THE EXTRAFLORAL NECTARIES OF IPOMOEA CARNEA (CONVOLVULACEAE)

Ipomoea carnea (Convolvulaceae) possesses two types of extrafloral nectaries, located on the petiole and on the pedicel. These secrete a complex nectar containing sugars and amino acids. The insects attracted to the extrafloral nectaries are predominantly ants and they are relatively abundant throughout the year. A number of incidents of plant defense as a result of the presence of extrafloral nectary visitors at the extrafloral nectaries of I. carnea were observed and are consistent with the ant-guard theory of the function of extrafloral nectaries.     

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.     

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     

FOSSIL EXTRAFLORAL NECTARIES,EVIDENCE FOR THE ANT-GUARD ANTIHERBIVORE DEFENSE IN AN OLIGOCENE POPULUS

Extrafloral nectaries are secretory glands, usually found on leaves, that have been shown to promote ant defense against the insect herbivores of many modem day plants. Extrafloral nectaries were found on the 35-million-year-old fossil leaves of the extinct Populus crassa from Florissant, Colorado. Extinct ant species (belonging to five still extant genera that have modem ant-guard species), and other predators and parasitoids (whose modem relatives frequent extrafloral nectaries) also lived at Florissant. The extrafloral nectaries of P. crassa (and perhaps other plants) probably operated to attract ants and/or other arthropod defenders as early as the Oligocene.     

FACULTATIVE MUTUALISM BETWEEN WEEDY VETCHES BEARING EXTRAFLORAL NECTARIES AND WEEDY ANTS IN CALIFORNIA

Vetches (Vicia spp.) were studied in the San Francisco Bay Area of California in the spring of 1978. The stipular nectaries of the vetches are visited by the Argentine ant, Iridomyrmex humilis Mayr. The nectaries were removed to exclude ants in controlled experiments to determine if these ants protect the vetches from herbivores or seed predators. Plants with excised nectaries suffered substantially greater damage to their foliage than control plants, indicating that ants protect the foliage. There was no indication that ants protect the vetches from seed predators, but fruit set was substantially lower in plants with excised nectaries. Analysis of sugar and amino acid composition of extrafloral nectar served as a basis for feeding tests with Argentine ants by using artificial nectar solutions. Ants preferred sucrose and glucose solutions over fructose. They showed no preference for any one sugar mixture over another, nor did they exhibit differential recruitment to artificial nectar solutions containing only sugars or sugars and amino acids.     

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.     

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.     

No Defensive Role of Ants throughout a Broad Latitudinal and Elevational Range of a Cactus

Defensive mutualisms mediated by extrafloral nectaries are particularly variable; their net results may change with seasons, communities and environmental contexts. Particularly, an environmental factor that can promote changes in outcomes of ant‐plant interactions is elevation in mountainous regions. We tested whether (1) the interaction between the cactus Opuntia sulphurea and ant visitors of extrafloral nectaries is a defensive mutualism; and (2) ant‐plant interaction outcomes vary with elevation as a result of changes in herbivory rate and ant activity. To evaluate if the outcome of interactions was consistent at two extremes of the range distribution of O. sulphurea, we performed an ant‐exclusion experiment with plants at two growth conditions (natural or potted) in two sites with contrasting elevation (1235–1787 m asl) in a temperate region (Villavicencio Nature Reserve, Mendoza, Argentina), and in a tropical region (Huajchilla, La Paz, Bolivia). Although herbivory rate and ant visitation frequency increased with elevation, herbivore damage, plant reproductive success, and cladode growth rate were similar between plants excluded and non‐excluded from ants among sites, geographic regions and growth conditions. These results do not support the hypotheses that the interaction between O. sulphurea and ants is a defensive mutualism, and that elevation affects the net outcome of this ant‐plant interaction.     

Nutrient transfer supports a beneficial relationship between the canopy ant,Azteca trigona,and its host tree

1. Energy fluxes between ants and plants have been a focal point for documenting mutualistic behaviour. Plants can provide resources to ants through the production of extrafloral nectaries. In exchange, ants can fertilise plants through their nutrient‐ and microbe‐rich refuse. 2. Here, we test a potential facultative mutualism between the carton‐nesting canopy ant, Azteca trigona, and their host trees. Through observational and experimental approaches, this study documents how nutrient transfer provides a basis for this beneficial ant–plant relationship. 3. In a greenhouse experiment, fertilisation with sterilised refuse (i.e. nutrients only) increased seedling growth three‐fold, while the refuse with its natural microbial community increased growth 11‐fold. 4. Total root density was doubled in refuse piles compared with the surrounding area in situ. On average, refuse provides host trees and the surrounding plant community with access to a > 800% increase in N, P and K relative to leaf litter. 5. Azteca trigona preferentially nests in trees with extrafloral nectaries and on large, longer‐lived tree species. 6. Given the nutrient‐poor nature of the Neotropics, host trees probably experience significant benefits from refuse fertilisation. Conversely, A. trigona benefit from long‐term stable structural support for nests and access to nutrient‐rich extrafloral nectaries. Without clear costs to either A. trigona or host trees, it is proposed that these positive interactions are preliminary evidence of a facultative mutualism.     

EXTRAFLORAL NECTARIES AND PLANT GUARDING IN IPOMOEA PANDURATA (L.) G. F. W. MEY. (CONVOLVULACEAE)

Throughout the range of Ipomoea pandurata in North and South Carolina, ants and wasps are attracted to the pedicellar extrafloral nectaries. These hymenopterans are aggressive toward phytophagous insects that visit the plants. Protection of the plant is afforded by these pugnacious hymenopteran nectar feeders.     

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.     

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.     

Response of fire ants (Formicidae: Solenopsis invicta and S.gerninata) to artificial nectars with amino acids

Abstract.

