A test of temporal and spatial density dependence in the parasitism rates of introduced parasitoids on host, the arrowhead scale (Unaspis yanonensis) in stable host–parasitoids system

Abstract: In 1980, two species of parasitoid wasps (Aphytis yanonensis DeBach et Rosen and Coccobius fulvus Compere et Annecke) were introduced to Japan from China as biological control agents to combat the arrowhead scale (Unaspis yanonensis Kuwana). These introductions represent one of the most successful projects in the history of biological control in Japan. To examine whether density dependent parasitism was inevitable for success of biological control, we tried to detect temporal and spatial density dependence in parasitism rates using time‐series data of scale density, as well as parasitism, over a 16‐year period. The work was conducted in a Satsuma mandarin orange (Citrus unshiu Marc.) orchard in which we previously demonstrated that the system appeared to have stabilized after a decline in scale density following the introduction of the parasitoids. Earlier work also indicated that C. fulvus contributes most to the reduction in, and the stability of, scale density. In this study, we examined: (1) the relationship, on a whole‐orchard basis, between scale density and the rates of parasitism by A. yanonensis, C. fulvus, and a combination of the two species; (2) whether parasitism was positively correlated to scale density on a single‐tree basis among generations and (3) whether spatial density dependence was detectable within generations on an individual‐tree basis. Parasitism by A. yanonensis was temporally density‐dependent on scale population density at the whole‐orchard level, while parasitism by C. fulvus was not. Parasitism by A. yanonensis or by C. fulvus was rarely positively correlated to scale density at the single‐tree level, and spatial density‐dependence was hardly detected at all at this level. Most analyses of combined parasitism rates were similar to rates of parasitism by C. fulvus alone. Contrary to conventional wisdom of biological control theory, this study demonstrates that density dependence is not necessarily detected, even in a system in which a natural enemy has long held pest density stable at low levels.     

Biological control by two exotic parasitoids: eight-year population dynamics and life tables of the arrowhead scale

To determine the process of regulation of Unaspis yanonensis (Kuwana) (Hemiptera: Diaspididae) by the two introduced parasitoids, Aphytis yanonensis DeBach et Rosen and Coccobius fulvus (Compere et Annecke) (Hymenoptera: Aphelinidae), the temporal changes in the population density of U. yanonensis as well as the parasitism rates were monitored for eight years before and after the release of the two parasitoids in a Satsuma mandarin orange (Citrus unshiu Marc. (Rutaceae)) orchard. From 2–4 years after the release, the parasitism rate by C. fulvus gradually increased, eventually reaching 70%, while that by A. yanonensis showed a weak increase, remaining under 12%. During this period, the host density decreased to about 1/100 of the initial density. After the drastic decrease, the host density remained under 1/60 of the level previous to the release for at least 2 years with the populations of both parasitoids persisting. To estimate the ability of the two parasitoids to regulate the populations of U. yanonensis, life tables of U. yanonensis under natural conditions and predator/parasitoid-exclusion (bagged) conditions were compared. It was demonstrated that C. fulvus and A. yanonensis impose about 70% mortality rate on the host at mature adult stages and about 30% on the host at immature adult stages. The results have strongly confirmed the high capability of the two parasitoids as biological control agents for U. yanonensis, which was suggested by earlier studies. However, contrary to those studies, the present study did not support the complementarity of the two parasitoids in regulating the host population, suggesting that the effectiveness of C. fulvus alone in regulating the host population at low levels.     

矢尖蚧发生动态及其寄生性天敌

柑桔矢尖蚧在福建闽北地区一年发生3代。以雌成虫和部分若虫及少数雄蛹越冬．一龄幼蚧盛期,第一代为4月中,下旬。第二代7月上．中旬,第三代9月中旬前后。二龄幼蚧盛期．第一代为5月上、中旬,第二代7月下旬,和第三代9月下旬．后期世代重叠．福建已知寄生蜂6种．其中一种为重寄生蜂,以矢尖蚧黄蚜小蜂为优势种．寄生生蜂自然寄生率最高达49.1%。     

Effect of oil emulsion sprays on parasitoids of the black parlatoria, Parlatoria ziziphi, in grapefruit

The black parlatoria, Parlatoria ziziphi, a common pest of citrus in the tropics and subtropics, has become the most important citrus pest in Upper Egypt. Spray oils may be a relatively safe alternative to harmful synthetic insecticides. However, the effect of spray oils on black parlatoria and associated parasitoids is unknown. Field studies were conducted in Giza, Egypt to assess the effect of two experimental spray oils on P. ziziphi and three associated parasitoid species on grapefruit (Citrus paradisi). Triona oil was more effective than Shecrona oil and reduced scale populations by up to 99% 75 days after application. The parasitoid Encarsia citrina was not affected significantly by either spray oil. Triona oil was slightly harmful to the other primary parasitoid, Habrolepis aspidioti and reduced parasitism rate by Marietta leopardina. However, because the latter species is a hyperparasitoid, the reduction in its number by Triona was beneficial. Triona application is therefore highly effective in controlling the black parlatoria and it reduced the rate of hyperparasitism by M. leopardina. The oils had only a minor negative impact and only on the less important primary parasitoid in the system.     

