Ecology of two-spotted ladybird, Adalia bipunctata: a review

Abstract:  Adalia bipunctata (Linnaeus) is a generalist aphidophagous ladybird having a wide prey range. It exhibits complex polymorphism. We reviewed the information on its general characteristics, polymorphism, sexual activity, foraging behaviour, food range and prey suitability, growth and development, heterospecific interactions including natural enemies, and its biocontrol potential. Although a poor biocontrol agent (only successful against aphid, Dysaphis plantaginea in Switzerland), it was used in the past as a good model to test various hypotheses and models facilitating ecological understanding in insects. In the present review, the empirical data are interpreted and inferences drawn and a checklist of its prey is provided.     

Egg cannibalism by ladybird larvae is less frequent than expected from the nutritional benefit accrued to cannibals

Egg cannibalism is a widespread phenomenon in predatory arthropods. However, conflicting results have been reported regarding the nutritional value of conspecific eggs. Therefore, evaluation of the value of a mixed diet of conspecific eggs and aphids for survival and growth of Adalia bipunctata (Coccinellidae) larvae was tested. Subsequently, the propensity for cannibalism of naive and experienced larvae was assessed in two experiments in which the relative density and quality of conspecific eggs were manipulated in an experimental arena. It was found that larvae that were fed a mixed diet of conspecific eggs and aphids moulted into larger adults than those fed either aphids or eggs, and those that fed on conspecific eggs lost less mass than those fed only aphids during pupal stage. Additionally, in an experimental arena, attacks on aphids were more frequent than expected when conspecific eggs occupied 50% and 75% of the patches. When 50% of patches were occupied by conspecific eggs, the preference for aphids was less marked when larvae had previously experienced cannibalism (76% vs. 52% respectively) or when offered in the arena conspecific egg the cuticular hydrocarbons of which had been removed (76% vs. 48%, respectively). However, cannibalism was not enhanced if larvae experienced heterospecific prey shortages, but were supplemented with an artificial diet. Given that prey choice in A. bipunctata larvae is driven by chemical cues and that hydrocarbons on the egg surfaces and in larval tracks are very similar, we hypothesize that the naive larvae avoid eggs because of the uncertainty that those hydrocarbons indicate either eggs or conspecific larvae.     

Characterization of the alimentary canal of the aphidophagous ladybird,Adalia bipunctata (Coleoptera: Coccinellidae): anatomical and histological approaches

The alimentary canal of the two‐spot ladybird Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae) presents the foregut (stomodeum), the midgut (mesenteron) and the hindgut (proctodeum). The shortest region is the foregut and the longest is the midgut. The relative proportions of the main regions were found to be similar for males and females. In the foregut it was possible to distinguish the pharynx, the esophagus and the proventriculus but no crop. The hindgut is composed of the ileum, rectum and rectal canal. Generally the organ width is similar for males and females, but females presented a wider proventriculus. The epithelium of the foregut varied from squamous to simple cuboidal and columnar. In the midgut the epithelium is simple columnar with goblet and regenerative cells. The epithelium of the hindgut varied from simple cuboidal to squamous. Females presented thicker midgut epithelium whereas males presented thicker epithelium in the esophagus. The anatomy of the alimentary canal of A. bipunctata seems to conform to its carnivorous and recent phylogenetic status within the family Coccinellidae.     

Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata

Female mating rate is an important variable for understanding the role of females in the evolution of mating systems. Polyandry influences patterns of sexual selection and has implications for sexual conflict over mating, as well as for wider issues such as patterns of gene flow and levels of genetic diversity. Despite this, remarkably few studies of insects have provided detailed estimates of polyandry in the wild. Here we combine behavioural and molecular genetic data to assess female mating frequency in wild populations of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). We also explore patterns of sperm use in a controlled laboratory environment to examine how sperm from multiple males is used over time by females, to link mating with fertilization. We confirm that females are highly polyandrous in the wild, both in terms of population mating rates (approximately 20% of the population found in copula at any given time) and the number of males siring offspring in a single clutch (three to four males, on average). These patterns are consistent across two study populations. Patterns of sperm use in the laboratory show that the number of mates does not exceed the number of fathers, suggesting that females have little postcopulatory influence on paternity. Instead, longer copulations result in higher paternity for males, probably due to the transfer of larger numbers of sperm in multiple spermatophores. Our results emphasize the importance of combining field and laboratory data to explore mating rates in the wild.     

