Bivoltine Life Cycle Research Articles

Nesting Biology of Megachile (Chrysosarus) jenseni (Hymenoptera: Megachilidae) in Two Contrasting Pampean Agroecosystems: A Potential Pollinator for Alfalfa?

Several crops depend on both managed and wild bees to produce fruits and/or seeds, and the efficiency of numerous wild bees is higher than that of some managed species. Therefore, knowing and understanding the required resources for wild bees could enabled the establishment of management practices to increase their populations. Here, we provide information about the nesting biology of Megachile (Chrysosarus) jenseni, a Faboideae-specialist bee species. Based on observations from two populations occurring in contrasting agroecosystems, this bivoltine species showed common behavioral features shared with other species of subgenus Chrysosarus, such as the use of petal pieces and mud as nesting materials and the utilization of pre-existing cavities. Both studied populations showed a bivoltine life cycle with a rapid early-summer generation and a second generation, with most individuals overwintering. Main causes of mortality were unknown diseases (or other factors), causing the death of preimaginal stages. Moreover, this species was attacked by a cleptoparasite megachilid (Coelioxys remissa), a parasitic eulophid wasp (Melittobia sp.), and a bee fly (Anthrax oedipus). Finally, we discussed the potential use of this leaf-cutter bee species for alfalfa pollination.

Life cycles and larval and pupal habitats of eleven Japanese Rhyacophila (Trichoptera) species at the mountain streams in central Honshu

The life cycles and microhabitats involved in aquatic stages of eleven Rhyacophila Stephens, 1836 species living in two neighboring Japanese mountain streams in Nara Prefecture, central Honshu, were investigated. Eight species had univoltine life cycles; seven species had spring to early summer emergence seasons. One species had an autumnal emergence. Four univoltine species had periods where no larvae or pupae were collected in aquatic stages, possibly a period of egg diapause. Three species had bivoltine life cycles, with early summer and autumn emergence seasons. Rhyacophila nipponica Iwata, 1927, R. manuleata AV Martynov, 1934, and R. shikotsuensis Iwata, 1927, in the nigrocephala species group Ross, 1956, have larvae which spend most of their larval stage in the hyporheos. The larvae of R. transquilla Tsuda, 1940, also inhabit the hyporheic zone, although the vertical microhabitat used by this species differed from the former three species. All four of these species have hyporheic larval stages, but in these species the first and final instar larvae reside on the surfaces of cobbles. The first instar larvae seem to live on stone surfaces immediately after hatching, and subsequently move to the interstices of sand. Final instar larvae live in the interstices of sandy bottom, and move to stone surfaces for pupation. Eleven species of the genus Rhyacophila had diverse life histories, microhabitat preferences, and experienced differing water temperature regimes during larval stages at the sites. Life history and habitat preference variation enhances the species richness of the genus and coexistence of species in upper stream of the Kinokawa River.

MACROHOMOTOMA GLADIATA (HEMIPTERA HOMOTOMIDAE) SEASONAL POPULATION FLUCTUATION AND ITS NATURAL ENEMIES ON FICUS MICROCARPA IN GREECE

Macrohomotoma gladiata (Kuwayama) (Hemiptera: Homotomidae) has been recently recorded in the Medi- terranean Basin causing serious damage on the widely cultivated ornamental tree Ficus microcarpa L.f. The population structure and seasonal fluctuation of M. gladiata were studied on F. microcarpa in Athens, Greece, from February 2019 to February 2020. In the samples, the presence of its natural enemies was recorded too. Eggs were recorded in May, August and from October to early January; the first two nymphal instars were recorded throughout the year but not in August and September whereas their densities reduced in early May; the middle-aged and the late instars nymphs were recorded in March and April and then appeared again in June and July. Based on our results 1) during winter, only young nymphs of M. gladiata were present; 2) under autumn and winter conditions, young nymphs do not develop further; and 3) most likely M. gladiata has a bivoltine life cycle or may complete a partial third generation in autumn. Parasitized M. gladiata nymphs by a Psyllaephagus Ashmead species were recorded from April to August, with the parasitism rate reaching to 81%. The predator Anthocoris nemoralis (Fabricius) (Hemiptera: Anthocoridae) was present in low numbers in spring. This work revealed useful information for the phenology and rational management of this pest and the potential of its natural enemies in its control. Key Words: Macrohomotoma gladiata, Ficus microcarpa, life cycle, biological control, Anthocoris nemoralis, Psyllaephagus

Male survivorship and the evolution of eusociality in partially bivoltine sweat bees.

