Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

Parasitism of the herbivore Pieris brassicae L. (Lep., Pieridae) by Cotesia glomerata L. (Hym., Braconidae) does not benefit the host plant by reduction of herbivory

Models of tritrophic interactions often imply that attraction of herbivore natural enemies by the plant constitutes a defence. Parasitoid attack on herbivores is assumed to result in a reduction in herbivory and/or an increase in plant fitness. Coupled with the active involvement of the plant in producing signals, this can be seen as indirect mediation of wound-induced defence. The assumption that parasitism of Pieris brassicae L. by the parasitoid Cotesia glomerata L. reduces leaf consumption of cabbage is tested. The effect of parasitism on the growth and feeding rates of P. brassicae larvae compared to unparasitized larvae. Either the defensive mechanism, if it exists, is more subtle, or the natural enemy is using an incidental chemical produced as a by-product of the herbivores feeding action as a cue for host-finding, with no increaction effects. This has implications for the study of tritrophic interactions, particularly in the context of agricultural systems and the assumption that in IPM strategies, parasitoids are a plant benefit.     

Biorhythms and pineal gland

Endocrine biorhythms are classified according to the period time, as one of the most characteristic properties of biorhythms. Each endocrine organ has parallel more than one biorhythms with different period time (e. g. circadian and circannual rhythms). The time of acrophase of the biorhythms at the different endocrine organs is fairly variant. This review summarizes the rhythmic function of the THS-thyroid, gonadotrophic-gonadal and ACTH-adrenocortical systems. Pineal gland plays an integrative role in the regulation of rhythmic function of the endocrine system. The melatonin secretion of this gland also reveals conspicuous circadian and circannual rhythms both in mammals and in birds. Mammalian pineal is functional only if its peripheral sympathetic innervation from the superior cervical ganglion is intact. In contrast, melatonin secretion and its circadian rhythm is also maintained in birds under isolated conditions (explanted into an in vitro superfusion system). The 24 hours period time of melatonin circadian rhythm can not be changed by light impulses. The phases of the circadian rhythm, however, can be turned by changing the time of environmental light-dark phases. The wavelength of the artificial light used for reversal of circadian rhythm is an important factor. The development of the entrainment and synchronization of the circadian melatonin rhythm in birds is independent of the rhythmic day-night changes in environmental lighting condition. The differences in the main elements of the biological clock between mammals and birds are discussed.     

Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies

Herbivore-damaged plants emit volatile organic compounds that attract natural enemies of the herbivores. This form of indirect plant defence occurs aboveground as well as belowground, but it remains unclear how simultaneous feeding by different herbivores attacking leaves and roots may affect the production of the respective defence signals. We employed a setup that combines trapping of volatile organic signals and simultaneous measurements of the attractiveness of these signals to above and belowground natural enemies. Young maize plants were infested with either the foliar herbivore Spodoptera littoralis , the root herbivore Diabrotica virgifera virgifera , or with both these important pest insects. The parasitic wasp Cotesia marginiventris and the entomopathogenic nematode Heterorhabditis megidis were strongly attracted if their respective host was feeding on a plant, but this attraction was significantly reduced if both herbivores were on a plant. The emission of the principal root attractant was indeed reduced due to double infestation, but this was not evident for the leaf volatiles. The parasitoid showed an ability to learn the differences in odour emissions and increased its response to the odour of a doubly infested plant after experiencing this odour during an encounter with hosts. This first study to measure effects of belowground herbivory on aboveground tritrophic signalling and vice-versa reemphasizes the important role of plants in bridging interactions between spatially distinct components of the ecosystem.     

