The influence of extrafloral nectaries on parasitism of an insect herbivore

The extrafloral nectaries of many plants promote ant defense against insect herbivores. We examined the influence of extrafloral nectaries on the levels of parasitism of a generalist insect herbivore, the gypsy moth (Lymantria dispar L.). Larvae and pupae of the moth were collected from trees with and without extrafloral nectaries growing in the same forests in South Korea and reared to evaluate parasitism. More parasitism occurred on plants with extrafloral nectaries in seven of the nine season-long collections at the six sites and in four out of five collecting periods. Parasitism was higher on the four main genera of plants with extrafloral nectaries than on any of five main genera of plants without extrafloral nectaries. There was no difference in parasitoid richness; nine species occurred in each group, eight of which were the same. There was a positive and almost significant correlation between the abundance of plants with extrafloral nectaries and the parasitism of gypsy moth at the sites. Extrafloral nectaries may reduce herbivory by inducing more parasitism of the insect herbivores that attack plants bearing the glands.     

Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism

Some species of the paleotropical tree genus Macaranga (Euphorbiaceae) live in close association with ants. The genus comprises the full range of species from those not regularly inhabited by ants to obligate myrmecophytes. In Malaysia (Peninsular and Borneo) 23 of the 52 species are known to be ant-associated (44%). The simplest structural adaptation of plants to attract ants are extrafloral nectaries. We studied the distribution of extrafloral nectaries in the genus Macaranga to assess the significance of this character as a possible predisposition for the evolution of obligate myrmecophytism. All species have marginal glands on the leaves. However, only the glands of non- myrmecophytic species function as nectaries, whereas liquids secreted by these glands in myrmecophytic species did not contain sugar. Some non-myrmecophytic Macaranga and transitional Macaranga species in addition have extrafloral nectaries on the leaf blade near the petiole insertion. All obligatorily myrmecophytic Macaranga species, however, lack additional glands on the lamina. The non-myrmecophytic species are visited by a variety of different ant species, whereas myrmecophytic Macaranga are associated only with one specific ant-partner. Since these ants keep scale insects in the hollow stems, reduction of nectary production in ant-inhabited Macaranga seems to be biologically significant. We interpret this as a means of (a) saving the assimilates and (b) stabilization of maintenance of the association's specificity. Competition with other ant species for food rewards is avoided and thereby danger of weakening the protective function of the obligate ant- partner for the plant is reduced. A comparison with other euphorb species living in the same habitats as Macaranga showed that in genera in which extrafloral nectaries are widespread, no myrmecophytes have evolved. Possession of extrafloral nectaries does not appear to be essential for the development of symbiotic ant-plant interactions. Other predispositions such as nesting space might have played a more important role.     

Ant visitation of extrafloral nectaries of Passiflora: the effects of nectary attributes and ant behavior on patterns in facultative ant-plant mutualisms

Extrafloral nectary (EFN) plants are widespread and can be quite species-rich in some communities. Thus, ants that utilize extrafloral nectar may have the opportunity to discriminate among a wide variety of nectar sources, resulting in variation in the ant attention EFN plants receive. In this study, we compare ant visitation rates of three Passiflora species that coexist in an early successional neotropical forest. These three vine species (Passiflora auriculata, P. biflora, and P. oerstedii) differ in their extrafloral nectary structure and placement, and thus may attract different numbers or species of ants. Through censuses of ants tending extrafloral nectaries, we found that P. auriculata received significantly higher numbers of ant visitors than P. oerstedii, but did not differ significantly from P. biflora in its attractiveness to ants. We also found that termite worker baits (simulating herbivores) placed on P. auriculata and P. biflora were discovered by ants significantly more quickly than baits placed on P. oerstedii. In both ant visitation censuses and in termite bait trials, we found no significant associations between Passiflora species and the species of ant visitors. We also performed experimental manipulations of several characteristics of P. auriculata, which resulted in changes in levels of ant visitation. When petiolar nectaries of P. auriculata were experimentally blocked, visitation by the common ant Ectatomma ruidum declined, even though nectaries on the leaf surfaces were still functional. Connections with other vegetation also had an effect on ant visitation. Though experimental creation of connections between growing P. auriculata shoots and other vegetation did not enhance ant visitation, eliminating connections resulted in a significant decline in the number of ant visitors. The results of this study suggest factors that may contribute to variation in ant visitation of extrafloral nectary plants. In addition, this study demonstrates that extrafloral nectary plants co-occurring in a habitat and available to the same ants may differ in patterns of visitation by ants and perhaps in the quality of protection from herbivores that they receive.     

