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.     

Defenders in the North American aphidPemphigus obesinymphae

Summary Gall-inhabiting individuals of the aphidPemphigus obesinymphae act as defenders, protecting other colony members against attack by dipteran and neuropteran larvae that are the primary predators of this species. As first instar nymphs, the progeny of the fundatrix patrol surfaces of galls and adjoining leaves. These first instar nymphs attack potential predators by mounting and grasping them and inserting their stylets. This defensive behavior, which is not exhibited by nymphs in later instars, appears to be effective in reducing predation. The fundatrix typically produces defenders throughout the extended gall-inhabiting phase, and her progeny delay development beyond the defensive first instar stage. By August, galls contain an average of 101 defenders. Early death of the fundatrix reduces the number of defenders in the gall and advances maturation of defenders into winged migrants, which otherwise mature in September and October. InPemphigus, defensive behavior by first instar nymphs appears to have evolved in the context of several types of derived life cycle, each involving an extended gall-inhabiting phase.     

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.     

Seasonal extension of the soldier instar as a route to increased defence investment in the social aphid Pemphigus spyrothecae

Abstract.  1. The possibility that the duration of the soldier instar could be extended over the course of the galling season was examined in Pemphigus spyrothecae Passerini (Hemiptera: Aphididae). In this species, the individuals of one morph of the dimorphic first instar are non-sterile specialised defenders known as soldiers.
2. In the face of a declining birth rate, the proportion of first-instar soldiers to first-instar non-soldiers was found to increase. This provides strong evidence of extension of the soldier instar over time.
3. Instar extension provides a mechanism for post-natal investment in soldiers and allows individuals with insufficient time to mature to remain in the defensive stage so that they may continue to make an indirect contribution to their clone's reproductive success.     

Maternal death relaxes developmental inhibition in nymphal aphid defenders

In certain aphids, first-instar nymphs defend their gall by attacking intruding arthropod predators. One correlate of such defensive behaviour is a lengthened duration of the first nymphal stadium during the galling phase of the life cycle. A prolonged first stadium allows a large army of first-instar defenders to accumulate, which may be advantageous for gall defence. The factors determining developmental delay have been unclear, however. Our field experiment with Pemphigus obesinymphae, a North American gall-forming aphid with defensive first-instar nymphs, tests whether first-stadium duration is influenced by the death of the colony''s fundatrix (mother). We killed fundatrices in certain galls, left those in control galls alive, and counted aphids in each stadium in each gall. Galls in which fundatrices were killed contained a lower proportion of first-instar defenders and more late-instar nymphs than did galls with living fundatrices, indicating that maternal death dramatically increased developmental rate of nymphs. Possibly nymphal aphids respond adaptively to environmental cues that signal a threat to the colony''s welfare. Alternatively, the fundatrix actively suppresses offspring development in order to maintain a large army of soldiers to protect her gall. The results add a new layer of complexity to our understanding of social aphid systems.     

The ontogeny of soldiers in Prorhinotermes simplex (Isoptera, Rhinotermitidae)

The ontogeny of the soldier caste in Prorhinotermes simplex is studied with emphasis on the instar origin of soldiers, the duration of the presoldier stage, and changes in external anatomy during the soldier morphogenesis. The soldiers of different instar origin are compared morphometrically and by analysis of the soldier defensive secretion. The soldiers were found to develop from larvae of the second up to the eighth instar, via a short (13–17 days) presoldier stage. The early soldier instars were found exclusively in incipient colonies while the mature colony contains late instar soldiers only. The abrupt change in the external anatomy occurs in two steps. During the larva-presoldier moult, the head increases in length but only slightly in width. During the presoldier-soldier moult, both the length and width of the head increase markedly and the typical cordate shape is attained; the relative size of the pronotum increases considerably. The long falcate mandibles develop mainly during the larva-presoldier moult. One antennal segment is added during these two moults. With increasing instar age of soldiers a relative increase of the pronotum and the head size in its posterior region was observed. No functional differences in external anatomy were found among the six soldier instars. The composition of the frontal gland secretion is similar in the six soldier instars, an extraordinarily high amount of a defensive substance, (E)-1-nitropentadecene, was detected together with (Z,E)-α-farnesene, presumably an alarm substance. The strategy of soldier production is discussed. We conclude that the observed patterns of soldier production in P. simplex correspond well to its ecological strategy of an advanced single-site nester able to migrate and form foraging groups. Received 16 August 2005; revised 21 November and 6 February 2006; accepted 16 February 2006.     