• 1 The role that amino acids in extrafloral nectars play in attracting ants to plants was investigated. Workers from laboratory colonies of Solenopsis invicta Buren and S.geminafa (F). (Formicidae) fed from artificial nectaries containing mimics of the extrafloral nectar of Passiflora menispermifoh and P.caerulea; P.menispermifoh nectar contains higher levels of amino acids (1347.3 pdml) than does the nectar of P.currulea (125.2 μm /ml).
• 2 When sugar-only and sugar—amino acid nectar mimics were presented simultaneously, more S.invicta workers were counted at sugar—amino acid nectar mimics than at sugar-only nectars. S.geminatu did not discriminate between the two nectars.
• 3 When the two Pamiflora L. nectar mimics were presented simultaneously, S.invicta and S.geminata workers were more abundant at the nectaries containing high levels of amino acids (P.menispermifolia HBK mimic) than at the nectaries containing low levels of amino acids (P.cuerulea L. mimic).
• 4 The behaviour shown by S.invicta and S.gerninata suggests that plants with high levels of amino acids in their extrafloral nectars attract more ant protectors and might suffer less herbivory than plants producing nectars with low levels of amino acids. If so, ants may favour, over evolutionary time, plants that produce nectars with high levels of amino acids.
• 5 Day-to-day variability in ant behaviour was considerable even among laboratory colonies maintained on the same diet in similar environmental conditions. This variability will reduce the selective impact that ants have on plants and may help to explain why most ant-plant interactions are facultative.

     

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.     

Relationships between the ant Brachymyrmex obscurior (Hymenoptera, Formicidae) and Acacia pennatula (Fabaceae)

Summary. In central Mexico, the ant Brachymyrmex obscurior Forel feeds on nectar produced by extrafloral nectaries of Acacia pennatula (Schlecht. & Cham.) Benth. However, no studies have determined whether the ants visitation is related to plant nectar availability and whether ants protect A. pennatula from herbivory. The objectives of this 2-yr study (2000–2001) were to assess whether seasonal changes in ant visitation coincide with extrafloral nectar productivity in A. pennatula and to determine whether ants protect the plant. At the end of the dry season (April–June) B. obscurior was the only ant species on A. pennatula and extrafloral nectar production is limited to this period. Exclusion experiments, performed at the end of the dry season showed that A. pennatula did not receive a protective benefit when visited by ants. Branches with ants and branches where ants are excluded had similar numbers of the nonmyrmecophile leafhopper Sibovia sp. which was the only herbivore observed under natural conditions.Received 24 March 2004; revised 4 September 2004; accepted 8 September 2004.     

Florivorous myrmecophilous caterpillars exploit an ant–plant mutualism and distract ants from extrafloral nectaries

Females of myrmecophilous butterflies tend to oviposit in plants visited by ant species that engage in stable associations with its larvae. In Banisteriopsis malifolia, caterpillars are attended by the same ants that feed on extrafloral nectaries. A conflict may arise when both the plant and caterpillars compete for ant attention, and ants are assumed to forage on the highest quality resource. By attending caterpillars, ants can be indirectly detrimental to plant fitness because florivorous larvae feed intensively until pupation. In this study, we specifically investigated (i) whether the occurrence of facultative myrmecophilous Synargis calyce (Riodinidae) caterpillars in B. malifolia was based on ant species (Camponotus blandus or Ectatomma tuberculatum) and abundance; (ii) the monopolization of ants by the butterfly larvae and (iii) the florivory rates incurred by the caterpillars on inflorescences. The abundance of S. calyce was six‐fold greater in plants with C. blandus, compared to E. tuberculatum treatments. Caterpillars monopolized up to 50% of C. blandus on the plants, indicating that the resources offered by S. calyce were more attractive to ants than extrafloral nectaries. Florivory by riodinids incurred losses of almost 60% of flower buds. Myrmecophilous riodinids exploited an ant–plant mutualism by attracting aggressive ants that become larvae bodyguards. Thus, this ecological interaction is potentially detrimental to B. malifolia, since the ants, which can provide protection against herbivores, shift to provide defence for one of these herbivores.     

Biotic resistance and invasional meltdown: consequences of acquired interspecific interactions for an invasive orchid,Spathoglottis plicata in Puerto Rico

Invasiveness of non-native species often depends on acquired interactions with either native or naturalized species. A natural colonizer, the autogamous, invasive orchid Spathoglottis plicata has acquired at least three interspecific interactions in Puerto Rico: a mycorrhizal fungus essential for seed germination and early development; a native, orchid-specialist weevil, Stethobaris polita, which eats perianth parts and oviposits in developing fruits; and ants, primarily invasive Solenopsis invicta, that forage at extrafloral nectaries. We tested in field experiments and from observational data whether weevils affect reproductive success in the orchid; and whether this interaction is density-dependent. We also examined the effectiveness of extrafloral nectaries in attracting ants that ward off weevils. Only at small spatial scales were weevil abundance and flower damage correlated with flower densities. Plants protected from weevils had less floral damage and higher fruit set than those accessible to weevils. The more abundant ants were on inflorescences, the less accessible fruits were to weevils, resulting in reduced fruit loss from larval infections. Ants did not exclude weevils, but they affected weevil activity. Native herbivores generally provide some biotic resistance to plant invasions yet Spathoglottis plicata remains an aggressive colonizer despite the acquisition of a herbivore/seed predator partly because invasive ants attracted to extrafloral nectaries inhibited weevil behavior. Thus, the invasion of one species facilitates the success of another as in invasional meltdowns. For invasive plant species of disturbed habitats, having ant-tended extrafloral nectaries and producing copious quantities of seed, biotic resistance to plant invasions can be minimal.     

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.     

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.     

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.