Historical and projected interactions between climate change and insect voltinism in a multivoltine species

Climate change can cause major changes to the dynamics of individual species and to those communities in which they interact. One effect of increasing temperatures is on insect voltinism, with the logical assumption that increases in surface temperatures would permit multivoltine species to increase the number of generations per year. Though insect development is primarily driven by temperature, most multivoltine insect species rely on photoperiodic cues, which do not change from year‐to‐year or in response to climate warming, to initiate diapause. Thus, the relationship between climate change and voltinism could be complex. We use a phenology model for grape berry moth, Paralobesia viteana (Clemens), which incorporates temperature‐dependent development and diapause termination, and photoperiod‐dependent diapause induction, to explore historical patterns in year‐to‐year voltinism fluctuations. We then extend this model to predict voltinism under varying scenarios of climate change to show the importance of both the quality and quantity of accumulated heat units. We also illustrate that increases in mean surface temperatures > 2 °C can have dramatic effects on insect voltinism by causing a shift in the ovipositional period that currently is subject to diapause‐inducing photoperiods.     

Effects of photoperiod and temperature on pupal diapause induction of grape berry moth Lobesia botrana

Abstract. The grape berry moth, Lobesia botrana Denn. & Sciff. (Lepidoptera: Tortricidae), one of the most injurious pest of grape berries in Greece, is a multivoltine species that overwinters as diapausing pupae. The effects of several diel and non-diel photoperiods and of temperature, experienced by eggs and larvae, on pupal diapause induction were investigated. The diapause response curve was of Type I (long day type) and the determining factor was the duration of scotophase (> 11 h), regardless of the duration of photophase. However, at very short (< 4 h) photoperiods, the incidence of diapause was also high. Diapause was positively and significantly correlated with the egg-larval developmental time, pupal mortality and the duration of the pupal stage. Eggs and larvae reared under LD 12 : 12 h photoperiod and various temperatures (from 12 to 30 °C) produced diapausing pupae (almost 100%), but the duration of the pupal stage (intensity of diapause) increased with increasing temperature. Under continuous darkness, however, the percentage diapause decreased with increasing temperature. Single and double 1-h light pulses were applied systematically at various times during the scotophase of six diapause-inducing diel photoperiods. Two photosensitive points in time (called A and B) were revealed, during which illumination resulted in a significant decrease of diapause induction. The decrease was much greater during the first sensitive period (early in scotophase) rather than in the second (late in the scotophase).     

Carbaryl resistance in populations of grape berry moth (Lepidoptera: Tortricidae) in New York and Pennsylvania

We collected grape berry moth, Endopiza viteana (Clemens) (from cultivated and wild Vitis along Lake Erie in Pennsylvania and New York), and measured carbaryl susceptibility in first instars. A model of susceptibility was based on the concentration-mortality curve of laboratory-maintained colonies originating from wild Vitis with no prior history of carbaryl exposure, and a noncommercial vineyard with modest previous exposure to carbaryl. We estimated LC50 and LC90 for susceptible grape berry moth larvae at 45.4 and 2319 microg/ml, respectively. Bioassays on field-collected larvae from commercial vineyards in both states, where grape growers were abiding by current pest management guidelines for carbaryl use, revealed carbaryl resistance ratios from 7 to 71 at the LC50 level. With the loss or restriction of alternative chemical control tactics in the Food Quality Protection Act era, resistance management programs for grape berry moth should be immediately developed and implemented to regain the efficacy of this once effective insecticide and other related chemical compounds.     

Photoperiodism and seasonality in neotropical population of Plutella xylostella L. (Lepidoptera: Yponomeutidae)

Neotropical populations of the diamondback moth Plutella xylostella L. have seasonal cycles of growth and decrease, and moth migration plays a fundamental role in generating such population dynamics. Since the oscillation of these populations is predictable, photoperiod might operate as a signal that triggers the migratory behaviour of the insect. Migration in insects is usually preceded by reproductive diapause, a photoperiodic response that can be characterised by morphological, physiological and behavioural alterations that permit to discriminate between migratory and non-migratory forms. In this study, I tested whether the pre-imaginal and reproductive development of P. xylostella from Minas Gerais (Brazil) is affected by artificial day-lengths that are equivalent to the periods of natural population growth or decrease. No evidence of photoperiodic response was found for the insect reared in laboratory on five different constant photoperiods, from 8h to 16h of light per day. There was no significant variation in survival and duration of egg, larva, and pupa stages or in pupal weight, adult size (forewing length), fecundity, and longevity. Although some species have geographically distinct photoperiodic responses, previous assumptions that cosmopolitan P. xylostella responds to photoperiod in temperate regions was questioned. Migratory and population seasonality among neotropical populations of P. xylostella certainly occurs independently of the photoperiodic announcement of seasonal changes in habitat quality.     