Eusociality, where workers typically forfeit their own reproduction to assist their mothers in raising siblings, is a fundamental paradox in evolutionary biology. By sacrificing personal reproduction, helpers pay a significant cost, which must be outweighed by indirect fitness benefits of helping to raise siblings. In 1983, Jon Seger developed a model showing how in the haplodiploid Hymenoptera (ants, wasps and bees), a partially bivoltine life cycle with alternating sex ratios may have promoted the evolution of eusociality. Seger predicted that eusociality would be more likely to evolve in hymenopterans where a foundress produces a male-biased first brood sex ratio and a female-biased second brood. This allows first brood females to capitalize on super-sister relatedness through helping to produce the female-biased second brood. In Seger's model, the key factor driving alternating sex ratios was that first brood males survive to mate with females of both the second and the first brood, reducing the reproductive value of second brood males. Despite being potentially critical in the evolution of eusociality, however, male survivorship has received little empirical attention. Here, we tested whether first brood males survive across broods in the facultatively eusocial sweat bee Halictus rubicundus. We obtained high estimates of survival and, while recapture rates were low, at least 10% of first brood males survived until the second brood. We provide empirical evidence supporting Seger's model. Further work, measuring brood sex ratios and comparing abilities of first and second brood males to compete for fertilizations, is required to fully parameterize the model.

Geographic Variation in Photoperiodic Response for Induction of Pseudopupal Diapause in Epicauta gorhami (Coleoptera: Meloidae).

Geographical variations in the threshold of environmental cues for diapause induction are important in understanding the life history strategy of insects. Larvae of the bean blister beetle, Epicauta gorhami (Coleoptera: Meloidae), feed on grasshopper eggs and undergo hypermetamorphosis. They normally enter diapause as a pseudopupa (fifth instar). However, when the larvae are reared under long-day and high-temperature conditions, they do not enter pseudopupal diapause but pupate directly from the fourth instar. In addition, this insect is known to modify its photoperiodic response for induction of pseudopupal diapause depending on food availability for larvae. In this study, the larval photoperiodic responses for diapause induction were examined for three populations of E. gorhami collected from the northernmost (Morioka, 39.7°N), central (Kazo, 36.1°N), and southernmost (Takanabe, 32.1°N) parts of its distribution range, and the responses were examined under both fully fed and food-deprived (FD) conditions. Diapause incidence decreased in FD larvae for all populations in long-day conditions, and the critical day-lengths for the diapause incidence were calculated as 14.81, 13.97, and 13.99 h in the Morioka, Kazo, and Takanabe populations, respectively. The results indicate the presence of a geographical variation in larval photoperiodic response, in which diapause is induced earlier in higher latitudinal areas. From these results, together with data for developmental threshold temperature and thermal constant, the Morioka and Kazo populations were suggested to have a partial bivoltine life cycle under the conditions of extremely early oviposition season, a sufficient summer temperature, and poor larval food availability.

Inverse density-dependent diapause and its influence on population dynamics in Monochamus alternatus alternatus (Coleoptera: Cerambycidae)

Monochamus alternatus alternatus Hope (Coleoptera: Cerambycidae) is the primary vector of pine wilt disease in China and Taiwan. It has a partially bivoltine life cycle with facultative diapause at the final larval instar that is mediated by the initial larval density. To evaluate the effect of density-related induction of diapause on population fluctuation, one, two or four newly hatched larvae were inoculated on individual Pinus thunbergii bolts and the life-history traits including diapause were investigated. This experiment indicated that as initial population size/bolt (crowding) increased, the diapause incidence, larval stage survival, adult body size, development time of nondiapause individuals and pupal period of diapause individuals decreased. The analysis indicated that larval interference as well as food shortage suppressed diapause induction. Increasing larval density decreased the probability of diapausing, survival, adult body mass and other traits. Using the data obtained from this study, a simple mathematical model indicated that inverse density-dependent induction of diapause in the first generation had a destabilizing effect on the population size of overwintering generation, which was composed of diapause larvae of the first and second generations; whereas, direct density-dependent induction of diapause exerted a stabilizing effect on it.

