Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

Experimental warming increases herbivory by leaf‐chewing insects in an alpine plant community

Climate warming is predicted to affect species and trophic interactions worldwide, and alpine ecosystems are expected to be especially sensitive to changes. In this study, we used two ongoing climate warming (open‐top chambers) experiments at Finse, southern Norway, to examine whether warming had an effect on herbivory by leaf‐chewing insects in an alpine Dryas heath community. We recorded feeding marks on the most common vascular plant species in warmed and control plots at two experimental sites at different elevations and carried out a brief inventory of insect herbivores. Experimental warming increased herbivory on Dryas octopetala and Bistorta vivipara. Dryas octopetala also experienced increased herbivory at the lower and warmer site, indicating an overall positive effect of warming, whereas B. vivipara experienced an increased herbivory at the colder and higher site indicating a mixed effect of warming. The Lepidoptera Zygaena exulans and Sympistis nigrita were the two most common leaf‐chewing insects in the Dryas heath. Based on the observed patterns of herbivory, the insects life cycles and feeding preferences, we argue that Z. exulans is the most important herbivore on B. vivipara, and S. nigrita the most important herbivore on D. octopetala. We conclude that if the degree of insect herbivory increases in a warmer world, as suggested by this study and others, complex interactions between plants, insects, and site‐specific conditions make it hard to predict overall effects on plant communities.     

Experimental evidence that the ecosystem effects of aquatic herbivory by moose and beaver may be contingent on water body type

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Trade-offs in plant responses to herbivory influence trophic routes of production in a freshwater wetland

Responses of aquatic macrophytes to leaf herbivory may differ from those documented for terrestrial plants, in part, because the potential to maximize growth following herbivory may be limited by the stress of being rooted in flooded, anaerobic sediments. Herbivory on aquatic macrophytes may have ecosystem consequences by altering the allocation of nutrients and production of biomass within individual plants and changing the quality and quantity of aboveground biomass available to consumers or decomposers. To test the effects of leaf herbivory on plant growth and production, herbivory of a dominant macrophyte, Nymphaea odorata, by chrysomelid beetles and crambid moths was controlled during a 2-year field experiment. Plants exposed to herbivory maintained, or tended to increase, biomass and aboveground net primary production relative to controls, which resulted in 1.5 times more aboveground primary production entering the detrital pathway of the wetland. In a complementary greenhouse experiment, the effects of simulated leaf herbivory on total plant responses, including biomass and nutrient allocation, were investigated. Plants in the greenhouse responded to moderate herbivory by maintaining aboveground biomass relative to controls, but this response occurred at the expense of belowground growth. Results of these studies suggest that N. odorata may tolerate moderate levels of herbivory by reallocating biomass and resources aboveground, which in turn influences the quantity, quality and fate of organic matter available to herbivores and decomposers.     

Water velocity regulates macro‐consumer herbivory on the benthic macrophyte Podostemum ceratophyllum Michx.

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Responses of four submerged macrophytes to freshwater snail density (Radix swinhoei) under clear‐water conditions: A mesocosm study

Macrophytes play a key role in stabilizing clear‐water conditions in shallow freshwater ecosystems. Their populations are maintained by a balance between plant grazing and plant growth. As a freshwater snail commonly found in shallow lakes, Radix swinhoei can affect the growth of submerged macrophytes by removing epiphyton from the surface of aquatic plants and by grazing directly on macrophyte organs. Thus, we conducted a long‐term (11‐month) experiment to explore the effects of snail density on macrophytes with distinctive structures in an outdoor clear‐water mesocosm system (with relatively low total nitrogen (TN, 0.66 ± 0.27 mg/L) and total phosphorus (TP, 36 ± 20 μg/L) and a phytoplankton chlorophyll a (Chla) range of 14.8 ± 4.9 μg/L) based on two different snail densities (low and high) and four macrophyte species treatments (Myriophyllum spicatum, Potamogeton wrightii, P. crispus, and P. oxyphyllus). In the high‐density treatment, snail biomass and abundance (36.5 ± 16.5 g/m² and 169 ± 92 ind/m², respectively) were approximately twice that observed in the low‐density treatment, resulting in lower total and aboveground biomass and ramet number in the macrophytes. In addition, plant height and plant volume inhabited (PVI) showed species‐specific responses to snail densities, that is, the height of P. oxyphyllus and PVI of M. spicatum were both higher under low‐density treatment. Thus, compared with low‐density treatment, the inhibitory effects of long‐term high snail density on macrophytes by direct feeding may be greater than the positive effects resulting from epiphyton clearance when under clear‐water conditions with low epiphyton biomass. Thus, under clear‐water conditions, the growth and community composition of submerged macrophytes could be potentially modified by the manual addition of invertebrates (i.e., snails) to lakes if the inhibitory effects from predatory fish are minor.     