Is one parasitoid enough? A test comparing one with a pair of parasitoid species in the biological control of arrowhead scales

In classic biological control using natural enemies, the question of whether a single species or multiple species should be introduced has been a matter of debate. The introduction of two parasitoids, Aphytis yanonensis and Coccobius fulvus (Hymenoptera: Aphelinidae), to control the arrowhead scale, Unaspis yanonensis (Hemoptera: Diaspididae), which is a serious pest in Japanese citrus orchards, has been one of the most successful biological control projects in Japan. The success of this program may be explained by two alternative hypotheses: (1) the parasitoid species work complementarily, or (2) only one of them plays a major role. To test which hypothesis is applicable to this host-parasitoid system, we conducted caging experiments and observed temporal changes in the proportion of the parasitisms and the densities of arrowhead scales enclosed with one of the following combinations of parasitoids: (1) A. yanonensis and C. fulvus together, (2) A. yanonensis alone, (3) C. fulvus alone, or (4) neither parasitoid. Parasitisms in the cohorts with A. yanonensis and C. fulvus together and C. fulvus alone rapidly increased to approximately 70%; parasitism with A. yanonensis alone also increased slightly, although it remained consistently lower that those with A. yanonensis and C. fulvus together and C. fulvus. At the end of the experiment, parasitisms with A. yanonensis and C. fulvus together and C. fulvus alone were significantly higher than that with A. yanonensis alone. Parasitism by C. fulvus constituted most of (74%) the parasitism in the cohort with A. yanonensis and C. fulvus together. Further, only C. fulvus suppressed the population growth rates of scales significantly. These results suggest that C. fulvus alone successfully suppresses scale populations as efficiently as both species together do.     

Refuge evolution and the population dynamics of coupled host—parasitoid associations

Summary We have investigated the theoretical consequences of character evolution for the population dynamics of a host—parasitoid interaction, assuming a monophagous parasitoid. In the purely ecological model it is assumed that hosts can escape parasitism by being in absolute refuges. A striking property of this model is a threshold effect in control of the host by the parasitoid, when host density dependence is weak. The approximate criteria for the parasitoid to regulate the host to low densities are (1) that the parasitoid's maximum population growth rate should exceed the host's and (2) that the maximum growth rate of the host in the refuge should be less than unity. We then use this ecological framework as a basis for a model which considers evolutionary changes in quantitative characters influencing the size of the absolute refuge. For each species, an increase in its refuge-determining character comes at a cost to maximum population growth rate. We show that refuge evolution can substantially alter the population dynamics of the purely ecological model, resulting in a number of emergent and sometimes counter-intuitive properties. In general, when the host has a high carrying capacity, systems are polarized either with low or minor refuge and top-down control of the host by the parasitoid or with a refuge and bottom-up control of the host by a combination of its own density dependence and the parasitoid. A particularly tantalizing result is that co-evolutionary dynamics can modify ecologically unstable systems into ones which are either stable or quasi-stable (with bouts of unstable dynamics, punctuating long-term periods of quasi-stable behaviour). We present five quantitative criteria which must all be met for the parasitoid to be the agent responsible for control of the host at a co-evolutionary equilibrium. The apparent stringency of this full set of requirements supports the empirically-based suggestion that monophagous parasitoid-driven systems should be less common in nature than those driven by multiple forms of density dependence. Further, we apply our theory to the question of whether exploiters may harvest their victims at maximum sustainable yields and to the evolutionary stability of biological control. Finally, we present a series of testable predictions of our theory and methods useful for testing them.     

Population dynamics of Siphoninus philyreae in California in the presence and absence of a parasitoid, Encarsia partenopea

Abstract. 1. Densities of the whitefly, Siphoninus phillyreae Haliday, remained at low levels at two sites where a parasitoid, Encarsia parknopea (Walker), was released on whitefly-infested ash, Fraxinus sp., and pomegranate, Punica granatum. Populations of S.phillyreae at control sites, where parasitoids were absent, were increasing in density at the beginning of the summer.
2. By mid-summer, E.partenopea had appeared at all four control sites, and densities of S.phillyreae declined to levels similar to those at the release sites.
3. In the absence of the parasitoid, the age structure of S.phillyreae populations was dominated by the egg stage, indicating a population increasing in density. After E.partenopea became abundant at a site, the age structure of the population had a decreasing proportion of young stages.
4. The changes in S.phillyreae age structures were explained by examining the percentage of fourth instar S.phillyreae from which E.partenopea , as opposed to adult whiteflies, emerged. After the parasitoid became abundant at a site, the majority of fourth instars produced parasitoids rather than whitefly adults. The result was that the adult S.phillyreae population declined, and few eggs were laid.
5. The dynamics of the interaction between E.partenopea and S.phillyreae were similar on ash and pomegranate.     

