Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug

Trophic eggs, which are inviable and usually function as a food supply for offspring, have been regarded as extended parental investment or the outcome of parent–offspring conflict in sibling oophagy. Adomerus triguttulus (Heteroptera: Cydnidae) is a sub-social bug showing a complex pattern of maternal care, including progressive provisioning of host seeds and trophic-egg production. To investigate the functions of trophic eggs, we removed trophic eggs from clutches under different resource conditions. The longevity of nymphs was greatly extended by feeding upon trophic eggs when seeds were excluded. When seeds were provided, trophic-egg feeding by nymphs enhanced their development, but there were no significant effects on brood survival. Some viable eggs were also fed upon by sibling nymphs. However, there was no difference in the proportion of viable eggs consumed between clutches with and without trophic eggs. Females lay viable eggs within the first oviposition day. The synchronous hatching resulting from this oviposition mode seems to prevent sib-cannibalism. The body size of females affected their relative investment in trophic eggs; larger females produced more viable eggs with relatively fewer trophic eggs. The functions and adaptive allocation of trophic eggs are discussed in light of the two hypotheses mentioned above.     

Symbiont acquisition alters behaviour of stinkbug nymphs

In parasitic associations, the evolutionary interest of a symbiont contradicts that of a host, which sometimes causes the phenomena so-called 'parasite manipulation' wherein symbiont infection alters host behaviour to facilitate its vertical/horizontal transmission. In mutualistic associations, meanwhile, symbiont-induced alteration of host behaviour that enhances its transmission has been little described. Here we report such a case in the stinkbug Megacopta punctatissima associated with an obligate gut bacterium. When female stinkbugs lay eggs, small particles called 'symbiont capsules' are deposited underside of the egg mass. Newborn nymphs immediately acquire the symbiont from the capsule, and then aggregate and become quiescent. By manipulating the levels of symbiont supply to newborn nymphs experimentally, we demonstrated that (i) experimental depletion of the symbiont resulted in the occurrence of wandering nymphs, (ii) the less symbiont supply, the more wandering nymphs, and (iii) almost all wandering nymphs were either symbiont-free or symbiont-depleted, whereas the majority of resting nymphs were infected with sufficient titres of the symbiont. These results strongly suggest that the nymphal behaviour is strongly influenced by the success/failure of the symbiont acquisition, thereby ensuring transmission of the essential symbiont and minimizing the energy and time spent for the activity.     

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.     

Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions

Adomerus triguttulus (Heteroptera: Cydnidae) females provision host Lamium spp. seeds to their nymphs. Females also produce trophic eggs, which are inviable and usually function as a food supply for hatched nymphs. Here we report experimental evidence of the potentially adaptive maternal effects of this unusual resource investment. To investigate the effects of food-resource environments on trophic-egg production, we reared females under different resource conditions prior to oviposition and then compared the subsequent allocations of trophic eggs. Females that had been supplied with less-developed seeds produced fewer viable eggs than those supplied with well-developed seeds. However, there was no difference in the number of trophic eggs produced between the two treatments, and thus the trophic-egg ratio, i.e. the number of trophic eggs per viable egg, was higher in females supplied with less-developed seeds. Trophic-egg feeding by hatched nymphs enhances their growth or survival, and a higher trophic-egg ratio would be adaptive particularly under limited resource conditions. In A . triguttulus , adults and offspring depend on the same food resource, i.e. host seeds, and the resource conditions experienced by females prior to oviposition should be well correlated with those experienced later by the offspring. This may enable females to adjust the trophic-egg ratio in response to varying resource environments prior to oviposition.     

Prey preference and consumption capacity of Nephus arcuatus (Coleoptera: Coccinellidae): the influence of prey stage,prey size and feeding experience

This study examined the feeding habits of Nephus arcuatus Kapur (Coleoptera: Coccinellidae), an important predator of mealybugs in south-western Iran. The consumption capacity of male and female N. arcuatus adults was determined by their feeding on eggs, first-instar nymphs, and adult females of two destructive mealybugs, Nipaecoccus viridis (Newstead) and Planococcus citri Risso, over a 24-h period. N arcuatus consumed significantly more first-instar nymphs than eggs, and more eggs than female adults of both prey species. In addition, we also studied the developmental stage prey preference of adults reared on either N. viridis or P. citri and found that the prey preference of females did not change with the developmental stage of the mealybug. Meanwhile, the males reared on either N. viridis or P. citri showed a significant preference for the first-instar nymphs of P. citri over first-instar nymphs of N. viridis, while a preference for the eggs or adult females of these two mealybugs was not observed. This selection of first-instar nymphs by males was not tied to its previous feeding experience. Our findings suggest that prey stage, prey size and previous feeding experience had no effect on the prey selection of N. arcuatus, making it a good candidate for the biological control of mealybugs.     

