Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate

Abstract.  1. Many moth and butterfly larvae are gregarious early in development, but become solitary in late instars. This ontogenetic variation in behaviour is probably the result of temporal changes in the costs and benefits associated with gregariousness. This study provides observational and experimental evidence that, in one particular moth species, a series of different ecological factors influence larval behaviour at different times during development.
2. Field observations show that young caterpillars of the limocodid Doratifera casta form large aggregations while foraging, but that mature larvae are largely solitary.
3. A field experiment revealed that individual first to third instar larvae in larger groups develop more rapidly, but that group size had no detectable influence on survival. The developmental advantage associated with gregariousness is affected by host plant species, but not by predator exclusion, suggesting that group living in these cryptic early instar larvae promotes feeding facilitation, but does not provide individuals with protection from natural enemies.
4. Laboratory experiments revealed that aposematic fourth instar caterpillars in large groups were less likely to be attacked by a generalist insect predator than those in small groups.
5. Field observations provided no evidence that group living affects body temperature, suggesting that microclimatic factors do not favour gregariousness in this species.
6. It is concluded that gregariousness in D. casta confers at least two different advantages on larvae at different stages early in development, but that these advantages disappear, or are outweighed by costs associated with intraspecific competition, in final instars.     

Host instar and host plant effects on Aphidius colemani

Abstract:  The effect of Myzus persicae age (I–IV instar nymphs) on parasitism by Aphidus colemani was investigated in choice experiments with either aubergine ( Solanum melongena L.) or pepper ( Capsicum annuum L.) as the aphid host plant species. Aphidius colemani could develop successfully to the mummy stage in all ages of aphid tested, on both pepper and aubergine plants. The greatest proportion of parasitoid mummies was found with II and III aphid instars on pepper and on I, II and III aphid instars on aubergine. On aubergine, I instar nymphs were also parasitized to an appreciable degree. Successful parasitism of IV instar nymphs was consistently low on both crops. The potential implications of host plant effects on the effectiveness of A. colemani as a biological control agent are discussed.     

Effects of a juvenile hormone analog, pyriproxyfen, on the apterous form of Lipaphis erysimi

Effects of a juvenile hormone analog, pyriproxyfen, on various developmental stadia of the apterous form of the turnip aphid, Lipaphis erysimi (Kaltenbach), were bioassayed at three concentrations (50, 100, and 150 mg [AI]/l) in the laboratory. Supernumerary-molted nymphs with 1-3 extra molts were found when the first three nymphal instars were treated, and all these nymphs died prematurely. In contrast, all treated fourth instar nymphs molted normally to adults. The longevity of all pyriproxyfen-treated L. erysimi nymphs and adults and the fecundity of treated adults were reduced by 50%. Higher concentrations of pyriproxyfen (100 and 150 mg [AI]/l) caused sterility in adults from treated fourth instars; whereas the lowest concentration (50 mg [AI]/l) did not cause any adult sterility. A majority of adults from treated fourth instars and treated adults produced normal nymphs, and some adults produced dead nymphs with normal appendages or dead and deformed nymphs without any appendages. Normal nymphs produced by the adults from treated adults or treated at fourth instars developed more slowly from first instar to adult than the water-treated nymphs, and all adults in the new generation apparently reproduced normally. The potential role of pyriproxyfen in a vegetable aphid IPM program was discussed.     

Altruistic defenders in a gall-forming aphid of the tribe Hormaphidini (Homoptera,Aphididae, Hormaphidinae) on its primary host

Summary. We found defensive behavior in the aphid Hamamelistes miyabei on its primary host plant, Hamamelis japonica, where it forms a spiny gall. Introduction of moth caterpillars into the galls elicited attacking behavior of aphid nymphs with their stylet. Although older nymphs sometimes attacked, first-instar nymphs were the main defenders. Immature and mature galls contained a large proportion of first-instar nymphs. Open galls still contained first-instar nymphs, but the proportion was remarkably smaller. In immature and mature galls, particularly, the molting rate of first-instar nymphs was significantly lower than that of older instars. These data suggest that the defensive strategy of H. miyabei is such that 1) molting of first-instar nymphs is suppressed, 2) the duration of the first instar is prolonged, 3) the proportion of defender nymphs in the gall is elevated, and 4) consequently the colony in the gall is effectively defended against predators. No morphological differences were found either between attacking and non-attacking first-instar nymphs or between molting and non-molting first-instar nymphs. Some first-instar nymphs in open galls had the next instar cuticle developing inside the body. These data suggest that first-instar nymphs of H. miyabei are monomorphic defenders, and that at least some of them are able to develop and reproduce. In addition to the attacking behavior, first-instar nymphs of H. miyabei performed characteristic behaviors such as gall cleaning and hindleg waving. This is the first time that altruistic defenders are described in the primary host generation of an aphid from the tribe Hormaphidini.     

