Ants suppressing plant pathogens: a review

Ant–plant mutualisms are usually regarded as driven by ants defending plants against herbivores in return for plant‐produced food rewards and housing. However, ants may provide additional services. In a review of published studies on ant–pathogen–plant interactions, we investigated whether ants’ extensive hygiene measures, including the use of ant‐produced antibiotics, extend to their host plants and reduce plant pathogen loads. From 30 reported species combinations, we found that the presence of ants lead to reduced pathogen levels in 18 combinations and to increased levels in 6. On average, ants significantly reduced pathogen incidence with 59%. This effect size did not differ significantly from effect sizes reported from meta‐analyses on herbivore protection. Thus, pathogen and herbivore protection could be of equal importance in ant–plant mutualisms. Considering the abundance of these interactions, ecological impacts are potentially high. Furthermore, awareness of this service may stimulate the development of new measures to control plant diseases in agriculture. It should be noted, though, that studies were biased toward tropical ant–plant symbioses and that the literature in the field is limited at present. Future research on plant pathogens is needed to enhance our understanding of ant–plant mutualisms and their evolution.     

The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores

Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores.     

Herbivore-herbivore interactions complicate links between soil fertility and pest resistance

Soil fertility is tightly linked with herbivore pressure because it affects the nutritional status of host plants as well as the production of anti-herbivore defenses. This in turn can influence whether herbivores in different feeding guilds render plants more or less susceptible to one another. Thus, growers’ fertility management choices may impact herbivores through a variety of indirect channels. We examined relationships between soil fertility and interactions between phloem-feeding and leaf-chewing herbivores on broccoli (Brassica oleracea) plants in the greenhouse, taking advantage of natural variation in nitrogen (N) and phosphorus (P) in soils from 20 working organic vegetable farms. Next, we experimentally fertilized soil in a field trial with N and/or P to examine the consequences of these nutrients for growth of and interactions between specialist and generalist herbivores. Soils on our cooperating farms varied widely in P and N concentrations, with 40% exceeding recommended pre-plant N concentrations and 90% exceeding P recommendations. In single-herbivore infestations, augmenting N in the soil increased caterpillar (Pieris rapae) growth, augmented N and P additively enhanced generalist green peach aphid (Myzus persicae) colonization, and augmented P (but not N) increased specialist cabbage aphid (Brevicoryne brassicae) growth. In dual-guild herbivore infestations, caterpillars facilitated specialist cabbage aphid growth in the absence of fertilizer, but this pattern disappeared under augmented N, and reversed under augmented P. We found that a complex web of indirect effects linked soil fertility to herbivore performance, depending on the identity of the nutrients being altered, the ecological roles of responding herbivore species (i.e., specialist versus generalist), and indirect interactions between chewing and sucking herbivores. More generally, we highlight that successful use of fertility management to improve pest resistance requires careful consideration of herbivore feeding niches and herbivore-herbivore interactions.     

Grazing refuges, external avoidance of herbivory and plant diversity

Avoidance and tolerance are the two means by which plants cope with herbivores. Avoidances internal to the plant, such as morphology, chemical repellants, thorns, etc., have received considerable attention in the plant‐herbivore literature, but relatively little consideration has been given to avoidances external to the plant. We develop a conceptual framework of external plant avoidances of herbivory based on foraging selection impedances (associational avoidances), behavioral impedances (indirect avoidances), and physical impedances (refuges) organized along axes of efficiency, degree of protection, and necessity of tolerance characteristics. Associational avoidances are uncommon for terrestrial mammalian herbivores compared to plant‐insect or marine situations. Indirect avoidances mediated through herbivore territoriality, predator avoidance, and other behaviors independent of foraging decisions are probably common in nature, but few have been formally documented. Biotic and geologic refuges providing a physical impedance are the only avoidances shown to have implications for plant biodiversity. This is particularly true for geologic refuges, where there is not a tradeoff between competition and the refuge effect. Small geologic refuges (rock outcrops, cliffs, etc.) are more likely to also positively or negatively alter associated plant microenvironments than large geologic refuges (mesas, islands, etc.). In a survey, 86% of small refuge studies reported positive effects on plant diversity compared to 50% for large refuges. Geologic refuges in more productive environments were more important in protecting diversity than refuges in less productive, semiarid environments, and the effects of protection were greater in communities with short compared to long evolutionary histories of grazing. Other characteristics of refuges such as extent across the landscape and the manner they alter or ameliorate the environment, as well as characteristics of the herbivore such as small or large, generalist or specialist may also determine the effectiveness of refuges, but there are too few studies to assess these factors.     

Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly

Variation of host quality affects population dynamics of parasitoids, even at the landscape scale. What causes host quality to vary and the subsequent mechanisms by which parasitoid population dynamics are affected can be complex. Here, we examine the indirect interaction of a plant pathogen with a parasitoid wasp. Under laboratory conditions, parasitoids from hosts fed fungus-infected plants weighed less than those from hosts fed uninfected plants, indicating that the fungus causes the hosts to be of poor quality. However, parasitoids reared from hosts fed fungal-infected diet also tended to be female, a characteristic associated with high host quality. The pathogen, herbivore and parasitoid persist regionally as metapopulations in a shared landscape in Aland, Finland. In an analysis of the metapopulation dynamics of the parasitoid over 6 years, the probability of colonization of a host population increased by more than twofold in patches occupied by the plant pathogen. While we cannot determine that the relationship is causal, a compelling explanation is that the plant pathogen facilitates the establishment by the parasitoid by increasing the fraction of female offspring. This is a novel mechanism of spatial multi-trophic level interactions.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

Habitat fragmentation and population features differently affect fruit predation,fecundity and offspring performance in a non‐specialist gypsum plant

• The effects of habitat fragmentation on plant populations are complex, as it might disrupt many ecological processes, including plant reproduction and plant–animal interactions. Gypsum specialist plants may be resilient to fragmentation due to their evolutionary history in fragmented landscapes, but the effects on non‐specialist plants occurring in gypsum are unknown.
• We conducted a study focusing on different aspects of the reproductive cycle of Astragalus incanus subsp. incanus, a plant facultatively linked to gypsum soils. We focused on plant fecundity and pre‐dispersal predation, obtained from field observations, and offspring performance, assessed in a common garden. Beyond fragment size and connectivity, we also considered habitat quality, population size and density and plant size as predictors.
• Fragment size and connectivity had no effect on plant fecundity, but jointly determined fruit predation, while fragment size was positively related to offspring growth. Population density, rather than population size, had a positive effect on predation but negatively affected plant fecundity and offspring performance. Habitat quality reduced both plant fecundity and predation incidence.
• In this non‐specialist species, habitat fragmentation, population features and habitat quality affect different facets of plant performance. Predation was the only process clearly affected by fragmentation variables, fecundity mainly depended on population features and offspring performance and was better explained by mother plant identity. Our results show the need to consider habitat and population features together with fragment size and connectivity in order to assess the effects of fragmentation. Importantly, these effects can involve different aspects of plant reproduction, including plant–animal interactions.

     

A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.     

The effects of plant population size on the interactions between the endangered plant Scorzonera humilis, a specialised herbivore, and a phytopathogenic fungus

We studied the effects of population size on the interactions between Scorzonera humilis (Asteraceae), its specialised seed-feeding fly Heterostylodes macrurus (Anthomyidae) and its specific systemic smut fungus Ustilago scorzonerae (Ustilaginales). The number of seeds developing per plant (potential seed production) strongly increased with population size in S. humilis. However, because seed predation by the seed feeding fly H. macrurus and the negative impact of the pathogen U. scorzonerae also increased, realised seed production was not related to population size. The probability of occurrence of H. macrurus increased with the population size of its host plant and its abundance increased more than proportionally. This suggests that Allee effects reduce insect abundance in small populations of S. humilis . The probability of occurrence of the fungus U. scorzonerae also increased with plant population size. Within populations, large genets were more likely to be infected than small ones. The systemic pathogen U. scorzonerae reduces the effective population size of its host because all flowers of an infected individual are sterilised. Nevertheless, in most populations the impact of the fly on reproduction was stronger than that of the pathogen, because most genets were not infected. Both parasites were rarer than the host plant itself, supporting the trophic-level hypothesis of island biogeography. Our results suggest that habitat fragmentation may release plants from parasites and pathogens. These positive effects of isolation and small population size may mask negative effects of fragmentation on, for instance, the quantity and quality of pollination.     

Model analysis for plant disease dynamics co-mediated by herbivory and herbivore-borne phytopathogens

Plants are subject to diseases caused by pathogens, many of which are transmitted by herbivorous arthropod vectors. To understand plant disease dynamics, we studied a minimum hybrid model combining consumer-resource (herbivore-plant) and susceptible-infected models, in which the disease is transmitted bi-directionally between the consumer and the resource from the infected to susceptible classes. Model analysis showed that: (i) the disease is more likely to persist when the herbivore feeds on the susceptible plants rather than the infected plants, and (ii) alternative stable states can exist in which the system converges to either a disease-free or an endemic state, depending on the initial conditions. The second finding is particularly important because it suggests that the disease may persist once established, even though the initial prevalence is low (i.e. the R(0) rule does not always hold). This situation is likely to occur when the infection improves the plant nutritive quality, and the herbivore preferentially feeds on the infected resource (i.e. indirect vector-pathogen mutualism). Our results highlight the importance of the eco-epidemiological perspective that integration of tripartite interactions among host plant, plant pathogen and herbivore vector is crucial for the successful control of plant diseases.     

