Laboratory and field studies supporting the development of Heringia calcarata as a candidate biological control agent for Eriosoma lanigerum in New Zealand

Studies supporting a project seeking to introduce Heringia calcarata (Loew) (Diptera: Syrphidae) to New Zealand (NZ) to supplement biological control of woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae) are reported. Annual surveys of H. calcarata presence and abundance in a Virginia, USA apple orchard revealed a bimodal distribution, with peaks in mid-June and mid-September. In the field, female H. calcarata oviposited on sentinel apple shoots infested with WAA, providing an efficient method for egg collection and larval production. Similarly, most field-collected females readily deposited viable eggs on WAA colonies in laboratory cages, demonstrating that mated females will oviposit in captivity. Survivorship of eggs and larvae transported to NZ was good, yielding adult flies in containment in Auckland. Adult, virgin female H. calcarata reared from eggs in captivity developed mature oocytes, providing an important step toward future mating studies in containment. Oviposition and larval feeding studies examined aspects of the intraguild interactions between H. calcarata and Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae), the sole biological control agent of WAA in NZ. Field tests using paired sentinel apple shoots with a non-parasitized or parasitized WAA colony revealed that although H. calcarata deposited eggs on both parasitized and non-parasitized colonies, fewest eggs were deposited on heavily parasitized colonies. Feeding studies showed that larval H. calcarata consumed fewer mummified aphids or aphids in an earlier stage of parasitization than non-parasitized aphids.     

Isolation and characterization of nine microsatellite loci from Aphelinus mali (Hymenoptera: Aphelinidae), a parasitoid of Eriosoma lanigerum (Hemiptera: Aphididae)

Abstract Nine novel microsatellite markers are presented for Aphelinus mali, a parasitoid of the woolly apple aphid Eriosoma lanigerum. Loci were characterized for 28 individuals from a single orchard in central Chile. Seven loci were polymorphic within A. mali (3–6 alleles per locus; observed heterozygosity ranging from 0.04 to 0.57) and are therefore useful for population genetic studies within this species.     

Development of Apheliuus mali an endoparasitoid of woolly apple aphid, Eriosoma lanigerum at different temperatures

Developmental times for both sexes of Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) an endoparasitoid of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Pemphigidae) were studied at 13, 15, 18, 20, 25 and 30°C and compared with those of E. lanigerum. Mean developmental times ranged from 11.7–53.3 days for males, 11.8–55.4 days for females and 11.8–54.4 days for both sexes combined and were significantly inversely related to temperature. A good linear model fit (r²>0.99) between developmental rate and temperature in the range 13–30°C was observed. Results indicate significant differences between developmental times of males and females at 13, 18, 20, and 25°C but no differences at 15 and 30°C. The notional developmental threshold was 8.3°C for both males and females. Compared with its host, A. mali has a higher lower developmental threshold. An average of 252.8, 256.7 and 254.8 degree-days (DD) above the lower threshold were required by A. mali to complete development from time of oviposition to adult emergence for males, females and both sexes combined, respectively. Field experimentation also indicated that the developmental time of A. mali lags significantly behind that of its aphid host throughout the year. These findings are discussed in relation to its status as a biological control agent for E. lanigerum.     

Abundance and natural control of the woolly aphid <Emphasis Type="Italic">Eriosoma lanigerum</Emphasis> in an Australian apple orchard IPM program

Woolly aphid (Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), was monitored over three growing seasons (1995--1998) to assess its abundance and management under apple IPM programs at Bathurst on the Central Tablelands of NSW, Australia. Woolly aphid infestations were found to be extremely low in IPM programs utilising mating disruption and fenoxycarb for codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) control. This was the direct result of increased numbers of natural enemies. No insecticides were applied for woolly aphid control. Under the IPM strategies tested the principal control agent was identified as European earwig (Forficula auricularia L.) (Dermaptera: Forficulidae). Earwigs in combination with Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) reduced woolly aphid infestations below the action threshold set by commercial growers. However, A. mali together with other flying natural enemies, e.g., ladybirds, lacewings and hoverflies, did not provide commercially acceptable control of woolly aphid in the absence of earwigs. Under the conventional spray program, using the broad-spectrum insecticide azinphos-methyl for codling moth control, the level of woolly aphid infestation increased with each successive season and biological control was not established. When azinphos-methyl was withdrawn, natural enemies migrated in and provided control of woolly aphid within one season. This is the first study to show that the biological control of woolly aphid can be achieved in a commercially viable IPM program.     