Importance of primary metabolites in canola in mediating interactions between a specialist leaf-feeding insect and its specialist solitary endoparasitoid

The role of primary plant chemistry on trophic interactions is not well studied. We examined the effect of primary plant metabolites, focusing on nitrogen, on several biological indices of second and third trophic level insects in a model tritrophic system, consisting of two strains of the crucifer, Brassica napus (canola) (SLM₀₄₆ and RGS₀₀₃), the specialist insect herbivore Plutella xylostella (L.) (Lepidoptera: Plutellidae), and its specialist koinobiont larval-pupal parasitoid Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae). In particular, we measured relative growth rate of the herbivore in relation to an index for plant quality (nitrogen content of leaf tissues), developmental time of the herbivore (sum of second, third, and fourth larval instars durations), and intrinsic rate of increase (r _m ) of the herbivore and the parasitoid. Tritrophic studies were conducted on development, survivorship curve analysis, reproductive potential, life history, parasitism, and several other fitness correlates of the parasitoid. The life table parameters of D. semiclausum were determined under laboratory conditions. The intrinsic rate of increase (r _m ) of the parasitoid was significantly higher on RGS₀₀₃ than SLM₀₄₆. In this tritrophic model, the results indicated that the bottom-up direct effect on the herbivore population growth rate was marginally as strong as the direct effect of top-down force due to the parasitoid population growth rate; but it was higher than its indirect counterpoint mediated with the parasitoid population growth rate. Consequently, D. semiclausum performed better on RGS₀₀₃, which was the most inferior host to P. xylostella in comparison with another plant cultivar and had the lowest content of nitrogen in its leaves.     

Elevated volatile concentrations in high‐nutrient plants: do insect herbivores pay a high price for good food?

1. A tritrophic perspective is fundamental for understanding the drivers of insect–plant interactions. While host plant traits can directly affect insect herbivore performance by either inhibiting or altering the nutritional benefits of consumption, they can also have an indirect effect on herbivores by influencing rates of predation or parasitism. 2. Enhancing soil nutrients available to trees of the genus Eucalyptus consistently modifies plant traits, typically improving the nutritional quality of the foliage for insect herbivores. We hypothesised that resulting increases in volatile essential oils could have an indirect negative effect on eucalypt‐feeding herbivores by providing their natural enemies with stronger host/prey location cues. 3. Eucalyptus tereticornis Smith seedlings were grown under low‐ and high‐nutrient conditions and the consequences for the release of volatile cues from damaged plants were examined. The influence of 1,8‐cineole (the major volatile terpene in many Eucalyptus species) on rates of predation on model caterpillars in the field was then examined. 4. It was found that the emission of cineole increased significantly after damage (artificial or herbivore), but continued only when damage was sustained by herbivore feeding. Importantly, more cineole was emitted from high‐ than low‐nutrient seedlings given an equivalent amount of damage. In the field, predation was significantly greater on model caterpillars baited with cineole than on unbaited models. 5. These findings are consistent with the hypothesis that any performance benefits insect herbivores derive from feeding on high‐nutrient eucalypt foliage could be at least partially offset by an increased risk of predation or parasitism via increased emission of attractive volatiles.     

Influence of the corticosterone rhythm on photic entrainment of locomotor activity in rats

The question of involvement of glucocorticoid hormones as temporal signals for the synchronization of the timekeeping system was addressed in rats with different corticosterone status. The authors showed that adrenalectomy had no effects on the synchronization of wheel-running activity rhythms to a steady-state LD 12:12 cycle, regardless of whether it was compensated for by a corticosterone replacement therapy that either reinstated constant plasma concentrations of the hormone or mimicked its natural rhythm. However, after a 12-h phase shift (daylight reversal), the lack of circulating corticosterone induced a significant shortening of the resynchronization rate (less than 3 days vs. 7 days). Normalization required restoration of a rhythmic corticosterone secretion that was synchronized to the new photoperiod. Under constant darkness, the corticosterone rhythm did not show any synchronizing effect, providing evidence that it participates in entrainment of the locomotor activity rhythm through modulation of light effects. It is proposed that, under stable lighting conditions, circulating glucocorticoids contribute to stabilizing activity rhythms by reinforcing resistance of the circadian timing system to variations of the photoperiod. Experimental evidence that serotonergic neurons are involved in relaying their modulatory effects to the clock is also presented.     