Among population variation in specialist and generalist seed predation – the importance of host plant distribution, alternative hosts and environmental variation

Pre-dispersal seed predators can have important effects on population dynamics and trait selection in their host plants. However, the factors determining spatial variation in predation intensity are poorly known. We assessed the relative importance of host plant distribution, alternative hosts and environmental factors for among-population variation in predation in a system with three host plants, a specialist and a generalist pre-dispersal seed predator.
Effects of host plant population size were relatively more important in the specialist than in the generalist seed predator. The specialist seed predator Apion opeticum , utilizing only Lathyrus vernus occurred in less than half of the patches, and specialist seed predation was influenced only by host plant population size. The generalist Bruchus atomarius was present in nearly all patches, and generalist predation was influenced by environmental factors and availability of alternative hosts. Predation on alternative hosts was not affected by L. vernus presence.
The results suggest that a wide range of factors influences the strength of plant–seed–predator interactions, and that the relative importance of different factors depend on the degree of specialization. This will result in highly complex selection mosaics and coevolutionary trajectories.     

Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant

Plants growing in natural environments experience myriad interactions with a diverse assemblage of pathogens, parasites and mutualists. Many of these interactions involve symbiotic bacteria and fungi, but they also include macroparasitic plants. In this study, we investigated the interactions among a host grass (Lolium pratense, ex., Festuca pratensis), its symbiotic endophytic fungus (Neotyphodium uncinatum), a root hemiparasitic plant (Rhinanthus serotinus) of the host grass and a generalist herbivore (aphid Aulacorthum solani) of the hemiparasite. We demonstrate that the hemiparasitic plant acquires defending mycotoxins produced by the endophytic fungus living within their shared host grass. The uptake of defensive mycotoxins from the endophyte‐infected host grass enhances the resistance of the hemiparasitic plant to the generalist aphid herbivore. Endophyte infection increases the performance of the hemiparasitic plant, but reduces the growth of the host grass. In other words, the mutualistic endophytic fungus becomes parasitic in the presence of the hemiparasitic plant. Our results suggest that the outcomes of grass–endophyte interactions are conditional on the complexity of community‐level interactions; thus, the outcome of multispecies interactions may not be predictable from pair‐wise combinations of species.     

Herbivore host plant selection: whitefly learns to avoid host plants that harbour predators of her offspring

Evidence is accumulating that herbivorous arthropods do not simply select host plants based on their quality, but also on the predation risk associated with different host plants. It has been suggested that herbivores exclude plant species with high predation risk from their host range. This assumes a constant, predictable predation risk as well as a rather static behaviour on the part of the herbivore; plants are ignored irrespective of the actual predation risk. We show that adult females of a small herbivore, the whitefly Bemisia tabaci, can learn to avoid plants with predatory mites that attack only juvenile whiteflies, while they accept host plants of the same species without predators. Predatory mites disperse more slowly than whiteflies; they cannot fly and walk from plant to plant. Hence, by avoiding plants with predators, the whiteflies create a temporary refuge for their offspring. We suggest that the experience of arthropod herbivores with risks associated with host plants plays an important role in their host plant selection.     

Profiling the extended phenotype of plant pathogens

One of the most fundamental questions in plant pathology is what determines whether a pathogen grows within a plant? This question is frequently studied in terms of the role of elicitors and pathogenicity factors in the triggering or overcoming of host defences. However, this focus fails to address the basic question of how the environment in host tissues acts to support or restrict pathogen growth. Efforts to understand this aspect of host–pathogen interactions are commonly confounded by several issues, including the complexity of the plant environment, the artificial nature of many experimental infection systems and the fact that the physiological properties of a pathogen growing in association with a plant can be very different from the properties of the pathogen in culture. It is also important to recognize that the phenotype and evolution of pathogen and host are inextricably linked through their interactions, such that the environment experienced by a pathogen within a host, and its phenotype within the host, is a product of both its interaction with its host and its evolutionary history, including its co‐evolution with host plants. As the phenotypic properties of a pathogen within a host cannot be defined in isolation from the host, it may be appropriate to think of pathogens as having an ‘extended phenotype’ that is the product of their genotype, host interactions and population structure within the host environment. This article reflects on the challenge of defining and studying this extended phenotype, in relation to the questions posed below, and considers how knowledge of the phenotype of pathogens in the host environment could be used to improve disease control.