How many symbionts are provided by mothers,acquired by offspring,and needed for successful vertical transmission in an obligate insect–bacterium mutualism?

Vertical symbiont transmission is among the most pivotal processes for maintenance of symbiotic associations. However, it is poorly understood whether and how the levels of resource allocation and investment upon vertical transmission are regulated. The stinkbug Megacopta punctatissima is obligatorily associated with the gut symbiotic bacterium 'Candidatus Ishikawaella capsulata', whose transmission is mediated by a unique mechanism called 'symbiont capsule'. We investigated the population dynamics of the symbiont during vertical transmission in the host-symbiont mutualism. The stinkbug mothers produced one capsule for around 3.6 eggs irrespective of clutch size, suggesting a strict maternal control over symbiont supply for the offspring. However, experimental manipulation of egg/capsule ratios revealed that one capsule is sufficient for symbiont transmission to six nymphs. Quantitative polymerase chain reaction analyses demonstrated that a capsule contains 1.2 x 10(8) symbionts, a newborn nymph possesses 2 x 10(7) symbionts from a capsule, and thus one capsule certainly contains a sufficient amount of symbiont cells for six nymphs. These results indicated that the stinkbug mothers produce 1.7 times more symbiont capsules than needed. The newborn nymphs consistently harboured around 2 x 10(7) symbionts, also suggesting a nymphal control over symbiont transmission. The threshold symbiont titre minimally needed for successful vertical transmission was estimated to be 1.9 x 10(6) symbionts, which is only 1/10 of the actual symbiont titre detected in a newborn nymph. These results illuminate several ecological factors that may be relevant to parental and offspring controls over symbiotic resource allocation through host insect generations.     

Intraclutch egg‐size variation in acanthosomatid bugs: adaptive allocation of maternal investment?

If there are differences in predation risk among the offspring within a clutch, parents may allocate less resources to the offspring facing higher risk. I examined parental investment in terms of egg size within clutches in five species of stink bugs (Heteroptera, Acanthosomatidae). In subsocial Elasmucha and Sastragala species, the female guards her eggs and first-instar nymphs against invertebrate predators by covering her clutch with her body. Large differences in survival from predation between offspring at the centre and offspring at the periphery of the clutch have been reported in such subsocial insects. I found that Elasmucha and Sastragala females laid significantly smaller eggs in the peripheral (and thus more vulnerable) part of the clutch. Phenotypic trade-offs between egg size and clutch size were detected in these subsocial species. Egg size was positively correlated with hatched first-instar nymph size: smaller nymphs hatched from smaller peripheral eggs. In asocial Elasmostethus humeralis , however, no significant difference in size was detected between the eggs at the centre of and those at the periphery of the clutch. Thus, in subsocial acanthosomatid bugs, females seem to allocate their resources according to the different predation risks faced by the offspring within the clutch.     

The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation

1. Dicyphus hesperus Knight (Heteroptera: Miridae) nymphs were fed from egg hatch to the adult stage on Ephestia kuehniella eggs provided either alone or in combination with tomato leaves or with a supplementary water source. 2. Only 6% of individuals completed nymphal development on a diet of eggs alone. In contrast, a high proportion of nymphs completed development on a diet of eggs when either tomato leaves (97%) or a supplementary water source (88%) were provided. 3. The development times of nymphs given access to leaves were significantly shorter than those of nymphs given access only to supplementary water. 4. Adult female D. hesperus that were given access to tomato leaves prior to feeding trials consumed significantly more eggs in a 4‐h period than females that were dehydrated before trials. Dehydrated females that were allowed access to water for 3 h before trials consumed an intermediate number of eggs. 5. Plant feeding or access to some other water source is required for prey feeding, growth, and development in D. hesperus, and acquisition of water is proposed as a primary function of plant feeding. In addition, D. hesperus derives nutrients from plant feeding that increase the rate of nymphal development, although nymphs cannot complete development when provided only with tomato leaves. 6. Three simple models are presented of feeding behaviour in predatory Heteroptera where the amount of plant feeding either decreases, increases, or is constant as a function of the amount of prey feeding. The models are discussed with reference to the results and the probable multifunctional nature of plant feeding in predatory Heteroptera.     