Leaf biomechanical properties as mechanisms of resistance to black cutworm (Agrotis ipsilon) among Poa species

Biomechanical properties can be important parameters in resistance of plants to herbivorous insects. As plants age, however, there can be dramatic changes in physical defenses that can then influence their susceptibility to insect herbivores. We measured changes in leaf biomechanical properties during ontogeny of Poa species and the relationship of these changes to the development of a generalist herbivore, the black cutworm, Agrotis ipsilon Hufnagel (Lepidoptera: Noctuidae), was investigated. Larvae were reared on two representative age classes, i.e., young (<60 days after planting) and old (>1 year after planting), of foliage in laboratory assays. Foliage generally reaches a peak fracture force between 80 and 109 days after planting depending on grass type. Foliage from old plants was significantly tougher than that of young plants, and black cutworm larvae reared on foliage from young plants gained significantly (ca. four times) more weight than those fed on foliage from old Poa plants. In addition, fracture force has a negative relationship with black cutworm development. Plant fiber, particularly neutral detergent fiber accounted for 65 and 46% of the variation in fracture force and larval development, respectively. These results provide additional insight into how plant ontogeny influences physical defenses to an insect herbivore in a grass system. Likewise, this is seemingly the first study to suggest a mechanism for host plant resistance to black cutworm. Plant fiber may be a useful trait to explore in plant improvement programs in which black cutworm is a primary pest (e.g., managed turfgrass).     

Do native and invasive herbivores have an effect on Brassica rapa pollination?

• Mutualistic (e.g. pollination) and antagonistic (e.g. herbivory) plant–insect interactions shape levels of plant fitness and can have interactive effects.
• By using experimental plots of Brassica rapa plants infested with generalist (Mamestra brassicae) and specialised (Pieris brassicae) native herbivores and with a generalist invasive (Spodoptera littoralis) herbivore, we estimated both pollen movement among treatments and the visiting behaviour of honeybees versus other wild pollinators.
• Overall, we found that herbivory has weak effects on plant pollen export, either in terms of inter‐treatment movements or of dispersion distance. Plants infested with the native specialised herbivore tend to export less pollen to other plants with the same treatment. Other wild pollinators preferentially visit non‐infested plants that differ from those of honeybees, which showed no preferences. Honeybees and other wild pollinators also showed different behaviours on plants infested with different herbivores, with the former tending to avoid revisiting the same treatment and the latter showing no avoidance behaviour. When taking into account the whole pollinator community, i.e. the interactive effects of honeybees and other wild pollinators, we found an increased avoidance of plants infested by the native specialised herbivore and a decreased avoidance of plants infested by the invasive herbivore.
• Taken together, our results suggest that herbivory may have an effect on B. rapa pollination, but this effect depends on the relative abundance of honeybees and other wild pollinators.