Life histories of two hyperbenthic mysids (Mysidacea: Mysidae) in an open estuary

ABSTRACT Mysidae are widely distributed in aquatic ecosystems and form a large proportion of the hyperbenthic biomass in estuaries. The seasonality, spatial distribution and reproductive biology of the two hyperbenthic mysid species, Tenagomysis chiltoni and Tenagomysis novaezealandiae, were studied in an open estuary. Sampling was conducted bi-monthly at night between February 2008 and April 2009. These two mysid species are spatially segregated along a salinity gradient, with T. chiltoni upstream and T. novaezealandiae downstream in the estuary. The life cycle and breeding dynamics of T. chiltoni (bivoltine life cycle) and T. novaezealandiae (multivoltine life cycle) were similar to those described in intermittently closed estuaries, but their breeding period (December to April) was relatively shorter and densities were lower. Life-stage specific segregation in summer in both mysid species likely provided favourable conditions for maximum growth rates, short maturation times, and sheltering, enhancing reproductive success of both mysid species.

Northward shift in temperature sum isoclines may favour Ips typographus outbreaks in European Russia

Abstract As the development of the eight‐toothed spruce bark beetle Ips typographus is temperature‐dependent, climate change may encourage development of its additional generations per year and facilitate mass outbreaks further north than previously known. The aim of the study was to analyse historical changes in effective temperature sums (ETSs) and early season swarming weather for I. typographus in different forest zones of European Russia between 1960 and 2016. The difference in ETSs was analysed with linear regression using daily temperature data from the 30 meteorological stations. Historical data regarding the location of I. typographus outbreaks were examined and changes in their distribution during the entire study period were analysed. There was a substantial increase in ETSs, especially in the latter half of the study period. Increased ETSs coincided with more favourable conditions for swarming of I. typographus. Areas with favourable ETSs for the complete development of bivoltine populations of I. typographus (>1500 DD) shifted northwards on average 450 km during the entire study period. The northward shift of ETSs may enhance the transition from univoltine to bivoltine life cycles of I. typographus in the south and middle taiga and from bivoltine to trivoltine life cycles in conifer‐broadleaf forests.

Lespesia archippivora (Diptera: Tachinidae) Survival and Sex Ratios within Monarch Butterfly (Lepidoptera: Nymphalidae) Hosts

We studied factors associated with survival, sex ratio, and seasonality of the tachinid fly Lespesia archippivora parasitizing monarch butterflies (Danaus plexippus). A total of 424 L. archippivora flies were collected from 124 parasitized monarch larvae in 2016 and 2017. The majority of flies emerged during the monarch's 5th larval instar. Both fly survival and brood size were higher for those emerging during the 5th instar relative to flies emerging during the 4th instar or pupal stage. Brood size ranged from 1 to 10 flies, and the proportion of each brood that successfully pupated to emerge as adults increased with brood size. Adults emerging from larger broods were lighter and smaller, which likely impacts subsequent fecundity and survival. Overall sex ratio was skewed towards males, with 222 male and 129 female adults identified. L. archippivora were recovered from monarchs both early in the season and at the end of the season, with a gap from mid-June to mid-July; a pattern consistent with a bivoltine life cycle.

Robustness of latitudinal life-cycle variations in a cricket Dianemobius nigrofasciatus (Orthoptera: Trigonidiidae) in Japan against climate warming over the last five decades

Recent climate warming is expected to have changed the phenology of organisms. The cricket Dianemobius nigrofasciatus (Matsumura) (Orthoptera: Trigonidiidae) has univoltine and bivoltine life cycles in northern and southern regions of Japan, respectively, because of latitudinal variation in the growing season length. Its adult body size increases with decreasing latitude, and decreases at a latitude where the number of annual generations increases. The present study aims to examine whether the range of the bivoltine life cycle has expanded northward due to climate warming. We compared a latitudinal saw-tooth body size cline between the 1960s and the 2010s. The body size showed a latitudinal saw-tooth cline in adults collected in recent years, as it did in adults collected five decades ago. However, no significant difference was observed between these two clines, suggesting that the bivoltine life cycle has not expanded in the last five decades. These results contrast to those recently reported in a closely related species, Polionemobius mikado (Shiraki) (Orthoptera: Trigonidiidae), in which the turning points of the saw-tooth cline had shifted northward in the last four decades. The stable latitudinal distribution of life cycles in D. nigrofasciatus might result from the different photoperiodic regulation of growth rate involved in the different responses to climate warming.

Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite.

The parasitic insect Xenos vesparum induces noticeable behavioral and physiological changes—e.g. castration—in its female host, the paper wasp Polistes dominula: parasitized putative workers avoid any colony task and desert the colony to survive in the nearby vegetation, like future queens and males do. In this long-term observational study, we describe the spectacular attraction of parasitized workers towards trumpet creeper bushes (Campsis radicans) in early-summer. Two thirds of all wasps that we sampled on these bushes were parasitized, whereas the parasite prevalence was much lower in our study area and most wasps sampled on other nearby flowering bushes were non-parasitized. First, we describe the occurrence and consistency of this phenomenon across different sites and years. Second, we evaluate the spatial behavior of parasitized wasps on C. radicans bushes, which includes site-fidelity, exploitation and defense of rich extra-floral nectaries on buds and calices. Third, we record two critical steps of the lifecycle of X. vesparum on C. radicans: the parasite’s mating and a summer release of parasitic larvae, that can infect larval stages of the host if transported to the host’s nest. In a nutshell, C. radicans bushes provide many benefits both to the parasite X. vesparum and to its host: they facilitate the parasite’s mating and bivoltine lifecycle, a phenomenon never described before for this parasite, while, at the same time, they provide the wasp host with shelter inside trumpet flowers and extrafloral gland secretions, thus likely enhancing host survival and making it a suitable vector for the infection.

Northward expansion of the bivoltine life cycle of the cricket over the last four decades.

Recent climate warming has affected some life-history traits of insects, including voltinism and body size. The magnitude of changes in these traits may differ latitudinally within a species because of the differing lengths of season available for growth. The present study aims to estimate the change in voltinism of the lawn ground cricket, Polionemobius mikado (Shiraki) (Orthoptera: Trigonidiidae), over the last four decades by comparing the body size between adults collected from a wide range of latitudes in Japan in recent years (2015-2017) and those collected four decades ago (1969-1976). The body size of adults collected in recent years showed a latitudinal saw-tooth cline, in the same way as body size did four decades ago, and the cline shifted northward over the last four decades: In 2015-2017, the body size decreased slightly with increasing latitude from 31°N to 36°N, and then increased to 40°N, and again decreased from 40°N to 44°N. Comparison of the body size between recent years and four decades ago revealed that the body size has decreased significantly at the middle latitudes (36-40°N), suggesting that the proportion of smaller bivoltine individuals there has increased over the last four decades. The sum of effective temperatures for postdiapause embryonic development at around 36°N in recent years was comparable to that at 31-35°N four decades ago, at which P.mikado populations were bivoltine. Taken together, these findings suggested that the latitudinal range suitable for the bivoltine life cycle of P.mikado has expanded northward over the last four decades because of climate warming. This is the first report that shows that a decrease in body size can be caused by climate warming via an increase in voltinism.

Field evaluation of the susceptibility of mill and table olive varieties to egg‐laying of olive fly

AbstractThe susceptibility of 20 widely distributed mill and table olive varieties to Bactrocera oleae (Rossi) as affected by irrigation, and fruit diameter and oil content was evaluated in a 3‐year trial in Southern Spain. Bactrocera oleae was bivoltine life cycle in the experimental site, with significant differences among population size throughout the study. Even though the olive fruit fly damaged all varieties, significant differences in susceptibility were detected. Among the mill olive varieties “Nevadillo Blanco de Jaén” was the most susceptible, with average infestation levels ranging between 6.7% and 52.2% and between 10.3% and 69.2% under rainfed and irrigated conditions, respectively, and “Arbequina” was the least susceptible, with average infestation levels ranging between 0.6% and 12.7% and between 2.3% and 18.5% under rainfed and irrigated conditions, respectively. Among the table olive varieties, “Gordal Sevillana,” “Ascolana Tenera” and “Ocal” were the most susceptible (with average infestation levels reaching 39.7%, 36.5% and 33.3%, respectively), while “Callosina” was the least susceptible (with infestation levels of only 8.4%). Irrigation tended to promote both B. oleae infestation and its earlier occurrence compared to the rainfed condition. Even though the diameter and oil content were positively correlated with B. oleae fruit infestation (correlation coefficients ranged between 0.5 and 0.95), the present work reveals that other yet‐unknown factors may influence B. oleae oviposition preferences. The results of this study can be useful for breeding programmes to develop olive varieties resistant to B. oleae and provide key information for wide‐area olive fly pest management decisions.