Trophic egg laying: hypotheses and tests

Trophic egg-laying – wherein mothers provide non-developing eggs for offspring to eat – has attracted much empirical attention to diverse taxa (e.g. amphibians, non-social and eusocial insects, fish, and marine gastropods). However, there has been been only a limited exchange of ideas among studies of different taxa. We advocate a unified approach to the study of trophic eggs within an evolutionary ecological framework. In this paper, we stress the importance of elucidating the adaptive function of trophic eggs through explicit hypothesis testing, and our primary objective is to outline key experiments that can test adaptive and functional hypotheses. Currently, some cases of hypothesized trophic eggs may simply represent offspring consumption of eggs that failed to develop for non-adaptive reasons (e.g. sperm limitation). Furthermore, in many trophic egg-laying species, it is unclear whether trophic eggs have evolved to provision offspring or to reduce cannibalism among offspring. With increased focus on theory and hypothesis testing, the study of trophic eggs can offer important insight into topics such as sibling rivalry, parent–offspring conflict, and parental care.     

Availability of unfertilised eggs increases the fitness of nymphal crickets (Gryllidae)

1. Female insects of many species lay both fertilised and unfertilised eggs, with the latter accounting for up to 50% of the total number laid. These unfertilised eggs do not hatch and so their relevance is unclear. 2. In the present study, it was found that nymphs of the cricket Velarifictorus aspersus ate unfertilised eggs regardless of whether there was other food available. This provision enabled nymphs to develop successfully when no other food was provided, and to gain additional body mass when other food was available under crowded conditions. These results suggest that unfertilised eggs have an important role in the survival and development of nymphs. 3. Nymphs preferred to eat unfertilised rather than fertilised eggs, suggesting that they may have the ability to distinguish between these two types of eggs. 4. Crowding promoted feeding on unfertilised eggs and accelerate nymphal development, suggesting that greater food consumption accounts for faster growth under grouped conditions.     

Trophic Egg Production in a Subsocial Shield Bug, Parastrachia japonensis Scott (Heteroptera: Parastrachiidae), and its Functional Value

Females of the gregarious shield bug, Parastrachia japonensis Scott (Heteroptera: Parastrachiidae) engage in extensive parental care behaviors that include egg and nymph guarding and progressive provisioning of drupes of the solitary host tree, Schoepfia jasminodora (Olacaceae: Rosidae: Santales). We noted that some eggs in every egg mass failed to turn pink and develop eye‐spots indicative of developing embryos, suggesting that they are infertile, and therefore non‐viable. We also observed newly hatched nymphs probing, and presumably feeding, on the egg mass remains. In the present report, through field observations and experiments involving removal of these non‐viable eggs in the laboratory, we demonstrate that their presence is correlated with significant increases in nymphal weight, developmental rate and survival in the absence of other food. Thus, we conclude that an additional manifestation of the parental care behaviors that P. japonensis females use to increase their reproductive success is the production of trophic eggs. Some physical traits of the trophic eggs and their functional role in this system are discussed in the context of our current theoretical understanding of extended parental care.     

Mothers modify eggs into shields to protect offspring from parasitism

Eggs are an immobile, vulnerable stage of development and their success often depends on the oviposition decisions of the mother. Studies show that female animals, and sometimes males, may invest parental resources in order to increase the survival of their offspring. Here, we describe a unique form of parental investment in offspring survival. The seed beetle Mimosestes amicus may lay eggs singly, or may cover eggs with additional egg(s). This egg stacking serves to significantly reduce the mortality of the protected egg from parasitism by the parasitic wasp, Uscana semifumipennis. The smaller top eggs serve only as protective shields; they are inviable, and wasps that develop in them suffer negative fitness consequences. Further, we found egg stacking to be inducible; M. amicus increase the number of stacks they lay when parasitoids are present. However, stacking invokes a cost. When wasps are absent, beetles lay more single eggs, and produce more offspring, highlighting the adaptive value of this extraordinary example of behavioural plasticity in parental investment.     

