Study of intrapopulational variability of duration and temperature norms of development of the linden bug Pyrrhocoris apterus (Heteroptera, Pyrrhocoridae)

The existence of significant variability in duration and temperature norms of development between families within insect populations has been shown for the first time. This variability is inferfamily and therefore has genetic ground. Revealed for the first time is the statistically significant positive correlation between the regression coefficient of the development rate for temperature and the temperature threshold for development of eggs and larvae from different families. The greater the slope of the regression line of the development rate for temperature, the higher the temperature threshold value in this particular family. These results demonstrate for the first time the existence of genetic co-variation between the regression coefficient and the temperature threshold within the insect populations. It is suggested that the source of the interpopulational and interspecies changes in the temperature reaction norms of the insect development might be the intrapopulational hereditary variability of the development duration, regression coefficient, and the development threshold, this variability being an object of natural selection. It was shown that in all studied families and populations the values of the linear regression coefficient of development rates for temperature in eggs of the linden bug Pyrrhocoris apterus were markedly and statistically significantly higher, while the temperature threshold values—lower as compared with the corresponding parameters in larvae. These results obviously are in contradiction with the concept of the “isomorphism of development rates” (Jarosik et al., 2002), according to which the development threshold for all life cycle stages of a species should be the same, whereas only slopes of the regression lines of the development rate for temperature can differ. For the first time the absence of genetic covariation has been shown between the temperature norms of development of different life cycle stages of the species—eggs and larvae. This means that the regression coefficient as well as the sum of the degree-days and the development threshold in eggs and larvae are inherited independently and therefore they can be independently changed in evolution in correspondence with specific environmental conditions, under which these life cycle stages take place.     

始红蝽越冬聚集行为对其能量代谢的影响

聚集行为是动物适应不良环境的一种生态对策。始红蝽Pyrrhocoris apterus在成虫滞育越冬期间具有显著的聚集行为。采用LI-6400型光合仪测定了5种聚集度(分别用1头、5头、10头、20头和50头的群体大小表示)下始红蝽的呼吸量,通过呼吸量计算得到各聚集度始红蝽的呼吸速率(rate of respiration,Rr)及能量代谢速率(rate of metabolism,Rm),旨在明确聚集行为是否能够对始红蝽越冬时的能量代谢产生影响。结果表明： 不同聚集度间始红蝽的Rm值存在显著性差异; 并且随聚集度的增加,Rm值与聚集度呈显著负相关,Rm值依次为0.052,0.044,0.041,0.037和0.033 W/g。结果说明聚集行为可以有效降低始红蝽新陈代谢速率,有利于种群成功越冬。     

Feeding behaviour, digestive physiology and lipid content in macropterous females of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae)

Abstract. Macropterous females of Pyrrhocoris apterus (L.) reared under short-day conditions (LD 12:12 h) were analysed for temporal patterns of feeding and drinking behaviour, activities of digestive enzymes in the gut, and lipid and glycogen content in the haemolymph and fat body. Peaks of drinking activity were recorded at days 3, 7 and 10 during the first 14 days after imaginal ecdysis. Feeding activity peaked on the third day, ceasing completely after the fourth day of adult life. Esterase, protease, amylase and aminopeptidase activities exhibited the highest overall activity in the first days after imaginal emergence; then enzyme activities decreased. In the fat body, the content of lipids was highest on day 5, then a decrease of about 40% was observed at day 14; the amount of glycogen was highest on day 1 at 11 μg of glucose equivalents/mg of fat body, then decreased to 2 μg at day 14 after the imaginal moult. In the haemolymph, the lipid content rose until day 8 when it reached almost 0.3 μmol/μl; at day 14 the value was slightly lower. The association of fasting with reproductive arrest in macropterous females of P. apterus, accompanied by a decrease in digestive enzyme activities and a mobilization of lipid reserves from the fat body, was demonstrated.     

