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.     

Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries

Background and Aims

Early ontogenetic stages of myrmecophytic plants are infrequently associated with ants, probably due to constraints on the production of rewards. This study reports for the first time the anatomical and histological limitations constraining the production of extrafloral nectar in young plants, and the implications that the absence of protective ants imposes for plants early during their ontogeny are discussed.

Methods

Juvenile, pre-reproductive and reproductive plants of Turnera velutina were selected in a natural population and their extrafloral nectaries (EFNs) per leaf were quantified. The anatomical and morphological changes in EFNs during plant ontogeny were studied using scanning electron and light microscopy. Extrafloral nectar volume and sugar concentration were determined as well as the number of patrolling ants.

Key Results

Juvenile plants were unable to secrete or contain nectar. Pre-reproductive plants secreted and contained nectar drops, but the highest production was achieved at the reproductive stage when the gland is fully cup-shaped and the secretory epidermis duplicates. No ants were observed in juvenile plants, and reproductive individuals received greater ant patrolling than pre-reproductive individuals. The issue of the mechanism of extrafloral nectar release in T. velutina was solved given that we found an anatomical, transcuticular pore that forms a channel-like structure and allows nectar to flow outward from the gland.

Conclusions

Juvenile stages had no ant protection against herbivores probably due to resource limitation but also due to anatomical constraints. The results are consistent with the growth-differentiation balance hypothesis. As plants age, they increase in size and have larger nutrient-acquiring, photosynthetic and storage capacity, so they are able to invest in defence via specialized organs, such as EFNs. Hence, the more vulnerable juvenile stage should rely on other defensive strategies to reduce the negative impacts of herbivory.     

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.     

Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries

Many plants secrete nectar from extrafloral nectaries (EFNs), specialized structures that usually attract ants which can act as plant defenders. We examined the nectar-mediated interactions between Chamaecrista nictitans (Caesalpineaceae) and jumping spiders (Araneae, Salticidae) for 2 years in old fields in New Jersey, USA. Previous research suggests that spiders are entirely carnivorous, yet jumping spiders (Eris sp. and Metaphidippus sp.) on C. nictitans collected nectar in addition to feeding on herbivores, ants, bees, and other spiders. In a controlled-environment experiment, when given a choice between C. nictitans with or without active EFNs, foraging spiders spent 86% of their time on plants with nectar. C. nictitans with resident jumping spiders did set significantly more seed than plants with no spiders, indicating a beneficial effect from these predators. However, the presence of jumping spiders did not decrease numbers of Sennius cruentatus (Bruchidae), a specialist seed predator of C. nictitans. Jumping spiders may provide additional, unexpected defense to plants possessing EFNs. Plants with EFNs may therefore have beneficial interactions with other arthropod predators in addition to nectar-collecting ants. Received: 27 May 1998 / Accepted: 23 December 1998     

The diversity,ecology and evolution of extrafloral nectaries: current perspectives and future challenges

Background

Plants in over one hundred families in habitats worldwide bear extrafloral nectaries (EFNs). EFNs display a remarkable diversity of evolutionary origins, as well as diverse morphology and location on the plant. They secrete extrafloral nectar, a carbohydrate-rich food that attracts ants and other arthropods, many of which protect the plant in return. By fostering ecologically important protective mutualisms, EFNs play a significant role in structuring both plant and animal communities. And yet researchers are only now beginning to appreciate their importance and the range of ecological, evolutionary and morphological diversity that EFNs exhibit.

Scope

This Highlight features a series of papers that illustrate some of the newest directions in the study of EFNs. Here, we introduce this set of papers by providing an overview of current understanding and new insights on EFN diversity, ecology and evolution. We highlight major gaps in our current knowledge, and outline future research directions.

Conclusions

Our understanding of the roles EFNs play in plant biology is being revolutionized with the use of new tools from developmental biology and genomics, new modes of analysis allowing hypothesis-testing in large-scale phylogenetic frameworks, and new levels of inquiry extending to community-scale interaction networks. But many central questions remain unanswered; indeed, many have not yet been asked. Thus, the EFN puzzle remains an intriguing challenge for the future.     

