Ecological factors promoting the evolution of colony defense in aphids: computer simulations

Summary Colony defense has been reported in a limited number of species of aphids. This paper examines which life-historical traits have promoted the evolution of colony defense using two kinds of deterministic simulation models. These models postulate that first-instar larvae can counterattack predators and that the duration of this instar stage is a variable, subject to selection. Prolonging the first-instar span increases the proportion of defenders in the colony, while it results in a delay in reproduction. By calculating the optimal first-instar span, the optimal defensive effort of a colony under various ecological conditions could be estimated. Simulations based on the general model, which regards the number of adults maturing in a period as performance, predicted that a lower birthrate leads to a longer first-instar span (larger investment in defense). This condition also allowed the evolution of dimorphism in the first-instar span, which may ultimately result in the appearance of soldiers. Where birthrate declines with time, the first-instar span was predicted to be prolonged in later stages. Colony duration had little influence on the optimal first-instar span if the season is long enough to repeat generations. The galling-aphid model that assumes a fixed number of generations predicted that a longer duration of colonies leads to a longer first-instar span, but that birthrate has little influence on the optimal first-instar span. A tendency in defense reported in pemphigid aphids was consistent with the prediction from the galling-aphid model.     

Shift in life-history strategy from reproduction to defense with colony age in the galling aphidHemipodaphis persimilis producing defensive first-instar larvae

Colony defense in some aphids is performed by sterile soldiers but in others by monomorphic larvae of a specific instar stage. This paper, focusing on a galling aphid Hemipodaphis persimilis with monomorphic defensive first instars, examined the mechanism by which the proportion of defenders is regulated in the colonies. Demographic analyses showed that the ratios of first instars (defenders) were kept constantly high (58% on average) from mid June to late September. High proportions of first instars could be explained by consistently high birth rates (birth rate hypothesis) or by a prolonged duration of the first instar stage (instar span hypothesis). With the progress of colony age, the mature-embryo content of apterous adults, used as an index of the birth rate, decreased and the proportions of advanced instars increased. These results did not support the birth rate hypothesis. By contrast, calculation of a newly proposed index, the molting rate, showed that the duration of the first-instar stage was short in incipient galls but became longer with colony age. The duration of other instar stages was always kept short. These results corroborate the instar span hypothesis and suggest that the prolongation of the first-instar stage is an adaptive mechanism by which the defender ratio is kept high in mature colonies where the birth rate is declining. The frequency of aggressive behavior in first instars increased from incipient to mature galls. Seasonal changes in the instar span and aggressiveness of first instars suggest that in H. persimilis colonies there is a strategic shift from the reproductive to defensive phase with colony age.     

Buying time for colony mates: the anti-predatory function of soldiers in the eusocial aphid Ceratovacuna japonica (Homoptera, Hormaphidinae)

Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species’ natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator’s body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers’ colony mates time to reproduce or to escape from the predator.     

Avoidance of occupied hosts by the Hessian fly: oviposition behaviour and consequences for larval survival

Abstract 1. Unoccupied wheat plants and wheat plants occupied by conspecific eggs or larvae were presented to ovipositing female Hessian flies in choice tests.
2. The presence of conspecific eggs on the leaf surfaces of wheat plants did not appear to have any effect on the responses of ovipositing Hessian fly females.
3. The presence of conspecific larvae at the base and nodes of wheat plants for 1, 6, or 11 days had significant effects on Hessian fly oviposition. Eggs oviposited on plants were inversely proportional to larval densities and days of larval occupation.
4. Feeding by Hessian fly larvae is associated with several changes in wheat plants. One of these changes, the growth arrestment of the plant, was measured by recording the heights of plants used in oviposition tests. Plant heights were inversely proportional to both larval densities and days of occupation. Plant heights were directly proportional to eggs oviposited on plants.
5. The consequences of adult female avoidance of plants occupied by conspecific larvae were investigated by allowing females to oviposit on unoccupied plants and 1-day, 6-day, and 11-day larval occupied plants, then scoring at the end of the first larval instar the survival of the offspring that resulted from this oviposition.
6. Survival during the first larval instar was 88% for the offspring of females that oviposited on unoccupied plants, decreasing to 82, 31, and 4% on the 1-day, 6-day, and 11-day occupied plant treatments. On these four plant treatments, a positive correlation was found between larval performance (i.e. survival) and the preferences of ovipositing females.
7. On the four plant treatments, relationships between first-instar larval density and first-instar larval survival varied significantly. On unoccupied plants, survival was inversely proportional to density. On plants oviposited on at 6 days of larval occupation, survival was directly proportional to density.     

