Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

Day length constrains the time budget of aphid predators

Phenology shifts and range expansions cause organisms to experience novel day length-temperature correlations.Depending on the temporal niche,organisms may benefit or suffer from changes in day length,thus potentially affecting phenological adaptation. We assessed the impact of day length changes on larvae of Chrysoperla carnea (Stephens) and Episyrphus balteatus (De Geer),both of which prey on aphids.Larvae ofE.balteatus are night-active,whereas those of C.carnea appear to be crepuscular.We subjected both species in climate chambers to day lengths of 16 :8 L :D and,to circumvent diapause responses,20 :4 L :D.We recorded development times and predation rates of both species. E.balteatus grew 13%faster in the 16 :8 L :D treatment and preyed on significantly more aphids.In contrast,C.carnea grew 13% faster in the 20 :4 L :D treatment and higher predation rates in 20 :4 L :D were marginally significant.Our results show that day length affects development and predation,but that the direction depends on species. Such differences in the use of day length may alter the efficiency ofbiocontrol agents in a changing climate.     

Visual pigment processes and prolonged pupillary responses in insect photoreceptor cells

The visual pigment in the peripheral retinular cells of the hoverfly Syrphus balteatus was investigated by absorbance difference measurements. Different visual pigments were found in the dorsal versus the ventral part of the eye in the male, but not in the female. In the male in the dorsal part of the eye the visual pigment has an isosbestic point at 513 nm; in the ventral part this value is 490 nm. The latter value is found in the female in both parts of the eye.Prolonged pupillary responses were studied in the male Syrphus and appeared to be most marked in the ventral part of the eye. In both hoverfly and blowfly prolonged pupillary responses are induced by short wavelength light only; i.e., by light which excessively can convert rhodopsin into metarhodopsin. By contrast, in butterflies red light (and a long dark adaptation time) is necessary to evoke a prolonged pupillary response. It was demonstrated in both hoverfly and blowfly that long wavelength light, which reconverts metarhodopsin into rhodopsin, inhibits a prolonged pupillary response; or, accelerates pupil opening.Based on material presented at the European Neurosciences Meeting, Florence, September 1978     

Tuned protection of aphids by ants against a predatory hoverfly

1. Aphid‐tending ants that feed on honeydew have evolved strategies against aphidophagous insects and tune their aggressive behaviour according to the level of danger for their trophobionts. Here we investigate how Lasius niger Linnaeus (Hymenoptera: Formicidae) ants react to different instars of Episyrphus balteatus De Geer (Diptera: Syrphidae) hoverflies which vary in their voracity and defensive abilities. 2. During pairwise encounters, early syrphid instars (eggs, L1, and L2 larvae) elicited lower aggression scores compared to third larval instars (L3), which was intensively bitten by ants. L3 tried to escape from ants by releasing a sticky and toxic secretion over biting ants that died or underwent severe morbidity. 3. In a standardised system including the host plant, aphid, tending ant, and hoverfly, the ability of ants to protect an Aphis fabae Scopoli (Hemiptera: Aphididae) colony was evaluated. Early E. balteatus instars placed onto the plant elicited no mobilisation of ants, which often removed the hoverfly successfully. Eggs and early instars appeared as the weak links for integrated pest management by hoverfly auxiliaries. 4. In contrast, L3 induced the number of ant patrollers to increase at a local scale without any further recruitment from inside the ant nest. L3 syrphids were quite efficient at gluing ants with defensive secretions and at resisting to removal attempts by ants. 5. While supporting the assumption that ants tune their defensive response to the aphidophagous predator, the present results also showed a lack of efficient protection of their trophobionts from the most voracious late syrphid instar.     

Intra‐specific variation affects the structure of the natural enemy assemblage attacking pea aphid colonies

