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.     

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.     

First incidence of inquilinism in gall-forming psyllids, with a description of the new inquiline species (Insecta, Hemiptera, Psylloidea, Psyllidae, Spondyliaspidinae)

The two largest lineages of holometabolous gall-forming insects, cynipid wasps and cecidomyiid flies, have given rise to numerous obligate inquilines, species which are unable to form galls themselves and survive by inhabiting galls formed by other species. In contrast, only a single obligate inquiline, an aphid, is known in the sternorrhynchous Hemiptera, the hemimetabolan lineage in which gall-forming is best developed. We describe the first known gall inquiline in psyllids (Sternorrhyncha, Psylloidea), Pachypsylla cohabitans Yang & Riemann sp. n. All other members of this genus produce closed galls on hackberries, Celtis spp. (Ulmaceae). Newly hatched nymphs of P. cohabitans feed next to nymphs of several species of leaf gall-makers, becoming incorporated into the gall as the stationary nymphs are gradually enveloped by leaf tissue. In the mature gall, the inquilines occupy separate, lateral cells surrounding a central cell containing a single gall-maker. Pachypsylla cohabitans is similar in morphology to leaf-gallers, but differs in nymphal and adult colour, allozyme frequency, especially in the malic enzyme, and in adult phenology. Laboratory-reared progeny of side-cell females, when caged alone, never form galls, while progeny of centre-cell individuals alone only form galls comprising single individuals. Multiple-cell galls are formed only when adults of side-cell and centre-cell individuals are caged together. Experimental removal of centre-cell nymphs in early stages of gall initiation leads to smaller galls or death of side-cell individuals. We conclude that the side-cell individual is an obligate inquiline that is incapable of forming a gall on its own but is derived from a leaf-galling ancestor. We speculate on selective forces that might favour this evolutionary transition.     

Host Feeding by an Herbivore Improves the Performance of Offspring

Herbivores have developed diverse strategies to manipulate host plants for their own benefits. The gall induction by the maize orange leafhopper Cicadulina bipunctata is different from that by other gall-inducing insects in that the galls are induced not on feeding sites but appear on distant, newly developing leaves. In addition, adult C. bipunctata are highly mobile and seldom feed on gall tissue that they have induced. These mean that the gall induction by C. bipunctata is unlikely to contribute to the fitness of the inducer itself. The objective of this study was to determine whether manipulation of the host plant by this leafhopper has a subsequent benefit to offspring. Adults feeding on maize seedlings caused a partial change in the glucose content and a remarkable change in the accumulation of free amino acids in the gall tissue. Increases in emergence and developmental rates were observed in nymphs feeding on gall tissue induced by prior adult feeding. Such improvements were not evident in nymphs feeding on a C. bipunctata-resistant variety, which rarely displays galls after C. bipunctata feeding, nor on maize seedlings previously foraged by another leafhopper, Psammotettix striatus. The results indicate that gall tissue induced by adult C. bipunctata contribute to better performance of its offspring through improvement of the nutritional components of host plants.     

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.     

Gall formation by a spittlebug, Aphelaenus nigripectus (Aphrophoridae: Auchenorrhyncha; Homoptera)

Few spittlebug species are gall formers, but the Homoptera as a whole contain many gall‐forming species in many families. Nymphs of a spittlebug, Aphelaenus nigripectus (Aphrophoridae, Auchenorrhyncha, Homoptera), were observed to induce leaf‐roll galls on cherry trees (Prunus speciosa, P. × yedoensis and P. pendula cv. pendula (Rosaceae)) in late April in Kyoto, Japan. Aphelaenus nigripectus nymphs aggregated on the ventral surface of the young leaves, fed on the ventral (abaxial) midvein, and excreted masses of froth in the rolled leaves. In a field experiment, it was discovered that feeding of A. nigripectus nymphs can induce rolling of the cherry leaves, and that the rolled leaves may provide protection from desiccation to A. nigripectus nymphs. This is the first record of gall‐forming habits in Japanese spittlebugs.     

Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid

1. The abundance and performance of the Eastern Spruce Gall Adelgid, Adelges abietis , was evaluated on young, open-grown trees of White Spruce, Picea glauca , whose growth rates had been increased through fertilization or decreased through root-pruning.
2. In general, gall densities were highest on control trees and on mid-crown branches. Reduced galling success on fertilized trees was largely due to higher overwintering mortality of first-generation nymphs. Foliar magnesium, total tannin and total phenol contents were positively, and nitrogen and total monoterpene contents negatively, related to gall density and/or galling success.
3. Although short shoots were more abundant, shoot length was parabolically related to gall density. There was a non-significant parabolic trend between shoot size and galling success and volume. The number and average size of A. abietis females emerging from galls were positively related to gall volume, and realized fecundity was positively correlated to female size. Consequently, fitness was approximately twice as high for nymphs colonizing intermediate-sized than small or large shoots.
4. These results do not support the plant vigour or plant stress hypotheses. The results do, however, agree with predictions of the modified plant stress hypothesis for sucking insects. It is speculated that Adelges abietis lacks the necessary resources for successful gall formation on small shoots and is unable to produce a stimulus large enough to induce gall formation on large shoots.     

Oviposition by introduced Ophelimus eucalypti (Hymenoptera: Eulophidae) and morphogenesis of female-induced galls on Eucalyptus saligna(Myrtaceae) in New Zealand

An Australian gall-inducing eulophid, Ophelimus eucalypti (Gahan) was first recorded on the foliage of Eucalyptus botryoides after it invaded New Zealand in 1987. It has spread throughout the eucalypt plantations in the North Island and in the northern parts of the South Island affecting several species of Eucalyptus in the section Transversaria (subgenus Symphyomyrtus). Because gall-inducing insects usually have extremely narrow host ranges, O. eucalypti that induces galls on E. saligna and E. botryoides is currently recognized as a biotype, O. eucalypti(Transversaria). Heavily galled leaves abscise from the plant. Repeated defoliation led to widespread die-back of susceptible eucalypt species in the 1990s. Female larvae of O. eucalypti induce circular, protruding galls on the leaves of E. botryoides and E. saligna, whereas the males induce pit galls on the same species. The biology of O. eucalypti females and the development of their galls are described. Adult female O. eucalypti antennate the leaf surface before inserting the ovipositor (otherwise concealed within the metasomal apex) into the young host leaf. The egg is inserted at approximately 45 degrees and discharged between differentiating palisade cells. Callus-type cells surround the egg chamber, but cytologically specialized nutritive cells appear once the egg hatches and the larva begins to feed. The gall also differentiates a multi-layered sclerenchymatous tissue around the nutritive tissue. After feeding for many months, the larva pupates and the active nutritive tissue degenerates. The adult wasp emerges after cutting an exit hole through to the outside of the gall. Abscission of heavily galled leaves results in widespread defoliation and loss of growth and vigour in susceptible trees in New Zealand.     

Soldier caste with morphological and reproductive division in the aphid tribe Nipponaphidini

Summary. We investigated demographic, morphological and histological aspects of Distylaphis foliorum, a gall-forming nipponaphidine aphid from Java, Indonesia, whose first instar nymphs had been reported to have enlarged forelegs and attack other insects. The gall inhabitants of D. foliorum consisted of two discrete populations; one developing normally and the other remaining at the first instar. Morphometric analysis identified two types of first instar nymphs; nymphs with relatively long forelegs and slender abdomen, and nymphs with relatively short forelegs and fat abdomen. The former nymphs were found from both young galls and mature galls, while the latter nymphs were from young galls only. Histological analysis strongly suggested a reproductive division in the first instar. In the former nymphs from mature galls, ovaries and mycetomes were degenerate and replaced by well-developed fat body cells. These results indicated that D. foliorum has a morphologically differentiated sterile soldier caste in the first instar. This study is the first report of a soldier caste with morphological and reproductive division in the aphid tribe Nipponaphidini, and suggests that highly specialized soldier castes have evolved at least four times in aphids.Received 25 June 2004; revised 24 September 2004; accepted 11 October 2004.     