Role of floral repellents in the regulation of flower visits of extrafloral nectary-visiting ants in an Indian crop plant

Abstract.  1. Field investigation of the association between sponge gourd, Luffa cylindrica plants and its ant visitors revealed that five of the six most frequent species: Camponotus compressus, C. paria, Pheidole sp., Pachycondyla tesserinoda and Tetramorium sp. mainly visited the extrafloral (EF) nectaries present on the leaves, bracts, bracteoles and calyx of the plant. Tapinoma melanocephalum was the only ant species observed at the floral as well as the EF nectaries.
2. A bioassay of ant behaviour revealed aversion to young and mature unisexual flowers of sponge gourd in the five predominantly EF nectary-visiting ant species, while floral preference was demonstrated in T. melanocephalum. A significant difference was not found in the number of insect pollinators visiting T. melanocephalum occupied and un-occupied flowers, suggesting the absence of deterrent effect of this tiny ant species on the pollinators.
3. Further behavioural assays showed preference for 2- and 4-day-old leaves and also 2-day-old buds, while the 4-day-old buds induced avoidance in all the species. Androecium and gynoecium had significantly higher repellent effects in comparison to the petals. Thus floral repellents, probably help to reduce nectar theft and prevent loss of pollen function.
4. This aversion was not demonstrated in the case of old flowers. A significantly greater number of insect pollinators visited young and mature flowers compared with old flowers, suggesting that selective exclusion of medium- and large-sized EF nectary-visiting ant species from the flowers, as a result of aversion to floral repellents, serves to avoid the threat of attack to insect pollinators of sponge gourd.     

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.     

Structure and biology of nectaries in Tabebuia serratifolia Nichols (Bignoniaceae)

THOMAS, V. & DAVE, Y., 1992. Structure and biology of nectaries in Tabebuia serratifolia Nichols (Bignoniaceae) . Tabebuia has both floral and extrafloral nectaries, situated on the petiole, bract, calyx, around the ovary and on the pericarp. The floral nectary present around the ovary base is differentiated into epidermis, secretory zone and sub-secretory zone. It is supplied by phloem strands up to the secretory zone. A mature extrafloral nectary consists of a single large basal cell and a head comprising a layer of vertically arranged elongated cells. Starch, protein and lipid are present in the floral nectary. The major insect visitors to both types of nectaries are honey bees, houseflies and ants.     

虎刺花外蜜腺的发育解剖学研究

应用扫描电镜、石蜡制片及组织化学技术对虎花外蜜腺的形态,结构及发育过程中结构及多糖变化进行了较为系统的研究,结果表明,虎刺花外密腺位于状花序外的总苞顶部5枚随圆形裂端,属于总苞上的密腺,由分泌表皮,产蜜组织和主要由韧皮部筛管组成的维管束构成,虎刺花外蜜腺起源于总苞裂片顶端表面的4－5层原始细胞,根据蜜腺结构特点及多糖变化分析,原蜜汁的贮存及多糖的降解主要在产蜜组织细胞中进行,而分泌表皮细胞则是原蜜汁的加工及蜜汁的合成与分泌的主要场所。     

Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in <Emphasis Type="Italic">Vicia faba</Emphasis>

Arbuscular mycorrhizal fungi (AMF) can alter the physiology and morphology of their host plant, and therefore may have indirect effects on insect herbivores and pollinators. We conducted this study to test the hypothesis that AMF can also affect insects involved in protection-for-food mutualisms. We examined the constitutive and inducible production of food rewards [extrafloral (EF) nectaries] in Vicia faba plants by manipulating the presence/absence of AMF and by simulating various levels of herbivory. Plants inoculated with AMF produced significantly fewer EF nectaries than uninoculated plants, even after accounting for differences in plant growth. In contrast to earlier studies, EF nectaries were not inducible: damaged plants produced significantly fewer EF nectaries than undamaged plants. Moreover, the effects of mycorrhizal and damage status on EF nectary production were additive. The reduction in EF nectaries in mycorrhizal plants potentially represents a mechanism for indirect effects of AMF on the protective insects that exploit EF nectaries as a food source (e.g., ants). Reduced reward size should result in reduced protection by ants, and could therefore be a previously unappreciated cost of the mycorrhizal symbiosis to host plants. However, the overall effect of AMF will depend upon the extent to which the reduction of EF nectaries affects the number and activity of ants and the extent to which AMF alter other aspects of host plant physiology. Our results emphasize the complexity of multitrophic interactions, particularly those that span belowground and aboveground ecology.     

Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation

Abstract. 1. Ants (Myrmica spp. and Formica lemani) visiting the extrafloral nectaries of bracken, Pteridium aquilinum, imposed heavy mortality on caterpillars of a novel moth species experimentally introduced onto bracken fronds. However, the exclusion of ants from bracken fronds had no significant effect on adapted bracken-feeding herbivores in Britain.
2. The feeding stages of British bracken-feeding insects are immune to, or can largely avoid, predation by ants in a variety of ways. Gall formers and miners cannot be attacked by these ants. Two other species hide, one inside tied leaves, the other in a mass of 'spittle'. Another group of species jumps away from, or falls off the plant when touched by ants. Sawfly caterpillars in the genera Strongylogaster, Aneugmenus and Tenthredo have viscous, distasteful haemolymph that repels ants.
3. No species of bracken herbivore has an absolute temporal refuge from ants; during their development they all overlap with ants to some degree.
4. Ant predation appears to have played a significant role in determining the contemporary structure of British bracken-feeding insect communities. Distasteful haemolymph in sawfly caterpillars may have evolved in response to selection from ant predation. Other species may fortuitously possess characteristics, evolved in response to a variety of selective forces, that also reduce the impact of ants; without such characteristics, however, we postulate that they would be unable to live on this plant. An absence of external, foliage feeding Lepidoptera early in the spring, a high proportion of sawfly species, and a high proportion of gall-formers and miners may all be characteristics of the bracken herbivore community which have been influenced by ant predation.     

Targeted predation of extrafloral nectaries by insects despite localized chemical defences

Extrafloral (EF) nectaries recruit carnivorous arthropods that protect plants from herbivory, but they can also be exploited by nectar thieves. We studied the opportunistic, targeted predation (and destruction) of EF nectaries by insects, and the localized chemical defences that plants presumably use to minimize this effect. In field and laboratory experiments, we identified insects that were possibly responsible for EF nectary predation in Vicia faba (fava bean) and determined the extent and accuracy of the feeding damage done to the EF nectaries by these insects. We also performed biochemical analyses of plant tissue samples in order to detect microscale distribution patterns of chemical defences in the area of the EF nectary. We observed selective, targeted feeding on EF nectaries by several insect species, including some that are otherwise not primarily herbivorous. Biochemical analyses revealed high concentrations of l-3,4-dihydroxyphenylalanine, a non-protein amino acid that is toxic to insects, near and within the EF nectaries. These results suggest that plants allocate defences to the protection of EF nectaries from predation, consistent with expectations of optimal defence theory, and that this may not be entirely effective, as insects limit their exposure to these defences by consuming only the secreting tissue of the nectary.     

The function of extrafloral nectaries in the pollination and reproduction of Sambucus javanica

Sambucus javanica is a perennial herb with extrafloral nectaries (EFNs) on its inflorescences. To explore the ecological functions of EFNs, a factorial combination experiment of ant (access or exclusion) and EFNs (with or without) at the plant level was created in two populations. The role of EFNs in the attraction of ants and flying pollinators, the defensive role of ants against foliar herbivores, the effects of ants on pollinator visitation and the effects of ant–pollinator interactions on fruit production in one or both populations were assessed. Ants were common on the ant-access plants with EFNs, but absent from the ant-access plants without EFNs. Foliar herbivory was independent of ant and EFN treatments and their interactions. The visitation frequency of flying pollinators (honeybees and syrphid flies) and fruit set were significantly higher for plants with EFNs than plants without EFNs, but were not affected by ant treatments or their interactions with EFN treatments. These results suggest that EFNs in S. javanica attracted both ants and flying pollinators, but ants did not present a defensive role against herbivores, did not deter flying pollinators from visiting inflorescences and had no effects on fruit production. In addition, ants were not significant pollen vectors.     

