Effect of ambient temperature on mechanosensory host location in two parasitic wasps of different climatic origin

Abstract.  Several parasitic wasps of the Pimplinae (Ichneumonidae) use self-produced vibrations transmitted through plant substrate to locate their concealed immobile hosts (lepidopteran pupae) by reflected signals. This mechanosensory mechanism of host location, called vibrational sounding, depends on the physical characteristics of the plant substrate and the wasp's body and is postulated to depend on ambient temperature. Adaptations of two parasitoid species to thermal conditions of their habitats and the influence of temperature on the trophic interaction during host location are investigated in the tropical Xanthopimpla stemmator (Thunberg) and compared with the temperate Pimpla turionellae (L.). Plant-stem models with hidden host mimics are offered to individual wasps under defined temperature treatments and scored for the number and location of ovipositor insertions. Significant effects of temperature are found on host-location activity and its success. The tropical species possesses an optimum temperature range for vibrational sounding between 26 and 32 °C, whereas the performance decreases both at low and high temperatures. The temperate species reveals substantial differences with respect to performance at the same thermal conditions. With increasing temperature, P. turionellae shows a reduced response to the host mimic, reduced numbers of ovipositor insertions, and decreased precision of mechanosensory host location. In the tropical X. stemmator , the female wasps are able to locate their host with high precision over a broad range of ambient temperatures, which suggests endothermic thermoregulation during vibrational sounding. Environmental physiology may therefore play a key role in adaptation of the host location mechanism to climatic conditions of the species' origin.     

Ambient temperature affects mechanosensory host location in a parasitic wasp

Certain parasitic wasps (Ichneumonidae, Pimplinae) use self-produced vibrations transmitted on plant substrate to locate their immobile concealed hosts (i.e. lepidopteran pupae). This mechanosensory mechanism, called the vibrational sounding, depends both on physical cues of the environment and physical activity of the parasitoid and is postulated to depend on ambient temperature. We analysed the influences of temperature on vibrational sounding by choice experiments using plant-stem models with hidden host mimics in the temperate species Pimpla turionellae. The results show a significant effect of temperature on host-location activity and on the success of this process. Outside an optimum range, the performance of the wasps decreased both at low and high temperatures. Below 10°C and beyond 24°C, the wasps displayed (1) substantial reduction in responsiveness, i.e. proportion of females showing ovipositor insertions, (2) reduction of quantitative activity with ovipositor insertions in the individuals, and (3) reduced precision of mechanosensory host location. Nevertheless, female wasps were able to locate their host over a surprisingly broad range of ambient temperatures which indicates that the wasps are able to compensate for temperature effects on vibrational sounding.     

Adjustment of vibratory signals to ambient temperature in a host-searching parasitoid

Abstract.  Certain ichneumonid parasitoids (Hymenoptera) use self-produced vibrations transmitted on plant substrate, so-called vibrational sounding, to locate their immobile concealed pupal hosts. An ambient temperature dependency with higher frequencies and intensities at higher temperatures is postulated because signals are of myogenic origin. Here, temperature influence on vibratory signals is analysed in the temperate parasitoid Pimpla turionellae under different thermal conditions using plant-stem models to elicit host-searching behaviour. Signals are measured with laser Doppler vibrometry and analysed for time parameters and frequency components applying fast-Fourier transformations. The results reveal an unexpected effect of ambient temperature on signals produced by the female wasps. Although average values of time parameters (pulse trains, pulse train periods, inter pulse duration) are unchanged by ambient temperature, the frequency parameters show an inverse thermal effect. Within the temperature range tested (8–26 °C), decreasing temperature leads to significantly higher frequency and intensity of the self-produced vibrations in the temperate species. This inverse thermal effect may be explained by a temperature-coupled signal production in the frequency domain to compensate negative low-temperature effects on the mechanoreceptors by increased muscle activity. The option of heterothermy to produce signals reliably during vibrational sounding under low temperature is also discussed.     