How climate change affects the occurrence of a second generation in the univoltine Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae)

1. Understanding the conditions that allow for the occurrence of an additional generation in populations that are usually univoltine is important under the present climate warming. In temperate areas, a second generation is enabled through the emergence of a time window that opens when first-generation individuals are ready to reproduce and closes when second-generation individuals cannot complete development before the onset of winter. 2. The conditions that limit the width of this window were studied in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae), a ground-inhabiting heteropteran overwintering in facultative adult diapause, whose populations in Central Europe have typically been univoltine until the 1980s. 3. The frequency of females of the first generation that started to lay eggs decreased from 70% in June to zero in early August, but oviposition of these females continued until the end of August. Using thermal constants for egg–adult development and temperature data, this study found that the development of most second-generation individuals could only be completed before the start of winter if hastened through behavioural thermoregulation. 4. Consequences of temperature increase on the width of the thermal window were calculated. Increasing temperature causes the time window to open earlier and close later by accelerating maturation of first-generation females and improving conditions for maturing of the second-generation individuals in late summer and autumn. 5. Climate warming will create conditions that facilitate the occurrence of a second generation in a year in typically univoltine populations of this species.     

Analysis of pteridines in Pyrrhocoris apterus (L.) (heteroptera,pyrrhocoridae) during development and in body-color mutants

By using thin-layer chromatography (TLC) and high-performance liquid chromatography (HPLC), five different pteridines have been quantified in extracts from Pyrrhocoris apterus: neopterin, isoxanthopterin, isoxantholumazine (violapterin), 7-methylxanthopterin, and erythropterin. Biopterin was also detected using HPLC. Pteridines have been analyzed separately in bodies and eyes of the wild type regarding developmental stage and sex. The pteridine content in both bodies and eyes increased from nymphs to 2-day-old adults. After this period, the concentration of pteridines in the eyes of adults remained approximately constant, while in the bodies isoxantholumazine, 7-methylxanthopterin, and isoxanthopterin kept increasing until 20 days. Considering the total amount of pteridines per insect, no qualitative or quantitative differences between males and females have been observed except a lower concentration of erythropterin in female bodies. But when pteridines are analyzed per unit body weight, a lower amount of pteridines is always detected in females due to its bigger size. A new body-color mutant, the yolk body mutant, that goes through developmental colour changes, was also analyzed during development, showing a general deficient accumulation of all pteridines, especially of 7-methylxanthopterin and isoxantholumazine in adult bodies. The effect on pteridine content of three other recessive (white, yellow, mosaic) and two dominant (Pale and Apricot) body-color mutations, has also been studied. A specific pteridine pattern different from the wild type was obtained for each mutant. © 1997 Wiley-Liss, Inc.     

Effect of temperature on photoperiodic response in a selected 'non-diapause' strain of Pyrrhocoris apterus (Heteroptera)

Abstract. The artificially selected 'non-diapause' strain of Pyrrhocoris apterus (L.) (Heteroptera) showed no diapause response to photoperiod at 26°C (Socha & Hodkova, 1994). However, the diapause response to short-day photoperiod (LD 12:12 h) became apparent at lower temperatures of 17°C (70% diapause) or 20°C (41% diapause). Diapause was induced in 60% females by short-day photoperiod combined with thermoperiod of 26/16°C, whereas only 20% diapause was induced by the same thermoperiod under continuous darkness. Thus the time-measuring system was not removed by artificial selection but the diapause response was shifted to lower temperatures. The diapause response to short days seems to be favoured rather by low temperature during scotophase than by low temperature throughout the whole light/dark cycle. If the percentage of diapause at 26°C is compared in F₁ hybrids and in wild and selected parental strains the diapause appears to be dominant at LD 13:11 h but recessive at LD 11:13 h and LD 10:14 h. A hypothesis is proposed that the inheritance of the percentage of diapause in F1 hybrids is determined by interactions of genes controlling the temperature dependence of photoperiodic response.     