Xylem feeding by periodical cicada nymphs on tree roots

Abstract. 1. Histological sections of tree roots on which periodical cicada nymphs of both the 17-year and the 13-year race arid various instars had fed showed that salivary sheaths made by the nymphs ended in xylem vessels.
2. Because no salivary sheaths were found in phloem cells, this observation indicates that cicada nymphs are xylem feeders throughout their developmental period.
3. The habit of feeding on xylem fluid, which is extremely dilute, may explain why periodical cicada nymphs require so many years (13 or 17) to mature. It may also explain why they excrete amino acids rather than sugars, as phloem feeders do.     

Differential cold hardiness in adults and nymphs of the peach-potato aphid Myzus persicae

The LT₅₀ (lethal temperature) of first instar and adult stages of the peach-potato aphid Myzus persicae was lowered following long term acclimation at low temperatures.
First instars consistently showed greater cold hardiness than adult stages at each acclimation temperature, with the differential increasing as the temperature was lowered. When maintained at 5°C (the lowest acclimation regime) nymphs and adults had dLT₅₀8.3°C and 4.7°C respectively lower than those for non-acclimated individuals.
When 10°C acclimated adults were returned to 20°C, the acclimation effect was retained in full for 6 days but complete deacclimation occurred by day 10. In contrast the LT₅₀ of their progeny increased gradually from the first day of adult deacclimation towards the level of the unacclimated control over a period of 10 days.
A change in cold hardiness was observed in first instars according to their position in the birth sequence. The LT₅₀ of first-born nymphs (day 1 of reproduction) from 20°C parents was - 15.9°C rising to - 8.3°C by day 4 and remaining at this level until the end of the reproductive period.
The differential mortality between nymphs and adults observed in the laboratory was supported by the results of a field experiment. Adult aphids kept in clip-cages on a crop of oilseed rape showed greater mortality compared with those introduced as nymphs when the minimum temperature fell below -4°C for the first time in winter. At - 10°C mortality of aphids introduced as adults approached 100% whereas more than 50% of those introduced as nymphs were still alive at this temperature.     

Separation of three Rubus-feeding species of aphid — Sitobion fragariae (Wlk.), Macrosiphum funestum (Macch.) and Amphorophora rubi (Kalt.) (Hemiptera: Aphididae) — by electrophoresis

Four species of aphid infest wild and cultivated blackberry (Rubus fruticosus agg., R. lachiatus, etc) and other Rubus species in Britain and Continental Europe, - Sitobion fragariae (Walker), Macrosiphum funestum (Macchiati), Amphorophora rubi (Kaltenbach) and Aphis ruborurn (Bösrner). The nymphs, especially the early instars, of the first three species are fairly difficult to differentiate morphologically. However, they can clearly be separated using electrophoresis. The present paper describes diagnostic enzyme/isoenzyme banding patterns which allow differentiation of the first three species as apterous and alate adults and their instars using two enzymes - carboxylesterase (EST) and phosphatase (PHOS).     

Heterogeneous selective pressures on egg-hatching time and the maintenance of its genetic variance in a Tetraneura gall-forming aphid

1. The performance of gall-forming aphids is largely dependent on the timing of egg hatch relative to host budburst. This study examined the mode of natural selection acting on egg-hatching time and the extent of its genetic variance in a Tetraneura aphid.
2. The budburst time of the primary host of the aphid varied greatly among individual trees. Egg hatch on a host tree was often asynchronous with host budburst.
3. Transplant experiments indicated that egg-hatching time was subject to heterogeneous selective pressures in heterogeneous host environments.
4. Hatching time was compared between half-sib families. Small nymphs in a half-sib family tended to hatch later, and this resulted in large within-family variance in hatching time.
5. Small nymphs that hatched late were likely to be selected out during the galling process. Thus, these nymphs may be produced not as bet-hedging but due to maternal effects. When such maladapted nymphs were not included in analysis, a significant amount of additive genetic variance was detected in hatching time.
6. Heterogeneous selection, coupled with density-dependent regulation of population on respective host trees, probably maintains additive genetic variance in this trait.     