Life-history and oviposition behaviour of Amitus bennetti, a parasitoid of Bemisia argentifolii

Amitus bennetti Viggiani & Evans (Hymenoptera: Platygasteridae) is a recently described parasitoid of the silverleaf whitefly, Bemisia argentifolii Bellows & Perring (Homoptera: Aleyrodidae). Behaviour and life history of the parasitoid are described. The first nymphal instar of B. argentifolii is preferred by the parasitoid, but the 1st through 4th instar may be parasitised. Females first investigate hosts with their antennae, then walk over the host, and eventually step with their front legs on the leaf and insert their ovipositor inside the host facing away from the host, while the hind legs are still on the host. The time from encounter to oviposition (=latency to oviposition) is shortest on the 1st instar. Oviposition duration (mean=39 s) comprises 50% of the handling time. Development time from egg to adult decreases from 72 days at 15 °C to 42 days at 20 °C to 28 days at 25 °C. We estimate that 400 degree days is required for development, with a development threshold of 10 °C. Adult longevity in the absence of hosts was 29, 26 and 19 days and with hosts present 8, 8 and 5 days at 15, 20 and 25 °C, respectively. Amitus bennetti is proovigenic and oviposits most eggs shortly after adult emergence. During the first day of their adult lives females laid 1, 31 and 49 eggs at 15, 20 and 25 °C, respectively. Compared with other parasitoid species, the development time of A. bennetti is very long, and the implications of this for management of B. argentifolii are discussed.     

Classical Biological Control of the Citrus Blackfly <Emphasis Type="Italic">Aleurocanthus Woglumi</Emphasis> by <Emphasis Type="Italic">Amitus Hesperidum</Emphasis> in Trinidad

The citrus blackfly Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae), a native of South East Asia, was first reported in Trinidad in 1998. As part of a classical biological control programme against the pest, releases of Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae) were made in Trinidad from June to August 2000. Field studies were conducted on three commercial citrus farms, two large estates ( >500 ha) and one small orchard (<50 ha) where releases were initially made. Adult blackfly and Amitus populations were monitored weekly with yellow sticky traps. Immature blackfly and parasitism rates were monitored monthly by field sampling. During the study period, citrus blackfly populations declined by more than 98% at all sites while parasitism increased to 60–90%. There were, however, differences between locations, with control at Cumuto being reached within 4 months, at Todd’s Road between 6 and 7 months and at La Gloria about 13 months. This was consistent with the parasitism rates recorded. Although Encarsia perplexa Huang and Polaszek (Hymenoptera: Aphelinidae) was also introduced, it would seem that A. hesperidum was capable of bringing down and maintaining citrus blackfly populations at acceptable levels by itself.     

Interspecific Interactions among Natural Enemies ofBemisiain an Inundative Biological Control Program

Interspecific interactions among insect natural enemies have seldom been investigated experimentally within the context of biological control. Research in this area is needed due to the often contradictory predictions provided by the many theoretical models, the increasing dependence on biological control, and the concern that biological control agents may adversely affect some nontarget organisms. We describe a study whereby the occurrence and dynamics of interspecific interactions among three natural enemies (two parasitoids:Encarsia formosaandEncarsia pergandiella;and one predatorDelphastus pusillus) of the whitefly,Bemisia argentifolii(previously referred to asBemisia tabacistrain “B”), were evaluated in greenhouse cage experiments. Eight populations consisting of all possible combinations of the three natural enemies and one population of whitefly alone were established to test the following hypotheses: (1) Natural enemy introductions are capable of suppressingB. argentifoliipopulations; (2) all interspecific interactions are detrimental to achieving biological control; (3) the likelihood of achieving biological control decreases as the potential number of interspecific interactions increases; and (4) the species composition of biological control agents is of greater consequence than the number of natural enemy species released. In addition, we tested the hypothesis (5) that the frequency of interspecific interactions increases with a decrease in host or prey availability. Our results demonstrate that all combinations of natural enemies provided significant levels of whitefly suppression. While the intensities of interspecific interactions among natural enemy species were frequently positively and significantly correlated with the densities of parasitized whitefly, interspecific interactions among natural enemies were not detrimental to achieving higher levels of biological control. The composition of species released, rather than the number of species released, was of greater importance to accomplishing biological control. Releases ofD. pusillusin combination with one or both of the parasitoids provided the greatest levels of whitefly suppression. These results suggest that the types of interspecific interactions rather than the numbers of interspecific interactions among natural enemies may be important to the outcome of inundative biological control programs.