Abstract 1. Intra‐specific variation in plant defence traits has been shown to profoundly affect herbivore community structure. Here we describe two experiments designed to test whether similar effects occur at higher trophic levels, by studying pea aphid–natural enemy interactions in a disused pasture in southern England. 2. In the first experiment, the numbers and identity of natural enemies attacking different monoclonal pea aphid colonies were recorded in a series of assays throughout the period of pea aphid activity. 3. In the summer assay, there was a significant effect of clone on the numbers of aphidophagous hoverfly larvae and the total number of non‐hoverfly natural enemies recruited. Clone also appeared to influence the attack rate suffered by the primary predator in the system, the hoverfly Episyrphus balteatus, by Diplazon laetatorius, an ichneumonid parasitoid. Colonies were generally driven to extinction by hoverfly attack, resulting in the recording of low numbers of parasitoids and entomopathogens, suggesting intense intra‐guild predation. 4. To further examine the influence of clonal variation on the recruitment of natural enemies, a second experiment was performed to monitor the temporal dynamics of community development. Colonies were destructively sampled every other day and the numbers of natural enemies attacking aphid colonies were recorded. These data demonstrated that clonal variation influenced the timing, abundance, and identity of natural enemies attacking aphid colonies. 5. Taken together, these data suggest that clonal variation may have a significant influence on the patterns of interactions between aphids and their natural enemies, and that such effects are likely to affect our understanding of the ecology and biological control of these insect herbivores.     

Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus

To cope with pathogen and insect attacks, plants develop different mechanisms of defence, in both direct （physical and chemical） and indirect ways （attractive volatiles to entomophagous beneficials）. Plants are then able to express traits that facilitate ＂top-down＂ control of pests by attracting herbivore predators. Here we investigate the indirect defence mechanism of potato plants by analyzing the volatile patterns of both healthy and aphid- infested plants. Important changes in the emitted terpene pattern by the Myzus persicae infested host plant were observed. Using Solid Phase MicroExtraction （SPME） and GC-MS, the （E）-fl-farnesene （EBF） appeared to be emitted by aphid-infested potato and not by healthy plants. To assess the infochemical role of these volatile releases after aphid damage on the aphidophagous predators Episyrphus balteams, the hoverfly foraging behavior was assessed using the Observer 5.0 software （Noldus, Wageningen, The Netherlands）. Aphidfree potato plants were also used as a control volatile source in the predator behavioral study. While aphid-infested plants induced efficient searching and acceptation behaviors leading to egg-laying, no kairomonal effect of healthy potato plants was observed, leading to longer immobility durations and shorter searching periods in the net cage. High oviposition rate of E. balteatus was observed when aphid-infested potato was used （mean of 48.9 eggs per laying and per female）. On the other hand, no egg was produced by the hoverfly on healthy aphid-free plants. The E. balteatus foraging and reproductive behaviors according to the volatile emission from aphid-infested plants are discussed in relation to the potential use of active infochemical molecules in integrated aphid pest management.     

Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus

Abstract 1. Diapause induction in monarch butterflies Danaus plexippus was studied using adults captured from the wild in Minnesota and Wisconsin, and individuals reared under outdoor and controlled conditions.
2. Oocyte presence in females and ejaculatory duct mass in males were used to indicate reproductive status.
3. Some wild individuals were in diapause in mid-August, and all males and females were in diapause by late August and early September respectively.
4. Individuals reared under decreasing day lengths and fluctuating temperatures were more likely to be in diapause than were individuals reared under long or short day lengths or constant temperatures.
5. Individuals fed potted old Asclepias curassavica plants were more likely to be in diapause than were those fed potted young host plants; when cuttings of Asclepias syriaca plants from the field or greenhouse pots were used, there was no effect of host plant age.
6. Extremely high temperatures increased the number of day-degrees required for development from egg to adult, while decreasing day lengths and older host plants tended to decrease the number of day-degrees required for development.
7. There appears to be a continuum of reproductive development in monarchs, with gradual declines in mean ejaculatory duct mass and oocyte production during the late summer.
8. None of the experimental treatments led to 100% diapause, and diapause was more likely to occur in monarchs subjected to more than one diapause-inducing cue.     

The effect of egg load and host deprivation on oviposition behaviour in aphidophagous hoverflies

1. Two species of aphidophagous hoverfly, Episyrphus balteatus and Syrphus ribesii, were tested for the effects of egg load and host deprivation on oviposition choices. 2. Egg load affected the total number of eggs laid in E. balteatus but not in S. ribesii, however it did not affect the proportion laid on any one aphid in E. balteatus but did affect the proportion laid on any one aphid in S. ribesii. The rank order of preferences remained unchanged by age or host deprivation. 3. The dominant effects on host choices were aphid species (in both syrphids) and presentation order (in E. balteatus). 4. Being deprived of hosts increased egg load substantially in E. balteatus, and increasing time of deprivation also had an effect on discrimination; there was no effect of host deprivation in S. ribesii. 5. Reasons for these patterns are discussed.     