Enemy-free space and the feeding niche ofan aphid

1. The nymphs of the aphid Monaphis antennata occupy an unusual feeding niche, being restricted to the upper surfaces of leaves and petioles. The possibility that this is a predator-avoidance strategy was investigated.
2. Nymphs could be induced to feed on the under surfaces of petioles and the mortality of these nymphs was then compared with the mortality of nymphs feeding from the upper surfaces when exposed to coccinellid predators.
3. Coccinellid larvae spent less time foraging on the upper surfaces of leaves and petioles than on the under surfaces of leaves and petioles.
4. The nymphs occupying the upper surfaces of petioles, the normal feeding position, were encountered by the coccinellids later and less often, and fewer were attacked compared with those occupying the under surfaces.
5. It is concluded that the feeding niche of the nymphs of this aphid is adaptive in that it reduces exposure to foraging predators and is the result of selection to occupy enemy-free space.     

Aggregation facilitates larval growth in the neotropical nymphalid butterfly Chlosyne janais

1. Larvae of Chlosyne janais (Lepidoptera: Nymphalidae) feed gregariously as early instars on the shrub Odontonema callistachyum (Acanthaceae). During the fourth instar, aggregations break up and larvae feed as solitary individuals.
2. The hypothesis that aggregation increases growth rate was tested by raising larvae on intact plants in the field in different group sizes and measuring their daily growth.
3. There was a striking effect of group size on larval growth whereby larvae more than doubled their weight gain by feeding in large rather than small aggregations on intact plants in the field.
4. This group-feeding advantage was lost altogether if larvae were raised on excised leaves in the laboratory, suggesting that large aggregations may facilitate growth either by inducing a nutrient sink or by overwhelming an induced allelochemical response in the plant.
5. Although larval survival was higher in cages that excluded enemies than in exposed aggregations, there was no influence of group size (experimentally manipulated) on short-term survival in the field. However, there was a weak positive relationship between short-term survival and the size of naturally occurring larval aggregations in the field. These data provide mixed support for the notion that gregarious feeding promotes defence against natural enemies.
6. Although the group defence hypothesis warrants further investigation, feeding facilitation is clearly an important factor contributing to the aggregation behaviour of C. janais larvae.     

The numbers and distribution of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.)

Abstract. 1. Subterranean aphids in old pasture were found to show extremely clumped distributions with about 3000 aphids (omitting first instars) per ant nest throughout the year.
2. They were generally distributed in and away from the nest mounds, but within the ant's foraging territories.
3. At summer temperatures, more than 3000 first instars are lost from the aphid population per ant nest per day and it is concluded that these are eaten by the ants in addition to some older aphids and the honeydew produced.
4. The aphids may therefore provide enough food to maintain the ants with very little extra needed in the form of other prey.     

Functional response of the ladybird, Cydonia vicina nilotica to cowpea aphid, Aphis craccivora in the laboratory

The functional response of Cydonia vicina nilotica Muls. （Coleoptera： Coccinellidae） to six densities of Aphis craccivora Koch （Homoptera： Aphididae） nymphs on broad bean （Viciafaba Linn.） was investigated in the laboratory. A linear relationship between the rate of consumption and prey density was observed with r^2 values between 0.58 and 0.97. Plotting prey density against prey killed by four larval instars, and adult males and females of C. vicina nilotica fit well with the type Ⅱ model of Holling＇ s disc equation. Adult females consumed the highest number of prey, followed by fourth instars and adult males. Based on the functional response data, the model predicts a maximum of 144.9, 116.3, 86.2, 80.0, 72.5 and 20.0 nymphs to be consumed per day by an individual adult female, fourth instar, adult male, third, second and first instars, respectively. The differences in the responses of the predator to aphid densities are discussed.     

Foraging by the carabid Agonum dorsale in the field

Abstract. 1. Small arenas in the field were used for observing adult Agonum dorsale (Pont.) foraging in a wheat crop.
2. The carabid showed no significant change in behaviour between low and high aphid density arenas.
3. Individuals foraged nocturnally and spent most of their time on the ground searching for prey. They climbed infrequently and then not high enough to reach aphid aggregations on the ears and flag leaves of wheat.
4. Gut dissection showed that more individuals had eaten aphids in the high aphid density arena than the low. Recording of aphid distribution within the arenas showed that this increase in aphid consumption could be explained by A.dorsale capturing aphids on the ground. Prey availability per unit area was in fact higher on the ground than on the wheat.
5. The contribution of ground-zone predators such as A.dorsale to the control of cereal aphids will be determined by the frequency with which aphids arrive on the ground and the proportion of these which reclimb the wheat and reproduce in the absence of predation.     