Ant Defense Versus Induced Defense in Lafoensia pacari (Lythraceae), a Myrmecophilous Tree of the Brazilian Cerrado1

We compared the effects of ant presence at extrafloral nectaries of Lafoensia pacari St. Hil. on herbivore damage and silicon accumulation. Plants that were accessible to ants experienced lower herbivory levels over the first 3 mo of the experiment. After 3 mo, most leaves were fully expanded with inactive extrafloral nectaries; by 6 mo there was no effect of ant access on herbivore damage. Along with experiencing higher herbivory, plants in the ant‐exclusion treatment had significantly higher silicon levels in their leaves, suggesting that silicon serves as an induced defense in this ant–plant–herbivore interaction.     

Testing for mycorrhizal fungi-plant-ant indirect effects

Abstract

Recent work has demonstrated indirect effects between mycorrhizal fungi and insect herbivores and pollinators. The existence of indirect effects between mycorrhizal fungi and protection-for-food mutualists, such as extrafloral nectar-foraging ‘bodyguard ants’, is unknown. In this study, we examined the potential for indirect effects of arbuscular mycorrhizal fungi on aggressive ant bodyguards, mediated by changes in the expression of extrafloral nectaries of a shared host plant. We found that mycorrhizal plants grew larger and produced more extrafloral nectaries compared to their non-mycorrhizal counterparts. The difference in the number of nectaries between mycorrhizal and non-mycorrhizal plants, however, was too small to elicit differences in ant attendance. In spite of the lack of a significant indirect effect of mycorrhizal fungi on ant attendance, mycorrhizal plants suffered damage to a significantly greater proportion of their leaves compared to non-mycorrhizal plants. This result likely stems from other (non-ant-mediated) indirect effects of mycorrhizal fungi on herbivores.     

The role of leaf cutting and fire on extrafloral nectaries and nectar production in Stryphnodendron adstringens (Fabaceae,Mimosoideae) plants

Herbivory pressure is an important ecological aspect to determine quantitative variation in plant defenses, such as the number of extrafloral nectaries (EFNs) and their nectar amount and quality. Extrafloral nectaries can attract ants, which can be considered a type of induced plant defense. Besides, plants tend to invest more in defense when they are more vulnerable to herbivores. Therefore, we aimed to elucidate if Stryphnodendron adstringens (Fabaceae), a common Cerrado tree species, when subjected to damage (by manual leaf cutting and experimental fire) would produce a greater number of EFNs and changes its nectar quality on newly produced leaves in comparison with plants not subjected to these treatments. Leaf damage was performed artificially directly on the plant branches and at the entire plant canopy (by means of scissors or fire events). Extrafloral nectary density was higher in new leaves produced after the treatment application (artificial herbivory and fire) in comparison with plants under control treatment. The amount of nectar was also higher under treatments in comparison with control, with a significant change on nectar quality in plants subjected to the treatments of artificial herbivory. The results provided support for the hypothesis that EFNs are an inducible defensive strategy in S. adstringens, confirming the existence of phenotypic plasticity given environmental pressures.     

Herbivory-induced extrafloral nectar increases native and invasive ant worker survival

Ascertaining the costs and benefits of mutualistic interactions is important for predicting their stability and effect on community dynamics. Despite widespread designation of the interaction between ants and extrafloral nectaries (EFNs) as a mutualism and over 100 years of studies on ant benefits to plants, the benefits to ants have never been experimentally quantified. The success of invasive ants is thought to be linked to the availability of carbohydrate-rich resources, though reports of invasive ant visits to EFNs are mixed. In two laboratory experiments, we compared worker survival of one native (Iridomyrmex chasei) and two invasive ant species (Linepithema humile and Pheidole megacephala) exposed to herbivorized or non-herbivorized EFN-bearing plants (Acacia saligna) or positive and negative controls. We found that non-herbivorized plants did not produce any measurable extrafloral nectar, and ants with access to non-herbivorized plants had the same survival as ants with access to an artificial plant and water (unfed ants). Ants given herbivorized plants had 7–11 times greater worker survival relative to unfed ants, but there were no differences in survival between native and invasive ants exposed to herbivorized plants. Our results reveal that ants cannot induce A. saligna extrafloral nectar production, but workers of both native and invasive ant species can benefit from extrafloral nectar as much as they benefit from sucrose.     