Temporal polyethism in incipient colonies of the primitive termiteZootermopsis angusticollis: A single multiage caste

Division of labor was studied in incipient colonies of the dampwood termite Zootermopsis angusticollisby recording repertoire size, behavior frequencies, and time budgets of larvae. Behavioral repertoire size increased with age: first- and secondinstar larvae were mainly inactive, whereas larvae of the third through seventh instars performed 64–100% of all tasks. The increase in repertoire size from the second to the third instar was abrupt; repertoire size and composition remained more or less constant for older instars. No correlation between age (instars III–VII) and tasks was identified, suggesting that colony labor is performed by a single functional caste that spans the third to the seventh instar without any age-based division of labor. Small colony size, low oviposition rate, simple nest architecture, a lack of spatial association of tasks, and the potential for attaining reproductive status appear to be associated with the lack of age-related behavioral specialization in Z. angusticollis.In effect, the absence of temporal polyethism in this species is likely a consequence of its nesting habits and physiological and developmental constraints.     

Analysis of the aggregation behavior in the larvae ofHarmonia axyridis Pallas (Coleoptera: Coccinellidae) to prey colony

Summary The searching and handling behaviors ofHarmonia axyridis larvae to the colony ofRhopalosiphum padi were experimentally examined and the processes of their aggregation to the prey colony was analyzed. All the instar larvae searched for the prey at random and they have no preference to the prey colony, but except the 1st instar they tend to aggregate to the plants with prey colonies. The 1st instar larvae tend to stay on the plants they once located. The 2nd to 4th instar larvae often emigrate from the plants without prey colony but seldom emigrate from the plants with prey colonies, and consequently, they aggregate to the plants with prey colonies. The expense of time to eat prey (in the 2nd and 3rd instars) and the change of searching behavior for the prey after feeding (in the 3rd and 4th instars) are responsible for the larval concentration to prey colony as a trapping effect for predators to prey colony.     

Effect of food and larval density on survival and growth of early instar greyback canegrub, Dermolepida albohirtum (Waterhouse) (Coleoptera: Scarabaeidae)

Abstract First- and early second-instar larvae of Dermolepida albohirtum (Coleoptera: Scarabaeidae) survived best and gained most weight on living roots of lawn seedlings, sugarcane or Guinea grass ( Panicum maximum var. maximum ) when compared with decaying plant material or soil alone. Survival of first-instar D. albohirtum was not density-dependent, but survival of older larvae (late first-instar and early second-instar) was reduced at high larval density. There was no evidence for larval combat between first instars. First instars kept at high density gained less weight and were slower to develop into second instars compared with first instars kept at low density. When food was limited, survival at high larval densities was reduced. Survival of early instars was high in sugarcane fields, probably reflecting the availability of suitable food. We conclude that food type and supply are critical factors affecting the survival and development of early instar D. albohirtum .     

Cues of Predation Risk Induce Instar‐ and Genotype‐Specific Changes in Pea Aphid Colony Spatial Structure

Deploying collective antipredator behaviors during periods of increased predation risk is a major determinant of individual fitness for most animal groups. Pea aphids, Acyrthosiphon pisum, which live in aggregations of genetically identical individuals produced via asexual reproduction warn nearby conspecifics of pending attack by secreting a volatile alarm pheromone. This alarm pheromone allows clone‐mates to evade predation by walking away or dropping off the host plant. Here, we test how a single alarm pheromone emission influences colony structure and defensive behavior in this species. Relative to control colonies, groups exposed to alarm pheromone exhibited pronounced escape behavior where many individuals relocated to adjacent leaves on the host plant. Alarm pheromone reception, however, also had subtle instar‐specific effects: The proportion of 1st instars feeding nearest the leaf petiole decreased as these individuals moved to adjacent leaves, while the proportion of 2nd–3rd instars feeding nearest the leaf petiole remained constant. Fourth instars also dispersed to neighboring leaves after pheromone exposure. Lastly, alarm pheromone reception caused maternal aphids to alter their preferred feeding sites in a genotype‐specific manner: Maternal aphids of the green genotype fed further from the petiole, while maternal aphids of the pink genotype fed closer to the petiole. Together, our results suggest that aphid colony responses to alarm pheromone constitute a diversity of nuanced instar‐ and genotype‐specific effects. These behavioral responses can dramatically change the spatial organization of colonies and their collective defensive behavior.     