Influence of Host Nutrients on the Parasitic Development of Mermis nigrescens (Mermithidae)

Schistocerca gregaria nymphs and adults of both sexes were infected with eggs of Mermis nigrescens. Mermithid larvae grew more slowly in nymphal hosts, and emerging larvae were smaller than those from adult hosts. The longer the larvae remained in the host, the greater their size. Those developing in adult female hosts were longest. Single mermithid larvae that were transferred to a second host continued to grow and were significantly longer at emergence than larvae that developed solely in one host. In adult hosts that were infected with 40-300 M. nigrescens eggs, the percentage of mermithids that became males was strongly dependent on host weight at infective doses of 90 eggs or more. Results are discussed in relation to nutrient stress on the larvae and its importance in developing in vitro culture techniques.     

Interactions of colonisation density and leaf environments on survival of Trioza eugeniae nymphs

1. Female eugenia psyllids Trioza eugeniae oviposit on the margins of expanding young Syzygium paniculatum leaves. The developing nymphs, feeding within pit‐shaped galls on the leaves, cause the leaves to become curled and deformed. The degree of leaf curling was correlated positively with densities of T. eugeniae nymphs. 2. High relative humidity increased persistence of nymphs on leaves at low insect densities, but persistence did not differ between high or low relative humidity conditions when nymphal densities were high and leaves were greatly curled. 3. Direct insolation increased nymphal mortality. Nymphs on the abaxial leaf surface in the direct sun had lower mortality than similarly exposed nymphs on the adaxial leaf surface. 4. Field populations showed high preference for abaxial leaf surfaces and a stronger preference for shaded adaxial surfaces than for exposed adaxial surfaces. 5. Adverse environmental conditions of direct insolation and low relative humidity may be mitigated by leaf curl associated with moderate populations, however competition at high nymphal density supersedes any potential benefit arising from leaf curling and has a negative effect on nymphal survival.     

Life table for Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) and prediction of damage in lodgepole pine seed orchards

Abstract 1 Fecundity, egg hatch and nymphal survivorship of Leptoglossus occidentalis Heidemann were determined and used to develop a damage prediction formula for seed bugs in lodgepole pine seed orchards. 2 A single overwintered L. occidentalis female may lay up to 80 eggs during early and mid‐season cone development. 3 Up to 83.4% of eggs that were attached to branches with tape hatched successfully, compared with 53.5% of eggs attached to needles with wire. Egg parasitism was only observed in egg masses attached with wire. 4 Egg masses attached with wire suffered approximately 30% mortality from parasitism, primarily by Gryon pennsylvanicum (Ashmead). 5 Approximately 15.1 and 2.5% of first instars survived to adulthood in 2000 and 2001, respectively. Survival of caged nymphs that were protected from predators was 14.5 and 17.8%, respectively. 6 A composite survival table indicated that 9.3% of eggs laid by L. occidentalis are expected to survive to adulthood. 7 Based on previously determined damage estimates for each life stage of feeding during three periods of cone development, a hypothetical density of one seed bug per tree early in the season will result in an expected seed loss of approximately 310 seeds.     

The effect of relative humidity on the behaviour and development of Triatoma brasiliensis

Abstract The preference for relative humidity (RH) and suitability of different levels of this environmental parameter were investigated in the haematophagous bug Triatoma brasiliensis Neiva, 1911 (Hemiptera, Reduviidae). The hygropreference of T. brasiliensis was studied using a RH gradient and the effect of different RHs on the egg hatching, nymph mortality and moulting success was also analysed. The results show that egg hatching in first-instar nymphs of T. brasiliensis was lower at extreme RHs and, particularly, it was lowest at 9.3% RH. The survival of starved nymphs was not affected by RH, but the percentage of engorged nymphs and the ecdysis success of these nymphs once fed was diminished strongly by high humidity. Fourth-instar nymphs preferred to stay at the lowest RH during the first 5 days after feeding and during ecdysis. This preference changed markedly during starvation. Fifteen days after ecdysis, the bugs moved towards intermediate humidities, and 30 days after ecdysis they even preferred the most humid sectors of the gradient. Females preferred to lay eggs in dry environments, suggesting that they may not have a particular hygropreference for oviposition, but that they simply lay their eggs at the RHs where they prefer to stay.     