Intuition, functional responses and the formulation of predator-prey models when there is a large disparity in the spatial domains of the interacting species

1. The disparity of the spatial domains used by predators and prey is a common feature of many terrestrial avian and mammalian predatory interactions, as predators are typically more mobile and have larger home ranges than their prey. 2. Incorporating these realistic behavioural features requires formulating spatial predator-prey models having local prey mortality due to predation and its spatial aggregation, in order to generate a numerical response at timescales longer than the local prey consumption. Coupling the population dynamics occurring at different spatial scales is far from intuitive, and involves making important behavioural and demographic assumptions. Previous spatial predator-prey models resorted to intuition to derive local functional responses from non-spatial equivalents, and often involve unrealistic biological assumptions that restrict their validity. 3. We propose a hierarchical framework for deriving generic models of spatial predator-prey interactions that explicitly considers the behavioural and demographic processes occurring at different spatial and temporal scales. 4. The proposed framework highlights the circumstances wherein static spatial patterns emerge and can be a stabilizing mechanism of consumer-resource interactions.     

Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata

Abstract. 1. Adult males of the two-spot ladybird beetle, Adalia bipunctata , did not show a functional response to increase in aphid abundance and consumed markedly fewer aphids than do the females.
2. At high densities of prey, females spent more time in area-restricted search than when prey was scarce. Males were always less active than females and they did not respond to an increase in prey abundance by a change in searching behaviour.
3. After a brief encounter with a female, a male showed area-restricted searching behaviour. This behaviour occurred in response to encountering a female's elytra and in particular to a chloroform-soluble component (sex pheromone) present on or in the elytra.
4. Males needed to encounter a female in order to respond to her presence, which indicated the pheromone is a contact pheromone.
5. The searching behaviour of males appeared to be mainly directed towards locating females; that of females towards locating aphids. This difference between the sexes should be taken into account when quantifying the predatory response of ladybirds to aphid abundance in the field.     

Temperature-dependent life attributes of an aphidophagous ladybird, Propylea dissecta

Reproductive attributes, age-specific fecundity and natality based life-tables of an aphidophagous ladybird, Propylea dissecta (Mulsant) were investigated at five temperatures, using aphid, Aphis gossypii as prey. Pre-oviposition period decreased significantly with increase in temperature up to 27°C and thereafter increased at a slower rate. Egg viability dropped significantly at temperature extremes. Females lived longer than males; however, longevity decreased significantly with increase in temperature. The predicted total fecundity and oviposition rate were 952.54 eggs and 35.15 eggs per day at 27°C predicted by a mathematical model compared to empirical estimates of 856.00±30.00 eggs and 39.7±2.26 eggs per day. Age-specific fecundity was triangular and temperature dependent. The peak in oviposition rate occurred earlier at higher temperatures. The highest values of net reproductive rate (R_o=431.1), intrinsic rate of increase (r_m=0.2134 day^-1) and finite rate of increase (λ=1.2379 day^-1) were recorded at 27°C, which suggests it is the optimum temperature for the mass rearing of P. dissecta.     

Vulnerability of larvae of two species of aphidophagous ladybirds, Adalia bipunctata Linnaeus and Harmonia axyridis Pallas, to cannibalism and intraguild predation

Vulnerability of larvae of two species of aphidophagous ladybirds, Adalia bipunctata Linnaeus and Harmonia axyridis Pallas, to cannibalism and intraguild predation was assessed in the laboratory. In the first experiment, a first instar of one of the two above species was kept with a fourth instar of the other species in a Petri dish. The number of times each first instar larva was encountered by the fourth instar larva and the fate of the first instar was determined over a period of 10 min. The fourth instar larvae captured and killed all the first instar larvae of their own species at the first encounter. However, when presented with fourth instar larvae of the other species the first instar larvae of A. bipunctata and H. axyridis were encountered 6.4 ± 1.3 ( n  = 10) and 19.4 ± 2.1 ( n  = 10), respectively. In this experiment no first instar larvae of H. axyridis , whereas all those of A. bipunctata , were killed.     