Morphometry and biological parameters of different instars of the giant brown peach aphid: Pterochloroides persicae Cholodkovsky 1899 (Hemiptera: Aphididae) in Tunisia

Summary. Individuals of Pterochloroides persicae reared under controlled conditions were used to describe the morphometry and biological parameters of instars of this aphid. Our results showed that P. persicae developed four instars before reaching the adult stage. The first and the second larval instars both have five antennal segments, although the others have six segments. A significant difference was observed between instars in the first antennal segment (F = 56.11; df = 4, P = 0.026), in the body length (F = 115.38; df = 4, p = 0.014) and in the cauda length (F = 72, 77; df = 4, p = 0.021). The study of developmental and reproductive performance of P. persicae showed that the first instar lasted for 3.17 days, the second instar 2.35 days, the third instar 4.68 days, the fourth instar 5.035 days and the adult 6.86 days. We demonstrate also that the generation time lasted for 15.26 days. The life span was 22.11 days. As for fecundity, a single female of P. persicae gave birth to 29.68 ± 7.38 nymphs with an average reproductive rate per day of 4.32 ± 2.16.     

The economics of brood raiding and nest consolidation during ant colony founding

Summary The most dangerous time for an ant colony is during the founding stage when the small colony is vulnerable to predation and competition. Colonies can grow more rapidly when multiple queens cooperate in raising the first worker brood (pleometrosis) or by raiding other incipient colonies for their brood. This brood raiding has been proposed to be the primary force selecting for pleometrosis, i.e. multiple-queen colonies may have a considerable advantage in destroying neighbours by aggressively stealing their brood. An alternative hypothesis is that incipient nests are part of a larger, interconnected population structure and that brood raiding reflects cooperative pleometrosis with subdivided colonies. A simple mathematical model supports the second hypothesis: workers of incipient colonies are especially favoured to peaceably abandon their nest and join with other colonies if the queens are related or queens from raided colonies can infiltrate the raiding colony. The latter condition is often met in ant species that brood raid and particularly exemplified in fire ants (Solenopsis invicta), where brood raiding involves little mortal combat and combines with pleometrosis to rapidly increase colony size. It is proposed that the term nest consolidation should replace brood raiding to more accurately reflect the relatively non-aggressive and potentially apparently cooperative nature of interactions between incipient ant colonies.     

The parasitoidCotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its hostPieris brassicae,on the basis of contact cues from frass,silk, and herbivore-damaged leaf tissue

Adult females of the larval parasitoidCotesia glomerata (L.) respond to chemical cues associated with feeding damage inflicted on cabbage plants by its host,Pieris brassicae (L.). The use of these infochemicals by the parasitoid during selection of the most suitable host instar was investigated. The parasitoid can successfully parasitize first-instar host larvae, while contacts with fifth-instar larvae are very risky since these caterpillars react to parasitization attempts by biting, spitting, and hitting, resulting in a high probability of the parasitoid being seriously injured or killed. Observations of the locomotor behavior of individual wasps on leaves with feeding damage inflicted by the first and the fifth larval instars and on host silk and frass showed that several cues affect the duration of searching by the parasitoids after reaching a leaf: cues on the margin of the feeding damage and cues in the host frass and silk. Whole frass, silk, and hexane extracts of frass obtained from first-instar elicited parasitoid's searching behavior significantly longer than frass, silk, and hexane extract of frass from the fifth instar. The results demonstrate thatC. glomerata can discriminate between first instars, which are more suitable hosts, and fifth instars ofP. brassicae without contacting the caterpillars, by exploiting instar-related cues.     

Defensive Behavior in Primary- and Secondary-Host Generations of the Soldier-Producing Aphid, Pemphigus bursarius (Hemiptera: Aphididae)

The genus Pemphigus comprises several species that produce soldiers (defensive morphs) in galls on the primary host. At the moment, it is unclear if host-alternating species also produce defenders on their secondary host. We therefore examined how P. bursarius morphs of the secondary host generations respond to predators to test whether they show defensive behavior. We further examined how this response compares with the antipredator behavior of soldiers in P. bursarius and P. spyrothecae occurring on the primary host. We performed two manipulative experiments using two predatory species to quantify the behavior of the different morphs in response to predators. In both experiments, secondary host morphs of P. bursarius showed no attacking behavior and antipredator behavior in these morphs was limited to escaping natural enemies by walking away. In contrast, the first instars of the primary host generations in both Pemphigus species showed attacking behavior and were capable of killing the predators.     