Predictive thresholds for forecasting the compatibility of <Emphasis Type="Italic">Forficula auricularia</Emphasis> and <Emphasis Type="Italic">Aphelinus mali</Emphasis> as biological control agents against woolly apple aphid in apple orchards

The woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae) is a well-known pest of apple orchards world-wide. Several studies have demonstrated variable control of WAA populations by the European earwig, Forficula auricularia (L.) (Dermaptera: Forficulidae) and the WAA parasitoid Aphelinus mali (Halderman) (Hymenoptera: Aphelinidae). We examine whether a beneficial interaction between F. auricularia and A. mali exists and calculate optimal numbers for each species to maintain WAA infestations below acceptable levels. We demonstrate that trees possessing >14 earwigs per trunk trap per week within the first seven weeks post-blossom contained WAA infestations well below acceptable levels. Where these earwig thresholds were not met, a first generation of A.mali greater than 0.5 wasps per tree was required. If these beneficial insect targets were not met, severe WAA infestations occurred. Our findings suggest that if F. auricularia and A. mali numbers exceed these thresholds chemical intervention may not be required.     

Patterns of change in secondary and tertiary sex ratios of the Terebrantian thrips,Frankliniella occidentalis

Adult sex ratios (tertiary sex ratios) of the haplo-diploid Terebrantian thrips species, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) were examined from several native and introduced hosts in an apple (Malus spp.) ecosystem. The ratios were variable and most were female-biased, ranging from 0 to 61% males. Populations in apple bud clusters during early bloom were female-biased (0–10% males). At later bloom states, populations were less female-biased in open blossom clusters (up to 33% males) compared with those in either unopened buds or older petalless blossoms (<11% males). Changes in tertiary sex ratio in all hosts were associated with changes in resource quality, suggesting a possible effect of host quality on sex allocation. In contrast, larval (secondary) sex ratios within apples were slightly male-biased (57%) with little change across apple bud reproductive stages or over time, indicating little to no differential sex allocation. Sex ratios of populations in flight were less female-biased than those found on plants in 62 of 65 comparisons, which suggests that males are more likely to be in flight relative to females. The evidence supports that differential dispersal and distribution of sexes toward various host qualities together with a shorter longevity of adult males determines the pattern of adult sex ratios rather than any significant differential sex allocation.     

Demographic dynamics of Platygaster demades in response to host density

Platygaster demades Walker (Hymenoptera: Platygastridae) is the only hymenopteran parasitoid of apple leaf-curling midge, Dasineura mali Kieffer (Diptera: Cecidomyiidae), in New Zealand. Prior to the present study the mechanisms behind the parasitoid–host density interactions were poorly understood. In this study we carried out both laboratory and field experiments to determine the response of P. demades to D. mali density. In the laboratory, when only a single parasitoid was allowed to forage D. mali eggs of a given density, P. demades displayed a Type II functional response leading to an inverse density-dependent parasitism. However, P. demades showed a Type III functional response in the field where females were able to freely search and disperse between apple shoots infested with D. mali eggs of different densities. As a result, the Type III response reflects a more realistic nature of P. demades in response to D. mali density. Our results also indicate that the numeric response and mutual interference in P. demades significantly contributed to the stability of the parasitoid–host system. The density-dependent parasitism in a host range of 50–300 D. mali eggs per apple shoot suggests that P. demades is highly efficient in controlling D. mali populations of the first, third and fourth generations and when necessary, argumentation measures may be taken before the onset of the second generation.     