‘Closing the Life Cycle’ of Andricus quercuslanigera (Hymenoptera: Cynipidae)

While the alternation of asexually and sexually reproducing generations is common among the oak gall wasps (Hymenoptera: Cynipidae: Cynipini), it has been hypothesized that the diversity of taxa displaying this unique life cycle is underestimated because either 1) the alternative generation has not yet been described or 2) each generation is currently described as two distinct species and should be collapsed into one heterogonic organism (referred to as ‘closing the life cycle’). Through field observations, experimental rearing, morphological identification, laboratory behavioral assays, and genetic analysis, we demonstrate heterogony in the cynipid species Andricus quercuslanigera (Ashmead 1881) (Hymenoptera: Cynipidae), which was previously only described from the asexual generation. We confirm that the asexual generation, which develops in ‘fuzzy’ galls on the central vein on the underside of leaves on live oaks in southeast Texas, Quercus virginiana, represents only one generation in a bivoltine life cycle that alternates with a newly discovered sexual generation that develops in galls on catkins on the same host. Our study highlights the need for detailed inspections of the life cycles of unisexual gall wasp species and we discuss the closure of the A. quercuslanigera life cycle in light of recent advances in the study of the ecology and evolution of heterogony in the Cynipidae.

Trapping the Walnut Twig Beetle to Determine Flight Patterns in Colorado

Abstract. The walnut twig beetle, Pityophthorus juglandis Blackman, and its fungal associate Geosmithia morbida Kolařik et al., produce thousand cankers disease, which has devastated black walnut (Juglans nigra L.) in several states of the western U.S.A. To better understand beetle flight dynamics and life history, flight times were documented in the urban corridor along the Colorado Front Range during 2 years -- in 2008 with yellow sticky card traps and in 2012 with baited multiple funnel traps. Walnut twig beetles were determined to be active throughout the trapping season from March through November, exhibited overlapping generations, and potentially a bivoltine life cycle. Most beetles were collected from traps between July and September, and the greatest trap density frequently occurred in August. The total number of beetles collected throughout the trapping season differed at each location. In 2008 the number of beetles collected ranged from 12 to 145, and from 60 to 12,909 in 2012. More beetles wer...

Adaptive significance of precocious pupation in the bean blister beetle, Epicauta gorhami (Coleoptera: Meloidae), a hypermetamorphic insect

Larvae of the bean blister beetle, Epicauta gorhami Marseul (Coleoptera: Meloidae), feed on grasshopper eggs in soil and undergo hypermetamorphosis. They normally enter diapause as a pseudopupa at the fifth instar, a form characteristic of hypermetamorphosis for meloid beetles. However, fourth-instar larvae exposed to long days and high temperature avoid pseudopupal diapause and pupate directly from the fourth instar. Fourth-instar larvae also tend to pupate precociously with a smaller body size if they are deprived of food. In these larvae, the critical day-length controlling induction of pseudopupal diapause becomes shorter than that for fully-fed larvae. In this study, we examined how the reaction norm of food-deprived E. gorhami larvae functions in nature by rearing insects from the egg stage outdoors in different seasons with manipulation of the food supply. The results indicated that most fully-fed larvae entered pseudopupal diapause, whereas food-deprived larvae tended to pupate precociously without entering diapause, especially early in the season. The resulting smaller adults reproduced early in the autumn and their progeny attained the pseudopupal stage before winter, indicating that the reaction norm may have an adaptive role in controlling seasonal development in the face of food shortages, producing a bivoltine life cycle.

