Entrapped carrion increases indirect plant resistance and intra‐guild predation on a sticky tarweed

Many plants employ indirect defenses against herbivores; often plants provide a shelter or nutritional resource to predators, increasing predator abundance, and lessening herbivory to the plant. Often, predators on the same plant represent different life stages and different species. In these situations intraguild predation (IGP) may occur and may decrease the efficacy of that defense. Recently, several sticky plants have been found to increase indirect defense by provisioning predatory insects with entrapped insects (hereafter: carrion). We conducted observational studies and feeding trials with herbivores and predators on two sticky, insect‐entrapping asters, Hemizonia congesta and Madia elegans, to construct food webs for these species and determine the prevalence of IGP in these carrion‐provisioning systems. In both systems, intraguild predation was the most common interaction observed. To determine whether IGP was driven by resource abundance, whether it reduced efficacy of this indirect defense and whether stickiness or predator attraction was induced by damage, we performed field manipulations on H. congesta. Carrion supplementation led to an increase in predator abundance and IGP. IGP was asymmetric within the predator guild: assassin bugs and spiders preyed on small stilt bugs but not vice versa. Despite increased IGP, carrion provisions decreased the abundance of the two most common herbivores (a weevil and a mealybug). Overall seed set was driven by plant size, but number of seeds produced per fruit significantly increased with increasing carrion, likely because of the reduction in the density of a seed‐feeding weevil. Observationally and experimentally, we found that carrion‐mediated indirect defense of tarweeds led to much intraguild predation, though predators effectively reduced herbivore abundance despite the increase in IGP.     

Arthropod carrion influences plant choice,oviposition, and cannibalism by a specialist predator on a sticky plant

1. Dead arthropods, entrapped by trichomes on plant surfaces, are an underappreciated form of plant-provided food. Specialist predatory arthropods able to manoeuvre on plants covered in trichomes facultatively scavenge on the alternative food resource, increasing their abundance and reducing plant damage by herbivores. 2. This protective mutualism dependent on arthropod carrion has been demonstrated in several plant species, but the mechanisms driving the increase in predator abundance have not been identified. Through a series of greenhouse and laboratory experiments, the effect of arthropod carrion on predator behaviour was assessed. 3. The predator Jalysus wickhami preferred Nicotiana tabacum plants augmented with arthropod carrion, spending significantly more time and laying more eggs on those plants than plants without arthropod carrion. 4. Under low J. wickhami densities, arthropod carrion did not reduce egg cannibalism by adults. Under high densities, egg cannibalism by J. wickhami adults was reduced in the presence of arthropod carrion, but cannibalism by fifth instars was not. 5. Arthropod carrion may be utilised by a wide range of predatory arthropods that facultatively scavenge, and this research demonstrates its potential for influencing arthropod–plant and arthropod–arthropod interactions.     

The three criteria for resistance by plant carrion‐provisioning: insect entrapment and predator enrichment on Mimulus bolanderi

1. Many sticky plants provision mutualistic scavenging arthropod predators with carrion, which in turn protect the plant from insect herbivores. While insect entrapment is a common trait across plants, which plants attract these predators and may derive protection is still largely unknown. 2. Three conditions were proposed that must be satisfied for observational data to suggest this defensive strategy: (i) the consistent presence of scavenging predators, (ii) positive correlation between predator numbers and carrion, and (iii) suitability of these predators for controlling known herbivores. 3. As a case study, we examined the fire‐following annual, Mimulus [Diplacus] bolanderi (Phyrmaceae), which is part of a well‐studied radiation of California monkeyflowers. Many monkeyflowers entrap insects, though attraction to predators has not been quantified in this genus. 4. A guild of scavenging arthropod predators on M. bolanderi (condition #1) was found, which correlated positively with carrion abundance (#2) and could consume the primary herbivore (#3), suggesting a carrion‐mediated defensive strategy. Lastly, as M. bolanderi is variable in time and space, these interactions are facultative, and these predators are quick to adopt ephemeral carrion resources on novel host plants.     

An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores

Plants produce defences that act directly on herbivores and indirectly via the attraction of natural enemies of herbivores. We examined the pleiotropic effects of direct chemical defence production on indirect defence employing near‐isogenic varieties of cucumber plants (Cucumis sativus) that differ qualitatively in the production of terpenoid cucurbitacins, the most bitter compounds known. In release–recapture experiments conducted in greenhouse common gardens, blind predatory mites were attracted to plants infested by herbivorous mites. Infested sweet plants (lacking cucurbitacins), however, attracted 37% more predatory mites than infested bitter plants (that produce constitutive and inducible cucurbitacins). Analysis of the headspace of plants revealed that production of cucurbitacins was genetically correlated with large increases in the qualitative and quantitative spectrum of volatile compounds produced by plants, including induced production of (E )‐β‐ocimene (3E )‐4,8‐dimethyl‐1,3,7‐nonatriene, (E,E)‐α‐farnesene, and methyl salicylate, all known to be attractants of predators. Nevertheless, plants that produced cucurbitacins were less attractive to predatory mites than plants that lacked cucurbitacins and predators were also half as fecund on these bitter plants. Thus, we provide novel evidence for an ecological trade‐off between direct and indirect plant defence. This cost of defence is mediated by the effects of cucurbitacins on predator fecundity and potentially by the production of volatile compounds that may be repellent to predators.     