Expansion of the geographical distribution of an exotic ladybird beetle, Adalia bipunctata (Coleoptera: Coccinellidae), and its interspecific relationships with native ladybird beetles in Japan

The first record of the exotic ladybird beetle, Adalia bipunctata (Coleoptera; Coccinellidae), in Japan was in 1993 at Osaka Nanko Central Park. Since that time, studies on the life history and geographical distribution of A. bipunctata have been ongoing, and its establishment in the Osaka Nanko area has been confirmed. A. bipunctata is a predacious ladybird beetle and a member of a guild that overlaps in habitat and prey with that of native ladybird beetles such as Harmonia axyridis and Menochilas sexmaculatus. We investigated the distribution of A. bipunctata and its interspecific relationships with native predacious ladybird beetles. In some areas, A. bipunctata was dominant in interspecific relationships with native ladybird beetles. For the first 10 years after A. bipunctata was discovered, it occurred only in the Osaka Nanko area, but the present geographical distribution indicates that it has expanded its range. Though the population density of this species was highest at the area recorded first, and tended to decrease in inverse proportion to the distance from Osaka Nanko Central Park, a satellite occurrence was observed in a remote area. The numbers of aphid and tree species (leaf shelter for aestivation and over-wintering) utilized by A. bipunctata have recently increased. Such increases will cause the rate of distribution of A. bipunctata to accelerate. Interspecific competition between H. axyridis and A. bipunctata, which occurs earlier than H. axyridis, may be avoided by desynchronization of the occurrence seasons, and another common predacious ladybird beetle, Coccinella septempunctata, may escape interspecific competition by habitat segregation.     

The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae)

Effects of two different mating regimes on sperm precedencein the two-spot ladybird, Adalia bipunctata, were studied usingthe polymorphic gene for melanism as a marker for paternity.Virgin nonmelanic females (homozygous recessive) were matedto nonmelanic male(s) and then, after laying fertilized eggs,were mated to a melanic male of known genotype. The resultsafter the two successive single matings showed a highly variabledegree of paternity of the second male. Initial multiple matingwith nonmelanic males did not alter the pattern of paternityafter the subsequent single mating with a melanic male, butit had two other effects: (1) the female showed an increasein rejection behavior, and (2) a longer copulation was requiredfor high success of the melanic male. Additional observationsin which families were reared from beetles collected in copulain the field demonstrated that sperm competition also occursunder natural conditions. The outcome of the competition wasvariable with frequent sperm mixing.     

Evolution of cuticular hydrocarbon diversity in ants

The cuticular hydrocarbons (CHCs) of ants provide important cues for nest-mate and caste recognition. There is enormous diversity in the composition of these CHCs, but the manner in which this diversity has evolved is poorly understood. We gathered data on CHC profiles for 56 ant species, relating this information to their phylogeny. We deduced the mode of evolution of CHC profiles by reconstructing character evolution and then relating the number of changes in CHC components along each branch of the phylogeny to the length of the branch. There was a strong correlation between branch length and number of component changes, with fewer changes occurring on short branches. Our analysis thereby indicated a gradual mode of evolution. Different ant species tend to use specific CHC structural types that are exclusive of other structural types, indicating that species differences may be generated in part by switching particular biosynthetic pathways on or off in different lineages. We found limited, and contradictory, evidence for abiotic factors (temperature and rainfall) driving change in CHC profiles.     

Rhythmicity in life events of an aphidophagous ladybird beetle, Cheilomenes sexmaculata

Abstract:  The present laboratory experiments have been carried out to investigate rhythms in various life events, viz. mating, oviposition, hatching, moulting, pupation and eclosion, of an aphidophagous ladybird beetle, Cheilomenes sexmaculata under laboratory conditions. Incidences of mating and eclosion occurred mostly (66% and 73% respectively) in photophase. While oviposition, hatching, moulting and pupation occurred during scotophase with the peaks of the former two distributed between time intervals 12:00–15:00 h and 21:00–00:00 h respectively. Confinement of life events that are associated with vulnerable stages in scotophase might be an adaptation to prevent their exposure to natural enemies.     