Seasonal pattern of oviposition by the North American grape berry moth (Lepidoptera: Tortricidae)

The seasonal patterns of oviposition by the North American grape berry moth, Paralobesia viteana (Clemens) (Lepidoptera: Tortricidae) were monitored in juice grape (Vitis labrusca) vineyards in southwest Michigan. Egg deposition was recorded throughout the growing season at two vineyards in 2006, and at four vineyards from 2007 to 2009. In each vineyard, a random sample of 100 grape clusters was visually inspected twice‐weekly and the number of newly laid eggs was counted. We found that oviposition was continuous but variable throughout the season. Egg deposition started in early June coinciding with early grape bloom, continued at low level until mid‐ to late July, intensified in August close to veraison, and ended in September often before harvest. There were no consistent periods without oviposition that would indicate distinct generations. To determine the contribution of moth immigration into the vineyard to the pattern of oviposition, six grape plants located at the edge of a vineyard next to woods were covered with field cages and stocked with infested fruit. Oviposition and berry infestation were followed weekly on covered and exposed plants. Although higher numbers of eggs and infested berries were found on fruit of exposed vines than enclosed vines, egg deposition and berry infestation followed the same pattern in both treatments. This result indicates that the seasonal pattern of egg deposition is not dependent on immigration of grape berry moth of wild grape origin. The pattern of oviposition by grape berry moth described here contributes to the difficulty of controlling this pest using conventional insecticides with short residual activity.     

Effect of photoperiod and temperature on diapause in a Florida strain of the tropical warehouse moth Ephestia cautella

A photoperiodically-controlled diapause of the long-day, short-day type was identified in a brown-winged, yellow-eyed strain of Ephestia cautella (Walker). The proportion of larvae diapausing in very long photoperiods was less than in short photoperiods. The mean critical photoperiod, here defined as that photoperiod giving half the maximum percentage of insects that diapause in response to photoperiod at a given temperature, was between 12 and 13 hr for the long-day reaction at both 20 and 25°C. The principal sensitive phase occurred near the time of the last larval moult. The mean duration of diapause was 2–3 months at 20°C and slightly longer at 25°C. The optimum temperature for diapause development was near 15°C, all larvae pupating within 24 days after a 45-day exposure at this temperature. Diapause could be terminated whenever larvae diapausing at 20°C were exposed to as few as five long (15 hr) photoperiods at 25°C. Long photoperiods at 20°C, or short photoperiods (9 hr) at 25°C were less effective in terminating diapause.     

Photoperiodic reaction in the beet webworm Loxostege sticticalis L. (Pyraloidea, Crambidae) from eastern and western parts of its Eurasian range

The beet webworm, Loxostege sticticalis L., is a very dangerous polyphagous insect pest whose outbreaks periodically occur in southern Russia and northern China. The aim of our work was to describe the photoperiodic response of beet webworm populations from western (Krasnodar Territory and Rostov Province) and eastern [Buryatia and China (Hebei Province)] parts of the pest range. The insects were reared under constant photoperiods of 12–18 h and constant temperatures of 19–25°C. Incidence of diapause at different photoperiods did not show any considerable geographic differences, and the critical day length at which 50% of prepupae arrested their development was about 14–15 h in all the populations studied at experimental temperatures. The results obtained agree with the hypothesis on the existence of an area (or areas) where the pest survives during adverse periods and wherefrom it spreads when an outbreak begins (Saulich et al., 1983; Goryshin et al., 1986). Presumably, the larger part of the pest native habitats (to the north of the steppe zone) is occupied by temporary populations, incapable of surviving for long periods without an inflow of migrants from more southerly steppe regions.     