Generalising indirect defence and resistance of plants

Indirect defence, the adaptive top‐down control of herbivores by plant traits that enhance predation, is a central component of plant–herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant–natural enemy mutualism. By considering the broader scope of plant–herbivore–natural enemy interactions that comprise indirect defence, we can better understand plant‐based food webs, as well as the evolutionary processes that have shaped them.     

An endophyte‐rich diet increases ant predation on a specialist herbivorous insect

1. All plants form symbioses with microfungi, known as endophytes, which live within plant tissues. Numerous studies have documented endophyte–herbivore antagonism in grass systems, but plant–endophyte–insect interactions are highly variable for forbs and woody plants. 2. The net effect of endophytes on insect herbivory may be modified by their interactions with higher trophic levels, such as predators. Including these multitrophic dynamics may explain some of the variability among endophyte studies of non‐grass plants, which are currently based exclusively on bitrophic studies. 3. The abundance of natural foliar endophytes in a Neotropical vine was manipulated and beetles were fed high or low endophyte diets. Experimental assays assessed whether dietary endophyte load affected beetle growth, leaf consumption, and susceptibility to ant predation. 4. Beetles feeding on high‐ versus low‐endophyte plants had almost identical growth and leaf consumption rates. 5. In a field bioassay, however, it was discovered that feeding on an endophyte‐rich diet increased a beetle's odds of capture by predatory ants nine‐fold. 6. Endophytes could thus provide an indirect, enemy‐mediated form of plant defence that operates even against specialist herbivores. We argue that a multitrophic approach is necessary to untangle the potentially diverse types of endophyte defence among plants.     

Intercropping hampers the nocturnal biological control of aphids

Increasing plant diversity in agroecosystems (i.e. intercropping) has been widely accepted as a means of promoting conservation biological control of mites and insect pests. Nevertheless, the contribution from underlying mechanisms such as the provision of non‐prey alternative food (i.e. pollen and nectar) and shelter have not been properly disentangled; and additionally, it remains unexplored whether the performance of nocturnal and diurnal natural enemies is improved when provided with diverse plant communities. Using open field experiments and a greenhouse microcosm, we investigated whether intercropping collards with parsley could create shelter for natural enemies in the lower stratum (parsley), and whether or not nocturnal and diurnal natural enemies would carry out aphid biological control equally well in this increased plant diversity scenario (intercropping). The results showed that the shelter alone provided by the lower stratum/companion plants (parsley) mediated an increase in the abundance of natural enemies without involving the provision of non‐prey alternative food. However, the biological control of aphids exerted by nocturnal predators was negatively affected by intercropping. The lower stratum (parsley) appeared to hamper the ability of nocturnal predators to reach aphids more quickly on the collard host plants (higher stratum). In total, our findings indicate that intercropping non‐flowering companion plants is likely enough to mediate an increase of natural enemies via shelter provision. In addition, the results suggest that nocturnal predators, or non‐flying predators for that matter, are hampered by complex lower stratum vegetation. Thus, considering natural enemy behaviour and plant characteristics when designing polyculture systems are vital for attaining conservation biological control success.     

Jasmonate-deficient plants have reduced direct and indirect defences against herbivores

Plants employ a variety of defence mechanisms, some of which act directly by having a negative effect on herbivores and others that act indirectly by attracting natural enemies of herbivores. In this study we asked if a common jasmonate‐signalling pathway links the regulation of direct and indirect defences in plants. We examined the performance of herbivores (direct defence) and the attraction of natural enemies of herbivores (indirect defence) to wild‐type tomato plants and mutant plants that are deficient in the production of the signalling hormone jasmonic acid. Wild‐type plants supported lower survivorship of caterpillars compared with jasmonic acid‐deficient plants. Damaged wild‐type plants were more attractive to predaceous mites compared with undamaged wild‐type plants, whereas damaged jasmonate‐deficient plants were not more attractive to predators. Damaged wild‐type plants induced a greater production of volatile compounds (primarily the sesquiterpene β‐caryophyllene and the monoterpenes α‐pinene, β‐pinene, 2‐carene and β‐phellandrene) compared with damaged jasmonate‐deficient plants. Treating jasmonate‐deficient plants with exogenous jasmonic acid restored both the direct and indirect defence capabilities, demonstrating that jasmonic acid is an essential regulatory component for the expression of direct and indirect plant defence.     