The effect of larval aggregation behaviour on larval growth of the spruce bark beetle Dendroctonus micans

1. The great spruce bark beetle Dendroctonus micans is a primary pest of spruce in Europe. It is unusual among Eurasian scolytids in that apparently healthy trees are attacked by solitary adults, but larvae feed en masse , in response to a larval aggregation pheromone.
2. The effect of brood size on larval growth was determined in experiments on detached bark, logs and living trees. A positive relationship was found between brood size and larval growth in experiments started with either eggs or larvae up to fifth instar. The relationship appeared to be independent of the effects of both preformed and induced defences in bark.
3. No evidence was found to support the hypothesis that larvae feeding in groups spend a greater proportion of time feeding. Addition of resin to egg chambers in detached bark pieces resulted in high mortality of first-instar larvae. A possible role for larval aggregation in minimizing the effects of host defences is 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.     

Caste allometries in the soldier-producing aphidPseudoregma alexanderi (Hormaphididae: Aphidoidea)

Summary Colonies of the aphidPseudoregma alexanderi produce morphologically-specialized first-instar larvae, termed soldiers, that defend the colony from predators. The environmental cues and physiological mechanisms governing soldier production are currently unknown. Here we present a morphometric study of soldiers and normal first-instar larvae ofP. alexanderi. Several morphological features (fore-leg length and width, hind-leg length, and horn length) plotted against body length display relationship that are similar to a sigmoidal curve. We found further support for an earlier finding that soldiers fall into two size categories, majors and minors, although both types of soldiers appear to follow the same allometry. The patterns of allometry in the soldier-producing aphids are very different from those found in other social insects and do not easily fit into the traditional categorization of allometries. We present two simple alternative models of soldier development as a framework for guiding future studies of the mechanisms of soldier production.     

Termite soldier differentiation in incipient colonies is related to parental proctodeal trophallactic behavior

Termite soldiers represent a peculiar caste among social insects in terms of their specific defensive roles. Numbers of soldiers are relatively low in a mature colony, and it is impossible to identify the individuals that will differentiate into soldiers. If it were possible to specify these individuals prior to soldier differentiation, it would facilitate a better understanding of the regulatory mechanisms of soldier differentiation under natural condition. Here we analyzed soldier differentiation in incipient colonies of Zootermopsis nevadensis, in which only a single soldier develops via a presoldier stage, and is stable during early colony ontogeny. We observed that the oldest third instar differentiated into a presoldier within about eight days from its appearance. Caste differentiation, however, was not strictly determined on an individual basis. The oldest third instars never differentiated into presoldiers if primary reproductives were removed soon after their appearance. Behavioral observations of primary reproductives and their offspring prior to presoldier differentiation, showed that primary reproductives transferred proctodeal materials to the oldest third instar significantly more frequently than to other larva. A high juvenile hormone (JH) titer is required for the soldier differentiation, and we suggest that the JH itself or some nutrients/factors increasing larval JH titer may be transferred to the oldest third instar via a parental proctodeal fluid.     

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.     

Studies on feeding and trophallaxis in the subterranean termite Odontotermes formosanus using rubidium chloride

Differences in feeding and trophallaxis among castes of the fungus‐cultivating higher subterranean termite Odontotermes formosanus Shiraki (Isoptera: Termitidae) were determined using rubidium (Rb) as a tracer. In the feeding study, workers and third instars fed directly on Rb‐treated filter paper and acquired the highest levels of Rb content. Although fifth and sixth instars obtained the Rb content over the marked level, the feeding ability of the caste was very poor. However, soldiers did not feed on Rb‐treated filter paper. In the trophallaxis study, worker, soldier, and fifth‐ and sixth‐instar recipients paired with Rb‐fed worker donors had a significantly higher Rb content than those paired with control donors. Results indicate that soldiers are completely dependent on workers for nutrition. Workers and fifth and sixth instars may obtain nutritional material from foraging workers. When third‐instar recipients were paired with Rb‐fed worker donors, they did not have a significantly higher Rb content than when they were paired with control donors, suggesting that the frequency of worker/third instar trophallaxis was very low. Transfer efficiency from the four trophallactic combinations ranged from 1.2 (worker donors to third‐instar recipients) to 12.9% (worker donors to soldier recipients). Accordingly, nutritional material from foraging workers could be transferred to non‐foraging workers, soldiers, and fifth and sixth instars by trophallaxis; however, third instars rarely obtain nutritional material from foraging workers, because they are capable of feeding within the nest.     