Thermoregulation in the primitively eusocial paper wasp, Polistes dominulus

Regulation of wing muscle temperature is important for sustaining flight in many insects, and has been well studied in honeybees. It has been much less well studied in wasps and has never been demonstrated in Polistes paper wasps. We measured thorax, head, and abdomen temperatures of inactive Polistes dominulus workers as they warmed after transfer from 8 to ~25°C ambient temperature, after removal from hibernacula, and after periods of flight in a variable temperature room. Thorax temperature (T _th) of non-flying live wasps increased more rapidly than that of dead wasps, and T _th of some live wasps reached more than 2°C above ambient temperature (T _a), indicating endothermy. Wasps removed from hibernacula had body region temperatures significantly above ambient. The T _th of flying wasps was 2.5°C above ambient at T _a = 21°C, and at or even below ambient at T _a = 40°C. At 40°C head and abdomen temperatures were both more than 2°C below T _a, indicating evaporative cooling. We conclude that P. dominulus individuals demonstrate clear, albeit limited, thermoregulatory capacity.     

The adaptive significance of host location by vibrational sounding in parasitoid wasps

Vibrational sounding, which is a form of echolocation, is a means of host location by some parasitoid wasps. The wasp taps the substrate (wood, stem or soil) and detects the position of a potential host through the returning 'echoes'. The deployment of vibrational sounding is inferred through the form of the subgenual organ in the female tibia in combination with the presence of modifications to the female antenna used for tapping the substrate. Vibrational sounding and its associated modifications were found in two families. The use of vibrational sounding by parasitoid wasps was positively correlated with the depth of the host in the substrate relative to the size of the parasitoid. There were also significant correlations between the use of vibrational sounding and parasitism of immobile and concealed hosts and between vibrational sounding and idiobiosis. The data suggested that vibrational sounding evolved under a variety of ecological conditions, being employed in the location of wood-boring, stem-boring, soil-dwelling and cocooned hosts and stem-nesting aculeates, often in situations in which the host does not produce vibrations itself.     

Effect of temperature and host stage on performance of Aphelinus varipes Förster (Hym., Aphelinidae) parasitizing the cotton aphid, Aphis gossypii Glover (Hom., Aphididae)

Development time, mummification, pupal mortality, host feeding and sex ratio of a Norwegian strain of Aphelinus varipes Förster parasitizing the cotton aphid, Aphis gossypii Glover were studied at 20, 25 and 30°C in controlled climate cabinets. Petri dishes with cucumber ( Cucumis sativus L) leaves on agar were used as experimental units. Cotton aphids in different larval instars and as adults, reared at the three different temperatures, were presented to A. varipes in a `no-choice' situation for 6 h. These presentations were done at 25°C in each experiment to avoid an influence of temperature on parasitization rate. More first instar aphids were parasitized than third and fourth instars among the aphids reared at 20°C. Pupal mortality of the parasitoid was not influenced by temperature. It was lower in aphids parasitized as adults than in aphids parasitized in second instar. The sex ratio of A. varipes was female-biased, and varied between 92% females developed from aphids reared at 25°C and 70% from aphids reared at 20°C. The sex ratio was not significantly influenced by host stage. The development time of A. varipes ranged from 17.5 days at 20°C to 9.8 days at 30°C.     

Host Location of a Pupal Parasitoid in a Tritrophic System Compared to a Model Offering Mechanosensory Cues Only

Several species of hymenopteran parasitoids are able to locate concealed pupal hosts by vibrational sounding. However, the specific role of this technique of mechanosensory host location has not yet been investigated in a natural, tritrophic system with multiple cues. Here we compared the host location of the pupal parasitoid Xanthopimpla stemmator in a tritrophic system with corn borer pupae in maize stem to the behavior on a paper model offering mechanosensory cues only. In general, the behavioral pattern and the behavioral states exhibited by host-searching female parasitoid were identical in the model and in the tritrophic system, while quantitative aspects differed. Our results demonstrate that vibrational sounding maintains its significance for host location in an environment with multiple cues, and that additional cues may increase responsiveness of females.     