The role of cereal growth stages and crowding in the induction of alatae in Sitobion avenae and its consequences for population growth

Abstract. 1. Alatiform nymphs of Sitobion avenae were first recorded on wheat in 1977 and 1978 when there were 0.6 aphids per tiller and reached a maximum proportion of 0.9 of the population despite a seventeen-fold difference in aphid density between years.
2. At the same aphid density per tiller there was a higher proportion of alatiform nymphs on the tillers at an advanced than at an earlier stage of plant growth.
3. Both pre- and post-natal crowding, and late stages of plant growth, were important in inducing the development of alatae in the laboratory.
4. Changes in the quality of the host plant through its previously reported effect on reproductive and survival rates, and its effect on alate induction and emigration was important in shaping the population dynamics of S.avenae on cereals.     

Efficacy and nontarget effects of reduced-risk insecticides on Aphis glycines (Hemiptera: Aphididae) and its biological control agent Harmonia axyridis (Coleoptera: Coccinellidae)

The efficacy of three reduced-risk insecticides (pyrethrins, insecticidal soap, and narrow-range mineral oil) was determined for nymphs and adults of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), an exotic pest of North American soybean, Glycine max (L.) Merr. These insecticides also were evaluated for nontarget effects on one of the aphid's key biological control agents, multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), including first and third instars, pupae, and adults. A Potter Spray Tower was used to conduct direct spray laboratory bioassays. Results indicated that although pyrethrins and narrow-range mineral oil caused 100% mortality to A. glycines nymphs and adults at 72 h posttreatment, insecticidal soap caused equivalent mortality to only the nymphs during the same time period. However, A. glycines adult mortality due to the insecticidal soap (83.3%) was significantly greater than the control. Pyrethrins were highly toxic to first instars of H. axyridis (98% mortality), but they had no effect on third instars, pupae, or adults. Mineral oil and insecticidal soap were moderately lethal to first (48.9 and 40% mortality, respectively) and third (31.9 and 38.8% mortality, respectively) instars of H. axyridis, but they had no effect on pupae and adults. Our results suggest that pyrethrins, insecticidal soap, and narrow-range mineral oil may prove useful for soybean aphid management in organic soybean due to efficacy against the aphid with differential nontarget effects on select stages of H. axyridis. Additional studies will be necessary to elucidate the efficacy of these insecticides under field conditions.     

Ecology of the parasites of a predatory bug, Blepharidopterus angulatus (Fall.)

Abstract. 1. On lime, Blepharidopterus angulatus is parasitized by a braconid, Peristenus sp., which is attacked by an ichneumonid hyperparasite, Mesochorus sp. The emergence and oviposition behaviour of the adult parasites and the growth of the larvae are described.
2. Parasitized B. angulatus are considerably heavier at maturity than normal, and nymphs parasitized by Peristenus consume, during their fifth instar, 2.1 times more in dry weight of prey (lime aphids). The growth efficiency of Peristenus is 30–37%.
3. An inverse relationship between percentage parasitism and host density on different trees may have been due to differences in synchronization.     

Life history characteristics of Orius insidiosus (Say) fed Aphis glycines Matsumura

The soybean aphid, Aphis glycines Matsumura, is a new invasive pest of soybeans throughout most of the soybean production areas of North America. Field studies have demonstrated that the indigenous predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid early the soybean crop season. Because soybean aphid is newly introduced into North America, the life history characteristics of predators fed this aphid are not known. In laboratory assays, we measured the survival, development, longevity and reproduction of O. insidiosus fed 1, 3, 6 or 12 seconds to third instars of soybean aphid. O. insidiosus nymphal development decreased from 34.0 to 21.4 days as the number of soybean aphid nymphs provided increased from 1 to 6 aphid nymphs daily. Stage-specific mortality was highest at 68% for first instar O. insidiosus nymphs fed 1 soybean aphid nymph per day. Adult longevity (43.9 days) and fecundity (49.7 eggs per female) was highest for O. insidiosus fed 6 soybean aphid nymphs daily, but longevity (23.5 days) and fecundity (10.1 eggs per female) declined for adults fed 1 soybean aphid nymph daily. The intrinsic rate of increase of O. insidiosus ranged from 0.048 to 0.133. Compared to other prey species, soybean aphid is an adequate prey item for O. insidiosus. Our results suggest that O. insidiosus will be most effective in suppressing soybean aphid population growth in the initial phase of the aphid’s colonization of soybeans.     