Larval gregariousness and neonate establishment of the eucalypt-feeding beetle Chrysophtharta agricola (Coleoptera: Chrysomelidae: Paropsini)

The selective advantage offered to individuals living within groups may relate to natural enemy defence, but in leaf feeding insects may also relate to overcoming plant defences, especially with respect to feeding establishment. We conducted a series of experiments focusing on neonate larval survival, examining the effect of group size and leaf age on the survival of a eucalypt-feeding beetle, Chrysophtharta agricola , which formed groups of up to 43 larvae on the foliage of Eucalyptus nitens in the field. In the laboratory, in the absence of natural enemies, we found that initial density, leaf age and damage to the leaf margin significantly affected larval survival. Survival of solitary first-instar larvae on young foliage was around 80% whereas on older foliage it was around 11%. Prior damage to the leaf margin significantly increased survival on older leaves to around 61%. Initial larval density also affected survival, although mortality was always significantly higher on older leaves. On older leaves the larval group size above which mortality increased no further was over two-fold that on young leaves. Observations of group feeding behaviour at each instar showed that the majority of larvae (75.7%) were aligned facing away from the feeding site and that only around 7.5%, or just 1–2 larvae per group, fed at any one time. Feeding larvae chewed the leaf edge by straddling the leaf margin. Measurements of leaf margins showed that older leaves had significantly thicker leaf margins and 'thickness' ratios (leaf margin to leaf lamina proper). In the field, approximately 85% of all larvae occurred on the first two expanded leaf pairs, and larval mortality was highest between eclosion and establishment of the first instar. However, beetles apparently did not adjust clutch size according to leaf age.     

Asymmetric intraspecific competition among larvae of the damselfly Ischnura elegans (Zygoptera: Coenagrionidae)

Abstract. 1. A laboratory competition experiment is described in which the growth and development rates of larvae of the damselfly Ischnura elegans (Lind.) were measured over an entire instar.
2. Two larval instars which commonly occur together in the field were used in the experiment; they were maintained with a superabundance of prey and either larvae from the same or the larger/smaller instar.
3. Small larvae suffered increased development times and decreased size increases at the moult in the presence of large larvae but similar interference effects were not evident when these smaller larvae were in the presence of other small larvae.
4. Development time and size increases of large larvae were not significantly affected by the presence of small larvae.
5. Irrespective of the instar combinations investigated, interference effects were reduced when there were more perches available, although in only a few cases was this reduction significant.
6. The consequences of the asymmetric competition reported in the experiment for the study of lifetime reproductive success in damselflies are discussed. Late emerging adults may incur reduced reproductive success.     

Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae)

Abstract.  1. Polyembryonic wasps provide dramatic examples of intra-specific developmental conflict. In these parasitoids, each egg proliferates into a clonal lineage of genetically identical larvae. If more than one egg is laid in a host (superparasitism), individuals of different clones may compete for food resources.
2. In the polyembryonic encyrtid Copidosoma koehleri , one larva per clone can differentiate into a sterile soldier. It is shown that soldiers are always females, and that they attack intra-specific competitors.
3. Research hypotheses were that (a) clones that develop in superparasitised hosts suffer heavier mortality than clones that develop in singly parasitised hosts, and (b) female clones cause higher mortality to their competitors than male clones, hence larval survival is lower in superparasitised hosts that contain females than in male-only broods.
4. The potential frequency of superparasitism in C. koehleri was manipulated by varying parasitoid–host ratios and exposure durations.
5. As parasitoid densities and exposure durations increased, the frequency of superparasitism rose, brood sizes increased, but the number of hosts that completed development was reduced. The number of offspring per parasitoid female decreased with increasing parasitoid–host ratios. Offspring size and longevity were inversely correlated with brood size. As superparasitism rates increased, fewer all-male broods were produced. Male–female broods were female-biased, suggesting selective killing of males by female soldiers. All-female broods were significantly smaller than all-male broods at high parasitoid densities only, possibly reflecting aggression among soldiers of competing clones.
6. The results support the working hypotheses, and suggest that female larvae outcompete males in superparasitised hosts.     

Life history characteristics and behaviour of the bamboo aphid,Pseudoregma bambucicola (Hemiptera: Pemphigidae), having sterile soldiers

Summary Life history and behavioural characteristics of the bamboo aphid,Pseudoregma bambucicola (Takahashi), which has sterile soldiers, were studied in the laboratory. The stadium of normal (fertile) first instar larvae was two times longer than that of second instar larvae, and the stadium of soldier-type (sterile) first instar larvae was much longer (max. 116 days) than the stadium of normal first instar, suggesting that soldiers are able to take nutrition from bamboo. Stimulation of larvae with breath, vibration of bamboo shoots or disturbing the larvae with the tip of a fine brush induced significantly more defensive acts by soldiers than those by normal larvae — the latter usually fled. Soldiers did not attack non-kin conspecific intruders or even aphids of different species, suggesting that, in this species, kin-recognition ability is low.     

