Extrafloral nectaries in Philodendron (Araceae): distribution and structure

Extrafloral nectaries (EFNs) are involved in animal–plant interactions that lead to protection against herbivory. The presence of EFNs in Araceae is rare, besides Philodendron, there is report for only two other genera. With the aim to investigate the occurrence of EFNs in Philodendron and to describe the distribution patterns and structural organization of these glands, 75 Philodendron spp. were examined, 16 of which were selected for study by light microscopy. Three Homalomena spp. were also examined for EFNs, but these were not found. Philodendron martianum was employed as a model for additional study using scanning and transmission electron microscopy. The studied EFNs showed a high degree of structural similarity. They were present in the prophyll, leaf and spathe, becoming functional in young organs. In surface view, EFNs consisted of small areas and showed one or more stomata through which secretions were released. The secretory cells formed a globular region surrounded by ground parenchyma. In P. martianum, nectariferous parenchyma cells exhibited typical features of cells with high metabolism related to nectar secretion. These results allow us to infer that EFNs have a widespread occurrence in Philodendron, and they remain an exclusive character for this group. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 229–240.     

Foliar Extrafloral Nectar of Humboldtia brunonis (Fabaceae), a Paleotropic Ant‐plant,is Richer than Phloem Sap and More Attractive than Honeydew

The ant‐plant Humboldtia brunonis secretes extrafloral nectar (EFN) despite the lack of antiherbivore protection from most ants. EFN was richer in composition than phloem sap and honeydew from untended Hemiptera on the plant, suggesting that EFN could potentially distract ants from honeydew, since ants rarely tended Hemiptera on this plant.     

Concentration and retention of chlorophyll around the extrafloral nectary of Mallotus japonicus

Plants need to allocate some of their limited resources for defense against herbivores as well as for growth and reproduction. However, the priority of resource allocation within plants has not been investigated. We hypothesized that plants with extrafloral nectaries (EFNs) invest more chlorophyll around their EFNs—to support a high rate of carbon fixation there—than in other leaf parts of young leaves. Additionally, this chlorophyll may remain around EFNs rather than in the other leaf parts. We used Mallotus japonicus plants to investigate the chlorophyll content at leaf centers and edges and around EFNs at four stages of leaf development: middle‐expanded young leaves, fully expanded mature leaves, senior leaves, and leaves prior to abscission. These four stages of development were located at the third, fifth, eighth, and eleventh leaf positions from the apex, respectively. The results revealed that the chlorophyll content around the EFN side of the third‐position leaves was higher than that at the leaf center or edge. Although the chlorophyll content in the fifth‐position leaves did not differ between those at the leaf edge and around EFNs, the chlorophyll content around EFNs in the eighth‐position leaves was higher than that at the leaf centre and edge. The volume of EF nectar was positively correlated with the chlorophyll content around EFN during the leaf stage, but it was not correlated with the chlorophyll content in the leaf center and edge, except in fifth‐position leaves. These findings suggest that M. japonicus plants facilitate and maintain secretion of EF nectar in their young and old leaves, respectively, through the concentration and retention of chlorophyll around EFNs.     

Host‐plant use by two Orthomeria (Phasmida: Aschiphasmatini) species feeding on Macaranga myrmecophytes

Myrmecophytes depend on symbiotic ants (plant‐ants) to defend against herbivores. Although these defensive mechanisms are highly effective, some herbivorous insects can use myrmecophytes as their host‐plants. The feeding habits of these phytophages on myrmecophytes and the impacts of the plant‐ants on their feeding behavior have been poorly studied. We examined two phasmid species, Orthomeria alexis and O. cuprinus, which are known to feed on Macaranga (Euphorbiaceae) myrmecophytes in a Bornean primary forest. Our observations revealed that: (i) each phasmid species relied on two closely‐related myrmecophytic Macaranga species for its host‐plants in spite of their normal plant‐ant symbioses; and (ii) there was little overlap between their host‐plant preferences. More O. cuprinus adults and nymphs were found on new leaves, which were attended by more plant‐ants than mature leaves, while most adults and nymphs of O. alexis tended to avoid new leaves. In a feeding choice experiment under ant‐excluded conditions, O. alexis adults chose a non‐host Macaranga myrmecophyte that was more intensively defended by plant‐ants and was more palatable than their usual host‐plants almost as frequently as their usual host‐plant, suggesting that the host‐plant range of O. alexis was restricted by the presence of plant‐ants on non‐host‐plants. Phasmid behavior that appeared to minimize plant‐ant attacks is described.     