Body temperature and thermoregulation in two species of yellowjackets,Vespula germanica and V. maculifrons

In spite of the abundance and broad distribution of social wasps, little information exists concerning thermoregulation by individuals. We measured body temperatures of the yellowjackets Vespula germanica and V. maculifrons and examined their thermoregulatory mechanisms. V. germanica demonstrated thermoregulation via a decreasing gradient between thorax temperature and ambient temperature as ambient temperature increased. V. maculifrons exhibited a constant gradient at lower ambient temperatures but thorax temperature was constant at high ambient temperatures. Head temperature exhibited similar patterns in both species. In spite of low thermal conductances, a simple heat budget model predicts substantial heat loads in warm conditions in the absence of thermoregulation. Both species regurgitated when heated on the head. A smaller volume of regurgitant was produced at lower head temperatures and a larger volume at higher head temperatures. Small regurgitations resulted in stabilization of head temperature, while large ones resulted in 4°C decreases in head temperature. Regurgitation was rare when wasps were heated upon the thorax. Abdomen temperature was 3–4°C above ambient temperature, and approached ambient temperature under the hottest conditions. No evidence was found for shunting of hot hemolymph from thorax to abdomen as a cooling mechanism. The frequency of regurgitation in workers returning to the nest increased with ambient temperature. Regurgitation may be an important thermoregulatory strategy during heat stress, but is probably not the only mechanism used in yellowjackets.Abbreviations M _b body mass - M _th thorax mass - T _a ambient temperature - T _ab abdomen temperature - T _b body temperature - T _h head temperature - T _th thorax temperature - C _t thermal conductance     

Thermal ecology of western tent caterpillars Malacosoma californicum pluviale and infection by nucleopolyhedrovirus

Abstract 1. Western tent caterpillars hatch in the early spring when temperatures are cool and variable. They compensate for sub-optimal air temperatures by basking in the sun.
2. Tent caterpillars have cyclic population dynamics and infection by nucleopolyhedrovirus (NPV) often occurs in populations at high density.
3. To determine whether climatic variation might influence viral infection, the environmental determinants of larval body temperature and the effects of temperature on growth and development rates and larval susceptibility to NPV were examined.
4. In the field, larval body temperature was determined by ambient temperature, irradiance, and larval stage. The relationship between larval body temperature and ambient temperature was curvilinear, a property consistent with, but not necessarily limited to, behaviourally thermoregulating organisms.
5. Larvae were reared at seven temperatures between 18 and 36 °C. Larval growth and development increased linearly with temperature to 30 °C, increased at a lower rate to 33 °C, then decreased to 36 °C. Pupal weights were highest for larvae reared between 27 and 30 °C.
6. The pathogenicity (LD₅₀) of NPV was not influenced by temperature, but the time to death of infected larvae declined asymptotically as temperature increased.
7. Taking into account larval growth, the theoretical yield of the virus increased significantly between 18 and 21 °C then decreased slightly as temperatures increased to 36 °C.
8. Control and infected larvae showed no difference in temperature preference on a thermal gradient. The modes of temperature preference were similar to those for optimal growth and asymptotic body temperatures measured in the field on sunny days.
9. Warmer temperatures attained by basking may increase the number of infection cycles in sunny springs but do not protect larvae from viral infection.     

Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis

Abstract.  Although the effects of temperature on insect behaviours are studied frequently, few studies report on the relationship between temperature and anti-predator behaviours. A negative relationship between ambient temperature and the intensity of death-feigning is found in adults of two seed beetle species, Callosobruchus maculatus (F.) and C. chinensis (L.) (Coleoptera: Bruchidae). Two traits representing the intensity of immobility, the frequency and the duration of death-feigning, are measured at different temperatures. Almost all adults feign death at 15 °C, but the frequency of death-feigning decreases at higher temperatures in C. maculatus , whereas all C. chinensis adults show this behaviour at 15 and 20 °C and almost all show it at 25 °C, but the frequency of death-feigning decreases at 30 and 35 °C. The difference between the two species might be due to the specific strain of each species used in the experiment. The duration of death-feigning is correlated negatively with the increase in ambient temperature in both species. The frequency at which adults feigned death is higher in females than in males in both species, but the duration of death-feigning is higher in females than in males only in C. maculatus . The relationships between temperature and death-feigning behaviours are discussed from physiological and ecological viewpoints.     