Effects of temperature elevation on the population dynamics of the upland heather psyllid Strophingia ericae (Curtis) (Homoptera: Psylloidea)

1 Cloches permeable to gas and water were used to simulate the effect of climate warming on upland populations of the heather psyllid Strophingia ericae at Moor House National Nature Reserve in the North Pennines, UK.
2 The cloches produced an average warming of about 1 °C in the heather canopy over a period of one year.
3 The density of S. ericae increased markedly in cloches within a few months of erection.
4 Species composition and numbers of potential predators were similar inside cloches and in control plots.
5 In the two year life-cycle of S. ericae , the warming effect advanced the phenology from the second to third instar in the first winter, but in the second winter, fifth instar nymphs did not moult prematurely to adult.
6 The density of S. ericae was higher on Calluna vulgaris at its boundary with Juncus squarrosus than in the pure C. vulgaris sward (in both cloched and control plots).     

Interference by the mantispid Mantispa uhleri with the development of the spider Lycosa rabida

Abstract. 1. The larvae of Mantispa uhleri Banks (Neuroptera: Mantispidae) board spiders to await the production of an egg sac containing their obligate developmental food. While aboard the spider, larvae maintain themselves by feeding on spider blood. This parasitic behaviour was investigated by allowing larvae to board sixth instar Lycosa rabida Walckenaer (Araneae: Lycosidae). Larval parasitism has a direct and indirect effect on the developmental physiology of the spider.
2. The direct effect, equal in both spider sexes, is an increase in development time and a decrease in adult size.
3. The indirect effect on development time and adult size is brought about by the loss of an instar in female spiders only. Parasitized females were mature at nine or ten instars; control females at ten or eleven. Male instar number was not affected; both control and parasitized males were mature at nine or ten instars.
4. The net result is that parasitized female spiders are even smaller than would be predicted from the direct effect alone, but actually mature faster than control females. In males there is only the direct effect. The adaptive significance of this sexually dimorphic response is discussed.     

Factors affecting the rate of attack by Cotesia rubecula (Hymenoptera: Braconidae)

Abstract. 1. The relationship between responses of the insect parasitoid Cotesia rubecula (Marshall) to kairomones produced by the feeding activities of its host, Pieris rapae (L.), and patterns of parasitism were investigated under field conditions.
2. Parasitoid adults aggregated in patches with the highest densities of host larvae but there was no commensurate increase in the rate of attack in these patches.
3. The rate of attack was not limited by the availability of eggs.
4. The rate of parasitoid attack was highest where feeding damage by the host was highest, irrespective of current host density.
5. The rate of parasitoid attack was further influenced by host age distribution. Late instar larvae were less susceptible to parasitism than were early instar larvae. The rate of attack on early instar larvae occupying the same plants as late instar larvae was reduced. This reduction in rate of attack was due to limitations on parasitoid search time imposed by the increased feeding damage associated with large host larvae and by the increased time the parasitoid required to recover from an attack on these large host larvae.     

On the pronymphal stage in the migratory locust (Locusta migratoria, Orthoptera, Acrididae)

The structure of the integument, somatic and visceral muscles, midgut, and Malpighian tubules were investigated at the late stages of the embryonic and early postembryonic development of the migratory locust, Locusta migratoria, to assess the organization of its pronymphal stage. In its morphogenetic features, the vermiform locust larva sometimes called the pronymph corresponds to the first nymphal instar covered with the second embryonic cuticle which has not been shed. Since the first-instar locust nymphs before and after the shedding of this embryonic cuticle differ significantly in many morphological characters, two consecutive phases of this nymphal instar can be distinguished: the first phase existing from the moment of development of the third embryonic cuticle to the shedding of the second one; the second phase existing from the shedding of the second embryonic cuticle to the formation of the cuticle of the second nymphal instar. Since the pronymphal stage should precede the nymph stage, it may be concluded that the pronymph of the locust is fully embryonized and covered with the second embryonic cuticle, which is also typical of other insects with hemimetabolous development (Konopová and Zrzavý, 2005). Therefore, it would be erroneous to refer to the vermiform first-instar nymph as the pronymph, because the two stages are separated by molting and formation of a new cuticle.     

Intraspecific variability in herbivore performance and host quality: a field study of Uroleucon caligatum (Homoptera: Aphididae) and its Solidago hosts (Asteraceae)

Abstract. 1. Performances of two clones of Uroleucon caligatum on eleven clones of Solidago were measured by caging aphids on plants in the field.
2. Several measures were obtained, including developmental time from birth to adulthood, size of first instar nymphs, adult weight, and total colony weight.
3. All measures of performance were strongly affected by plant clone.
4. Effect of aphid clone-plant clone interaction was significant only for first instar size.
5. In a subsequent screenhouse experiment, plant clones were subjected to uniform conditions and still exhibited large differences in host quality.