Effects of brief exposures to low temperature on the development, longevity and fecundity of the grain aphid Sitobion auenae (Hemiptera: Aphididae)

First instar nymphs and adults of the grain aphid Sirobion auenae that had been reared at 10°C and 20°C over a number of generations, were cooled to -5°C and -10°C for 1 h and 6 h and returned to 20°C to assess the effects of brief exposures to low temperatures (cold-pulses) on their survival. rate of development, longevity and fecundity. A strong acclimation response was observed in first instar nymphs, with significantly less mortality in groups reared to 10°C compared to 20°C. Mean development time from first instar to adult was not significantly affected by low temperature exposure at the first nymphal stage. Longevity in all groups cooled as first instars was reduced by the sub-zero cold-pulses, and was also dependent on temperature and exposure time. Acclimated aphids survived longer than non-acclimated individuals. Reproductive rate, in terms of the number of nymphs born per aphid per day, was unaffected by cold stress applied at the first instar stage. Total fecundity was however reduced, being a function of the number and longevity of the survivors. Adult aphids were less cold hardy than nymphs; mortality was higher at -10°C than -5°C increasing with duration of exposure from 1 h to 6 h. Mean fecundity was reduced significantly in aphids cooled at the adult stage, the number of aphids born per day decreasing as the exposure period of the cold-pulse increased, suggesting that low temperature had affected embryogenesis. All the nymphs born to adults surviving exposure to -5°C for 6 h died within 48 h of birth, indicating that low temperature has a pre-natal effect on mortality.     

Relationships between feeding of Philaenus spumarius (L.) and the amino acid concentration in the xylem sap

Summary. 1. P.spwnarius nymphs selected young, upper leaves of Xanthium strumarium plants, which have a relatively high amino acid concentration in the xylem sap.
2. Nymphs selected or rejected a host leaf as a feeding site after a test ingestion of plant sap.
3. Nymphs fed on detached leaves kept with their petioles in a solution of amino acids, in preference to leaves with petioles in a solution containing no amino acids.
4. Nymphs caged on leaves with relatively high amino acid concentrations in the xylem sap suffered a lower mortality after 7 days than nymphs caged on leaves with low amino acid concentrations in the xylem sap.
5. Mean excretory rate increased with the increase in the amino acid concentration in the xylem sap for third and fourth instar nymphs, and adults, but not in fifth instars.     

Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress

Abstract 1. Natural populations of pea aphids in California contain at least two facultative bacterial secondary symbionts (pea aphid secondary symbiont, PASS, or pea aphid rickettsia, PAR) in a range of frequencies throughout the state.
2. Two pea aphid clones without either of these facultative associates failed to reproduce in the first 8 days after the final moult if they had been heat-stressed for a period of about 4 h at 39 °C as 1-day-old larvae in the laboratory.
3. Aphids infected artificially with PASS, however, were able to produce up to 48% of the normal complement of offspring produced by PASS-positive aphids that had not been heat-stressed. Clones infected artificially with PAR did not have the same advantage as those with PASS after heat stress.
4. In aphids without PASS or PAR, heat stress reduced the number of bacteriocytes (in which the obligate primary symbiont, Buchnera , resides) to 7% of non-heat-stressed aphids, while aphids with only PASS retained 70% of their bacteriocytes. Bacteriocytes in aphids with PAR but not PASS were reduced to 42% of controls.
5. When larvae were heat-stressed as older instars (5 days old), a similar pattern emerged, though the effect of heat stress was less extreme. Clones containing PASS produced the most offspring, three to 14 times as many as aphids without PASS or PAR. Aphids with PAR only, or PASS and PAR together, had reduced or no advantage over aphids without facultative symbionts.
6. Aphids of all clones that had been heat-stressed as later instars gave birth to a variable number of stillborn offspring. Aphids without facultative symbionts produced the most stillborn larvae.
7. Field studies showed a higher incidence of PASS in aphids collected in California in summer compared with aphids from the same sites collected 2–4 months earlier. The difference was significant in two of three widely dispersed locations.