Wing Movement Behavior in Long- and Short-Winged Morphs of the Flightless Bug Pyrrhocoris apterus L. (Heteroptera: Pyrrhocoridae)

The aim of the present paper was to study, with the use of video-recordering and computerized methods, the flight and wing movement behavior in two wing morphs of the flightless bug Pyrrhocoris apterus during the first 14 days of their adult life. We demonstrated the capability of macropterous males and females of this heteropteran to flap their fore- and hindwings for the first time. Flight was not observed in any of the tested males and females. We revealed that wing flapping does not occur earlier than on the fourth and fifth day after adult emergence in males and females, respectively. Time-series analysis of the obtained data showed that the maximum activity of wing flaps is limited to the light phase of the 12-h light/12-h dark photocycle, with the peak occurring in the morning, i.e., about 3 h after turning the light on. No substantial differences in the peaks of wing flapping activities in males versus females were found. The present paper is the first experimental demonstration of wing flap activity in a representative species with a nonfunctional alary polymorphism.     

Feeding, drinking and digestive enzyme activities in long- and short-day females of Pyrrhocoris apterus (Heteroptera)

Abstract. .Reproducing females of the firebug, Pyrrhocoris apterus (Linnaeus) (Heteroptera: Pyrrhocoridae), reared under long-day (LD 18:6h) photocycle (long-day females), and diapausing females reared under short-day (LD 12:12h) conditions (short-day females) were analysed for temporal patterns of feeding, drinking and gut digestive enzyme activities. In long-day females the highest activities of feeding and drinking were found at the beginning of each reproductive cycle. Significant correlation between feeding and drinking activities in both reproducing long-day females and short-day females during pre-diapause state was found. In pre-diapausing short-day females the cyclical pattern of feeding and drinking was maintained despite the inhibition of reproduction. After entering the diapause their feeding activity became very low. Analysis of five gut enzymes revealed that short-day females differ significantly from long-day females in higher protease, amylase and esterase activities, in case of lipase only at certain times of their adult life; no significant difference was found in the aminopeptidase activity. Positive correlations between intensity of feeding and gut enzyme activities were observed in short-day females. Using several protease inhibitors most protease activity in the gut of P.apterus was identified as cysteine and aspartyl proteases, and only a small part of the activity could be caused by some serine proteases.     

The first proof of a possibility of change of temperature norms of insect development as a result of artificial selection for fast or slow development by the example of the red soldier bug <Emphasis Type="Italic">Pyrrhocoris apterus</Emphasis> (Heteroptera,Pyrrhocoridae)

For 3–4 generations, selection of the nymphs most rapidly and slowly developing at 28°C was performed in four families of the red soldier bug Pyrrhocoris apterus L. In each generation, duration of development of nymphs was determined at 5 constant temperatures from 20°C to 28°C. From these data the linear regression coefficient of the development rate against temperature (the development thermolability coefficient) for each generation was calculated. As a result of the selection the average duration of the nymph development was shortened or increased statistically significantly depending on its direction. The artificial selection for the development duration has been established to change not only this parameter, but also the temperature norms of the insect development. At selection for fast development the regression straight line slope (i.e., the regression coefficient value) increased statistically significantly, i.e., development became more dependent on temperature. As a rule, the temperature threshold of development increased. At selection for slow development the values of the regression coefficient and of the threshold decreased, but these differences were not statistically significant. The effect of artificial selection for the development duration on temperature norms of insect development has been revealed for the first time.     

Differences in adipokinetic response of Pyrrhocoris apterus (Heteroptera) in relation to wing dimorphism and diapause

Three experimental groups of adult females (reproductive and diapausing brachypters, and macropters with reproductive arrest) of Pyrrhocoris apterus (Linnaeus) (Heteroptera: Pyrrhocoridae) from a temperate population were analysed for their adipokinetic responses. The adipokinetic response, expressed as an increase of haemolymph lipids after injection of adipokinetic hormone from Locusta migratoria (Lom-AKH-I), was assessed in relation to age, wing dimorphism and type of reproductive arrest. Two pmols of Lom-AKH-I were used for determination of adipokinetic responses. The increase of haemolymph lipids in all experimental groups of females induced by this dose of the hormone was comparable with that induced by crude extract of the bug’s own corpora cardiaca. The level of adipokinetic response after injection of 2 pmol of Lom-AKH-I was significantly higher in macropterous and diapausing brachypterous females than in reproductive brachypterous females. However, significantly higher contents of haemolymph lipids in control macropterous females than those found in the control reproductive and diapausing brachypterous females of the corresponding age revealed wing-morph-related differences in lipid metabolism. The observed wing morph- and diapause-related differences in the content of haemolymph lipids and adipokinetic response, respectively, are discussed in relation to the different roles of two wing morphs in the life history of this heteropteran.     