Fortress repair in the social aphid species Pemphigus spyrothecae

Nest repair is a vital element in the cooperative brood care that is a distinctive feature of eusocial animals. We investigated the repair role of individuals of the social aphid Pemphigus spyrothecae by prematurely opening their gall by cutting a hole of the same size and position as a natural opening. This resulted in increased mortality from predation. No subsequent responsive shift towards increased investment in soldiers was detected. However, repair of the holes by compensatory regrowth from undamaged adjoining areas of the gall was observed in 97.5% of the experimental galls that were protected from predation. Subsequent experiments confirmed that the aphids were responsible for this repair, with soldiers likely to be the major agents. Active maintenance of the integrity of the gall represents another altruistic task for which soldiers are predominantly responsible and indicates that social complexity in the order Hemiptera is greater than previously assumed.     

Prey Preference of Aphidoletes Aphidimyza on Acyrthosiphon Pisum: Effect of Prey Color and Size

Color polymorphism in insects as well as factors contributing to its occurrence and maintenance have been of a great interest. Pea aphid (A. pisum) exhibits a noteworthy color polymorphism which occurs as red and green. The preference of the predatory gall midge Aphidoletes aphidimyza (Rondani) for the two color morphs of pea aphid at two life stages (adult and second instar) was investigated. Red adults, red nymphs, green adults, and green nymphs were offered to the larvae of the predator in different sets. The larvae attacked red aphids more than green ones of a same size. But whenever adults were offered along with nymphs, the nymphs experienced significantly more attacks. Although visual cues could result in more predation on red aphids, our findings showed that the size of aphids was the more important factor. The results showed that previous findings, suggesting more predation on the red morph, are valid when the same size of aphids is used. The ovipositing females exhibited no differences in oviposition choice between stalks infested with either of two colors.     

Plant-mediated competition facilitates a phoretic association between a gall mite and a psyllid vector

Phoretic associations between mites and insects commonly occur in patchy and ephemeral habitats. As plants provide stable habitats for herbivores, herbivorous mites are rarely dependent on other animals for phoretic dispersal. However, a phoretic gall mite, Aceria pallida, which is found on plants, seasonally attaches to a herbivorous insect, Bactericera gobica, for overwintering survival. After detachment, the gall mite shares a habitat with its vector and is likely to compete with this vector for plant resources. However, excessive competition works against the sustainability of the seasonal phoretic association. How the gall mite, as an obligate phoretic mite, balances this relationship with its vector during the growing season to achieve phoresy is unknown. Here, the plant-mediated interspecific interaction between the gall mite and the psyllid after detachment was studied in the laboratory and field. The laboratory results showed that infestation by the gall mite had detrimental effects on the survival and development of psyllid nymphs. Meanwhile, the mite population and the gall size were also adversely affected. The results from the field showed that the mean densities of the mite galls and psyllids were lower in the mixed-species infestation treatment than in the single-species infestation treatment across the investigation period. However, the interspecific interaction between the gall mite and the psyllid decreased rather than accelerated leaf abscission caused by the psyllid, which promoted the persistence of the psyllid population and then indirectly contributed to phoretic association. Our results suggest that the plant-mediated competition between the phoretic gall mite and its vector after detachment facilitates the maintenance of the phoretic association.     

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.     

Do aphid galls provide good nutrients for the aphids?: Comparisons of amino acid concentrations in galls among Tetraneura species (Aphididae: Eriosomatinae)

Some aphid species induce leaf galls, in which the fundatrix parthenogenetically produces many nymphs. In order to ensure high performance, galls have to provide the aphids with sufficient nutrients, in particular, amino acids as a nitrogen source. We tested this hypothesis using six Tetraneura aphid species that induce closed galls. We extracted free amino acids from the whole gall tissues of unit weight and quantified the concentration of each amino acid. There were large differences in the total amino acid concentrations among galls of the Tetraneura species. Tetraneura species in which higher concentrations of total amino acids were found in the gall tended to produce larger numbers of offspring. Of the amino acids found, asparagine was predominant in the gall. The asparagine concentration in T. yezoensis galls was several hundred times as high as in control leaves. We discussed why such a high level of asparagine accumulates in aphid galls.     

Morphogenesis of galls induced by Baccharopelma dracunculifoliae (Hemiptera: Psyllidae) on Baccharis dracunculifolia (Asteraceae) leaves.