Effect of rearing strategy and gamma radiation on fecundity and fertility of codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae)

The codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) is a serious pest of pome fruit worldwide. In an effort to reduce the use of pesticides to control this pest, the sterile insect technique (SIT) is used or considered for use as a component of area‐wide integrated pest management programmes. Rearing codling moths through diapause has been shown to improve the competitiveness of sterile moths released in orchards, and provides management alternatives that would allow mass‐rearing facilities to increase their yearly production of sterile moths. Because radiosensitivity in insects can be influenced by numerous biological factors, laboratory tests were conducted to examine whether the response to increasing doses of radiation, as expressed in the fecundity and fertility of cohorts of moths, is similar for adult moths mass‐reared through diapause or through standard (non‐diapause) production protocols. Our data revealed that the effect of increasing doses of radiation on fecundity and fertility of codling moths reared through both rearing strategies was similar. In the case of fertility, this is a particularly important finding for the expanded application of codling moth SIT. If mass‐rearing facilities use year‐round diapause rearing, the dose required to treat the insects prior to release will be similar to that used when codling moths are reared through standard production protocols.     

Comparison of three dispenser distribution patterns for pheromone mating disruption of Paralobesia viteana (Lepidoptera: Tortricidae) in vineyards

Over two growing seasons, Isomate GBM-Plus tube-type dispensers releasing the major pheromone component of grape berry moth, Paralobesia viteana (Clemens) (Lepidoptera: Tortricidae), were evaluated in vineyards (Vitis spp.) in Michigan, New York, and Pennsylvania. Dispensers were deployed in three different density-arrangement treatments: 124 dispensers per ha, 494 dispensers per ha, and a combined treatment with 124 dispensers per ha in the vineyard interior and 988 dispensers per ha at the vineyard border, equivalent to an overall density of 494 dispensers per ha. Moth captures and cluster infestation levels were compared at the perimeter and interior of vineyards receiving these different pheromone treatments and in vineyards receiving no pheromone. Orientation of male moths to pheromone-baited traps positioned at the perimeter and interior of vineyards was reduced as a result of mating disruption treatments compared with the nontreated control. These findings were consistent over both years of the study. Disruption of male moth captures in traps varied from 93 to 100% in treated vineyards, with the 494 dispensers per ha application rates providing significantly higher level of disruption than the 124 dispensers per ha rate, but only in 2007. Measurements of percentage of cluster infestation indicated much higher infestation at perimeters than in the interior of the vineyards in all three regions, but in both sample positions there was no significant effect of dispenser density on cluster infestation levels in either year. The contrasting results of high disruption of moth orientation to traps in vineyards that also had low levels of crop protection from this pheromone treatment are discussed in the context of strategies to improve mating disruption of this tortricid pest.     

Biology and ecology of the Northern walkingstick,Diapheromera femorata (Say) (Phasmatodea: Diapheromerinae): A review

The northern walkingstick, Diapheromera femorata (Say), is the only stick insect of economic importance native to the United States. Young nymphs feed on various understory shrubs and trees whereas older nymphs and adults prefer oaks and cherries. Occasionally, field populations reach outbreak levels and cause complete tree defoliation. Widespread damage rarely occurs except those reported from Michigan (1930–1960), Wisconsin (1950–1960) and Arkansas and Oklahoma (1960–1975) where thousands to tens of thousands of hectares of trees were affected. The most recent infestations were detected in Arkansas, Maryland, and Pennsylvania with severe damage observed in localized areas. The morphology, life stages, host species, damage, biology, life history, natural enemies and management of this insect were reviewed. Host preference and insect predation were confirmed in Pennsylvania. Other notable stick insects in the United States and economically important species around the world are discussed to raise awareness about the ecological impacts of this understudied group of mostly nocturnal herbivores.     