Diapause‐inducing signals prolong nymphal development in the two‐spotted spider mite Tetranychus urticae

Female two‐spotted spider mite Tetranychus urticae are grown under different photoperiods and the photoperiodic regulation of diapause is examined. The photoperiodic response curve for diapause induction was of the long day–short day type, with critical day lengths (CDLs) of 2 and 12.5 h; diapause was induced between these CDLs. The preimaginal period is significantly longer in diapausing females than in non‐diapausing females; moreover, a significant positive correlation is detected between diapause incidence and deutonymphal period. Diapause incidence is high when long‐night photoperiods are applied against a background of continuous darkness in the stages including the deutonymph; this stage appears to be the most sensitive to photoperiod. These observations suggest that diapause‐inducing conditions inhibit nymphal development, particularly in the deutonymphal stage when photoperiodic time measurement for determination of reproduction or diapause is carried out.     

Photoperiodic induction of prepupal diapause and its role in synchronization with host phenology in the hibiscus caterpillar,Xanthodes transversa

The hibiscus caterpillar, Xanthodes transversa (Lepidoptera: Noctuidae), is a multivoltine insect that is an important pest of Malvaceae plants such as the okra, Abelmoschus esculentus, and the common rose mallow, Hibiscus mutabilis, in Japan. In the present study, the effects of photoperiod and temperature on the induction of prepupal diapause and the adaptive significance of this diapause were examined in a local population of X. transversa in Miyazaki, Kyushu, southwestern Japan. Larvae showed a long‐day photoperiodic response for controlling the induction of prepupal diapause with a critical day length between 13 and 14 h at 20 to 25°C. Under long‐day conditions larvae rapidly pupated from the sixth instar, but under short‐day conditions they entered diapause in the prepupal stage. Diapause occurrence in the field increased in late September, which was consistent with the laboratory results in terms of the photoperiodic response. Non‐diapause development after this time is maladaptive because most larvae of the next generation could not reach the critical stage (prepupae) before winter and died during early winter in outdoor experiments. Larvae suffered from a high rate of mortality when fed leaves collected late in autumn. The photoperiodic response for controlling the induction of diapause in this insect may play an important role in synchronizing the life cycle with the seasonal changes in food and temperature conditions.     

Dealing with food shortage: larval dispersal behaviour and survival on non‐prey food of the hoverfly Episyrphus balteatus

1. Predatory larvae often have to face food shortages during their development, and thus the ability to disperse and find new feeding sites is crucial for survival. However, the dispersal capacity of predatory larvae, the host finding cues employed, and their use of alternative food sources are largely unknown. These aspects of the foraging behaviour of the aphidophagous hoverfly (Episyrphus balteatus De Geer) larvae were investigated in the present study. 2. It was shown that these hoverfly larvae do not leave a plant as long as there are aphids available, but that dispersing larvae are able to find other aphid colonies in the field. Dispersing hoverfly larvae accumulated on large aphid colonies, but did not distinguish between different pea aphid race–plant species combinations. Large aphid colonies might be easier to detect because of intensified searching by hoverfly larvae following the encounter of aphid cues like honeydew that accumulate around large colonies. 3. It was further shown that non‐prey food, such as diluted honey or pollen, was insufficient for hoverfly larvae to gain weight, but prolonged the survival of the larvae compared with unfed individuals. As soon as larvae were switched back to an aphid diet, they rapidly gained weight and some pupated after a few days. Although pupation and adult hatching rates were strongly reduced compared with hoverflies continuously fed with aphids, the consumption of non‐prey food most probably increases the probability that hoverfly larvae find an aphid colony and complete their development.     

Diapause induction and termination in the predatory mite Euseius finlandicus in peach orchards in northern Greece

The course of diapause induction as well as of diapause termination infemales of the predatory mite Euseius (Amblyseius)finlandicus Oudemans (Acari: Phytoseiidae) in Northern Greece wasdetermined by transferring females during winter and early spring from peachtrees to a short day (LD 8:16) or a long day (LD 16:8) photoperiod both at 20°C. The first diapause females were found in mid September andby the first week of October all the females were in diapause. The mean numberof days required for diapause termination under the short day photoperiod LD8:16 was gradually reduced from 93.7 days in the beginning of October to lessthan 20 days in mid February and early March. Under the long day photoperiod ofLD 16:8 diapause was terminated in less than 20 days irrespective of the dateof collection. These results indicate that by mid February photoperiodicsensitivity of females was lost and diapause was terminated. However, femaleswere found in their overwintering sites until the second half of March,probablybecause of the prevailing relatively low temperatures and lack of adequatefood.     