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.     

Costs of induced volatile production in maize

Herbivore‐induced plant volatiles have been shown to serve as indirect defence signals that attract natural enemies of herbivores. Parasitoids and predators exploit these plant‐provided cues to locate their victims and several herbivores are repelled by the volatiles. Recently, benefits, in terms of plant fitness, from the action of the parasitoids were shown for a few systems. However, the cost of production of herbivore‐induced volatiles for the plant remains unknown. Here, we estimate the fitness cost of the production of induced volatiles in maize, Zea mays. Plants were treated with regurgitant of Spodoptera littoralis or with the elicitor volicitin and we measured dry weight of plant parts at specific times after treatments. After a two‐week treatment period, the dry‐weight of leaves of induced plants was lower than that of un‐induced plants, suggesting a metabolic cost for induced defence. However, maize plants seem to compensate for this loss during subsequent growth, since seed production at maturity was not different for unharmed plants and plants treated with caterpillar regurgitant. For volicitin treated plants a small but significant reduction in seed production was found. It is likely that the treatments also induced the production of other defence compounds, which will contribute to the cost. Yet, a comparison of six maize inbred lines with distinct differences in volatile emissions showed a strong correlation between the intensity of induced emissions and reduction in plant performance. An analysis of the terpenoids that accumulated in the leaves of the inbred lines revealed non‐volatilised compounds are constitutively present in maize and only the volatilised compounds are induced. Interestingly, the lines that released the largest amounts of induced volatiles also contained more of the non‐volatile terpenoids. Based on these results and results from a previous study on the benefits of attracting parasitoids, we conclude that costs of induced volatile production in plants are counterbalanced by the benefits as long as natural enemies of the herbivores are present in the environment.     

Plant traits mediate effects of predators across pepper (Capsicum annuum) varieties

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Trophic consequences of a biological invasion: do plant invasions increase predator abundance?

As invasive species become integrated into existing communities, they engage in a wide variety of trophic interactions with other community members. Many of these interactions are direct (e.g. predator–prey interactions or interference competition), but invasive species also can affect native community members indirectly, by influencing the abundances of intermediary species in trophic webs. Observational studies suggest that invasive plant species affect herbivorous arthropod communities and that these effects may flow up trophic webs to influence the abundance of predators. However, few studies have experimentally manipulated the presence of invasive plants to quantify the effects of plant invasion on higher trophic levels. Here, I use comparisons across sites that have or have not been invaded by the invasive plant Medicago polymorpha, combined with experimental removals of Medicago and insect herbivores, to investigate how a plant invasion affects the abundance of predators. Both manipulative and observational experiments showed that Medicago increased the abundance of the exotic herbivore Hypera and predatory spiders, suggesting positive bottom–up effects of plant invasions on higher trophic levels. Path analyses conducted on data from natural habitats revealed that Medicago primarily increased spider abundance through herbivore‐mediated indirect pathways. Specifically, Medicago density was positively correlated with the abundance of the dominant herbivore Hypera, and increased Hypera densities were correlated with increased spider abundance. Smaller‐scale experimental studies confirmed that Medicago may increase spider abundance through herbivore‐mediated indirect pathways, but also showed that the effects of Medicago varied across sites, including having no effect or having direct effects on spider abundance. If effects of invasive species commonly flow through trophic webs, then invasive species have the potential to affect numerous species throughout the community, especially those species whose dynamics are tightly connected to highly‐impacted community members through trophic linkages.     

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.     

Root herbivory induces an above-ground indirect defence

Indirect plant defences have largely been studied within the scope of above‐ground interactions. Here we provide novel evidence that root herbivory can induce an above‐ground indirect defence. Cotton plants (Gossypium herbaceum) exposed to root‐feeding wireworms (Agriotes lineatus) increased their foliar extrafloral nectar production ten‐fold in comparison to undamaged control plants. Mechanical root damage also yielded an increase in nectar production. In nature, extrafloral nectar production allows plants to recruit predators, which in turn protect the plant against above‐ground insect herbivores. Our results show that root‐feeding herbivores may alter such above‐ground defensive interactions.     