夏季苹果新梢生理指标与抗苹果绵蚜的关系

研究苹果生理指标与其对苹果绵蚜(Eriosoma lanigerum Hausmann)抗性的关系,为筛选培育抗性品种,实现持续有效治理苹果绵蚜提供依据.田间调查不同苹果品种对苹果绵蚜的抗性,测定比较各品种正常枝条生理指标,以及被苹果绵蚜危害后生理指标的变化.结果表明,正常枝条中可溶性糖(r=0.99)、蛋白质(r=0.86)含量与感蚜率呈正相关;氨基酸含量与感蚜率呈负相关(r=-0.96);酚类物质和4种酶活性与苹果感蚜率均不存在明显相关性.被害后昭锦108可溶性糖含量有所下降,红富士、金冠分别上升1.4％、7.0％;蛋白质、氨基酸、酚类物质含量均有所下降,其中红富士总酚含量明显下降,达23.5％,总酚下降率与感蚜率呈正相关(r=0.94);超氧化物歧化酶(Superoxide Dismutase,SOD)、过氧化氢酶(Catalase,CAT)活性均上升,其中CAT变化率与感蚜率存在相关性(r=-0.92),昭锦108 CAT活性明显上升,达91.2％;多酚氧化酶(Polyphenol Oxidase,PPO)、过氧化物酶(Peroxidase,POD)活性增减不一;金冠4种酶活性均上升.研究表明,对苹果绵蚜抗性较强的品种:可溶性糖、蛋白质含量较低,游离氨基酸含量较高;受害后可溶性糖含量下降,总酚含量下降率较低,游离氨基酸含量下降率较高.酶活性对抗蚜性的影响不明显.     

苹果绵蚜对不同苹果品种春梢生长期生理指标的影响

为了筛选培育对苹果绵蚜(Eriosoma lanigerum Hausmann)的抗性品种,实现持续有效治理苹果绵蚜的目的,通过测定红富士、金帅、昭锦108、秦冠、红将军等5种不同苹果品种春梢生长期被苹果绵蚜危害前后枝条内可溶性糖、蛋白质、游离氨基酸、总酚含量以及防御性酶的活性变化,探讨苹果生理指标与抗蚜性的关系。结果表明,被害后可溶性糖含量除红将军外均有所上升,其中红富士上升达13.7%;蛋白质含量除红富士外均有所降低;氨基酸含量均有所上升,其中红将军变化明显,变化率达68.8%。酚类物质是一种重要的抗蚜物质,红富士、昭锦108、秦冠被害后总酚含量均升高,其中昭锦108、秦冠中总酚含量上升率约为红富士的2倍。红富士品种正常枝条内超氧化物歧化酶(Superoxide Dismutase,SOD)、多酚氧化酶(Polyphenol Oxidase,PPO)、过氧化物酶(Peroxidase,POD)以及过氧化氢酶(Catalase,CAT)活性均显著低于昭锦108,被害后各苹果枝条SOD活性均出现上升趋势,除红将军的PPO、POD活性降低外,其他品种均升高;金帅、红富士的CAT活性上升明显,分别为110.8%、45.5%。植物的防御性酶与其抗虫性有密切关系,苹果春梢生长期对苹果绵蚜的抗性与苹果体内的可溶性糖、游离氨基酸、SOD、PPO、POD以及CAT活性均有关,而且不同苹果品种被害后生理指标的变化也与其抗蚜性有一定关系。     

Susceptibility of the woolly apple aphid parasitoid,Aphelinus mali (Hym.: Aphelinidae), to common pesticides used in apple orchards in Israel

The effects of one acaricide (cyhexatin), two fungicides (penconazole and sulfur), and six insecticides (azinphos-methyl, chlorpyrifos, imidacloprid, pirimicarb, triazamate and vamidothion) on the adult stage of the parasitoidAphelinus mali (Haldeman), a parasite of the woolly apple aphidEriosoma lanigerum (Hausmann), were investigated under laboratory conditions. Chlorpyrifos (an organophosphorus insecticide-OP) was found to be highly toxic to the adult wasps. Vamidothion (OP) was more toxic to the parasitoid than azinphos-methyl (OP). On the other hand, both chlorpyrifos and azinphos-methyl were found to be harmless to the immature stages of the parasitoid in a test conducted under semi-field conditions. Of the other insecticides, imidacloprid was more toxic to the adult parasitoid than pirimicarb and triazamate. Neither cyhexatin nor penconazole had a considerable toxic effect upon the parasitoid. In contrast, sulfur was found to be moderately toxic to the parasitoid under laboratory conditions, as well as in a field survey in which we followed populations ofE. lanigerum andA. mali parasitization in sulfur-treated plots, and in a plot treated withAmpelomyces quisqualis Ces., a fungus antagonist to powdery mildew. The implications of these results to IPM programs of apple orchards in Israel are discussed     