The commonest insect gall on Baccharis dracunculifolia (Asteraceae) leaves is induced by Baccharopelma dracunculifoliae (Hemiptera, Psyllidae). The gall-inducing insect attacks young leaves in both the unfolded and the fully expanded stages. Four developmental phases were observed in this type of gall: 1) A folding phase, during which the leaf lamina folded upward alongside the midrib and the edges of the upper portion of the leaf approached each other, forming a longitudinal slit. A single chamber was formed on the adaxial surface of the leaf; 2) A swelling phase, in which the folded leaf tissues thickened and the edges of the leaf drew closer together, narrowing the slit. In this phase the gall matured, turning succulent, fusiform and pale green. The single nymphal chamber was lined with white wax and was able to house from one to several nymphs; 3) A dehiscence phase, characterized by the opening of the slit to release inducers; and 4) A senescence phase, when the gall turned dark and dry. The dermal system of the mature gall was composed of a single-layered epidermis. The mesophyll was swollen, and the swelling was due mainly to hyperplasia of the parenchyma. The vascular tissues along the midrib vein were conspicuous and the perivascular fibers resembled parenchymal cells. The hypertrophied secretory cavities contained low lipophylic content. This gall does not form nutritive tissue, but salivary sheaths left by the inducers were observed near the parenchyma, vascular bundles and secretory cavities. This study complements our current knowledge of gall biology and sheds further light on the plasticity of plant tissues stimulated by biotic factors.     

Life history of <Emphasis Type="Italic">Stenopsylla nigricornis</Emphasis> (Hemiptera: Psylloidea: Triozidae) and phytohormones involved in its gall induction

Many phytophagous insects have an ability to manipulate plant tissue and induce galls, but the mechanism is not yet fully understood. Some insects have multivoltine life cycles, and each generation induces galls on different plant species or different organs in the same host. Such host-use patterns are interesting study subjects to clarify the gall-inducing mechanisms of insects. We focused on a multivoltine and gall-inducing psyllid Stenopsylla nigricornis Kuwayama (Hemiptera: Psylloidea: Triozidae), which is associated with Symplocos lucida Sieb. (Symplocaceae). Based on periodic field surveys in Kyushu, Japan, S. nigricornis is revealed to have a bivoltine life history. Then, we revealed that the spring generation induces galls on leaves, while the autumn generation does so on flower buds and overwintering leaf buds. We also analyzed phytohormones in normal plant tissue, S. nigricornis nymphs, and their galls. As a result, nymphs were discovered to contain much higher concentrations of isopentenyladenosine and its possible precursor, isopentenyladenosine riboside than plant tissues, strongly suggesting that the phytohormone is involved in gall induction by S. nigricornis. Because flower bud galls contained significantly lower concentrations of abscisic acid (ABA) than normal flower bud, the autumn generation nymphs are considered to regulate the ABA level and to promote the earlier opening of host flower buds.     

Host plant effects on the development and survivorship of the galling insect Neopelma baccharidis (Homoptera: Psyllidae)

In this study, the mortality factors acting upon the galling psyllid Neopelma baccharidis Burckhardt (Homoptera) caused by its host plant, Baccharis dracunculifolia De Candole (Asteraceae) were analysed. In March 1999, 982 galls of the same cohort were randomly marked on 109 individuals of B. dracunculifolia in the field. Galls were censused each month during their development, from April to August, and dead galls were collected and analysed for mortality factors. Gall dehiscence rates were calculated for each month. The major mortality source of N. baccharidis was gall dropping (13.2% of the original cohort), which is probably a normal outcome of previous mortality caused by the other factors observed in this study. Unknown factors killed 11.7% of this gall population and were ascribed to plant resistance during gall development. Empty galls represented 7.7% of the observed mortality and may be a consequence of egg retention or egg mortality/abortion related to variations in plant quality. Shoot mortality was high during the dry season and killed 7.5% of the galls, but this impact was minimized after the third month from gall formation due to the ability of nymphs to accelerate development and emerge from galls on dying shoots. However, the size of dehisced galls on dead shoots tended to be smaller, possibly affecting adult performance. Mortality of N. baccharidis attributed to B. dracunculifolia strongly controlled the galling insect population, killing 40.7% of the original cohort of galls. Plant‐mediated mortality was caused by often neglected factors acting predominantly during the first 3 months of development, which are critical to gall survivorship. These results reinforce the importance of bottom‐up forces in plant‐insect systems.     