A biotrophic fungal infection of the great burnet Sanguisorba officinalis indirectly affects caterpillar performance of the endangered scarce large blue butterfly Phengaris teleius

Interactions between ecological communities of herbivores and microbes are commonly mediated by a shared plant. A tripartite interaction between a pathogenic fungus-host plant-herbivorous insect is an example of such mutual influences. In such a system a fungal pathogen commonly has a negative influence on the morphology and biochemistry of the host plant, with consequences for insect herbivore performance. Here we studied whether the biotrophic fbngus Podosphaera ferruginea, attacking the great burnet Sanguisorba officinalis, affects caterpillar performance of the endangered scarce large blue butterfly Phengaris teleius. Our results showed that the pathogenic ftmgus affected the number and size of inflorescences produced by food-plants and, more importantly, had in direct, plant-mediated effects on the abun dance, body mass and immune response of caterpillars. Specifically, we found the relationship between caterpillar abundance and variability in inflorescence size on a plant to be positive among healthy food-plants, and negative among infected food-plants. Caterpillars that fed on healthy food-plants were smaller than those that fed on infected food-plants in one studied season, while there was no such difference in the other season. We observed the relationship between caterpillar immune response and the proportion of infected great burnets within a habitat patch to be positive when caterpillars fed on healthy food-plants, and negative when caterpillars fed on infected food-plants. Our results suggest that this biotrophic fungal infection of the great burnet may impose a significant indirect influence on P. teleius caterpillar performance with potential consequences for the population dynamics and structure of this endangered butterfly.     

Larval parasitism rate increases in herbivore‐damaged trees: a field experiment with cyclic birch feeding moths

Indirect plant defence mechanisms enhance the effectiveness of natural enemies of herbivores. Herbivore‐induced plant volatiles (HIPVs) attract the parasitoids of insect herbivores as shown both in numerous choice tests conducted under laboratory conditions and in relatively few common‐garden setups in agro‐ecosystems. However, the importance of this indirect defence trait at higher levels of biological organization has yet to be investigated through natural field experiments. Here, we report a field experiment of larval parasitism of two cyclic geometrid defoliators in herbivore‐damaged and fairly intact mountain birch Betula pubescens ssp. czerepanovii under natural conditions. Parasitism rates in larvae of the autumnal (Epirrita autumnata) and winter moth (Operophtera brumata) exposed for 30 h on defoliated trees were more than twice as high as those on control trees. This finding indicates that hymenopteran parasitoids were attracted to previously defoliated trees by some cues from the host plants, HIPVs being the most likely candidates. The third trophic level should thus be considered in natural plant herbivore interactions. Furthermore, parasitoids and food resources are key factors in the population regulation of forest insect pests, and indirect plant defences could be important in their interactions. Our research also emphasizes the quality of control treatments in field experiments, since immediate plant responses easily obscure the results as soon as control trees become infested by herbivorous insects.     

Signal transduction downstream of salicylic and jasmonic acid in herbivory-induced parasitoid attraction by Arabidopsis is independent of JAR1 and NPR1

Plants can defend themselves indirectly against herbivores by emitting a volatile blend upon herbivory that attracts the natural enemies of these herbivores, either predators or parasitoids. Although signal transduction in plants from herbivory to induced volatile production depends on jasmonic acid (JA) and salicylic acid (SA), the pathways downstream of JA and SA are unknown. Use of Arabidopsis provides a unique possibility to study signal transduction by use of signalling mutants, which so far has not been exploited in studies on indirect plant defence. In the present study it was demonstrated that jar1‐1 and npr1‐1 mutants are not affected in caterpillar (Pieris rapae)‐induced attraction of the parasitoid Cotesia rubecula. Both JAR1 and NPR1 (also known as NIM1) are involved in signalling downstream of JA in induced defence against pathogens such as induced systemic resistance (ISR). NPR1 is also involved in signalling downstream of SA in defence against pathogens such as systemic acquired resistance (SAR). These results demonstrate that signalling downstream of JA and SA differs between induced indirect defence against herbivores and defence against pathogens such as SAR and ISR. Furthermore, it was demonstrated that herbivore‐derived elicitors are involved in induced attraction of the parasitoid Cotesia rubecula     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Plant neighbours mediate bird predation effects on arthropod abundance and herbivory

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Top predator control of plant biodiversity and productivity in an old-field ecosystem

Abstract Predators can have strong indirect effects on plants by altering the way herbivores impact plants. Yet, many current evaluations of plant species diversity and ecosystem function ignore the effects of predators and focus directly on the plant trophic level. This report presents results of a 3‐year field experiment in a temperate old‐field ecosystem that excluded either predators, or predators and herbivores and evaluated the consequence of those manipulations on plant species diversity (richness and evenness) and plant productivity. Sustained predator and predator and herbivore exclusion resulted in lower plant species evenness and higher plant biomass production than control field plots representing the intact natural ecosystem. Predators had this diversity‐enhancing effect on plants by causing herbivores to suppress the abundance of a competitively dominant plant species that offered herbivores a refuge from predation risk.