Effects of constant and changing temperature conditions on diapause induction in Helicoverpa armigera (Lepidoptera: Noctuidae)

The effects of photoperiod and temperature on the induction and termination of facultative pupal diapause in Helicoverpa armigera (Lepidoptera: Noctuidae) were investigated under laboratory conditions. Exposing H. armigera larvae to both constant and fluctuating temperature regimes with a mean of 25°C and 20°C resulted in a type-III photoperiodic response curve of a short-long day insect. The long-day critical daylengths for diapause induction were ten hours and 12 hours at the constant temperatures of 25°C and 20°C, respectively. Higher incidences of diapause and higher values both for the longer and the shorter critical photoperiods for diapause induction were observed at fluctuating regimes compared with the corresponding constant ones. At alternating temperatures, the incidence of diapause ranged from 4.2% to 33.3% and was determined by the temperature amplitude of the thermoperiod and by the interaction of cryophase or thermophase with the photoperiod. Helicoverpa armigera larvae seem to respond to photoperiodic stimuli at temperatures >15°C and <30°C; all insects entered diapause at a constant temperature of 15°C, whereas none did so at a constant temperature of 30°C under all the photoperiodic regimes examined. Although chilling was not a prerequisite for diapause termination, exposure of diapausing pupae to chilling conditions significantly accelerated diapause development and the time of adult emergence. Therefore, temperature may be the primary factor controlling the termination of diapause in H. armigera.     

Intermittent character of adult diapause in Aelia acuminata (Heteroptera)

The response to photoperiod of field-collected Aelia acuminata was studied by exposing insects to three photoperiodic regimes. After the completion of diapause the insects do not respond to photoperiod: in mid-February the length of the pre-oviposition period is the same under both long and short photoperiods. After the onset of oviposition, insects again become responsive to photoperiod regardless of the time of year: under long day, oviposition lasts until death, whereas under short day the females cease oviposition after about 3 weeks. After a further 2 or 3 months without ovipositing, these females which are still experiencing short-day conditions resume reproduction for a further 4–7 weeks and long-lived individuals have three oviposition periods. A regulatory mechanism is suggested for the alternation between oviposition and diapause.     

Sexual differences in the crucial environmental factors for the timing of postdiapause development in the rice bug Leptocorisa chinensis

Although the regulation of reproductive diapause by environmental factors has been extensively studied in a variety of insect orders, sexual differences in the regulation of diapause are still poorly understood. We examined the effects of environmental factors including photoperiod, temperature and food on the regulation of reproductive diapause in both sexes of the rice bug Leptocorisa chinensis (Dallas) (Hemiptera: Alydidae) in the laboratory and under natural conditions. There was no significant difference in critical daylength (CDL) for diapause induction between the sexes. The CDL corresponded to the daylength in which development of the gonads was suppressed in half the insects caught in the field. Both sexes enter diapause at the same time in successive seasons. In diapause insects, on the other hand, there were sexual differences not only in retention of responsiveness to photoperiod and temperature but also in the food requirement, and these sexual differences lead to different timing of the resumption of reproductive development after overwintering.     

The Influence of Diurnal Temperature Variation on Degree-Day Accumulation and Insect Life History

Ectotherms, such as insects, experience non-constant temperatures in nature. Daily mean temperatures can be derived from the daily maximum and minimum temperatures. However, the converse is not true and environments with the same mean temperature can exhibit very different diurnal temperate ranges. Here we apply a degree-day model for development of the grape berry moth (Paralobesia viteana, a significant vineyard pest in the northeastern USA) to investigate how different diurnal temperature range conditions can influence degree-day accumulation and, hence, insect life history. We first consider changes in diurnal temperature range independent of changes in mean temperatures. We then investigate grape berry moth life history under potential climate change conditions, increasing mean temperature via variable patterns of change to diurnal temperature range. We predict that diurnal temperature range change can substantially alter insect life history. Altering diurnal temperature range independent of the mean temperature can affect development rate and voltinism, with the magnitude of the effects dependent on whether changes occur to the daily minimum temperature (Tmin), daily maximum temperature (Tmax), or both. Allowing for an increase in mean temperature produces more marked effects on life history but, again, the patterns and magnitude depend on the nature of the change to diurnal temperature range together with the starting conditions in the local environment. The study highlights the importance of characterizing the influence of diurnal temperature range in addition to mean temperature alone.     