Fertilizer application decreases insect abundance on Plantago lanceolata: a large-scale experiment in three geographic regions

Humans have substantially altered the nitrogen cycle of ecosystems through the application of agricultural fertilizer. Fertilization may not only affect plant species diversity, but also insect dynamics by altering plant nitrogen supplies. We investigated the effect of experimental fertilization on the vegetation, with the ribwort plantain as the focal plant, and on higher trophic levels on differently managed grasslands throughout Germany. Over a period of 2 years, we examined two specialist herbivores and their parasitoid on Plantago lanceolata L., and the composition and structure of the surrounding vegetation. Over 70 sites in three geographic regions, within the large-scale project “German Biodiversity Exploratories”, were included in the study. The model system consisted of the host plant P. lanceolata L., the monophagous weevils Mecinus labilis Herbst and M. pascuorum Gyllenhal, and their parasitoid Mesopolobus incultus Walker. Fertilization decreased plant species richness and host plant abundance, whereas it enhanced the total vegetation growth. The increased size and heigher leaf nitrogen content did not improve herbivore performance. On the contrary, the abundance of the two herbivores was decreased by fertilization. The parasitoid depended on the abundance of one of its hosts, M. pascuorum (positively density-dependent). Reduced herbivore abundance due to fertilization might be explained by a lower abundance of the host plant, a lower stalk number, and by changed patterns of host localization within higher vegetation. Fertilization negatively affected the third trophic level by cascading up via host abundance. The relationships between fertilization, surrounding vegetation and the tritrophic system were measured throughout the three regions and over the 2-year period. Our findings present consequences of intensification for a plant–herbivore–parasitoid system, and may have significant implications for the conservation of multitrophic systems in managed grasslands.     

Parasitism on seed predators overcomes the detrimental effects of defoliation on plant fitness in a tritrophic system

It is widely recognised that the interaction between plants and herbivores cannot be completely understood if the natural enemies of the latter are not included. Most studies looking at the effects of herbivores and their enemies on plant fitness only consider one herbivore species or guild; however, plants in nature usually face the attack of more than one herbivore guild simultaneously and these herbivores may have a non-additive effect on the attraction with bodyguards and plant fitness. In this study, we asked whether folivory affects the activity of parasitoids on seed predators and whether this effect cascades down to plant fitness. We assessed these questions in a tritrophic system: the plant Ruellia nudiflora, its pre-dispersal seed predators and the parasitoids of the latter. Plants were submitted to either 50 % artificial defoliation or no defoliation (control). The number of seeds, fruit production and parasitoid incidence was assessed periodically in both sets of plants. Parasitoids indirectly and positively affected seed number, while defoliation had a direct negative effect on the number of seeds and an indirect negative effect on parasitoid incidence. However, the combined effect of defoliation and seed predation increased the indirect positive effect of the parasitoids on seed production, which overcame the negative effects of defoliation.     

The role of the plant in attracting parasitoids: response to progressive mechanical wounding

Based on the model system of Brussels sprouts [Brassica oleracea var. gemmifera (Brassicaceae)], the herbivore cabbage white caterpillar, Pieris brassicae (L.) (Lepidoptera: Pieridae), and the parasitoid wasp, Cotesia glomerata (L.) (Hymenoptera: Braconidae), the influence of plant damage type, and damage duration were assessed on plant volatile emission and subsequent recruitment of natural antagonists of the herbivore. Plants were damaged by three methods for a period of either 3 or 8 h: herbivore damage (HD), progressive mechanical damage, and final mechanical damage inflicted in a single event. Wind‐tunnel bioassays evaluated whether the mode of damage affected female parasitoid oriented flight. After both periods of damage, all treatments were highly significantly preferred by naïve C. glomerata to undamaged control plants. After 3 h, herbivore‐damaged plants were significantly preferred to plants with final damage (FD). Most remarkably, following 8‐h damage, the parasitoid preferred both herbivore‐damaged and progressively damaged plants to plants with FD and did not significantly discriminate between herbivore and progressively damaged plants, thus indicating a similarity in plant response to herbivore and progressive mechanical damage. In addition to wind‐tunnel bioassays, emitted plant volatiles were collected and analysed by thermal desorption gas chromatography/mass spectrometry, following 3 and 8 h of damage in order to correlate volatiles released from different damage types with the attraction of the parasitoid. Differences in volatile profiles from all damage types were similar following both 3 and 8 h of damage, with only (Z)‐3‐hexenyl acetate found to be emitted in significantly higher quantities by final mechanical damage compared with HD after 3 h. In conclusion, the plant's response to progressive mechanical damage was more similar to HD than final mechanical damage deployed at a single point in time, irrespective of damage duration, and C. glomerata did not significantly discriminate between progressive damage and HD.     

Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata , a parasitoid of the leaf herbivore Pieris brassicae , mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.     

Effect of Bt genetic engineering on indirect defense in cotton via a tritrophic interaction

We present a tritrophic analysis of the potential non-intended pleiotropic effects of cry1Ac gene derived from Bacillus thurigiensis (Bt) insertion in cotton (DeltaPine 404 Bt Bollgard® variety) on the emission of herbivore induced volatile compounds and on the attraction of the egg parasitoid Trichogramma pretisoum (Hymenoptera: Trichogrammatidae). Both the herbivore damaged Bt variety and its non-Bt isoline (DeltaPine DP4049 variety) produced volatiles in higher quantity when compared to undamaged plants and significantly attracted the egg parasitoids (T. pretiosum) when compared to undamaged plants. However, Trichogramma pretiosum did not differentiate between the transgenic and nontransgenic varieties, suggesting that the ratios between the compounds released by herbivory damaged -Bt cotton and herbivory damaged-nonBt cotton did not change significantly. Finally, no detrimental effect of the Bt genetic engineering was detected related to the volatile compounds released by Bollgard cotton on the behavior of the natural enemy studied.     

With or without you: Effects of the concurrent range expansion of an herbivore and its natural enemy on native species interactions

Global climatic changes may lead to the arrival of multiple range‐expanding species from different trophic levels into new habitats, either simultaneously or in quick succession, potentially causing the introduction of manifold novel interactions into native food webs. Unraveling the complex biotic interactions between native and range‐expanding species is critical to understand the impact of climate change on community ecology, but experimental evidence is lacking. In a series of laboratory experiments that simulated direct and indirect species interactions, we investigated the effects of the concurrent arrival of a range‐expanding insect herbivore in Europe, Spodoptera littoralis, and its associated parasitoid Microplitis rufiventris, on the native herbivore Mamestra brassicae, and its associated parasitoid Microplitis mediator, when co‐occurring on a native plant, Brassica rapa. Overall, direct interactions between the herbivores were beneficial for the exotic herbivore (higher pupal weight than the native herbivore), and negative for the native herbivore (higher mortality than the exotic herbivore). At the third trophic level, both parasitoids were unable to parasitize the herbivore they did not coexist with, but the presence of the exotic parasitoid still negatively affected the native herbivore (increased mortality) and the native parasitoid (decreased parasitism rate), through failed parasitism attempts and interference effects. Our results suggest different interaction scenarios depending on whether S. littoralis and its parasitoid arrive to the native tritrophic system separately or concurrently, as the negative effects associated with the presence of the parasitoid were dependent on the presence of the exotic herbivore. These findings illustrate the complexity and interconnectedness of multitrophic changes resulting from concurrent species arrival to new environments, and the need for integrating the ecological effects of such arrivals into the general theoretical framework of global invasion patterns driven by climatic change.     

Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses

Abstract.  1. Little is known about underlying mechanisms by which plants indirectly affect parasitism success in hymenopteran endoparasitoids. The hypothesis that host-plant effects can challenge the innate immune system of an insect host was experimentally tested in this study using a model tritrophic, crucifer – lepidopteran [ Plutella xylostella (L.)] – parasitoid [ Cotesia plutellae (Kurdjumov)], system.
2. The effects of host-plant suitability on herbivore performance and parasitism were examined. The bottom-up effect of plant suitability on host-parasitoid immune responses was then evaluated using measures of cellular and humoral effectors.
3. Host-plant quality showed a significant effect on the encapsulation response of P. xylostella to first instar but not to second instar parasitoid larvae. Encapsulation was never sufficient to prevent parasitoid emergence.
4. Poor host-plant suitability suppressed phenoloxidase activity in the absence of the parasitoid. The suppressive effect of C. plutellae on phenoloxidase activity was much greater and no plant effects were detectable after insects had been parasitized.
5. Despite strong plant effects on parasitism, those on immune effectors of the host were transitory or overwhelmed by the effect of the parasitoid.
6. These results demonstrated that plant-mediated variation in parasitism success by C. plutellae were not as a result of plant nutritional status or other attributes affecting the immune function of P. xylostella , nor to host-plant effects on superparasitism.
7. In these experiments, P. xylostella was a fully permissive host to C. plutellae and host-plant-mediated effects on the innate immune response appeared to play no part in parasitoid survival within hosts.     