     

A trophic cascade in a macrophyte-based food web at the land–water ecotone

Trophic cascades may purportedly be more common in aquatic than terrestrial food webs, but herbivory on freshwater vascular plants has historically been considered low. Water lilies are an exception, suffering severe grazing damage by leaf beetles. To test whether a central prediction of cascade models—that predator effects propagate downwards to plants—operates in a macrophyte-based food web, we experimentally manipulated predation pressure on a key herbivore of water lilies in the littoral zone of a lake in Michigan, USA. Field experiments comprised combinations of caging treatments to alter the number of predators (larvae of the ladybird beetle Coleomegilla maculata) that hunt the grazers of the macrophytes (larvae of the leaf beetles Galerucella nymphaeae) on the leaves of the water lily Nuphar advena. Predatory larvae of the ladybird beetles significantly reduced grazing damage to water-lily leaves by 35–43%. The predators reduced plant damage chiefly via density-mediated effects, when lower densities of grazers translated to significant declines in plant damage. Plant damage caused by the surviving herbivores was less than predicted from individual grazing rates under predator-free conditions. This suggests that trait-mediated effects may possibly also operate in this cascade. The observed strong effect of predators on a non-adjacent trophic level concurs with an essential component of the trophic cascade model, and the cascade occurred at the ecotone between aquatic and terrestrial habitats: Nuphar is an aquatic macrophyte with emergent and floating leaves, whereas both beetle species are semi-terrestrial and use the dry, emergent and floating leaves of the water lily as habitat. Also, the cascade is underpinned by freshwater macrophytes—a group for which trophic processes have often been underappreciated in the past.     

Differential toxic effects of Ulva lactuca (Chlorophyta) on the herbivorous gastropods,Littorina littorea and L. obtusata (Mollusca)

Members of the genus Ulva are widespread and abundant in intertidal and shallow subtidal areas but there are conflicting data regarding susceptibility to herbivory. While some studies have documented that Ulva spp. were favored by a diversity of marine herbivores, other work has revealed herbivore deterrence. We investigated grazing and growth rates of the littorinid species, Littorina littorea and L. obtusata, when offered Fucus vesiculosus, Ascophyllum nodosum, Ulva lactuca, and Chondrus crispus, highlighting distinctive vulnerabilities to toxic effects of U. lactuca. Ulva lactuca was the preferred food of L. littorea, while L. obtusata showed no grazing on this ephemeral algal species. In contrast, F. vesiculosus was highly preferred by L. obtusata. Although L. littorea demonstrated a grazing preference for U. lactuca, growth rate of this gastropod species was nearly 3× greater when fed F. vesiculosus, suggesting a non‐lethal, negative effect of U. lactuca on L. littorea with long‐term exposure. Mortality of L. obtusata ranged from 0% to 100% when held in the presence of various Ulva densities for 1 week, and Ulva exudate depressed herbivory of this gastropod. We conclude that the water‐soluble, toxic exudate produced by U. lactuca in response to herbivory had allelochemical properties, and may contain a cleavage product (acrylic acid) of dimethylsulfoniopropionate or reactive oxygen species (i.e., H₂O₂). Observed differences in susceptibility to Ulva toxicity by the littorinid species may be related to generalist versus specialist feeding and habitat strategies.     

Induced indirect defence in a spider–plant system mediated by pericarpial nectaries

Some plant species attacked by herbivore species produce additional resources to attract predators and induce an indirect defence process. We evaluated whether Palicourea rigida (Rubiaceae) individuals can induce indirect defences as response to herbivory simulation by increasing pericarpial nectar production and volatile emissions, as well as whether spiders are attracted by such induced indirect defences. We selected 30 P. rigida individuals and simulated herbivory in 15 of them by cutting out half of all leaves using pruning shears. We did not manipulate the other 15 plants (control group). At three different times, we measured nectar volume and calories of the pericarpial nectary in the inflorescences of all plants of control and treatment groups. We also quantified spider abundance on these plants. In another experiment, we selected salticid spider, Thiodina sp., to determine whether predators detect chemical tracks of plant volatiles produced by the plant after herbivory simulations. We also tested whether the honey solution could emit olfactory signals capable of attractive spiders. We showed that P. rigida produced higher volume of pericarpial nectar presenting more calories after herbivory simulation. The abundance of spiders was higher in plants subjected to herbivory simulation than control plants. Thiodina sp. did not respond to the volatile chemical tracks produced by the leaves after the simulation, but it had a positive response to olfactory tracks associated with the sucrose solution. Such an outcome indicates the ability of this spider to locate nectar honey plants and olfactory signals of honey. Thus, plants respond to the action of herbivores by producing more pericarpial nectar and nectar with more calories. Although our knowledge about the olfactory physiology of arachnids remains incipient, we highlight the importance of chemical and olfactory tracks for decision‐making of spiders in foraging on plants and the herbivory influence on the behaviour of cursorial spiders.     