Temperature affects interaction of visual and vibrational cues in parasitoid host location

Parasitoid host location in nature is facilitated by simultaneously using different information sources. How multisensory orientation on the same spatial scale is influenced by environmental conditions is however poorly understood. Here we test whether changes in reliability of cues can cause parasitoids to alter multisensory orientation and to switch to cues that are more reliable under extreme temperatures. In the ichneumonid wasp Pimpla turionellae, multisensory use of thermally insensitive vision and thermally sensitive mechanosensory host location by vibrational sounding (echolocation on solid substrate) was investigated with choice experiments on plant-stem models under optimum temperature (18°C), at high- (28°C) and low-temperature limits (8°C) of vibrational sounding. Temperature affected relative importance of vibrational sounding whereas visual orientation did not vary. At 18°C, parasitoids used visual and vibrational cues with comparable relative importance. At 8 and 28°C, the role of vibrational sounding in multisensory orientation was significantly reduced in line with decreased reliability. Wasps nearly exclusively chose visual cues at 8°C. The parasitoids switch between cues and sensory systems depending on temperature. As overall precision of ovipositor insertions was not affected by temperature, the parasitoids fully compensate the loss of one cue provided another reliable cue is available on the same spatial scale.     

Take-off performance under optimal and suboptimal thermal conditions in the butterfly <Emphasis Type="Italic">Pararge aegeria</Emphasis>

Realized fitness in a fluctuating environment depends on the capacity of an ectothermic organism to function at different temperatures. Flying heliotherms like butterflies use flight for almost all activities like mate location, foraging and host plant searching and oviposition. Several studies tested the importance of ambient temperature, thermoregulation and butterfly activity. Here, we test the influence of variation in flight morphology in interaction with differences in body temperature on locomotor performance, which has not been thoroughly examined so far. Take-off free flight performance was tested at two different body temperatures in males and females of the speckled wood butterfly Pararge aegeria. We found that both males and females accelerated faster at the optimal body temperature compared to the suboptimal one. The multivariate analyses showed significant sex-specific contributions of flight morphology, body temperature treatment and feeding load to explain variation in acceleration performance. Female and male butterflies with a large relative thorax (i.e. flight muscle investment) mass and large, slender wings (i.e. aspect ratio) accelerated fast at optimal temperature. However, high aspect ratio individuals accelerated slowly at suboptimal temperature. Females of low body mass accelerated fast at optimal, but slowly at suboptimal body temperature. In males, there was an interaction effect between body and relative thorax mass: light males with high relative thorax mass had higher performance than males with a low relative thorax mass. In addition, relative distance to the centre of forewing area was positively related to acceleration at both temperatures in males. Males and females with higher feeding loads had lower levels of acceleration. Finally, males that were able to accelerate fast under both temperatures, had a highly significantly heavier relative thorax, lower body and abdomen mass. More generally, this study shows that the significance of butterfly flight morphology in terms of flight performance is at least partially dependent on body temperature.     

The effect of host stage and temperature on selected developmental parameters of the solitary endoparasitoid Meteorus gyrator (Thun.) (Hym., Braconidae)

Abstract:  The development of the solitary endoparasitoid Meteorus gyrator was compared in the six larval stages of its host, the tomato moth Lacanobia oleracea , and at five constant temperatures. The host instar at the time of parasitism had a marked effect on the larval developmental period of the parasitoid, such that larvae derived from eggs oviposited in first instar hosts took approximately 18 days to egress, whilst those derived from eggs oviposited in sixth instar hosts took <10 days. The weight of cocoons was greatest when oviposition was into final instar hosts, where female cocoons averaged 12.8 mg, and lowest in those derived from eggs oviposited into first instars (9.2 mg). The parasitoid's larval development rate in third instar hosts increased with temperature increments in a linear fashion up to 25°C , after which development times were only marginally increased. At 10°C, the mean larval development time was approximately 90 days and pupal development 35–40 days, whilst at 25°C development times were 10–11 days for larvae and 6–7 days for the pupae. In the majority of cases, overall development times were marginally longer (<1 day) in females than in males.     