Should aphids attract or repel ants? Effect of rival aphids and extrafloral nectaries on ant–aphid interactions

Among plants and herbivores, two types of conflicts occur in relation to mutualism with ants: one is competition for ant mutualism among myrmecophilous herbivores and plants, and the other is the conflict whether to attract or repel ants between myrmecophiles and nonmyrmecophiles that are damaged by ants. We investigated the extent to which two species of aphids (Megoura crassicauda and Aphis craccivora) and extrafloral nectaries on their host plant (Vicia faba var. minor) interact with one another for their relationships with ants. We designed an experiment where ants can choose to visit seedlings colonized by (1) M. crassicauda, (2) A. cracivora, (3) both aphid species, or (4) neither aphid species. Ants preferred A. craccivora to extrafloral nectaries and avoided tending M. crassicauda. We also analyzed the population growth of each aphid when it coexists with (1) ants, (2) the other aphid species, (3) ants and the other aphid species, or (4) neither of them. Under ant-free conditions, we detected an exploitative competition between the two aphid species. The ants had no significant effect on the population of A. craccivora, whereas they had negative effects on the population growth of M. crassicauda by attacking some individuals. When both aphids coexisted, M. crassicauda suffered ant attack more intensely because A. craccivora attracted more ants than extrafloral nectaries despite ant-repelling by M. crassicauda. On the other hand, the ants benefited A. craccivora by eliminating its competitor. To avoid ant attack, aphids may have been selected either to be more attractive to ants than other sympatric sugar sources or to repel the ants attracted to them. We hypothesize that competition among sympatric sugar sources including rival aphids and extrafloral nectaries is a factor restricting aphids to be myrmecophilous. Received: January 17, 2000 / Accepted: July 4, 2000     

THE FUNCTION OF EXTRAFLORAL NECTARIES IN OPUNTIA ACANTHOCARPA (CACTACEAE)

Opuntia acanthocarpa (Cactaceae) possesses extrafloral nectaries embedded in the areoles of new reproductive and vegetative growth. The nectar secreted by these glands attracts ants and is a nutritional food source. Members of one attracted ant species, Crematogaster opuntiae (Myrmicinae), are aggressive and efficient defenders of the plants against cactus-feeding insects. The results of our study are consistent with the ant-guard hypothesis for the role of extrafloral nectaries in O. acanthocarpa. Additionally, individuals of O. acanthocarpa are well protected in comparison with those of O. phaeacantha. The latter generally possess ephemeral extrafloral nectaries and consistently maintain fewer ants.     

Induced Floral and Extrafloral Nectar Production Affect Ant‐pollinator Interactions and Plant Fitness

Thousands of plant species throughout tropical and temperate zones secrete extrafloral nectar to attract ants, whose presence provides an indirect defense against herbivores. Extrafloral nectaries are located close to flowers and may modify competition between ants and pollinators. Here, we used Lima bean (Phaseolus lunatus L.) to study the plants interaction between ants and flower visitors and its consequences for plant fitness. To test these objectives, we carried out two field experiments in which we manipulated the presence of ants and nectar production via induction with jasmonic acid (JA). We then measured floral and extrafloral nectar production, the number of patrolling ants and flower visitors as well as specific plant fitness traits. Lima bean plants under JA induction produced more nectar in both extrafloral nectaries and flowers, attracted more ants and produced more flowers and seeds than non‐induced plants. Despite an increase in floral nectar in JA plants, application of this hormone had no significant effects on flower visitor attraction. Finally, ant presence did not result in a decrease in the number of visits, but our results suggest that ants could negatively affect pollination efficiency. In particular, JA‐induced plants without ants produced a greater number of seeds compared with the JA‐treated plants with ants.     

MORPHOLOGY AND DISTRIBUTION OF PETIOLAR NECTARIES IN IPOMOEA (CONVOLVULACEAE)

The distribution of petiolar nectaries in 24 species of Ipomoea was investigated. Petiolar nectaries were found on 12 species (8 new reports, 4 confirmations of previous reports) and quoted from the literature as being found on 3 other species; they were absent from 9 species investigated. The structure of petiolar nectaries in the genus ranges from simple beds of superficial nectar-secreting trichomes (1 species), to slightly recessed “basin nectaries” (8 species), to “crypt nectaries,” which are structurally the most complex extrafloral nectaries known (3 species). (Structures were not determined for 3 species.) Petiolar nectaries are present in all subgenera, but all crypt nectaries occur in the same section (Eriospermum). Species with extrafloral nectaries tend to be perennial; species lacking extrafloral nectaries tend to be annual. There is no relationship between temperate or tropical habitat and presence of nectaries.     

Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents

Summary Qualea grandiflora is a typical tree of Brazilian cerrados (savanna-like vegetation) that bears paired extrafloral nectaries (EFNs) along its stems. Results show that possession of EFNs increases ant density on Q. grandiflora shrubs over that of neighbouring non-nectariferous plants. Frequency of ant occupancy and mean number of ants per plant were much higher on Qualea than on plants lacking EFNs. These differences resulted in many more live termitebaits being attacked by foraging ants on Qualea than on neighbours without EFNs. Termites were attacked in equal numbers and with equal speeds on different-aged leaves of Qualea. The greatest potential for herbivore deterrence was presented by Camponotus ants (C. crassus, C. rufipes and C. aff. blandus), which together attacked significantly more termites than nine other ant species grouped. EFNs are regarded as important promoters of ant activity on cerado plants.     

Young leaf protection in the shrub Leea glabra in south-west China: the role of extrafloral nectaries and ants

Field experiments on Leea glabra in its natural forest habitat of southern Yunnan, China were conducted to study the effects of artificial damage of young and old leaves on extrafloral nectaries (EFNs) secretion quantity and sugar concentration, as well as the effects on ant abundance on the plants following the damage treatments. We found there were no rapid changes in extrafloral nectar volume or nectar sugar concentration which would indicate an induced reaction following artificial damage. However, both cutting and punching of young leaves resulted in a significant increase (2–4-fold) of ants within 6 h after damage compared to undamaged controls. In another experiment, disks of fresh young L. glabra leaves that were pinned on young leaves of another L.glabra plant also resulted in a significant increase in the number of ants compared to treatment with paper disks, indicating that ants were most probably attracted by volatile organic compounds (VOCs) released from damaged young leaves. Furthermore, we found that portion of damaged leaf area of young leaves was significantly lower than that of old leaves and the concentration of tannins was significantly higher in young than in medium and old leaves. In conclusion, our results show that young leaves of L. glabra are protected against attacks by herbivores by multiple mechanisms, which include: (1) the activity of EFNs, which attract different ant species from the surrounding ground; (2) a mechanism induced by the damage of young leaves, which leads to rapidly increased ant recruitment and is most probably caused by the release of volatiles from damaged leaf and (3) a higher allocation of tannins in young than in older leaves.     

Variation in the composition and activity of ants on defense of host plant <Emphasis Type="Italic">Turnera subulata</Emphasis> (Turneraceae): strong response to simulated herbivore attacks and to herbivore’s baits

Plants with extrafloral nectaries attract a variety of ant species, in associations commonly considered mutualistic. However, the results of such interactions can be context dependent. Turnera subulata is a shrub widely distributed among disturbed areas which has extrafloral nectaries at the base of leaves. Here, we evaluated whether the ants associated with T. subulata (i) vary in space and/or time; (ii) respond to simulated herbivory, and (iii) reduce herbivory rates. For this, we quantified the abundance and species richness of ants associated with T. subulata throughout the day in six different sites and the defensive capability of these ants under simulated herbivory in the leaves and stems of T. subulata plants (N = 60). We also checked the proportion of the lost leaf area and quantified leaf damage by chewing herbivores in the host plant. We found that a total of 21 ant species associated with the host plant. Species composition showed significant variation across the sampled sites and throughout the day. Visitation rates and predation by ants were higher in plant stems than in leaves. In general, herbivory rates were not correlated with ant association or activity, with the exception of the proportion of leaf area consumed; there was a significant lower herbivory rate on plants in which ants defended the leaves. Our results suggest that the benefits of association may depend on the ecological context. This context dependence may mask the correlation between the defense of ants and herbivory rates.     

FOLIAR NECTARIES OF UNUSUAL STRUCTURE IN LEONARDOXA AFRICANA (LEGUMINOSAE), AN AFRICAN OBLIGATE MYRMECOPHYTE

Extrafloral nectaries of an African myrmecophyte, Leonardoxa africana (Baill.) Aubr., are disc-shaped, non-vascularized, embedded in the leaf mesophyll, and have a tiny neck extending to the abaxial leaf surface. These structural features differ from those found in other members of the Leguminosae, and represent an unusual type among flowering plants. These embedded foliar nectaries apparently have an energetic advantage over external nectaries and their presence supports the idea of independent and repeated evolution of nectaries in the legume family.     

