Naoya Osawa

Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics

Abstract To clarify functional and numerical responses to temporal and spatial variations of resources (resource tracking), and the population characteristics of the ladybird beetle Harmonia axyridis, I analyzed the results of a 3-year field observation at 24 sites (seven plant species) on eight species of aphids. The seasonal changes in the number of beetles estimated by the Jolly–Seber method were significantly correlated with those of aphids in the total area. The estimated values of population parameters suggested frequent immigration and emigration of the H. axyridis population, although reproductive rates between spring and summer were rather stable all 3 years (1.87–3.49). The staying time and the daily number of adults and eggs at each site were influenced not only by a single factor but also by interactions among time and quantity and quality of the prey. The adult movement showed two patterns, which corresponded with the movement within and between the subpopulations when an assemblage of H. axyridis occurring on the plants of the same species or genus was regarded as a subpopulation. Adult movement intensely occurred within a subpopulation, although the beetles moving between subpopulations had a significantly greater chance to reach the habitat with a high aphid density. The habitats of H. axyridis could be categorized into a suitable habitat for survival and reproduction and a temporal refuge. The results obtained here suggest that H. axyridis, with high ability of prey searching and reproduction, maintains a stable population in heterogeneous and temporal habitats by its resource tracking mechanisms.

Sibling and non-sibling cannibalism by larvae of a lady beetleHarmonia axyridis Pallas (Coleoptera: Coccinellidae) in the field

Sibling (cannibalism among siblings) and non-sibling cannibalism (cannibalism among non-siblings) were studied in a natural population of a lady beetle,Harmonia axyridis Pallas. Of all the eggs laid (n=2269), 24.76% (n=562) were killed by sibling cannibalism and 36.10% (n=819) were killed by non-sibling cannibalism. Sibling cannibalism occurred constantly and intensively in most egg batches throughout the entire oviposition period. On the other hand, non-sibling cannibalism was more intense in the middle and late oviposition periods, and when the egg batches were close to an aphid colony. This may be due to the high density ofH. axyridis larvae relative to aphid density in the middle and late oviposition periods and also the larvae searching intensively near an aphid colony.

Sibling cannibalism in the ladybird beetleHarmonia axyridis: Fitness consequences for mother and offspring

The adaptive significance of sibling cannibalism was analyzed in the ladybird beetleHarmonia axyridis at two prey densities. Possible costs and benefits were considered from three points of view: the mother, the cannibal and the victim. Cannibals ate both infertile and fertile eggs, thereby increasing in body length and survival rate with the intensity of sibling cannibalism. The cannibalistic trait was clearly beneficial to the cannibal when aphid density was low. However, it was not always beneficial when aphid density was high and the victims were full siblings. The altruistic behavior of being a victim was beneficial only when the victim was cannibalized by full siblings at low aphid density. The mother attained almost equal fitness at low aphid density, regardless of the intensity of sibling cannibalism. This suggests that sibling cannibalism is not maladaptive for the mother. At high aphid density, however, mother’s fitness decreased with the intensity of sibling cannibalism, indicating that sibling cannibalism is maladaptive for the mother when larval food availability is high.

Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating

Seasonal variation in the frequency of elytral colour polymorphism in the ladybird beetle, Harmonia axyridis, was analysed through the combination of field observations and laboratory mate-choice experiments. Field observations involving daily mark-recapture of a local population revealed an overall preponderance of melanic morphs in the population, but the proportion of non-melanics notably increased from spring to summer due to their higher frequency of mating among different morphs of the spring generation. In the laboratory experiments, both melanic and non-melanic females preferentially chose non-melanic males in spring, but non-melanics were less successful at mating than melanics in summer. Therefore, the relative frequencies of melanics and non-melanics within a population vary throughout the seasons, with non-melanics increasing in proportion towards summer and decreasing thereafter. Laboratory experiments revealed that non-random mating among morphs is the basis of this variation, with females and, to a lesser degree, males being involved in the process of mate selection. The results of an artificial colour-change experiment indicate that male elytral colour is an important factor in female mate selection but other factors such as behaviour and chemical cues must also be involved.

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Population field studies of the aphidophagous ladybird beetleHarmonia axyridis (Coleoptera: Coccinellidae): Life tables and key factor analysis

1) Life tables of the predatory ladybird beetleHarmonia axyridis were analysed by taking samples from twenty or twenty four sites colonized by eight species of aphids for two years. 2) Larval mortality was a key factor in theH. axyridis populations. Mortality of all the stages tended to be density-dependent when life cycles were divided into four developmental stages, except in the case of mortality at hatching due to sibling cannibalism. 3) Sibling and non-sibling cannibalism played an important role on population stability and persistence. Life tables of the predatory ladybird beetleHarmonia axyridis were analysed by taking samples from twenty or twenty four sites colonized by eight species of aphids for two years. Larval mortality was a key factor in theH. axyridis populations. Mortality of all the stages tended to be density-dependent when life cycles were divided into four developmental stages, except in the case of mortality at hatching due to sibling cannibalism. Sibling and non-sibling cannibalism played an important role on population stability and persistence.