Gestation temperature affects sexual phenotype, morphology, locomotor performance, and growth of neonatal brown forest skinks, Sphenomorphus indicus

We maintained pregnant Sphenomorphus indicus under four thermal conditions for the whole gestation period to assess the effects of gestation temperature on offspring phenotypes. Parturition occurred between late June and early August, with females at high body temperatures giving birth earlier than those maintained at low body temperatures. Litter size, litter mass, and postpartum body mass did not differ among treatments, and females with relatively higher fecundity produced smaller offspring. Females gave birth to predominantly female offspring (85.7% of the 14 sexed offspring were females) at 24 °C and to predominantly male offspring (76.5% of the 17 sexed offspring were males) at 28 °C. Females with the opportunity to regulate body temperature produced a mix of sexes that did not differ from equality. Offspring produced in different treatments differed in head size, hind-limb length, and tympanum length, but not in snout-vent length, tail length, body mass, fore-limb length, and eye length. Offspring produced at 28 °C were not only smaller in head size, but also shorter in hind-limb length and tympanum length than those offspring produced at lower temperatures. Offspring produced at 28 °C performed more poorly in the racetrack and grew more slowly than offspring produced in the other three treatments. Taken together, our results show that S. indicus might be a temperature-dependent sex determination species and that offspring phenotypes are impaired at high gestation temperatures but maximized at relatively low gestation temperatures.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 453–463.     

Efficiency of vibrational sounding in parasitoid host location depends on substrate density

Parasitoids of concealed hosts have to drill through a substrate with their ovipositor for successful parasitization. Hymenopteran species in this drill-and-sting guild locate immobile pupal hosts by vibrational sounding, i.e., echolocation on solid substrate. Although this host location strategy is assumed to be common among the Orussidae and Ichneumonidae there is no information yet whether it is adapted to characteristics of the host microhabitat. This study examined the effect of substrate density on responsiveness and host location efficiency in two pupal parasitoids, Pimpla turionellae and Xanthopimpla stemmator (Hymenoptera: Ichneumonidae), with different host-niche specialization and corresponding ovipositor morphology. Location and frequency of ovipositor insertions were scored on cylindrical plant stem models of various densities. Substrate density had a significant negative effect on responsiveness, number of ovipositor insertions, and host location precision in both species. The more niche-specific species X. stemmator showed a higher host location precision and insertion activity. We could show that vibrational sounding is obviously adapted to the host microhabitat of the parasitoid species using this host location strategy. We suggest the attenuation of pulses during vibrational sounding as the energetically costly limiting factor for this adaptation.     

Vibratory stimuli in host location by parasitic wasps

Parasitic wasps use a broad spectrum of different stimuli for host location and host acceptance. Here we review the published evidence for the use of mechanical stimuli, i.e. substrate born vibrations which are invariably regarded as vibrotaxis. We propose a set of criteria to class behavioural reactions as vibrotaxis or vibrokinesis and characterize 14 studies reporting the use of host-associated vibrations by parasitoids. The studies are compared concerning (i) experimental design; (ii) characterisation of vibrational signals; and (iii) progress of the parasitoid towards the host.The recent experimental development based on new measurement techniques shows the growing body of evidence that host-associated vibrations are exploited by parasitic wasps. Nevertheless a definite proof for vibrotaxis is still lacking. To assess the exact mechanisms by which parasitoids use vibrations bioassays comparing reactions to natural and artificially generated signals are needed. Vibrotaxis as well as vibrokinesis are both helpful host location strategies for parasitoids foraging in a multimodal environment. At the community level they may lead to niche differentiation.     

Assessment of temperature effects on the development and fecundity of Pullus mediterraneus (Col., Coccinellidae) and consumption of Saissetia oleae eggs (Hom., Coccoida)

Eggs, larval and nymphal periods and fecundity of Pullus mediterraneus were examined under 16 h light : 8 h dark combined with six constant temperatures: 15, 20, 25, 30, 35 and 40°C. Eggs of Saissetia oleae were used as prey. The developmental time at 15, 20, 25, 30 and 35°C was 17.23, 4.5, 2.64, 1.67, 1.28 days for eggs and 98.47, 68.88, 53.94, 28.96, 36.51 days for larval–pupal duration, respectively. At 7°C no eggs hatched, and at 40°C all the stages died after 36 h of maximum exposure except the three last stages. The fecundity of females rearing at different temperatures ranged between 1.7 eggs at 15°C and 601.86 eggs at 30°C. The pre-oviposition period ranged between 23.75 days at 15°C and 3.47 days at 35°C. The consumption of S. oleae eggs by the larvae reached 597.69 eggs during the pre-imaginal development. Females attacked more eggs than males averaging 77.69 ± 22.34 eggs per 4 day period compared with 46.97 ± 10.12 eggs per 4 day period for males.     