Life cycle and secondary production of two species of Campsurus (Ephemeroptera, Polymitarcyidae) in reservoirs of southeastern Brazil

ABSTRACTThe aim of this paper was to study the life cycle, the annual secondary production, and the spatial and temporal variation of the species Campsurus truncatus and C. violaceus in two reservoirs in Minas Gerais, Brazil. Campsurus truncatus was recorded in 11 months and had a multivoltine lifecycle with a secondary production of 4.61 g.m−2.year−1. Campsurus violaceus was collected in eight months and had a bivoltine lifecycle with a secondary productivity of 1.96 g.m−2.year−1.

Partial bivoltinism and emergence patterns in the North African endemic damselfly Calopteryx exul: conservation implications

AbstractCalopteryx exul is an endemic endangered damselfly that suffers considerable habitat degradation and local extinctions throughout its geographic range. Although recent studies have investigated its distribution, ecology and larval systematics, the life history of the species is still unknown. In this study, a field survey was conducted to determine larval development, temporal pattern of emergence and teneral spatial distribution of the species in the Seybouse watershed, north‐east Algeria. Larval growth was investigated in two populations: one at about 200 m (low‐elevation population) and the second at 600 m of elevation (high‐elevation population). The species showed partial bivoltine life cycle in both low‐ and high‐elevation population. The temporal pattern of emergence of the first flight season of the year at low‐elevation population was asynchronous with an emergence season lasting 46 days and half of the population emerging in 15 days. The second flight season was shorter with a most likely smaller population size. Sex ratio at emergence was slightly male biased. After ecdysis, tenerals stayed next to the water within a mean distance of 4.76 ± 4.35 m (± SD) with no significant difference between sexes. Conservation measures that should be taken into account in the elaboration of future management plans for the species are discussed.

The life histories of Meridialaris chiloeensis (Demoulin, 1955) (Ephemeroptera: Leptophlebiidae) and Gigantodax rufescens (Edwards, 1931) (Diptera: Simuliidae) on a Magellanic sub-Antarctic island (55°S)

ABSTRACTThe life histories of Meridialaris chiloeensis (Demoulin, 1955) (Leptophlebiidae: Ephemeroptera) and Gigantodax rufescens (Edwards, 1931) (Simuliidae: Diptera) were studied in a Magellanic sub-Antarctic river in Navarino Island (55°S). Both species are distributed along the whole length of the watershed. Phenology was studied in the field for a period of 12 months between August 2009 and September 2010, at a site near the river's mouth (sea level). Cumulative degree-days were calculated along the gradient at five representative altitudinal locations, starting at the river's headwaters. Samples were obtained during January of 2010 at all the remaining altitudinal locations to assess possible changes in voltinism during the austral summer season through the watershed. Results show that M. chiloeensis and G. rufescens have a bivoltine and multivoltine life cycle, respectively, at sea level. Based on degree-days obtained and field observations at the remaining stations, possible voltinism patterns are discussed for both species along the altitudinal gradient. These species are proposed as suitable long-term indicators for climate change studies in the sub-Antarctic ecoregion of Magallanes, as monitoring their responses will be important in the interpretation of changes in ecosystem function, community structure, and distributions of aquatic taxa in this region of the world.

Characterization of silk gland ribosomes from a bivoltine caddisfly, Stenopsyche marmorata: translational suppression of a silk protein in cold conditions

Larval Stenopsyche marmorata constructs food capture nets and fixed retreats underwater using self-produced proteinaceous silk fibers. In the Chikuma River (Nagano Prefecture, Japan) S. marmorata has a bivoltine life cycle; overwintering larvae grow slowly with reduced net spinning activity in winter. We recently reported constant transcript abundance of S. marmorata silk protein 1 (Smsp-1), a core S. marmorata silk fiber component, in all seasons, implying translational suppression in the silk gland during winter. Herein, we prepared and characterized silk gland ribosomes from seasonally collected S. marmorata larvae. Ribosomes from silk glands immediately frozen in liquid nitrogen (LN2) after dissection exhibited comparable translation elongation activity in spring, summer, and autumn. Conversely, silk glands obtained in winter did not contain active ribosomes and Smsp-1. Ribosomes from silk glands immersed in ice-cold physiological saline solution for approximately 4 h were translationally inactive, despite summer collection and Smsp-1 expression. The ribosomal inactivation occurs because of defects in the formation of 80S ribosomes, presumably due to splitting of 60S subunits containing 28S rRNA with central hidden break, in response to cold stress. These results suggest a novel-type ribosome-regulated translation control mechanism.