Behavioral regulation of developmental cycle in Pyrrhocoris apterus L. (Heteroptera: Pyrrhocoridae)

Summary During the warm season the larvae of Pyrrhocoris apterus select in their natural habitats places with temperatures which do not exceed 24°C on average even at the hours of maximum sunshine. At the same time other places of their habitats have temperatures up to 50°C. This active behavioral selection of the microclimate regulates the speed of P. apterus development and entertains the monovoltine cycle in climatic, conditions of Central Europe. A less rigorous choice of the microclimate, even when higher temperatures were tolerated and the development was not disturbed by them, would cause the disturbance of the monovoltine cycle and would probably endanger the survival of the population.     

Wing morph-related physiological differences in adults of temperate population of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae)

The reproductive and diapausing adult females of brachypterous morph and macropterous females with reproductive arrest of non-diapause type, originating from the laboratory cultures of Pyrrhocoris apterus, were studied for their feeding and drinking behaviour, digestive enzyme activities, and carbohydrate and lipid contents. The highest feeding and drinking activities were observed in reproductive brachypters, the lowest in macropters. Macropters also differed from brachypters by lower activities of gut lipase, peptidase and protease, lower concentration of haemolymph sugars, and lower weight of fat body, which probably reflects their low feeding activity. The total content of fat body lipids was also lower in macropters (0.6 mg) than in reproductive and diapausing brachypters (4.6 and 7.5 mg, respectively) on day 14. A very high amount of glycogen was found in the fat body of diapausing brachypters, 363 micrograms on day 14, as opposed to 15 and 80 micrograms in macropterous and reproductive brachypterous females, respectively. The obtained data indicate that the most important difference between macropterous and brachypterous females with different types of reproductive arrest consists of an enhanced mobilization of lipids for dispersal in macropters and accumulation of energetic reserves for hibernation in brachypters.     

Regulation of body size in a heteropteran bug, Pyrrhocoris apterus

The determination of body size (length or weight) of teneral adults of Pyrrhocoris apterus L. was investigated. About 50% of size variation was determined already in the egg stage (average egg weight adult length correlations were 0.67 in males and 0.71 in females). During the larval development, starvation, low temperature, and pollution by excreta combined with crowding reduced adult size and usually increased the development length. The effects were directly proportionate to the length of the stress period, and increased with larval age. Photoperiod or intrinsic variation of development time did not affect adult size. The effects of stress were largely compensated when it was followed by a period of compensation growth at optimum conditions. A dramatic reduction of size appeared when last inster larvae starved and moulted to adults without access to food. Average adult weight was then reduced by up to 48%. Threshold weight for adult moulting was 18 mg, being attained after 1–2 day feeding of the last instar.

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Zusammenfassung Die Körpergrösse bei den Imagines eines Wildstammes der Feuerwanze Pyrrhocoris apterus wurde teilweise durch die Veränderlichkeit der Eigrösse determiniert, teilweise auch durch Hungern der Larven, niedrige Temperatur und metabolischen Produkten beeinflusst. Der Effekt letzterer Faktoren stieg mit deren Dauer und war je grösser desto näher sich die Wirkungsperiode zur Imaginalhäutung befand. Unterschiedliche Photoperioden wirkten auf die Körperlänge nicht. Wurden die Larven zwischen der ungünstigen Periode und der Imaginalhäutung noch den optimalen Bedingungen ausgesetzt, kompensierten sich die negativen Einflüsse weitgehend. Zu einer drastischen Verkleinerung der Imagines kam es nur, wenn das letzte Larven-stadium mit Hunger beeinflusst wurde und bis zur Imaginalhäutung keinen Zutritt zum Futter hatte. Minimales Gewicht, wo die Metamorphose der Larven noch möglich war, wurde zu 18 mg festgestellt.

