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.     

Rapid change in the settling behavior of the arrowhead scale Unaspis yanonensis as an avoidance mechanism against introduced parasitoids, Aphytis yanonensis and Coccobius fulvus

Abstract Parasitoids are thought to exert immense selection pressures that shape the traits of herbivores. We examined whether two species of parasitoid wasps, Aphytis yanonensis DeBach et Rosen and Coccobius fulvus Compere et Annecke (Hymenoptera: Aphelinidae), affect the settling behavior of the arrowhead scale Unaspis yanonensis Kuwana (Hemiptera: Diaspididae), in order to demonstrate the evolution of antiparasitism behavior of herbivores using parasitoids in the field. We used the following five methods: a comparison of parasitism risk in different settling behaviors‐parasitoid introduction into a parasitoid‐free population; a comparison of the settling behavior between parasitoid‐present and parasitoid‐free populations; a common garden experiment, in which scales were transferred from parasitoid‐present and parasitoid‐free populations into the same garden; and a laboratory observation of the settling behavior of the first instars derived from the two population categories. Both parasitoids were introduced into a parasitoid‐free population in Wakayama in 1987, and the settling mode of the scales was examined in 1987, 1994, and 1995. The introduction of parasitoids modified the scale‐settling mode so that more crawlers settled under another scale (called burrowing), which was consistent with the results observed in parasitoid‐present (including South China) and parasitoid‐free populations. Moreover, only the burrowing scale exhibited a lower parasitism rate compared to scales settling singly and being burrowed. The common garden experiment demonstrated that scales introduced from the parasitoid‐present population had a greater proportion of burrowers than the parasitoid‐free population, even in the same field cage under parasitoid‐free conditions. Laboratory observations demonstrated that the population difference in parasitism rate was principally due to intrinsic differences in the settling behavior of nymphs; some first‐instar nymphs derived from the parasitoid‐present population burrowed under another scale settled. These results strongly suggest that the natural selection pressure imposed by the parasitoids modified the settling behavior of the arrowhead scale.     

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.     

Invertebrate predation of 15N-marked prey in semi-field wheat enclosures

One of the most famous examples of successful, classical biological control in Japan is the introduction of the parasitoids Coccobius fulvus and Aphytis yanonensis against the citrus pest arrowhead scale Unaspis yanonensis. Together, they comprise a host‐parasitoid system that has been demonstrated to be stable. To test the conventional theory that successful biological control of pests occurs through the establishment of a low stable equilibrium, brought about by the density‐dependent responses of natural enemies to the pest species, sampling was carried out at five sites in the field during 2000 and 2001 to examine the relationship between the rate of parasitism by C. fulvus and the density of its host. The data were analysed using three statistical techniques at nine spatial scales. Contrary to conventional theoretical predictions, each method of analysis detected very little density‐dependence at any spatial level in this study. Parasitoid aggregations independent of host density were not sufficient to stabilise host–parasitoid interactions. Our results suggest that neither spatial density‐dependent nor density‐independent parasitism is necessary for successful biological control, or for the stability of the host–parasitoid system. We propose an alternative mechanism: a spatial refuge induced by parasitoid introduction may stabilise a system.