Patterns of exclusion in an intraguild predator-prey system depend on initial conditions

1. When intraguild (IG)-prey are superior to IG-predators in competing for a shared resource, theory predicts coexistence of the IG-prey or the IG-predator with the resource depending on the productivity level: (a) resource and IG prey coexist when productivity is low; (b) IG-predator and resource coexist at high productivity; (c) if IG-prey and IG-predators can coexist, it is only at intermediate productivity levels. 2. We tested the existence of productivity-dependent regions of coexistence using an experimental system of two predatory mites and a shared food source (pollen). 3. At high levels of pollen supply (i.e. high productivity), the IG-predator excluded the IG-prey in most, but not all, cases. The same pattern of exclusion was observed at low productivity, at which the IG-prey was expected to exclude the IG-predator. Therefore, species composition could not be predicted by productivity levels. Instead, our results show that initial conditions affected strongly the outcome of the interaction. 4. We emphasize the need for theory on IG-predation that takes the effects of stage structure, initial conditions and transient dynamics into account.     

Effect of age on reproductive attributes of an aphidophagous ladybird, Cheilomenes sexmaculata

The effect of both male and female age was investigated on certain reproductive attributes, viz. mating incidence, mating duration, fecundity, percent egg viability, ratio of reproductive and non‐reproductive periods and reproductive rate, of an aphidophagous ladybird, Cheilomenes sexmaculata (Fabricius). Females started mating at the age of 8 hours post‐emergence (PE) and males at the age of 2 days PE. Mating in the laboratory was a male‐dominated phenomenon. The mating duration and reproductive rate of 10‐day‐old females when mated with males of varying ages increased up to the male age of 60 days, and thereafter decreased, whereas, fecundity, egg viability and ratio of reproductive and non‐reproductive periods increased up to the male age of 50 days, and thereafter declined. However, when females of varying ages were mated with 10‐day‐old males, fecundity and reproductive rate increased up to 40 days of female age, respectively, then decreased. The ratio of reproductive and non‐reproductive periods increased with increasing age of females. Mating age for optimal reproductive output was 10J50‐day‐old males and NE to 40‐day‐old females. Reproductive cessation in males was recorded after 50 days PE, whereas in females at the age of 40 days PE. Higher mating durations lead to elevated reproductive rates. Delay in the reproductive phase was positively correlated with longevity. The results of this study may aid mass multiplication of this ladybird by identifying and promoting usage of adults of optimal age. Our results also enhance our understanding of the effect of age on reproductive attributes in ladybirds.     

Mating behavior of an aphidophagous ladybird beetle,Propylea dissecta （Mulsant）

Abstract The mating behavior of Propylea dissecta (Mulsant) was investigated in detail. Protandry was evident, as males mature earlier than females. Predicted age of sexual maturation of male and female ladybirds was 7.12 and 9.33 days, respectively. Males performed courtship in six steps, viz. approach, watch, examine, embrace, mount and attempt. Embrace is possibly an appeasement act, while examine serves to recognize mate. Chemical signals initiate male attraction toward females. Visual and tactile cues appear to secondarily help in mate recognition. Mating lasted longest (275.40±12.23 min) when it occurred between unmated individuals. It was much shorter (176.60±5.60 min) when prior mated individuals copulated. There was a significant decrease in mating durations when adults were subjected to five successive matings. Fecundity and percent egg viability increased significantly with increase in the number of matings.     

The importance of cytoplasmic male killing elements in natural populations of the two spot ladybird, Adalia bipunctata (Linnaeus) (Goleoptera: Goccinellidae)

Adalia bipunctata , the two spot ladybird, is polymorphic for a cytoplasmically inherited element which produces female-biased sex ratios by effecting the death of male offspring during embryogenesis. The levels of this element were assessed in Cambridge populations. Six out of 82 females tested showed both a female-biased sex ratio and low egg hatch rates consistent with the presence of this element. Population sex ratios were assessed by collecting pupae from the Cambridge area. The population sex ratio was found to be 1.15: 1, female biased, significantly different from 1:1, and consistent with predictions based on a model incorporating the observed level of the sex ratio element in the population.     