Fire triggers the activity of extrafloral nectaries,but ants fail to protect the plant against herbivores in a neotropical savanna

Herbivores are attracted to young shoots and leaves because of their tender tissues. However, in extrafloral nectaried plants, young leaves also attract patrolling ants, which may chase or prey on herbivores. We examined this scenario in extrafloral nectaried shrubs of Banisteriopsis malifolia resprouting after fire, which promoted both the aseasonal production of leaves and the activity of extrafloral nectaries (EFNs). Results were compared between resprouting (burned) and unburned control plants. The aggressive ant species Camponotus crassus and the herbivorous thrips Pseudophilothrips obscuricornis were respectively rapidly attracted to resprouting plants because of the active EFNs and their less sclerophyllous leaves. The abundance of these insects was almost negligible in the control (unburned) shrubs. Ants failed to protect B. malifolia, as no thrips were preyed upon or injured by ants in resprouting plants. Consequently, on average, 37 % of leaves from resprouting shrubs had necrosis marks. Upon contact with ants, thrips released small liquid droplets from their abdomen, which rapidly displaced ants from the surroundings. This study shows that P. obscuricornis disrupted the facultative mutualism between C. crassus and B. malifolia, since ants received extrafloral nectar from plants, but were unable to deter herbivore thrips.     

Extrafloral Nectaries of Dioscorea rotundata Poir.: Their Structure and Secretions

Extrafloral nectaries are to be found embedded in the leaf laminaof Dioscorea rotundata Poir., with a pore opening on to thelower leaf surface. The nectaries comprise small, densely cytoplasmiccells and are bounded by a layer of cells containing littleor no cytoplasm. Their secretion contains sucrose, fructoseand glucose with traces of galactose. Ninhydrin-positive compoundsare also present. Diosorra rotunrdata Poir, extrafloral nectaries, secretion, ultrastructure     

The occurrence and abundance of plants with extrafloral nectaries, the basis for antiherbivore defensive mutualisms, along a latitudinal gradient in east Asia

Abstract. The occurrence and abundance of indigenous plants with extrafloral nectaries was evaluated within local communities and regional floras along a north to south gradient from tundra in northeastern Russia (64–70°N) through temperate types in eastern Russia and Korea to subtropical vegetation in the Bonin Islands (26–27°N) south of Japan. Moving from tundra to subtropical vegetation, there is a pattern of increasing abundance of extrafloral bearing plants as a function of total plant cover (from 10.25 to 40.18%), number of species per sampled area (from 0.11 to 1.13/100 m), and proportion of species within regional floras (from 0.32 to 7.46%). There were some plants with extrafloral nectaries in all communities but their abundance varied greatly, c. 1–25% in the four northern latitudes and c. 7–70% in the subtropical region. Ants, the primary mutualists associated with plants bearing extrafloral nectaries, have a similar pattern of increasing abundance (species richness, nest density, and colony size) along the same north–south latitudinal gradient.     

A novel indirect defence in Brassicaceae: Structure and function of extrafloral nectaries in Brassica juncea

While nectaries are commonly found in flowers, some plants also form extrafloral nectaries on stems or leaves. For the first time in the family Brassicaceae, here we report extrafloral nectaries in Brassica juncea. The extrafloral nectar (EFN) was secreted from previously amorphic sites on stems, flowering stalks and leaf axils from the onset of flowering until silique formation. Transverse sections at the point of nectar secretion revealed a pocket‐like structure whose opening was surrounded by modified stomatal guard cells. The EFN droplets were viscous and up to 50% of the total weight was sugars, 97% of which was sucrose in the five varieties of B. juncea examined. Threonine, glutamine, arginine and glutamate were the most abundant amino acids. EFN droplets also contained glucosinolates, mainly gluconapin and sinigrin. Nectar secretion was increased when the plants were damaged by chewing above‐ and belowground herbivores and sap‐sucking aphids. Parasitoids of each herbivore species were tested for their preference, of which three parasitoids preferred EFN and sucrose solutions over water. Moreover, the survival and fecundity of parasitoids were positively affected by feeding on EFN. We conclude that EFN production in B. juncea may contribute to the indirect defence of this plant species.     

Alien and native tree species having extrafloral nectaries as favorite hunting area for arboreal endemic Philippine tiger beetles (Coleoptera: Cicindelidae) in human‐disturbed habitat in Lanao del Sur Province,Mindanao, Philippines

To document a relation between abundance of arboreal, predatory tiger beetles, their ant prey, and extrafloral nectaries attracting the ants, we gathered data from more than 10 species of native and introduced trees and large, tree‐like perennial plants in Lanao del Sur Province, Mindanao, Philippines. All specimens of tiger beetles (two Tricondyla and two Neocollyris species, all endemic to the country) were noted on five tree species characterized by presence of extrafloral nectaries, including three alien/invasive and two native ones. Invasive Spathodea campanulata and native Hibiscus tiliaceus were the most inhabited ones (respectively, 56% and 19% of beetles). Presence of tiger beetles on these trees most probably depends on high abundance of ants, which are typical prey for arboreal Cicindelidae, while occurrence of ants can result from presence of extrafloral nectaries on different parts of the plants. This suggests a new mutualistic insect–plant interaction between native and invasive species.