Flowers for better pest control? The effects of apple orchard ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), their predators and the canopy insect community

Effects of habitat diversification through ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), woolly apple aphid (Eriosoma lanigerum [Haussmann]) (Hemiptera: Aphididae), their insect natural enemies and the most abundant canopy insects (in the Neuroptera, Fulgoromorpha, Cicadomorpha, Heteroptera, Coleoptera and Formicidae) were studied in an apple orchard over 6 years. The composition and diversity of the main functional groups of canopy insects was also compared. Habitat diversification was achieved by changing ground cover conditions within the orchard. In the treatment termed FLOWER, annual and/or perennial flowering plants were sown in the alleys of an apple orchard. Other ground cover treatments were weed-free bare ground (termed BAREgr) and orchard plots with alleys of mowed grass (termed GRASS), which served as control treatments. We found no evidence that habitat diversification enhanced the biological control of green apple aphids compared to the control treatments. However, the greater plant cover in FLOWER resulted in increased woolly apple aphid infestations compared to BAREgr or GRASS. The abundance of various beneficial or neutral canopy insects – Chrysoperla carnea sensu lato (Neuroptera, Chrysopidae) adults, leafhoppers and treehoppers, planthoppers, herbivorous (non-apple feeding) beetles, dipterans and parasitoid wasps – also increased in FLOWER as compared to BAREgr, with GRASS being intermediate between the other treatments. Significantly greater species richness and diversity was found in FLOWER than in BAREgr for most of the functional groups sampled, although the number of predacious insect species was similar among treatments. The composition of the studied functional groups showed high similarity in FLOWER and GRASS, but these treatments were different from BAREgr. Effects of groundcover management on the dominant insect species are discussed.     

Effect of mating combinations on the host parasitisation and sex allocation in solitary endoparasitoid,Aenasius arizonensis (Hymenoptera: Encyrtidae)

Aenasius arizonensis (Girault) is an important solitary endoparasitoid of Phenacoccus solenopsis Tinsley. To optimise the mass production of high-quality females, it is important to assess the influence of mating regimes on the progeny fitness and sex allocation. We, therefore, hypothesise that mating combinations in A. arizonensis adults emerged from different host instars may influence parasitism and sex allocation in the subsequent generation. Therefore, we compared three nymphal instars (1st, 2nd and 3rd) and adults host stages of P. solenopsis for parasitism and sex allocation by A. arizonensis. Further, F₁ female progeny of the parasitoid emerged from different host instars was henceforth evaluated for its fitness in six mating combinations. A. arizonensis females parasitised all the host stages except the 1st instar nymphs. The parasitised 2nd instar nymphs yielded only males, while the sex ratio in the later host instars was strongly female-biased. The parasitoid females preferred 3rd instar nymphs with respect to higher parasitism (74.0–84.0%) and produced more females in the F₁ progeny as compared to other host stages. F₁ females that emerged from 3rd instar nymphs produced significantly higher parasitism (74.0–79.0%). These mating combinations also yielded more female progeny in the F₂ generation. However, parasitism by F₁ females was significantly lower (9.0–12.0%) when mated with males that emerged from 2nd instar P. solenopsis nymphs. Moreover, latter combinations yielded only male progeny in F₂ generation. These findings can be used in laboratory mass rearing of this parasitoid vis-à-vis biological control of P. solenopsis.     

Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai

A study aimed at determining the effect of host size on the pattern of sex allocation by an aphid parasitoid Lysiphlebia mirzai Shuja-Uddin (Hymenoptera: Braconidae: Aphidiinae) was undertaken to test the validity of the following three hypotheses: (1) larger hosts will yield a greater proportion of daughters, (2) differential mortality of the sexes of the parasitoid during development is a function of host-size, and (3) daughters emerging from larger hosts are more fecund. The results suggested a propensity in the parasitoid to deposit fertilised (diploid) eggs in large hosts (third instar nymph) and unfertilised (haploid) eggs in small hosts (first and second instar nymphs). Unpreferred fourth instar nymphs and apterous aphid adults also received more haploid eggs despite being larger in size than the preferred third instar nymphs. However, the perception of host size by the mother was dependent on the extent of temporal variation in the host size distribution and on her previous experience of host size. Developmental period, longevity, mating potential, fecundity and progeny sex ratio of L. mirzai emerging from small versus large hosts indicated that the host size affected the fitness of the daughters more than that of sons. No differential mortality of the sexes during development of L. mirzai was observed in small versus large hosts. This shows that L. mirzai, while ovipositing in growing stages of the host, adjusts progeny sex ratio according to the host size and by doing so she tends to contribute maximally to progeny fitness without knowing about the future host quality.     

In-field production of parasitoids of Dysaphis plantaginea by using the rowan aphid Dysaphis sorbi as substitute host

A system was developed to provide the parasitic wasp Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae), which attacks the rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), with the alternative host Dysaphis sorbi Kaltenbach (Homoptera: Aphididae) in apple orchards. Rowan trees (Sorbus aucuparia L.) arranged along the side of an unsprayed orchard were artificially infested in late February 2002 with eggs of D. sorbi. Colonies of D. sorbi successfully developed from the introduced eggs and persisted on several trees until the end of June. The only primary parasitoid species emerging from a sample of mummified aphids collected in spring from the infested rowan trees was the braconid wasp species E. persicae. In a host-switching experiment, nymphs of D. plantaginea proved suitable for female parasitoids originating from mummified D. sorbi. A series of mummies collected from the rowan trees in early summer contained diapausing parasitoids and hyperparasitoids that only hatched in April of the following spring. These observations suggest the possibility of establishing a local population of E. persicae in apple orchards, so that D. plantaginea can be readily attacked by diapause-emerging parasitoids in early spring.     

How parasitoid sex ratio,size and emergence time are associated with fruit tree cultivar,within-orchard tree position and ants

The biocontrol potential of naturally occurring parasitoids is influenced by the parasitoids’ population and individual characteristics. We studied field determinants of characteristics of the parasitoid Scambus pomorum (Hymenoptera: Ichneumonidae) emerging from weevils (Anthonomus pomorum; Coleoptera: Curculionidae) hidden in damaged apple blossoms. The studied determinants comprised local-scale factors that can be managed by individual growers: tree cultivar, distance between apple trees and forest, and presence of ants. The studied parasitoid characteristics were sex ratio, body size and emergence time. Parasitoid sex ratio, in general female-biased, was significantly different for parasitoids emerging from hosts feeding on different apple cultivars. This finding suggests sex ratio adjustment driven by plant genotype-dependent variation in parasitoid host quality. The detected significant increase of sex ratio (more males) with increasing distance to forest might be explained by sperm depletion of ovipositing parasitoid females immigrating into the orchard. Exclusion of ants significantly increased female-bias in sex ratio in one of the studied apple cultivars. Body size of female and male parasitoids was significantly different between parasitoids emerging from different apple cultivars, supporting the view of cultivar-dependent variation in the quality of the parasitoid’s host. Distance to forest was positively correlated with parasitoid size, indicating farther dispersal of larger individuals. Emergence time varied significantly between apple cultivars, probably due to differences in plant phenology. By demonstrating that parasitoid characteristics vary widely within an orchard, this study shows that parasitoid characteristics that are relevant for biological control might be improved via appropriate management of the orchard and its immediate surroundings.     