Interaction of Anthonomus grandis and cotton genotypes: biological and behavioral responses

The boll weevil, Anthonomus grandisBoheman (Coleoptera: Curculionidae), is a key pest of cotton, Gossypium hirsutumL. (Malvaceae). Knowledge about boll weevil feeding and oviposition behavior and its response to plant volatiles can underpin our understanding of host plant resistance, and contribute to improved monitoring and mass capture of this pest. Boll weevil oviposition preference and immature development in four cotton genotypes (CNPA TB90, TB85, TB15, and BRS Rubi) were investigated in the laboratory and greenhouse. Volatile organic compounds (VOCs) produced by TB90 and Rubi genotypes were obtained from herbivore‐damaged and undamaged control plants at two phenological stages – vegetative (prior to squaring) and reproductive (during squaring) – and four collection times – 24, 48, 72, and 96 h following herbivore damage. The boll weevil exhibited similar feeding and oviposition behavior across the four tested cotton genotypes. The chemical profiles of herbivore‐damaged plants of both genotypes across the two phenological stages were qualitatively similar, but differed in the amount of volatiles produced. Boll weevil response to VOC extracts was studied using a Y‐tube olfactometer. The boll weevil exhibited similar feeding and oviposition behavior at the four tested cotton genotypes, although delayed development and production of smaller adults was found when fed TB85. The chemical profile of herbivore‐damaged plants of both genotypes at the two phenological stages and time periods (24–96 h) was similar qualitatively, with 30 identified compounds, but differed in the amount of volatiles produced. Additionally, boll weevil olfactory response was positive to herbivory‐induced volatiles. The results help to understand the interaction between A. grandis and cotton plants, and why it is difficult to obtain cotton genotypes possessing constitutive resistance to this pest.     

Insect herbivory on water mint: you can't get there from here?

Aquatic plants are thought to have fewer herbivore species than their terrestinal counterparts, and possibly to suffer less herbivory I examined herbivory on water mint Mentha aquatica growing in and out of water and tested possible processes determining the observed pattern of leaf damage Plants growing on land had much more herbivore damage than those growing in water The most common herbivore of Mentha at the site (a chrysomelid beetle) showed no p reference for leaves from terrestrial plants over those from aquatic plants Caging aquatic plants to exclude moorhens suggested that these predators were not having a strong effect in removing insect herbivores (though this conclusion is tentative due to low insect numbers) Transplanting aquatic plants to a terrestrial location, while keeping their roots in water, resulted in marked increases in herbivore damage, relative to control aquatic plants The results suggest that the water barrier may prevent effective exploitation of emergent aquatic plants by terrestrial herbivores This may have consequences for observed patterns of herbivore richness on such plants, plant fitness, and a more speculative suggestion, for the mode of reproduction in aquatic plants     

Temporal changes in olfactory and oviposition responses of the diamondback moth to herbivore‐induced host plants

Temporal changes in the pre‐ and post‐alighting responses of mated female diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), to two species of Brassica (Brassicaceae) host plants induced by larval feeding were studied using olfactometer and oviposition assays. Females displayed strong olfactory and oviposition preferences for herbivore‐induced common cabbage (Brassica oleracea var. capitata L. cv. sugarloaf) plants over intact plants; these preferences decreased with time and disappeared by the 7th day after induction. In herbivore‐induced common cabbage plants, eggs were clustered near feeding damage on the younger leaves (leaves 5–7), whereas in intact plants, eggs were clustered on the stem and lower leaves (leaves 1–4) . However, as the time interval between larval feeding and oviposition increased, more eggs were laid on the lower leaves of induced plants. This demonstrates a change in egg distribution from the pattern associated with induced plants to that associated with intact plants. In contrast, females displayed strong olfactory and oviposition preferences for intact Chinese cabbage [Brassica rapa ssp. pekinensis (Lour.) Hanelt cv. Wombok] plants over induced plants; these preferences decreased with time and disappeared by the 5th day after induction. More eggs were laid on the upper leaves (leaves 4–6) than on the lower leaves (leaves 1–3) of intact Chinese cabbage plants at first, but the distribution changed over time until there were no significant differences in the egg count between upper and lower leaves by the 4th day post induction. For both host plant species, pre‐alighting responses of moths were reliable indicators of post‐alighting responses on the first 2 days post induction. The results suggest that temporal changes in a plant's profile (chemical or otherwise) following herbivory may influence attractiveness to an insect herbivore and be accompanied by changes in olfactory and oviposition preferences.     