Effects of photoperiod and temperature on diapause induction and termination in the swallowtail,Sericinus montelus

Abstract Sericinus montelus overwinters as diapausing pupae. In the present study, the effects of photoperiod and temperature on diapause induction and termination of diapause are investigated. The results obtained demonstrate that high temperature can reverse the effect of short day‐lengths on diapause induction. Under an LD 12 : 12 h photoperiod, all pupae enter diapause at 15, 20 and 25 °C, whereas all pupae develop without diapause at 35 °C. No pupae enter diapause under an LD 14 : 10 h photoperiod when the temperature is above 20 °C. Photoperiodic response curves obtained at 25 and 30 °C indicate that S. montelus is a long‐day species and the critical day‐length is approximately 13 h at 25 °C. At 25 °C, the duration of diapause is shortest when the diapausing pupae are maintained under an LD 16 : 8 h photoperiod and increases under LD 14 : 10 h and LD 12 : 12 h photoperiods. Under an LD 16 : 8 h photoperiod, the duration of diapause is shortest when the diapausing pupae are maintained at 25 °C, followed by 20 and 30 °C, and then at 15 °C. These results suggest that a moderate temperature favours diapause development under a diapause‐averting photoperiod in this species. The duration of diapause induced by an LD 12 : 12 h photoperiod is significantly longer at 25 °C than those at 15, 20 and 30 °C, and is shortest at 15 °C. At 25 °C, the duration of diapause induced by LD 6 : 18, LD 12 : 12 and LD 13 : 11 h photoperiods is similar and longer than 90 days. Thus, the diapause‐inducing conditions may affect diapause intensity and a photoperiod close to the critical day‐length has significant influence on diapause intensity in S. montelus.     

Seasonal regulation of dormancy in Chrysopa carnea (Neuroptera)

In Ithaca, New York, diapause incidence in Chrysopa carnea exceeds 50 per cent among adults emerging between 31 August and 3 September. Apparently, decreasing late summer day lengths, which exceed the stationary critical photoperiod in the laboratory, act on the sensitive stages and induce diapause. Full diapause intensity occurs about 2 weeks after adult emergence; complete winter coloration appears approximately 2 weeks later. Photoperiodic stimili in combination with the geographic strain largely determine diapause depth.Decreasing autumn day lengths decelerate diapause development and maintain diapause until the winter solstice. Subsequently, short day lengths and cold temperatures slow diapause development. In nature, neither long days, increasing day lengths, nor chilling hasten diapause termination. Diapause duration is largely determined by the interaction between inducing photoperiod, maintaining photoperiodic and thermal stimuli, and geographic strain. In Ithaca, diapause ends (all response to photoperiod ceases) between 22 January and 12 March.After diapause ends, the animals retain their diapause characteristics until temperatures exceed 4°C. Post-diapause reproductive development in females requires approximately 100 heat units above 4°C; however, below 8°C mating and oviposition are absent. Although the winter coloration remains, mating occurs within 1 day after transfer from 4 to 24°C. Temperature determines the rate at which the green summer colour returns.     

Geographic variation in diapause response of adult Rhipicephalus appendiculatus ticks

Diapause in adults of the African brown ear tick Rhipicephalus appendiculatus is dependent on latitude and stock origin. Lower latitude populations, that is, those nearer the equator, show no diapause response to long or short day exposure. Diapause response to short day lengths is found in higher latitude populations, further south, and increases with increasing latitude. Nearly all individuals in the southernmost population, used in this study, enter diapause under short and long day exposure which implies that the onset of diapause in this population is obligatory. Diapause termination in higher latitude populations is induced by increasing photo period, further north, but still south of the equator, diapause is terminated by ageing. The differences in diapausing behaviour of the different populations are discussed in relation to their climatic conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

Seasonal changes in the reproductive and life-history traits of Chrysomela populi L. (Coleoptera: Chrysomelidae)