中华通草蛉自然越冬成虫在长、 短光周期下滞育解除中体内相关酶活力变化

光周期信号在昆虫的环境适应中发挥着重要作用, 昆虫能够通过感受光周期的变化来调节体内生理生化过程, 以适应环境的变化。为明确光周期对中华通草蛉Chrysoperla sinica越冬成虫滞育解除过程中酶活力的影响, 本研究测定了长光周期（15L∶9D）和短光周期（9L∶15D）条件下, 成虫体内过氧化氢酶（CAT）、 超氧化物歧化酶（SOD）、 Na⁺K⁺-ATP酶和乳酸脱氢酶（LDH） 4种重要酶活力的变化。结果表明： 中华通草蛉雌、 雄成虫CAT活性在长光周期处理5 d达最高值后呈下降趋势; 短光周期处理CAT活性在处理5 d达最高值, 且高于长光周期处理, 在处理10 d迅速下降至最低值, 且均显著低于长光周期处理的CAT活性（P=0.005）, 后迅速上升并在处理15 d （P<0.05）和20 d （P<0.005）活性显著高于长光周期处理。雌、 雄成虫SOD活性在长光周期下处理10 d达最高值, 且显著高于对照（P<0.001）, 且除处理5 d雄虫SOD活性与对照无显著性差异外（P=0.558）其余处理活性均显著低于对照（P<0.05）。雌成虫长光周期处理5 d 的SOD活性显著低于短光周期（P<0.001）, 其余处理活性均显著高于短光周期; 雄成虫长光周期下处理的SOD活性均高于短光周期下, 且处理5 d （P=0.04）, 15 d （P<0.001）和20 d （P=0.003）的活性差异显著。两种光周期条件下雌、 雄成虫Na⁺K⁺-ATP酶活性随处理时间延长呈上升-下降-上升趋势, 且均显著高于处理0 d成虫酶活性（P<0.001）; 短光周期处理不同时间Na⁺K⁺-ATP酶活性均高于长光周期处理, 且除雄成虫处理15 d无显著性差异（P=0.142）外, 其余均差异显著（P<0.05）。两种光周期条件下雌、 雄成虫LDH活性随处理时间延长呈下降趋势, 且均显著低于对照（P<0.001）。中华通草蛉越冬成虫在长、 短两种光周期条件下体内酶活力的差异可能是影响两种光周期下成虫滞育解除过程中体内不同生化物质含量与生殖状态的重要因子。     

Projecting insect voltinism under high and low greenhouse gas emission conditions

We develop individual-based Monte Carlo methods to explore how climate change can alter insect voltinism under varying greenhouse gas emissions scenarios by using input distributions of diapause termination or spring emergence, development rate, and diapause initiation, linked to daily temperature and photoperiod. We show concurrence of these projections with a field dataset, and then explore changes in grape berry moth, Paralobesia viteana (Clemens), voltinism that may occur with climate projections developed from the average of three climate models using two different future emissions scenarios from the International Panel of Climate Change (IPCC). Based on historical climate data from 1960 to 2008, and projected downscaled climate data until 2099 under both high (A1fi) and low (B1) greenhouse gas emission scenarios, we used concepts of P. viteana biology to estimate distributions of individuals entering successive generations per year. Under the low emissions scenario, we observed an earlier emergence from diapause and a shift in mean voltinism from 2.8 to 3.1 generations per year, with a fraction of the population achieving a fourth generation. Under the high emissions scenario, up to 3.6 mean generations per year were projected by the end of this century, with a very small fraction of the population achieving a fifth generation. Changes in voltinism in this and other species in response to climate change likely will cause significant economic and ecological impacts, and the methods presented here can be readily adapted to other species for which the input distributions are reasonably approximated.     

Variability in diapause propensity within populations of a temperate insect species: interactions between insecticide resistance genes and photoperiodism

Temperate insects generally use day length as a reliable cue for long-term seasonal changes in their environment. Significant variation in photoperiodism between and within populations is thought to be associated with genetic variation resulting from local adaptation. In this study, we investigated whether genetic variation associated with selection for insecticide resistance may be a source of divergence in the photoperiodic timing of diapause through pleiotropic interactions. Critical photoperiods for diapause induction were estimated in one susceptible and two insecticide-resistant homozygous strains of the codling moth Cydia pomonella , as well as in their reciprocal F₁ progeny. Diapause responses to naturally decreasing day length were subsequently followed in the laboratory strains and in two field populations of C. pomonella in south-eastern France. We found higher critical photoperiods for diapause induction in homozygous resistant individuals than in both homozygous susceptible and heterozygous ones. This partly explained the significantly earlier timings of diapause found in homozygous resistant individuals of both laboratory and field populations of C. pomonella under natural photoperiods, relative to those found in both homozygous susceptible and heterozygous ones. We assume that adaptive genetic changes associated with selection for insecticide resistance may generate substantial variation in the seasonal timing of diapause, an essential ecological feature of the fitness of insecticide resistance genes in this species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 341–351.     