Specificity of herbivore‐induced responses in an invasive species,Alternanthera philoxeroides (alligator weed)

Herbivory‐induced responses in plants can both negatively affect subsequently colonizing herbivores and mitigate the effect of herbivory on the host. However, it is still less known whether plants exhibit specific responses to specialist and generalist herbivores in non‐secondary metabolite traits and how specificity to specialists and generalists differs between invasive and native plant populations. We exposed an invasive plant, Alternanthera philoxeroides, to Agasicles hygrophila (Coleoptera, Chrysomelidae; specialist), Spodoptera litura (Lepidoptera, Noctuidae; generalist), manual clipping, or application of exogenous jasmonic acid and examined both the specificity of elicitation in traits of fitness (e.g., aboveground biomass), morphology (e.g., root:shoot ratio), and chemistry (e.g., C/N ratio and lignin), and specificity of effect on the subsequent performance of A. hygrophila and S. litura. Then, we assessed variation of the specificity between invasive and native populations (USA and Argentina, respectively). The results showed S. litura induced higher branching intensity and specific leaf area but lower C/N ratio than A. hygrophila, whereas A. hygrophila induced higher trichome density than S. litura. The negative effect of induction on subsequent larval growth was greater for S. litura than for A. hygrophila. Invasive populations had a weaker response to S. litura than to A. hygrophila in triterpenoid saponins and C/N ratio, while native populations responded similarly to these two herbivores. The specific effect on the two herbivores feeding on induced plants did not vary between invasive and native populations. Overall, we demonstrate specificity of elicitation to specialist and generalist herbivores in non‐secondary metabolite traits, and that the generalist is more susceptible to induction than the specialist. Furthermore, chemical responses specific to specialist and generalist herbivores only exist in the invasive populations, consistent with an evolutionary change in specificity in the invasive populations.     

Timing of induced resistance in a clonal plant network

After local herbivory, plants can activate defense traits both at the damaged site and in undamaged plant parts such as in connected ramets of clonal plants. Since defense induction has costs, a mismatch in time and space between defense activation and herbivore feeding might result in negative consequences for plant fitness. A short time lag between attack and defense activation is important to ensure efficient protection of the plant. Additionally, the duration of induced defense production once the attack has stopped is also relevant in assessing the cost–benefit balance of inducible defenses, which will depend on the absence or presence of subsequent attacks. In this study we quantified the timing of induced responses in ramet networks of the stoloniferous herb Trifolium repens after local damage by Mamestra brassicae larvae. We studied the activation time of systemic defense induction in undamaged ramets and the decay time of the response after local attack. Undamaged ramets became defense‐induced 38–51 h after the initial attack. Defense induction was measured as a reduction in leaf palatability. Defense induction lasted at least 28 days, and there was strong genotypic variation in the duration of this response. Ramets formed after the initial attack were also defense‐induced, implying that induced defense can extend to new ramet generations, thereby contributing to protection of plant tissue that is both very vulnerable to herbivores and most valuable in terms of future plant growth and fitness.     

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores.Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied.We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses.Plant quality was quantified through oviposifion of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species.Spider-mite oviposifion data show that T.evansi could suppress an earlier induction of plant defenses by T.urticae,and T.urticae could induce defenses in plants previously attacked by T.evansi in 1 day.Longer attacks by the second species did not result in further changes in oviposifion.Proteinase inhibitor activity levels showed that T.evansi suppressed the high activity levels induced by T.urticae to constitutive levels in 1 day,and further suppressed activity to levels similar to those in plants attacked by T.evansi alone.Attacks by T.urticae induced proteinase inhibitor activity in plants previously attacked by T.evansi,eventually to similar levels as induced by T.urticae alone.Hence,plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance,but does affect proteinase inhibitor activity levels.Based on our results,we discuss the evolution of suppression of plant defenses.     

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.     

Conservation of an Ant–plant Mutualism in Native Forests and Ecologically‐managed Tree Monocultures

The Brazilian Atlantic Forest has been replaced by homogeneous tree monocultures with potentially drastic effect on ecological interactions. We expect that ecologically‐managed tree monocultures, however, can help to mitigate this impact. Here, we carried out an experiment with Inga vera (Fabaceae), an extrafloral nectary bearing plant, to test if the efficiency of ants as anti‐herbivory defense is affected by the replacement of its natural habitat (Araucaria Forest) by ecologically‐managed tree monocultures (plantations of Araucaria, Pinus, and Eucalyptus). Seedlings of Inga vera were transplanted to three patches of each habitat and ants were excluded from half of the plants. The abundance of ants and herbivores was low, similar among habitats, and exhibited temporal asynchrony. Number of herbivores and accumulated herbivory levels were lower in plant with ants. Rates of herbivory were extremely low and lower for young leaves than for mature leaves. The presence of ants did not affect plant performance traits measured by their growth in height, and their final numbers of leaves and leaflets. Contrary to what might be expected, ant‐protected plants produced fewer leaves and leaflets than unprotected ones. In conclusion, Inga vera‐ant interaction was similar between its natural habitat and the tree monocultures, indicating that potentially both species diversity and ecological processes can be conserved in ecologically‐managed tree monocultures.     

Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human‐driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.     

Ant Species Identity has a Greater Effect than Fire on the Outcome of an Ant Protection System in Brazilian Cerrado

Although fire‐ and ant–plant interactions influence the community structure and dynamics of Neotropical savannas, no previous studies have considered their simultaneous effects on target host plants. We monitored the effect of ant exclusion for 3 years on leaf area loss to leaf chewing insects, thrips abundance, and reproductive output of the extrafloral nectary‐bearing shrub, Peixotoa tomentosa (Malpighiaceae). We predicted that the impact of ants on herbivores and plants would depend on the ant species, and that fire would reduce the effect of ants. We deliberately chose control plants that differed in their occupant ant species. Fire occurred in the second year of the study, allowing us to determine its effect on the benefit afforded by ants. Ants reduced leaf area loss and thrips abundance, and increased fruit and seed production in all 3 years. Some ant species were more effective than others, while plants with multiple ant species suffered higher leaf area loss than plants with a single ant species. In the year following the fire, leaf damage was greater than in the other years, regardless of the ant species, and the proportional effect of ants in reducing damage was less. Interactions affecting thrips abundance did not change following fire, nor was the benefit to the plant proportionally reduced. Overall, the identity of the ant species had a greater effect than did the occurrence of fire on the ant–herbivore–plant interaction: the identity of the ant species influenced leaf area loss, thrips numbers, and bud and seed production, while fire only modified the impact of ants on the amount of leaf area consumed by insect herbivores.     

Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species

The present study examined whether or not coexisting congeneric plant species have different defense strategies against herbivores, and the intensity of defense changes ontogenetically. We focused on nine myrmecophytic Macaranga species and estimated the intensity of non-biotic and biotic defense by the degree of leaf damage in ant-free and ant-occupied plants, respectively. Ant colonization of myrmecophytic Macaranga species occurred in the early stage of plant development (5–50 cm-tall seedlings). Following the colonization, damage by leaf eaters was minimized and stable during the ontogenetic development of the host plants due to protection by ants. In ant-free trees, however, herbivore damage was immense in seedlings and decreased as trees grew. Interspecific comparison of leaf damage and herbivore fauna supported that coexisting congeneric plants differ in their types of non-biotic (chemical/structural) defense: without ant protection, Macaranga beccariana, for example, was somewhat resistant to leaf eaters but susceptible to gall-makers, Macaranga trachyphylla was heavily infested by generalist leaf eaters, and Macaranga winkleri was exploited by ant-predatory birds. Despite these variations in chemical/structural defense, ant-colonized plants were generally well defended by ants against all kinds of herbivores. This suggests that the individual host-specific ant mutualists are well adapted to deter the chemically or structurally adapted herbivores. These results imply that in the history of diversification in the Macaranga–ant–herbivore system, a sequence of mutual counter adaptation took place not only between plants and herbivores but also between ants and herbivores.     

Aquatic grazers reduce the establishment and growth of riparian plants along an environmental gradient

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Nectar quality affects ant aggressiveness and biotic defense provided to plants

Ant–plant mutualisms are useful models for investigating how plant traits mediate interspecific interactions. As plant‐derived resources are essential components of ant diets, plants that offer more nutritious food to ants should be better defended in return, as a result of more aggressive behavior toward natural enemies. We tested this hypothesis in a field experiment by adding artificial nectaries to individuals of the species Vochysia elliptica (Vochysiaceae). Ants were offered one of four liquid foods of different nutritional quality: amino acids, sugar, sugar + amino acids, and water (control). We used live termites (Nasutitermes coxipoensis) as herbivore competitors and observed ant behavior toward them. In 88 hr of observations, we recorded 1,009 interactions with artificial nectaries involving 1,923 individual ants of 26 species. We recorded 381 encounters between ants and termites, of which 38% led to attack. Sixty‐one percent of these attacks led to termite exclusion from the plants. Recruitment and patrolling were highest when ants fed upon nectaries providing sugar + amino acids, the most nutritious food. This increase in recruitment and patrolling led to higher encounter rates between ants and termites, more frequent attacks, and faster and more complete termite removal. Our results are consistent with the hypothesis that plant biotic defense is mediated by resource quality. We highlight the importance of qualitative differences in nectar composition for the outcome of ant–plant interactions. Abstract in Portuguese is available with online material.     