     

Locomotor activity in adult Pyrrhocoris apterus (Heteroptera) in relation to sex, physiological status and wing dimorphism

The pattern of locomotor (walking) activity was studied in adult males and females of short‐winged (brachypterous) and long‐winged (macropterous) morph of the flightless bug Pyrrhocoris apterus (Linnaeus) (Heteroptera: Pyrrhocoridae) under constant laboratory conditions. Walking activity was measured with a computerized video system and analysed with respect to sex, physiological status (reproduction, diapause and reproductive arrest of non‐diapause type) and wing dimorphism of the bugs. The largest duration was observed in the macropterous females with reproductive arrest of non‐diapause type (average 6 h per day) and the shortest duration in diapausing brachypterous females and males (average less than 2 h per day). This was reflected also in the overall time spent by walking during the first 14 days after imaginal ecdysis. The time spent by walking significantly increased in the macropterous morph as the bugs aged, whereas in diapausing brachypters the time spent by walking decreased with age. No linear relationship between walking activity and age was found in reproductive brachypterous morph. The bugs of all experimental groups moved mostly during the photophase and were almost inactive during the scotophase. Thus, walking activity in P. apterus is diurnal, irrespective of the wing morph, physiological status, sex and age. Contrary to the macropterous morph, where the locomotor activity of females during photophase was significantly higher than in males, no significant differences were found between the locomotor activities of brachypterous males and females. The observed differences in locomotor activity are discussed in relation to different roles of two wing morphs in the life history of this heteropteran.     

The effect of allatectomy and photoperiod on the supercooling point in Pyrrhocoris apterus adults

Abstract Adults of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae) reared at 26°C had a considerably lower supercooling point (SCP) in diapause-inducing (LD 12:12 h) than in diapause-inhibiting (LD 18:6 h) photoperiodic regimes. Exposure of the insects to diapause-inducing acclimation conditions (LD 8:16 h and a temperature of 20°C during photophase and 5°C during scotophase) for 2–3 weeks had very little effect on the SCP, irrespective of the rearing photoperiod. Allatectomized adults kept continuously at LD 18:6 h and 26°C had high SCP similar to intact or sham-operated insects. In contrast to non-allatectomized insects, the SCP of allatectomized insects decreased after an exposure of from 2 to 3 weeks to diapause-inducing acclimation conditions (see above) almost to the level found in the intact diapausing insects. The relationship between the decrease of SCP and ‘diapause syndrome’ (de Wilde, 1970) is discussed.     

Altered anteroposterior polarity of micropyle ring formation in the eggs of Pyrrhocoris apterus L. (Heteroptera : Pyrrhocoridae)

The anterior pole of the normal eggs of Pyrrhocoris apterus (Heteroptera : Pyrrhocoridae) carries a ring of aeromicropyles. In DMR (double micropyle ring) eggs, an additional aeromicropyle ring occurs on the posterior egg pole. The number of micropyles forming this supernumerary ring varies, being usually considerably lower than that observed in the normal (anterior) ring. More than 6% of eggs laid by the Apricot (Ap) mutant of P. apterus are of the DMR type. Reciprocal crosses between the wild-type and Ap homozygous bugs demonstrate a maternal effect of the Ap mutation on the DMR egg production. Since DMR eggs are segregated at a low frequency in the wild-type strains as well as in all analyzed mutations of the bug, the DMR trait is most probably not primarily coded by the Ap gene. Physiological mechanisms involved in the formation of DMR eggs and the correlations between altered egg shell morphology and embryogenesis are also discussed.     

The effect of adipokinetic hormone on midgut characteristics in Pyrrhocoris apterus L. (Heteroptera)

Digestive processes and the effect of adipokinetic hormone (Pyrap-AKH) on the amount of nutrients (lipids, proteins, and carbohydrates), and on the activity of digestive enzymes (lipases, peptidases, and carbohydrases) were studied in the midgut of the firebug, Pyrrhocoris apterus. The analyses were performed on samples of anterior (AM), middle (MM) and posterior (PM) midgut parts. The results revealed that the digestion of lipids, carbohydrates and proteins take place in the acidic milieu. The Pyrap-AKH treatment increased significantly the level of lipids and proteins in the midgut, and also the level of triacylglycerols (TGs) predominantly in the AM, and the level of diacylglycerols (DGs) in the MM. The increase was not uniform for all present TG and DG species - those containing the linoleic fatty acid were predominant. No hormonal effect on lipase activity was recorded, while peptidase and glucosidase activity was increased in the MM and PM. All these facts indicate that the Pyrap-AKH probably stimulates digestion by more intensive food ingestion or turnover, and perhaps by the stimulation of metabolite absorption; the activation of digestive enzymes seems to be secondary or controlled by other mechanisms.     