Multi-scale effects of resource patchiness on foraging behaviour and habitat use by longnose dace, Rhinichthys cataractae

1. We examined the response of a predatory benthic fish, the longnose dace ( Rhinichthys cataractae ), to patchiness in the distribution of benthic macroinvertebrates on cobbles at three hierarchical spatial scales during summer and autumn 1996, and spring 1997 in a southern Appalachian stream. 2. At the primary scale (four to five individual cobbles separated by <1 m), the intensity of foraging was not correlated with the biomass of benthic macroinvertebrates/cobble, regardless of season. 3. At the secondary scale (i.e. foraging patches <5 m in diameter) we found that benthic macroinvertebrates were patchily distributed in summer, but not in autumn or spring. Concomitantly, in summer, longnose dace foraged on cobbles with a significantly higher biomass of benthic macronvertebrates than nearby, randomly selected cobbles with similar physical conditions (i.e. longnose dace tended to avoid low-prey foraging patches). In contrast, when benthic macroinvertebrates were distributed homogeneously (spring and autumn), dace did not select patches with a significantly higher biomass of benthic macroinvertebrates than that available on randomly selected cobbles. 4. At the tertiary scale (i.e. stream reaches 11–19 m long), the biomass of benthic macroinvertebrates (per cobble per reach) was patchily distributed (i.e. differed significantly among reaches) in all seasons. Among reaches with physical characteristics preferred by longnose dace, (i.e. erosional reaches dominated by cobble/boulder substratum and high current velocity), we detected a significant, positive correlation between the biomass of benthic macroinvertebrates/cobble and longnose dace density in all seasons. 5. Our results demonstrated that both spatial and temporal patchiness in resource availability influenced significantly the use of both foraging patches and stream reaches by longnose dace.     

Bacteria in ovarioles of females from maleless families of ladybird beetles Adalia bipunctata L. (Coleoptera: Coccinellidae) naturally infected with Rickettsia,Wolbachia, and Spiroplasma

Ovarioles were found to be infected with Spiroplasma, Wolbachia, and Rickettsia in Adalia bipunctata females with maleless progeny in different natural populations. Ooplasm was infected with few Wolbachia bacteria. In ooplasm infected by Rickettsia, bacteria were present in small foci. Spiroplasmas were found encapsulated into ooplasm from the wider intercellular spaces between epithelial and oocyte cells. The cytoplasm of follicular epithelia infected with Rickettsia was heavily destroyed, but the nucleus was intact and free from bacteria. The essential feature of follicular epithelium cells from Spiroplasma and Wolbachia infected A. bipunctata females was inclusions of three types: crystalline, filaments, and concentric myelin-like lamellae. Observations of smears prepared from ovaries of A. bipunctata from natural populations revealed a low concentration of bacteria within a microscopy field (less 10 bacteria) in more than 90% of specimens, and only a few ovaries were heavily infected. Two different ways of bacterial invasion of the oocyte are suggested: Spiroplasma-like, through the intercellular spaces in the epithelium and Rickettsia-like, through the cytoplasm of follicular epithelium cells. Bacteria were not found in germarium zones and we suggest that each follicle is infected from haemolymph.     

Influence of parental age on reproductive performance of an aphidophagous ladybird, Propylea dissecta (Mulsant)

Abstract:  In the present study the influence of maternal and paternal ages on reproductive performance of an aphidophagous ladybird, Propylea dissecta (Mulsant) were investigated. Maternal age strongly influenced fecundity and pre-oviposition period while paternal age strongly influenced the egg viability. Maternal age also influenced percent egg viability, however, at lower levels of significance. The results revealed that the fecundity and percent egg viability increased up to the respective maternal and paternal ages of 30 days and thereafter declined, indicating the onset of senescence. The results of the present study can help in better mass multiplication of the ladybird concerned and in laying foundation for further age-related studies.