Lack of fire and insect herbivory constrain recruitment in a rare legume from Western Australia

We investigated factors influencing recruitment in the rare endemic shrub Acacia insolita subsp. recurva (Fabaceae) from the heavily cleared south‐west of Western Australia. We examined annual seed production over 4 years, including the impact of herbivory on reproductive output. Conversion of bud to fruit was low (overall 0.02%). The lack of significant difference in canopy dimensions between caged and uncaged plants suggested that vertebrate herbivore grazing was negligible, but invertebrate predation had a negative impact on seed production (loss of >80% of fruiting potential). Soil cores determined the presence of soil‐stored seeds and an experimental burn confirmed that plants are fire‐killed and can regenerate from the seed bank. This seed reserve was found to contain <5 seeds m^?2, and both freshly collected seeds and seeds retrieved from the soil had high viability (99% vs. 91%) when subjected to a germination test. Seedling recruitment 29 months post‐fire resulted in a ratio of three seedlings for every adult killed by fire. We also compared reproductive success in this rare Acacia with its common conspecific and although the rare species produced more flowers, the success of flowering did not translate into better fruit set. We conclude that insect damage to reproductive branchlets and lack of appropriate disturbance are major factors constraining recruitment. Active site management may be required for the continued persistence of this fire‐dependent legume.     

Jasmonoyl‐l‐isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant defenses against herbivores

For most plant hormones, biological activity is suppressed by reversible conjugation to sugars, amino acids and other small molecules. In contrast, the conjugation of jasmonic acid (JA) to isoleucine (Ile) is known to enhance the activity of JA. Whereas hydroxylation and carboxylation of JA‐Ile permanently inactivates JA‐Ile‐mediated signaling in plants, the alternative deactivation pathway of JA‐Ile by its direct hydrolysis to JA remains unstudied. We show that Nicotiana attenuata jasmonoyl‐l ‐isoleucine hydrolase 1 (JIH1), a close homologue of previously characterized indoleacetic acid alanine resistant 3 (IAR3) gene in Arabidopsis, hydrolyzes both JA‐Ile and IAA‐Ala in vitro. When the herbivory‐inducible NaJIH1 gene was silenced by RNA interference, JA‐Ile levels increased dramatically after simulated herbivory in irJIH1, compared with wild‐type (WT) plants. When specialist (Manduca sexta) or generalist (Spodoptera littoralis) herbivores fed on irJIH1 plants they gained significantly less mass compared with those feeding on wild‐type (WT) plants. The poor larval performance was strongly correlated with the higher accumulation of several JA‐Ile‐dependent direct defense metabolites in irJIH1 plants. In the field, irJIH1 plants attracted substantially more Geocoris predators to the experimentally attached M. sexta eggs on their leaves, compared with empty vector plants, which correlated with higher herbivory‐elicited emissions of volatiles known to function as indirect defenses. We conclude that NaJIH1 encodes a new homeostatic step in JA metabolism that, together with JA and JA‐Ile‐hydroxylation and carboxylation of JA‐Ile, rapidly attenuates the JA‐Ile burst, allowing plants to tailor the expression of direct and indirect defenses against herbivore attack in nature.     

Plant chemistry underlies herbivore‐mediated inbreeding depression in nature

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant–herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore‐mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.