Voltinism and seasonal changes in haemolymph protein pattern of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae) in relation to diapause

Abstract. The red firebug, Pyrrhocoris apterus (L.), was shown not to be strictly a monovoltine species in Czechoslovakia. A second generation arises from eggs laid by females emerging between June and the beginning of August. Oviposition takes place before diapause is induced in the females by shortening of photophase. Adults that moult later, enter diapause without having laid eggs.
Electrophoretic patterns of haemolymph proteins of adults collected in the field throughout a year showed a characteristic temporal pattern of changes correlated not only with the stages of ovarian development, but also with the progression of diapause and post-diapause quiescence. The changes mainly concerned vitellogenin and polypeptides of molecular weight 78 and 80 kDa.
Vitellogenin was present only in the haemolymph of reproductive females. The polypeptides of 78 and 80 kDa, belonging to the group of storage proteins, accumulated conspicuously in the haemolymph of adults undergoing diapause and post-diapause quiescence. However, the occurrence of these polypeptides seems not to be connected exclusively with cold, because their titres increased with the length of diapause development, even in diapausing adults reared in the laboratory at a constant 26.C     

Topical application of Pya-AKH stimulates lipid mobilization and locomotion in the flightless bug, Pyrrhocoris apterus (L.) (Heteroptera)

Abstract Two different methods of applying Pya -AKH to long-winged (macropterous) females of the firebug, Pyrrhocoris apterus (Linnaeus) (Heteroptera) were compared: both injection and topical application increased the levels of lipids in the haemolymph and stimulated locomotor activity. Lipid mobilization was maximal when 10 pmol was applied by injection or 40–100 pmol by topical application, with the first significant responses occurring 1.5 h after injection and 2 h after topical application. The highest elevations of lipid concentration in the haemolymph were comparable between the treatments, i.e. 14.36 ± 3.59 mg/mL for injection and 14.43 ± 4.07 mg/mL for topical application. However, these maximal elevations were achieved at different times: 3 h after the injection and 7 h after the topical application.
Injection of 10 and 40 pmol of Pya -AKH stimulated locomotor activity with maximal activity 3 h later but, surprisingly, injection of 80 pmol showed no effect initially and than a slight inhibitory effect after 6–8 h.
Increased locomotor activity was found after topical application of Pya -AKH, but the response was lower than after injection and appeared later, 5–9 h after the hormone application. In addition, the greatest increase in walking activity required topical application of 300 pmol and was still less dramatic than the response to injection. The stimulatory effect of Pya -AKH on locomotion was positively correlated with its effect on lipid mobilization only for injection of the hormone. It is argued that a stress caused by injection could play a role in the appearance of the complex response to adipokinetic hormone.     

The first proof of a possibility of change of temperature norms of insect development as a result of artificial selection for rapid or slow development by the example of the red soldier bug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae)

For 3-4 generations, selection of the most rapidly and slowly developing nymphs at 28 degrees C was performed on four families of the red soldier bug Pyrrhocoris apterus L. In each generation, duration of development of nymphs was determined at 5 constant temperatures from 20 degrees C to 28 degrees C. From these data there were calculated the linear regression coefficient of the development rate for temperature (the coefficient of the thermolability of development) and the temperature development threshold for each generation. As a result of the selection the mean duration of the nymph development was shortened or increased statistically significantly depending on its direction. The artificial selection for the development duration has been established to change not only this parameter, but also the temperature norms of the insect development. At selection for rapid development the regression line scope (i. e., the regression coefficient value) increased statistically significantly, i. e., development became more dependent on temperature. The temperature threshold of development increased. At selection for slow development the values of the regression coefficient and of the threshold decrease, but these differences were not statistically significant. The effect of artificial selection for duration of development on temperature norms of insect development has been revealed for the first time.