Genome mapping of an apple scab,a powdery mildew and a woolly apple aphid resistance gene from open-pollinated Mildew Immune Selection

Apple is host to a wide range of pests and diseases, with several of these, such as apple scab, powdery mildew and woolly apple aphid, being major causes of damage in most areas around the world. Resistance breeding is an effective way of controlling pests and diseases, provided that the resistance is durable. As the gene pyramiding strategy for increasing durability requires a sufficient supply of resistance genes with different modes of action, the identification and mapping of new resistance genes is an ongoing process in breeding. In this paper, we describe the mapping of an apple scab, a powdery mildew and a woolly apple aphid gene from progeny of open-pollinated mildew immune selection. The scab resistance gene Rvi16 was identified in progeny 93.051 G07-098 and mapped to linkage group 3 of apple. The mildew and woolly aphid genes were identified in accession 93.051 G02-054. The woolly aphid resistance gene Er4 mapped to linkage group 7 to a region close to where previously the genes Sd1 and Sd2, for resistance to the rosy apple leaf-curling aphid, had been mapped. The mildew resistance gene Pl-m mapped to the same region on linkage group 11 where Pl2 had been mapped previously. Flanking markers useful for marker-assisted selection have been identified for each gene.     

Influence of host size variation on the development of a koinobiont aphid parasitoid, Lysiphlebus ambiguus Haliday (Braconidae, Hymenoptera)

To determine whether host body size is the currency used by the aphidiine parasitoid, Lysiphlebus ambiguus Haliday (Hymenoptera: Braconidae), in assessing host quality, the aphid, Aphis fabae Scopoli (Homoptera: Aphididae), was reared at either high or low temperature to yield hosts of the same instar with different body sizes. Cohorts of A. fabae raised at 15 degrees C and 30 degrees C and exposed to individual female L. ambiguus in no-choice tests were successfully parasitized in all host stages from 1st instar nymphs to adults. However, younger and smaller aphids were more susceptible to parasitism than older and larger nymphs or adults, as measured by the number of mummies produced. For aphid cohorts reared at 15 degrees C, the proportion of female progeny, progeny adult size, and development time all increased linearly with aphid size at the time of attack. In contrast, for aphid cohorts raised at 30 degrees C, the proportion of female progeny and progeny adult size declined with aphid size, while development time remained unaffected. Through manipulation of host rearing temperature, we have shown that at cooler temperatures the koinobiont parasitoid, L. ambiguus, responds to host size in the same way as an idiobiont parasitoid, but that this response is compromised at higher temperatures. Our results suggest that differential mortality during development is likely to influence the observed secondary sex ratio in relation to aphid size for aphid cohorts raised at higher temperatures due to disruption of the activity of the host's primary endosymbiont and that such reduced nutritional quality of aphids cannot be compensated by increased development time.     

Mating and host density affect host feeding and parasitism in two species of whitefly parasitoids

Abstract The parasitoids in the genera of Encarsia and Eretmocerus (Hymenoptera: Aphelinidae) are important biological control agents of whiteflies, and some of them not only parasitize hosts but also kill them with strong host‐feeding capacity. Two whitefly parasitoid species, Encarsia sophia and Eretmocerus melanoscutus were examined to determine if mating and host density affected their host feeding and parasitism. The whitefly host, Bemisia tabaci, was presented to these two wasp species in densities of 10, 20, 30, 40, 50 and 60 third‐instar nymphs per clip cage. Mated whitefly parasitoid females fed on more hosts than unmated females under a range of host densities (under all six host densities for En. sophia; under the densities of 40 nymphs or more for Er. melanoscutus). Meanwhile, mated females parasitized more whitefly nymphs than unmated females under all host densities for both species. With increase of host density, mated or unmated Er. melanoscutus females killed more hosts by host feeding and parasitism. Mated En. sophia females killed more hosts by host feeding with increase of host density, whereas unmated females did not parasitze whitefly nymphs at all. Our results suggest that only mated female parasitoids with host‐feeding behavior should be released in crop systems to increase their bio‐control efficiency.     

用海棠苗饲养苹果绵蚜的方法

报道了用1年生海棠苗作为寄主植物饲养苹果绵蚜Eriosomalanigerum(Hausmann)的方法,包括寄主植物的选取、栽培管理、接虫方法及试验结果。该方法既能为苹果绵蚜提供长期新鲜的寄主植物,又能使仔蚜很快定殖成活,十分有利于试验的连续进行,且简单经济。