Diapause induction in the codling moth, Cydia pomonella: effect of prediapause temperatures

The effect of four prediapause temperatures (18, 22, 26 and 30°C) on the photoperiodic response of the codling moth, Cydia pomonella (L.), was studied under controlled conditions. The highest rates of diapause were recorded, for all day-lengths, at temperatures of 22 and 26°C while relatively lower rates of diapause were elicited at 18 and 30°C. The same trend was demonstrated by projecting the values of the critical photoperiod which induces 50% diapause (=CPhP₅₀) over the prediapause temperature. The change in diapause incidence as a function of photoperiod, at all prediapause temperatures, exhibited a response characteristic of long-day insects, i.e. high rates of diapause at short days (12–13.5 h) and a decrease in diapause incidence at long days (14–15 h). The results for temperatures 22, 26 and 30°C support the view that lower prediapause temperatures enhance diapause induction, at a give photoperiod, while higher temperatures tend to avert or diminish the process. On the other hand, the low rates of diapause obtained at 18°C contradict this view. Nevertheless, high correlation was found between the laboratory evidence and field data, indicating the adaptability of the Israeli codling moth to subtropical climate.     

Changes of biogenic amine levels in haemolymph during diapausing and non-diapausing status in Pieris brassicae L

During the larval development of Pieris brassicae, photoperiod status induces either direct (non-diapausing) development or diapausing development. Biogenic amines such as dopamine and serotonin and their derivatives may be implicated in the physiological control and adaptation of these insects to different photoperiods. High performance liquid chromatography coupled with electrochemical detection was used to measure biogenic amine concentrations in insect haemolymph in different photoperiod conditions. At the end of the higher photosensitivity phase, dopamine levels were two-fold higher in diapausing (0.914 pmol/microl+/-0.025) as compared to non-diapausing insects (0.415 pmol/microl+/-0.02; P<0.001). Globally, dopamine catabolites are found in higher levels in non-diapausing insects (in prepupa, near seven times more for NADA, and 25 times more for DOPAc), thus indicating a higher dopamine turn-over. Serotonin levels were detected only at the beginning of this instar in diapausing insects but not in direct development insects. During pupal life, dopamine levels were significantly higher in diapausing than in non-diapausing insects (in 3-day pupae, dopamine was 28 times higher), and remained at high levels throughout diapausing life. At the beginning of diapause, serotonin levels were higher in diapausing insects than in non-diapausing insects (in 3-day pupae, serotonin was 13 times higher). These levels decreased in the middle of diapause period, and then increased just before its breaking. Dopamine and serotonin levels presented the typical kinetics of diapause development and may be used as an indicator of the evolution of diapause status.     

Fate of codling moth (Lepidoptera: Tortricidae) in harvested apples held under short photoperiod

Codling moth, Cydia pomonella L., is a cosmopolitan pest of pome and stone fruits. It has been identified as a quarantine pest of concern in a number of countries where it is not known to occur, most of them tropical or subtropical countries. Although considerable work has been done on the basic biology and physiology of this temperate pest, little is known on its potential to develop and establish in tropical environments with short photoperiods and few to no days below 10 degrees C. Apples were harvested over three field seasons (2007-2009) from unmanaged orchards in central Washington State and subjected to simulated commercial cold storage at 1.1 +/- 2 degrees C for up to 119 d. After cold storage, infested fruits were held at 20 degrees C under a 12:12 L:D photoperiod for up to 6 mo. Over the entire experiment only 27% of the larvae collected exited the fruit and cocooned. Of those 27%, only 1.06% of larvae held under a 12:12 L:D photoperiod successfully emerged as moths. No moths emerged when host fruit would be available in a representative importing country in the tropics over the 3 yr of testing. These results indicate that codling moth in apples from the Pacific Northwest pose little threat of surviving and establishing in tropical regions where daylength is insufficient to break diapause and the chilling requirement is not met.