Energetics and development of incipient colonies of the harvester termite, <Emphasis Type="Italic">Trinervitermes trinervoides</Emphasis> (Sjöstedt) (Termitidae,Nasutitermitinae)

Energy dynamics within incipient colonies of the southern African mound dwelling harvester termite Trinervitermes trinervoides (Sj?stedt) (Termitidae: Nasutitermitinae) were investigated. Development of incipient colonies established from field collected alates and changes in energy content of reproductives and brood were studied over a 25 week period in the laboratory. Colonies were then transferred into the field to study the established of the first mound. An initial four-week egg-laying cycle started within a week of pairing. Hatching occurred six weeks later. Two lines emerged from first instar undifferentiated larvae. Small larvae moulted first into minor presoldiers and then minor soldiers. Large larvae developed into major workers. Foraging began once second instar major workers had differentiated 20 weeks after colony foundation. First instar major workers did not forage but there is evidence of pre-foraging utilisation of soil humus. The epigeous mound was produced after three years. The energy available to maintain incipient termite colonies until the first workers start foraging is crucial to their survival. The royal pair of T. trinervoides does not feed during the rearing of the first brood, the fate of which depends largely on the reproductives accumulated energy reserves. The males and females expended 84.54 and 83.07% respectively of their total energy during this period. Once foraging started, the energy content of the royal pair increased and a second egg-laying cycle began. Received 25 July 2007; revised 19 March and 22 May 2008; accepted 4 September 2008.     

Colony‐age‐dependent variation in cuticular hydrocarbon profiles in subterranean termite colonies

Cuticular hydrocarbons (CHCs) have, in insects, important physiological and ecological functions, such as protection against desiccation and as semiochemicals in social taxa, including termites. CHCs are, in termites, known to vary qualitatively and/or quantitatively among species, populations, castes, or seasons. Changes to hydrocarbon profile composition have been linked to varying degrees of aggression between termite colonies, although the variability of results among studies suggests that additional factors might have been involved. One source of such variability may be colony age, as termite colony demographics significantly change over time, with different caste and instar compositions throughout the life of the colony. We here hypothesize that the intracolonial chemical profile heterogeneity would be high in incipient termite colonies but would homogenize over time as a colony ages and accumulates older workers in improved homeostatic conditions. We studied caste‐specific patterns of CHC profiles in Coptotermes gestroi colonies of four different age classes (6, 18, 30, and 42 months). The CHC profiles were variable among castes in the youngest colonies, but progressively converged toward a colony‐wide homogenized chemical profile. Young colonies had a less‐defined CHC identity, which implies a potentially high acceptance threshold for non‐nestmates conspecifics in young colonies. Our results also suggest that there was no selective pressure for an early‐defined colony CHC profile to evolve in termites, potentially allowing an incipient colony to merge nonagonistically with another conspecific incipient colony, with both colonies indirectly and passively avoiding mutual destruction as a result.     

Secondary host generation of the gall aphid Cerataphis jamuritsu (Homoptera)

Colonies of a Cerataphis species with well‐developed horns were found on the rattan Calamus quinquesstinervis in southern Taiwan. The morphology of first instar nymphs from the colonies accorded well with the morphology of first instar nymphs laid by alates of Cerataphis jamuritsu from galls on Styrax suberifolia, indicating that the rattan aphids are the secondary host generation of C. jamuritsu. Although the aphid colonies were attended by ants, the sharp horns of the first instar nymphs suggest that they might attack predators.     

Spatiotemporal fluctuations in natural selection acting on the gall‐parasitic aphid Tetraneura sorini

The measurement of the selection gradient is crucial for understanding the magnitude of selection acting directly on a trait and predicting the evolutionary trajectory of that trait. This study evaluated the selection gradient acting on the morphology of the gall‐parasitic aphid Tetraneura sorini during the galling process and compared the strength among populations. Gall formers (first instars) frequently fight with conspecifics or heterospecifics for usurping incipient galls using their well‐developed hind legs. First instars that successfully acquired galls were found within galls, whereas those that failed were found dead on leaf surfaces. Selection gradients were estimated using logistic stepwise regression and partial least square (PLS) regression. Calculated selection differentials indicated that first instars that secured galls were larger in body size than failed individuals through all populations. However, selection gradients on weapon traits varied largely among populations or among years in the same population. We confirmed microevolutionary changes in the relationship between traits, which accorded with the expectation from changes in the selection gradients. When gall formers were transferred onto developing buds individually, individuals that successfully induced galls had smaller body size than failed individuals. Available evidence suggests that the selection gradient on body size becomes higher with an increasing proportion of T. sorini in the Tetraneura species community. Thus, we concluded that more intense fighting with conspecifics leads to stronger selective pressure on body size, but that selective pressure for each trait is variable depending on differences in the tactics and species composition among populations.