寄生蜂抗药性研究进展

植物-植食性昆虫-寄生蜂三级营养结构之间由于长期相互适应和协同进化,产生了一系列独特的相互关系。选择压力将对害虫和寄生蜂的抗药性演化产生影响,但由于寄生蜂具有与植食性昆虫不同的生物学及生态学特性,选择压力对害虫和寄生蜂抗药性演化的影响作用也是不同的。研究结果表明,除体外杀虫剂对寄生蜂的直接汰选因素外,进入寄主昆虫体内的杀虫剂成分、寄主昆虫取食不同植物的特有成分以及气候因子等均会对寄生蜂的抗药性演化产生影响。     

虫害诱导的植物挥发物:植物与植食性昆虫及其天敌相互作用的进化产物

综述了植物、植食性昆虫及其天敌相互作用的进化过程。虫害诱导的植物挥发物的特征和功能是植物-植食性昆虫-天敌之间长期进化的结果。在植物、植食性昆虫与天敌相互作用的进化过程中,3个不同营养级,包括植物、植食性昆虫和天敌有着各自的调节和利用虫害诱导的植物挥发物的策略。但有一些问题,如通过实验研究得出的诱导防御在田间是否真正能起到保护作用等需进一步研究、阐明。     

The investigation of the synchronization between rhythms in the human cardiovascular system from time series of R-R-intervals

We demonstrated that, from the sequence of R-R intervals, it is possible to calculate the instantaneous phases and instantaneous frequencies of the main rhythmic processes governing the cardiovascular dynamics in humans, namely, the main heart rhythm, respiration, and the process of slow regulation of blood pressure with basic frequency close to 0.1 Hz. For the cases of spontaneous respiration and paced respiration with a fixed frequency, the synchronization between the rhythms of the cardiovascular system was investigated based on the analysis of only the time series of R-R intervals. It is shown that the main heart rhythm and the rhythm of low-frequency regulation of blood pressure can be synchronized with respiration.     

Physiological function and ecological aspects of fatty acid-amino acid conjugates in insects†

In tritrophic interactions, plants recognize herbivore-produced elicitors and release a blend of volatile compounds (VOCs), which work as chemical cues for parasitoids or predators to locate their hosts. From detection of elicitors to VOC emissions, plants utilize sophisticated systems that resemble the plant–microbe interaction system. Fatty acid–amino acid conjugates (FACs), a class of insect elicitors, resemble compounds synthesized by microbes in nature. Recent evidence suggests that the recognition of insect elicitors by an ancestral microbe-associated defense system may be the origin of tritrophic interactions mediated by FACs. Here we discuss our findings in light of how plants have customized this defense to be effective against insect herbivores, and how some insects have successfully adapted to these defenses.     

动物内源褪黑素调控生物节律的研究进展

内源褪黑素对人类和其他哺乳动物的节律行为具有调控功能。生物节律是自然进化赋予生命的基本特征之一,生物体的生命活动受到生物节律的控制与影响。在哺乳动物中,节律调控中心是松果体,其主要功能是合成和分泌褪黑素。褪黑素广泛参与生物体节律行为的调节,本文从褪黑素的产生和作用机制,分别阐述褪黑素对昼夜节律行为和多种年节律行为的调控作用,同时明确褪黑素与生物钟及神经内分泌系统的直接作用和反馈互动的复杂集合,进一步揭示褪黑素调控生物节律的重要作用,以期为褪黑素的基础研究以及未来探究生物体的生物钟内源性发生机制提供参考。