• What determines whether a pathogen grows within a plant?
• What aspects of pathogen biology should be considered in describing the extended phenotype of a pathogen within a host?
• How can we study the extended phenotype in ways that provide insights into the phenotypic properties of pathogens during natural infections?

     

Resistance to Plant Invasion? A Native Specialist Herbivore Shows Preference for and Higher Fitness on an Introduced Host

The response of native herbivores to the introduction of a new plant to the community has important implications for plant invasion. Under the Enemy Release Hypothesis introduced species become invasive because of reduced enemy control in the new range, while under the New Association Hypothesis introduced species lack effective defenses against native enemies because they do not share an evolutionary history. I tested the response of a native South-American specialist herbivore Utetheisa ornatrix (Lepidoptera: Arctiidae) to a native (Crotalaria incana) and an introduced host (Crotalaria pallida) (Fabaceae: Papilionoideae). I compared seed predation rates between the two hosts in the field, and I tested preference and performance traits with common garden experiments. Utetheisa ornatrix caused much higher seed predation rates on the introduced host than on the native host. Females also preferred to oviposit on the introduced over the native host. Additionally, larvae feeding on the introduced host had higher fitness (higher pupal weight) than larvae feeding on the native host. I discuss how the response of this specialist herbivore to this introduced host plant contradicts the predictions of the Enemy Release Hypothesis and support the New Association Hypothesis. This study shows that the New Association Hypothesis can also be true for specialist herbivores.     

Plant‐mediated effects of host plant density on a specialist herbivore of Solanum carolinense

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Species-specific herbivore–herbivore interactions and plant responses to sequential attack by multiple herbivores on a perennial woody plant

When plants are sequentially attacked by multiple herbivores, herbivore identity and host specialization can greatly influence the patterns of herbivore–herbivore and plant–herbivore interactions. However, how prior herbivory and the resulting induced plant responses potentially affect subsequent herbivores deserves further investigation. In this study, we conducted a common-garden experiment that manipulated sequential herbivory by the specialist caterpillar Gadirtha fusca Pogue (Lepidoptera: Nolidae) and the generalist caterpillar Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) on Chinese tallow, Triadica sebifera (L.) Small (Euphorbiaceae). We tested how prior exposure to herbivores with different levels of host specialization affected the performance of subsequently arriving con- and heterospecifics, as well as plant growth and defense responses under subsequent herbivory. We found that prior exposure to the specialist G. fusca facilitated the performance of subsequent conspecifics, resulting in a significant decrease in the growth (height and stem diameter at ground level) of tallow plants. However, prior exposure to the generalist S. litura did not affect the feeding of subsequent con- or heterospecifics or the growth of tallow plants. Sequential herbivory by specialist and generalist conspecifics resulted in lower levels of tannins and flavonoids, respectively, in leaves of tallow plants, whereas sequential herbivory by the two species did not affect the levels of tannins or flavonoids, compared to a single damage event. We conclude that herbivore species-specific plant responses appear to be more important than herbivore identity or specialization in determining herbivore–herbivore interactions and plant responses to sequential herbivore attack.     

Intraspecific variation in host plant traits mediates taxonomic and functional composition of local insect herbivore communities

1. Host plant phenotypic traits affect the structure of the associated consumer community and mediate species interactions. Intraspecific variation in host traits is well documented, although a functional understanding of variable traits that drive herbivore community response is lacking. We address this gap by modelling the trait-environment relationship using insect traits and host plant traits in a multilevel model. 2. We compare herbivore assemblages from the canopy of the phenotypically variable tree Metrosideros polymorpha on Hawai‘i Island. Multiple distinct varieties of M. polymorpha frequently co-occur, with variation in morphological traits. Using this system, we identify host and insect traits that underlie patterns of herbivore abundance and quantify the strength of host-insect trait interactions. 3. This work examines plant-insect interactions at a community scale, across 36 herbivore species in three orders. We find that co-occurring trees of varying phenotype support distinct communities. Leaf traits, including specific leaf area, trichome presence, and leaf nutrients, explain 46% of variation in insect communities. We find that feeding guild and nymphal life history are correlated with host plant traits, and we show that model predictions are improved by including the host and insect trait interaction. 4. This study demonstrates how insect herbivores traits influence community response to morphologically variable hosts. Environmental heterogeneity indirectly affected herbivore community structure via intraspecific variation in host plants, providing an important source of variation for maintaining diversity in the broader community.