Oviposition site preference and developmental performance of a gall‐inducing leafhopper on galled and non‐galled host plants

Oviposition preferences of herbivorous insects affect offspring performance. Both positive and negative links between oviposition preference and offspring performance have been reported for many species. A gall‐inducing leafhopper, Cicadulina bipunctata Melichar (Hemiptera: Cicadellidae), feeds on various Poaceae plants and induces galls of enhanced nutritional value for their offspring. Although gall induction by C. bipunctata improves nymphal performance, the oviposition preference of females between galled and non‐galled host plants is still unclear. In this paper, the nymphal performance and oviposition and feeding‐site preference of C. bipunctata were investigated using galled wheat, Triticum aestivum L., and non‐galled barley, Hordeum vulgare L., as host plants. The survival rate of C. bipunctata on wheat was significantly higher than on barley. In the choice test, significantly more eggs were laid into barley, whereas the number of eggs deposited on both hosts was not significantly different in the no‐choice test. The number of settling individuals per leaf area was not significantly different between wheat and barley, suggesting no clear preference for oviposition between these plants. Experience as a nymph with a growing host did not affect oviposition preference as adult female. The inconsistent correspondence between offspring performance and oviposition preference of C. bipunctata may reflect the high mobility of nymphs and/or differences in leaf area between host plants. The results indicate that the previous finding that oviposition preference and offspring performance are not always positively correlated in herbivorous insects is applicable to gall‐inducing insects.     

Augmentation of the assassin bug Pristhesancus plagipennis (Walker) (Hemiptera: Reduviidae) as a biological control agent for Helicoverpa spp. in cotton

Third-instar nymphs of the Australian assassin bug, Pristhesancus plagipennis (Walker), were released into cotton plots at two release densities and two crop growth stages to test their biological control potential. Release rates of 2 and 5 nymphs per metre row resulted in field populations of 0.51 and 1.38 nymphs per metre row, respectively, indicating that over 70% of nymphs died or emigrated within two weeks of release. Effective release rates of 1.38 nymphs per metre row reduced the number of Helicoverpa spp. larvae in the plots for a 7-week period. Crop yields were significantly greater in the plots to which P. plagipennis nymphs were released, with the effective release rate of 1.38 nymphs per metre row providing equivalent yields as insecticide treated plots. The data suggest that P. plagipennis has the capacity to reduce Helicoverpa spp. larvae densities in cotton crops when augmented through inundative release.     

A preliminary histological investigation of gall induction in an unconventional galling system

In an unusual case involving a candidate biological control agent, the histologically complex stem galls of the weevil, Rhinusa pilosa (Coleoptera: Curculionidae) on yellow toadflax (Linaria vulgaris), are rapidly induced during oviposition and reach full size by larval hatch. To investigate gall induction, the oviposition behavior of R. pilosa was described. We experimentally disrupted ovipositing weevils at three key points in the oviposition sequence and compared host-plant tissue responses post disruption, to what occurs during normal gall induction using histological methods. De novo xylem production, intercellular spaces in the cortex, and hyperplasia and hypertrophy of the procambium and pith parenchyma surrounding the egg were some of the tissue- and cellular-level modifications observed only 3?C5?days after normal oviposition. Normal gall development was not observed after any of the oviposition disruption treatments, although some of the cellular and tissue responses resembled those found after undisrupted oviposition. Feeding by the female during oviposition canal formation induced wound meristem and callus tissue formation, but no other modifications consistent with gall formation. When females were disrupted about 20?s into oviposition, a homogenously dense substance was observed, which was suspected to be ovipositional fluid. There was minor stem swelling 10?days later and histologically, periclinal cell divisions, de novo xylem, and pith cells with numerous stained plastids were observed as in normal gall development, thus suggesting that ovipositional fluid plays a role in gall induction.