Seasonal changes in the reproductive and life‐history traits of Chrysomela populi L. were investigated in Shobara (34°52′N, 133°01′E), Japan, in 2004 and 2005. Larvae were hatched and reared under natural photoperiod and temperature in 8 different periods between late April and early September in 2004. The incidence of adult diapause increased with progression of the season in 2004. The critical timing of diapause induction, as defined by 50% of females entering diapause, was estimated to occur between late July and early August. No effects of season on the survival rate from hatching to adult emergence, percentage ovipositing females and percentage females that deposited viable eggs were clearly detected. Adult weight at emergence fluctuated seasonally, which was probably caused by air temperature. No effect of season on the oviposition period was observed among females that averted diapause. Females that entered diapause in 2004 started oviposition from the first day of May in 2005. Reproductive output was significantly greater in diapause females than in non‐diapause females. This increase in the reproductive output of diapause females was caused by elongation of the oviposition period and consequently by enlargement of the number of egg clutches deposited. These results suggest that the seasonal timing of diapause induction in females of C. populi would be affected by various risks and benefits to reproduction and survival.     

Geographical variation and inheritance of the photoperiodic response controlling larval diapause in two distinct voltine ecotypes of the Asian cornborer Ostrinia furnacalis

The Asian corn borer Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) enters facultative diapause as fully‐grown larvae in response to short day lengths during autumn. As a result of geographical variations in photoperiodic response, the moths from Nanchang (28.8°N, 115.9°E; NC strain) judge both LD 14 : 10 h and LD 15 : 9 h photocycles as long days and develop directly, whereas moths from Haerbin (44.9°N, 127.2°E; HB strain) judge the same photocycles as short days and enter diapause. Crosses between the two strains are used to evaluate the inheritance of diapause. The critical day lengths for diapause induction in the HB strain are significantly longer than those in the NC strain at all temperatures. The critical day length of F₁ progeny is intermediate between the two strains. However, the critical day length in all crosses is significantly longer with HB strain fathers or grandfathers than with NC strain fathers or grandfathers, indicating that the male parent has significantly more influence on the critical day length of subsequent progeny than the female. The results from all crosses under LD 14 : 10 h or LD 15 : 9 h photocycles at 25 °C show that the inheritance of diapause in O. furnacalis does not fit a purely additive hypothesis and that the capacity for diapause is transmitted genetically in the manner of incomplete dominance. The incidence of diapause for F₁ progeny under an LD 14 : 10 h photocycle is significantly higher than that under an LD 15 : 9 h photocycle, suggesting that the induction of diapause can be influenced by interactions between the F₁ genotype and photoperiod.     

Dispersion of flightless adults of the Asian lady beetle, Harmonia axyridis, in greenhouses containing cucumbers infested with the aphid Aphis gossypii: effect of the presence of conspecific larvae

Nezara viridula (L.) (Heteroptera: Pentatomidae) recently expanded its distribution range in Japan and reached Osaka. In the southern temperate zone, the species overwinters in the adult stage and reproductive diapause is associated with a body colour change from green to russet. In Osaka, the reproductive diapause is only induced in September–October and nymphs from late egg masses are destined to die during winter. However, the fate of adults emerging late in the season remained unknown. Survival, body colour change, and post‐diapause reproduction were studied under quasi‐natural conditions in Osaka in 1999–2000 in those adults that attained adulthood as late as in November. Two experimental cohorts were used: in the Outdoor cohort, insects were reared outdoors starting in their second instar (28 September); in the Laboratory cohort, nymphs and subsequently adults were reared from the same day under diapause‐inducing conditions (L10:D14 at 25 °C), then acclimatized (5 days at 20 °C and 5 days at 15 °C; L10:D14) and transferred outdoors on 1 December. Adults in both cohorts did not reproduce in autumn and survived the winter with a low mortality. More than 20% of adults in the Outdoor cohort failed to change body colour from green to russet during winter, apparently because of the low ambient temperature, suggesting that the environmental conditions required for colour change do not completely coincide with those required for diapause induction, and that the colour of the adults is not always a reliable indicator of diapause in this species. After overwintering, females from the Outdoor cohort produced significantly fewer egg masses and eggs and had a significantly shorter period of oviposition than females that entered diapause under short‐day conditions in the Laboratory cohort. Thus, if progeny from the late egg masses attain adulthood late in the autumn, these adults have high chances of successful overwintering, but their reproductive output after the winter diapause is significantly reduced.