleoptera: Curculionidae), has been introduced into South Africa to supplement a gall wasp,Trichilogaster acaciaelongifoliae (Hymenoptera: Pteromalidae), in the biological control programme against an alien invasive tree, Acacia longifolia (Mimosaceae), from Australia. The gall wasp debilitates most of the flower buds on A. longifolia andreduces seed-set by >95%. The intended rolefor M. ventralis is to destroy theresidual seeds. To achieve this, the gravidfemales need to be able to locate a food sourcethat is both heterogeneously dispersed andfrequently scarce due to damage caused by T.acaciaelongifoliae. Observations showedthat M. ventralis females are meticulousin choosing sites to oviposit so that larvae donot become overcrowded and food limited. Cagetests and field observations revealed thatfemales located pods regardless of density andposition, and that the duration of time spenton branches was proportional to the number ofpods on the branches and to the condition ofpods. The females spent little time onbranches of acacia species other than A.longifolia, but some time was spent onbranches with pods of A. melanoxylon thathad been coated with juice extracted from A.longifolia. All indications are that M.ventralis has the attributes needed to bean excellent supplementary biological controlagent to T. acaciaelongifoliae and theprogress of the weevil continues to be monitored.     

Experimental evolution of competing bean beetle species reveals long‐term reversals of short‐term evolution,but no consistent character displacement

Interspecific competition for shared resources should select for evolutionary divergence in resource use between competing species, termed character displacement. Many purported examples of character displacement exist, but few completely rule out alternative explanations. We reared genetically diverse populations of two species of bean beetles, Callosobruchus maculatus and Callosobruchus chinensis, in allopatry and sympatry on a mixture of adzuki beans and lentils, and assayed oviposition preference and other phenotypic traits after four, eight, and twelve generations of (co)evolution. C. maculatus specializes on adzuki beans; the generalist C. chinensis uses both beans. C. chinensis growing in allopatry emerged equally from both bean species. In sympatry, the two species competing strongly and coexisted via strong realized resource partitioning, with C. chinensis emerging almost exclusively from lentils and C. maculatus emerging almost exclusively from adzuki beans. However, oviposition preferences, larval survival traits, and larval development rates in both beetle species did not vary consistently between allopatric versus sympatric treatments. Rather, traits evolved in treatment‐independent fashion, with several traits exhibiting reversals in their evolutionary trajectories. For example, C. chinensis initially evolved a slower egg‐to‐adult development rate on adzuki beans in both allopatry and sympatry, then subsequently evolved back toward the faster ancestral development rate. Lack of character displacement is consistent with a previous similar experiment in bean beetles and may reflect lack of evolutionary trade‐offs in resource use. However, evolutionary reversals were unexpected and remain unexplained. Together with other empirical and theoretical work, our results illustrate the stringency of the conditions for character displacement.     

Age specificity of inbreeding depression during a life cycle ofCallosobruchus chinensis (Coleoptera: Bruchidae)

Age-specific effects of inbreeding on fecundity were assayed for adzuki bean weevil Callosobruchus chinensis by comparing inbred lines and their cross. Four consecutive full-sib matings reduced only 10.3 percent in total fecundity, and did not decrease early fecundity at all until third day from the onset of reproduction. It is suggested that recessive detrimental genes have been eliminated from the early period of adult life span when reproductive value is high. There was a slight tendency that inbreeding depression increased as age proceeded though not statistically significant.     

Distribution of social wasps (Hymenoptera: Vespidae) in New Zealand in 1987

Abstract

More than 50 000 social wasps (Hymenoptera: Vespidae) were collected between March and August 1987 from throughout New Zealand. The most widespread species is the German wasp (Vespula germanica). The common wasp (V. vulgaris) has colonised about half the country and appears to be still spreading. It tends to appear in urban areas first, presumably because it is transported there with people and/or their belongings. The Asian paper wasp (Polistes chinensis) and Australian paper wasp (P. humilis), are confined to the northern half of the North Island, but the former species is spreading south.     

Overwintering stages of Callosobruchus chinensis (L.) in the field

Adzuki bean beetle, Callosobruchus chinensis, is a worldwide oligophagous and a field‐to‐storage pest of legumes including adzuki beans (Vigna angularis). Its over‐wintering stage is yet to be confirmed. A series of experiments was carried out at Jinju, in the southern part of the Republic of Korea, to elucidate the overwintering stages. Top‐ and sub‐soil samplings followed by pod and seed samplings from left over plants from adzuki bean fields in the winter of 2015, and an outdoor overwintering test (during Nov 2018 to Jun 2019) by exposing bean seeds harboring different stages (eggs, larvae, pupae, pharates and adults) of laboratory reared C. chinensis to the winter environment were carried out. None of the C. chinensis stages was detected from the top‐ and sub‐soil samples. When the pods and seeds from left over plants were sampled, only a few live pupae were obtained. In the outdoor test with laboratory reared C. chinensis, all the stages (larvae, pupae, and adults), except eggs, were detected on every other weekly samples of infested adzuki bean seeds throughout the winter. These results showed that the overwintering stages of C. chinensis in Jinju, southern Korea, are larvae, pupae, pharates and adults.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.     

Inbreeding depression in development,survival, and reproduction in the adzuki bean beetle (<Emphasis Type="Italic">Callosobruchus chinensis</Emphasis>)

Inbreeding depression of an aspect of fitness is observed in many insects, but the traits that are of importance for inbreeding depression of fitness remain poorly understood. Here the magnitude of inbreeding depression of fitness-related traits in the development and adult stages was measured in a captive population of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Beetles produced by full-sib matings had 8% lower survival in the development stage than did beetles produced by unrelated matings. Although inbred and outbred offspring did not differ in body size after emergence, inbred offspring took 2–3% longer to develop to emergence. This indicates inbreeding depression of growth rate. At the adult stage, inbreeding had no significant effect on longevity, however lifetime offspring production was reduced by 11%. Thus, the magnitude of inbreeding depression was relatively large for offspring production. This suggests inbreeding depression of fitness manifests, to a particularly significant extent, in reduced productivity. This study shows the C. chinensis population, which has been in captivity for more than 100 generations, harbors genetic loads.     

Competitive exclusion between contest and scramble strategists in <Emphasis Type="Italic">Callosobruchus</Emphasis> seed–beetle modeling

Interspecific competition between an intermediate contest strain of Callosobruchus maculatus and a scramble strain of C. chinensis was investigated on two types of resource beans: the azuki (Vigna anguralis, small seed) and the black-eye bean (Vigna unguiculata, large seed). We conducted both single-generation competition experiments and multiple-generation experiments and then analyzed the system with a discrete version of the Lotka–Volterra competition model. The estimated competition coefficients showed the competitive dominance of the C. maculatus strain over the C. chinensis strain in both types of bean. Zero-growth isocline analysis based on the predicted model showed that an overall dominance of the contest species, C. maculatus, in azuki beans, whereas the outcome of competition was dependent on the initial population size of each species in the black-eye beans. In the multiple-generation experiments, C. maculatus was the successful competitor irrespective of the ratio of the two beans, whereas C. chinensis overcame C. maculatus in one of five replicates with the black-eye beans system. When we incorporated the cost of scramble competition, or density-dependent reduction in body mass into the predicted model, the model alteration decreased the survival region of C. chinensis in phase space on the black-eye bean. Thus, the competitive equations, which do not consider the density-dependent body size reduction, tend to overestimate the advantages of scramble strategists. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.