Asymmetric reproductive interference between specialist and generalist predatory ladybirds

1. Closely related species often differ greatly in the quality and breadth of resources exploited, but the actual mechanisms causing these differences are poorly understood. Because in the laboratory specialized species often survive and perform as well or better on host species that are never utilized in nature, negative ecological interactions restricting host range must exist. Here, we focused on reproductive interference, which has been theoretically predicted to drive niche separation between closely related species with overlapping mating signals. 2. We examined the interspecific sexual interactions in relation to ecological specialization and generalization in two sibling ladybird species, Harmonia yedoensis and Harmonia axyridis. Harmonia yedoensis is a specialist predator that preys only on pine aphids, which are highly elusive prey for ladybird hatchlings, whereas H. axyridis is a generalist predator with a broad prey and habitat range. 3. We experimentally showed that conspecific sperm fertilized the vast majority of eggs regardless of mating order (i.e. conspecific sperm precedence) when a female of H. yedoensis or H. axyridis mated with both a conspecific and a heterospecific male. Moreover, we demonstrated that mating opportunities of H. yedoensis females strongly decreased as heterospecific density increased relative to conspecific density. In contrast, in H. axyridis, female mating success was high regardless of conspecific or heterospecific density. 4. Our results suggest that the generalist H. axyridis should be dominant to the specialist H. yedoensis in terms of reproductive interference. Our results support the hypothesis that asymmetric reproductive interference from the dominant species may force the non-dominant species to become a specialist predator that exclusively utilizes less preferred prey in nature.

Ecology of Harmonia axyridis in natural habitats within its native range

Originally distributed in northeast Asia, Harmonia axyridis (Coleoptera: Coccinellidae) is now found throughout much of the temperate zone. In its native area, H. axyridis maintains stable populations in heterogeneous and temporary habitats because of its great ability to find prey and reproduce, coupled with density-dependent and self-regulatory population regulation. A negative correlation of H. axyridis on the biodiversity of the aphidophagous community has been observed in its native range. The decrease in biodiversity may be mainly caused by the wider range of habitats available to H. axyridis than to the coexisting species. From a theoretical perspective, density-dependent regulation of H. axyridis populations, e.g., cannibalism, may be more important in maintaining the H. axyridis-dominated system, probably than is intraguild predation. Habitat heterogeneity may also be important to the coexistence of H. axyridis and other predators in both native and invaded areas.

The occurrence of multiple mating in a wild population of the ladybird beetleHarmonia axyridisPallas (Coleoptera: Coccinellidae)

Female insects of many species often have multiple copulations, while a single copulation usually can provide sufficient sperm quantity and quality for lifetime fertilization. This controversial phenomenon has recently received much attention (Parker 1984: Curtsinger 1991: Halliday & Arnold 1987: Harvey & May 1989; Knowlton & Greenwell 1984). In some insect taxa, a lifetime copulation number can be easily estimated by counting number of spermatophores remaining in the spermatheca (e.g. Matsumoto & Suzuki 1992), but more clarification is needed on the actual conditions for multiple mating in a wild population. In coccinellid ladybird beetles, mating behavior was observed in laboratory conditions by Obata (1987, 1988). However, mating behavior in field conditions was only partially interpreted. This study reports the occurrence of multiple mating of the ladybird beetle Harmonia axyridis PALLAS in a wild population, with laboratory observations on mating behavior concerning multiple mating.

Increase in male reproductive success and female reproductive investment in invasive populations of the harlequin ladybird Harmonia axyridis.

Reproductive strategy affects population dynamics and genetic parameters that can, in turn, affect evolutionary processes during the course of biological invasion. Life-history traits associated with reproductive strategy are therefore potentially good candidates for rapid evolutionary shifts during invasions. In a series of mating trials, we examined mixed groups of four males from invasive and native populations of the harlequin ladybird Harmonia axyridis mating freely during 48 hours with one female of either type. We recorded the identity of the first male to copulate and after the 48 h-period, we examined female fecundity and share of paternity, using molecular markers. We found that invasive populations have a different profile of male and female reproductive output. Males from invasive populations are more likely to mate first and gain a higher proportion of offspring with both invasive and native females. Females from invasive populations reproduce sooner, lay more eggs, and have offspring sired by a larger number of fathers than females from native populations. We found no evidence of direct inbreeding avoidance behaviour in both invasive and native females. This study highlights the importance of investigating evolutionary changes in reproductive strategy and associated traits during biological invasions.