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.     

Specific developmental window for establishment of an insect-microbe gut symbiosis

The alydid stinkbug Riptortus pedestris is specifically associated with a beneficial Burkholderia symbiont in the midgut crypts. Exceptional among insect-microbe mutualistic associations, the Burkholderia symbiont is not vertically transmitted but orally acquired by nymphal insects from the environment every generation. Here we experimentally investigated the process of symbiont acquisition during the nymphal development of R. pedestris. In a field population, many 2nd instar nymphs were Burkholderia free, while all 3rd, 4th, and 5th instar nymphs were infected. When reared on soil-grown potted soybean plants, Burkholderia acquisition occurred at a drastically higher frequency in the 2nd instar than in the other instars. Oral administration of cultured Burkholderia cells showed that 2nd and 3rd instar nymphs are significantly more susceptible to the symbiont infection than 1st, 4th, and 5th instar nymphs. Histological observations revealed rudimentary midgut crypts in the 1st instar, in contrast to well-developed midgut crypts in the 2nd and later instars. These results indicate that R. pedestris acquires the Burkholderia symbiont from the environment mainly during the 2nd instar period and strongly suggest that the competence for the symbiont infection is developmentally regulated by the host side. Potential mechanisms involved in infection competence and possible reasons why the infection preferentially occurs in the 2nd instar are discussed.     

Effect of temperature on the biology of Creontiades dilutus (Stål) (Heteroptera: Miridae)

The egg and nymphal development, fecundity and survival of the green mirid, Creontiades dilutus were examined at a range of temperatures and a modified day-degree model fitted to the data. Day degree (DD) requirements for egg and nymphal development, and threshold temperatures were calculated from the fitted lines. Female fecundity and longevity, egg and nymphal development, and survival of C. dilutus were significantly influenced by temperature. Eggs and nymphs failed to complete development at temperatures below 17 and at 38°C. Females also failed to produce any eggs at 11 and 38°C. The optimum temperature range for female fecundity was found to be 26–32°C. The optimum temperature for the development of eggs was calculated from the model as 30.5°C and for nymphs as 31.5°C. The threshold temperature for development was 15.8°C for egg and 15.1°C for nymph; 69.4 and 156.7 DD were required for completing the egg and the nymphal development, respectively. At the optimum temperature, it was estimated that development from egg to adult took 15 days. Survival was highest at 26°C for eggs and at 30–32°C for nymphs.     

Independence of resistance in Brachiaria spp. to nymphs or to adult spittlebugs (Hemiptera: Cercopidae): implications for breeding for resistance

Both nymphal and adult spittlebugs (Hemiptera: Cercopidae) cause serious economic damage to susceptible brachiariagrass [genus Brachiaria (Trin.) Griseb], pastures in tropical America. Both life stages are xylem feeders: nymphs feed primarily on roots and stems, whereas the adults feed mainly on foliage. Numerous interspecific brachiariagrass hybrids with high levels of antibiosis resistance to nymphs of several important spittlebug species have been obtained. Recent studies revealed major inconsistencies between reaction to nymphs and reaction to adults on the same host genotype. Because both insect life stages can cause severe economic damage on susceptible brachiariagrass pastures, a cultivar development strategy must take into account resistance to both life stages. To assess the degree of association between resistance to spittlebug nymphs and to adult feeding, we tested 164 hybrids and six check genotypes for resistance to both life stages of three spittlebug species: Aeneolamia varia (F.), Aeneolamia reducta (Lallemand), and Zulia carbonaria (Lallemand). Most hybrids tested were classified as resistant to nymphs. On the contrary, for all three species, the overall mean damage score of the 164 hybrids did not differ from the mean score of the susceptible checks. None of the hybrids was classified as resistant to adult feeding damage. Correlations between percentage nymph survival and adult damage scores were consistently low (r = 0.0104-0.0191). Correlations between nymphal and adult damage scores were also low (0.109-0.271), suggesting that resistances to the different life stages are largely independent. Chi-square analyses comparing frequency distributions of responses of the 164 breeding hybrids to nymphs or adults confirmed essential genetic independence of these two traits. We conclude that attention to improving genetic resistance specifically to adult feeding damage is warranted.