Late autumn eclosion in the winter moth Operophtera brumata: compromise of selective forces in life-cycle timing

Abstract. 1. In eclosion experiments at constant temperatures (6, 9, 12, 15, 18, 21, and 25 °C), Operophtera brumata (L.) pupae were found to respond nonlinearly to temperature, with 9 °C giving the highest developmental rate.
2. Pupal development rate decreased and mortality increased at the highest and lowest temperatures. No pupae eclosed at 6, 21, or 25 °C.
3. Exposing pupae to periods of cold did not enhance their rate of development consistently, indicating that no pupal diapause occurred. Light did not affect the length of the pupal period significantly.
4. Variation in mean developmental rates across temperatures was modelled both for data in the present study (northern Norway) and for a previously published German study (20° further south). The German population had a longer pupal period at all temperatures than the northern population (mean difference of 88 days). The difference is assumed to be genetically based, and hence an adaption to (and not a consequence of) differences in phenology between the two sites.
5. The diversity of the life cycle of O. brumata is discussed. Timing of eclosion can be explained by the selective forces of predation by birds on the one hand and mortality due to early snowfall on the other.     

Daily progeny production and thermal influence on development and adult longevity of the leafminer parasitoid, Gronotoma micromorpha (Hym., Eucoilidae)

Abstract:  To evaluate the potential of the parasitoid Gronotoma micromorpha (Perkins) as a biological control agent for the serpentine leafminer Liriomyza trifolii (Burgess) in greenhouses, we determined daily progeny production and thermal influence on both total development (oviposition to adult emergence) and adult longevity of this wasp in the laboratory in the host L. trifolii . The mean total number of progeny produced was 75.6 per female at 25°C under a 15-h light/9-h dark (15L : 9D) photoregime. The developmental rate of G. micromorpha significantly correlated with constant temperature between 18 and 30°C. The lower thermal threshold and thermal constant for total development of this wasp were 11.7°C and 333.3 heat degree-days, respectively. The results indicate that adult female G. micromorpha do not oviposit at 15°C and that the lower threshold for oviposition is approximately 18°C. In heated greenhouses in Japan, leafminers and their parasitoids are exposed to both high temperatures and a short photoregime from late autumn to winter, but these conditions (25°C, 10L : 14D) did not significantly affect the total development of G. micromorpha . When wasps were not exposed to hosts, the mean adult longevity at 15 or 20°C was significantly longer than that at 25°C. When wasps were allowed to oviposit into hosts at 25°C, the mean adult longevity was significantly longer than when wasps were not exposed to hosts. As adult female G. micromorpha do not feed on hosts and are pro-ovigenic, suppression of oviposition probably decreased adult longevity. The biological traits of G. micromorpha elucidated by this and previous studies indicate that this wasp is suitable as a biological control agent for L. trifolii in greenhouses.     

Thermal Behaviour of Honeybees During Aggressive Interactions

We report here on the interrelationship of aggressive behaviour and thermoregulation in honeybees. Body temperature measurements were carried out without behavioural disturbance by infrared thermography. Guard bees, foragers, drones, and queens involved in aggressive interactions were always endothermic, i.e. had their flight muscles activated. Guards made differential use of their endothermic capacity. Mean thorax temperature was 34.2–35.1°C during examination of bees but higher during fights with wasps (37°C) or attack of humans (38.6°C). They usually cooled down when examining bees whereas examinees often heated up during prolonged interceptions (maximum >47°C). Guards neither adjusted their thorax temperature (and thus flight muscle function and agility) to that of examined workers, nor to that of drones, which were 2–7°C warmer. Guards examined cool bees (<33°C) longer than warmer ones, supporting the hypothesis that heating of examinees facilitates odour identification by guards, probably because of vapour pressure increase of semiochemicals with temperature. Guards in the core of aggressive balls clinged to the attacked insects to fix them and kill them by heat (maximum 46.5°C). Bees in the outer cluster layers resembled normal guards behaviourally and thermally. They served as active core insulators by heating up to 43.9°C. While balled wasps were cooler (maximum 42.5°C) than clinging guards balled bees behaved like examinees with maximum temperatures of 46.6°C, which further supports the hypothesis that the examinees heat up to facilitate odour identification.