Effects of host plant on life‐history traits in the polyphagous spider mite Tetranychus urticae

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.     

Maize plants prime anti-herbivore responses by the memorizing and recalling of airborne information in their genome

Intact maize plants prime for defensive action against herbivory in response to herbivore-induced plant volatiles (HIPVs) emitted from caterpillar-infested conspecific plants. The recent research showed that the primed defense in receiver plants that had been exposed to HIPVs was maintained for at least 5 d after exposure. Herbivory triggered the receiver plants to enhance the expression of a defense gene for trypsin inhibitor (TI). At the upstream sequence of a TI gene, non-methylated cytosine residues were observed in the genome of HIPV-exposed plants more frequently than in that of healthy plant volatile-exposed plants. These findings provide an innovative mechanism for the memory of HIPV-mediated habituation for plant defense. This mechanism and further innovations for priming of defenses via plant communications will contribute to the development of plant volatile-based pest management methods in agriculture and horticulture.     

Sugar and amino acid composition of ant‐attended nectar and honeydew sources from an Australian rainforest

Abstract Ants (Hymenoptera: Formicidae) consume a broad spectrum of liquid food sources including nectar and honeydew, which play a key role in their diet especially in tropical forests. This study compares carbohydrates and amino acids from a representative spectrum of liquid sources used by ants in the canopy and understorey of a tropical rainforest in northern Queensland, Australia. Eighteen floral nectars, 16 extrafloral nectars, two wound sap and four homopteran honeydew sources were analysed using high performance liquid chromatography. Wounds comprised flower abscission scars on Normanbya normanbyi L. H. Bailey and bitemarks on Cardwellia sublimis F. Muell. where ants were actively involved in wounding. Discriminant analysis was performed to model differences between food sources in sugar and amino acid concentration and composition. All characteristics varied significantly among plant species. Honeydew contained a broader spectrum of sugars (including melezitose, raffinose, melibiose, lactose and maltose) than nectar (sucrose, glucose, fructose), but certain extrafloral nectars had similar amino acid profiles and, like honeydew sources, were often monopolized by ants. Most common amino acids across the sources were proline, alanine and threonine among 17 α‐amino acids identified. Interspecific variability concealed characteristic differences in sugar and amino acid parameters between nectar, honeydew and wound sap across all plants, but these types differed significantly when found on the same plant. Among all sources studied, only a few flower nectars were naturally not consumed by ants and they were significantly less attended than sugar controls in feeding trials. These nectars did not differ in sugars and amino acids from ant‐attended flower nectars, suggesting the activity of repellents. Apart from these exceptions, variability in amino acids and carbohydrates is proposed to play a key role in ant preferences and nutrition.     

Foraging behavior of Brachygastra lecheguana (Hymenoptera: Vespidae) on Banisteriopsis malifolia (Malpighiaceae): Extrafloral nectar consumption and herbivore predation in a tending ant system

In the Brazilian savanna many plant species bear regular associations with patrolling ants that are aggressive towards insect herbivores. However, not only ants but also several species of predatory wasps are attracted to plants due to the extrafloral nectaries (EFNs). Such wasps feed on both herbivores and plant exudates. In this study we describe the foraging behavior of the social Polistinae wasp Brachygastra lecheguana in the extrafloral nectaried shrub Banisteriopsis malifolia, and investigated the influence of patrolling ants Camponotus blandus on the activity of the wasp. Brachygastra lecheguana fed on the endophytic larvae of Anthonomus (Curculionidae) beetles that developed inside flower buds. The wasp lacerated the bud layers to reach the beetle larvae located at the bud core. The wasp visits to Ba. malifolia were statistically related to the abundance of flower buds and beetles. Ant exclusion experiments revealed that the hunting behavior of B. lecheguana on beetles was not related to the absence of C. blandus. However we found that wasps spent more time consuming extrafloral nectar on branches where ants were excluded. This is the first study reporting extrafloral nectar consumption by B. lecheguana, as well as the predation on herbivores in natural areas. In cerrado vegetation, ants benefit the plant by reducing insect herbivores, and our study provides evidence that the B. lecheguana – Ba. malifolia system represents a potential interaction where the wasp may also benefit the host plant. The value of this wasp species as a plant‐guard is discussed.