Herbivory-induced overcompensation and resource-dependent production of extrafloral nectaries in Luffa cylindrica (Cucurbitaceae)

Extrafloral nectaries (EFNs) are nectar secretory structures involved in the indirect defense of plants. In the sponge gourd (Luffa cylindrica), EFNs commonly occur on the lower surface of leaf blades and stipules and remain functional until leaf senescence. To test the hypothesis that the development of EFNs is influenced by herbivore damage and resource availability, we grew Luffa cylindrica under different concentrations of Hoagland's nutrient solution (nutrient-poor conditions: 10%, 50%; and control condition: 100%) and two herbivory treatments (damaged and undamaged leaves). We collected ten leaves from treated plants to quantify leaf area and EFN density. Overall, leaf area increased and EFN decreased in damaged plants, but this significantly depended on nutritional status. In undamaged plants, EFN density tended to remain constant, whereas foliar area increased with nutrient input. Under herbivory, foliar area increased at 10% but decreased at 50 and 100% of nutrients in relation to undamaged plants, whereas EFN density tended to increase with nutrient availability to exceed undamaged plants under control concentrations. Plants under nutrient-poor conditions subjected to herbivory exhibited an increased foliar area, characterizing a compensatory mechanism. Our results suggest that herbivore-induced indirect defense is a damage- and resource-dependent response in Luffa cylindrica. These findings contribute to understanding the factors that modulate indirect defenses and plant-herbivore-environment interactions.     

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.     

Distribution and abundance of plants with extrafloral nectaries in the woody flora of a lowland primary forest in Malaysia

The first data on the taxonomic distribution and abundance of woody plants with extrafloral nectaries (EFN) from SE Asia are reported. The species richness and frequency of woody angiosperm plants with extrafloral nectaries was studied in the Pasoh Forest Reserve, a primary lowland forest in Peninsular Malaysia. EFN were present on 12.3% of the 741 species surveyed. 91 plant species belonging to 47 genera and 16 families were found to have EFN. Euphorbiaceae, Dipterocarpaceae, Rosaceae, Leguminosae, and Ebenaceae were the families most frequently bearing EFN whereas EFN were rare in the more primitive subclasses of the Magnoliopsida and common in the more advanced taxa (Dilleniidae, Rosidae, Asteridae). Most common were flattened glands associated with the leaf blade. A comparison with data from the Neotropics showed a great similarity in regard to the taxonomic distribution of plants with EFN. EFN-plants occupied 19.3% of the cover of the Pasoh Forest 50 ha plot.Species with EFN were under-represented among shrubs and trees of the understorey. We found an increase in the number of species with EFN as well as in their cover from the understorey to the canopy emergents. EFN were found more often among the abundant species (species with n>500/50 ha). Percentage occurrence and cover of EFN-bearing plants in the 50 ha plot of primary forest was lower than recorded for secondary habitats in tropical areas. At present, in the core zone of the Pasoh Forest Reserve which has been investigated only few species known to indicate disturbance occur. Therefore most of the recorded EFN-species cannot be regarded as secondary forest plants.The interactions between ants and EFN-bearing plants appear to be rather facultative and nonspecific. In Pasoh we found 28 ant species from seven genera visiting EFN. Most of the EFN-associated ants belonged to the subfamily Myrmicinae while Ponerines were rare, a pattern which was also reported for the Neotropics.In cooperation with the Forest Research Institute Malaysia, Kepong, 52109 Kuala Lumpur, Selangor, Malaysia.     

The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae)

1. Shrubs of Caryocar brasiliense are intensively visited by many ant species in the cerrado vegetation of south-east Brazil. Ants collect nectar from the extrafloral nectaries (EFNs) located on the buds at the apex of the plant.
2. The proportion of C. brasiliense shrubs occupied by ants greatly surpassed that of neighbouring plants without EFNs and this resulted in many more termites being attacked and removed on this plant than on plants lacking EFNs. Ant attacks on Caryocar were more frequent near the EFNs.
3. Ant-exclusion experiments with Caryocar shrubs revealed that ants significantly reduce the infestation levels by the butterfly Eunica bechina , the sucking bud Edessa rufomarginata , the bud-destroying fly Prodiplosis floricola and by a stem-galling wasp. Ants had no effect on the infestation by a leaf-galling wasp.
4. Control (ants present) and treatment (ants excluded) plants produced equal numbers of buds but flower and initial fruit production was significantly greater for ant-visited plants. Higher abortion rates of initial fruits by control plants resulted in similar final fruit and seed sets for plants in either experimental category.
5. The extremely low fertility of cerrado soils is suggested as a possible factor constraining the ability of Caryocar shrubs to provide the resources necessary for growth and development of their heavy fleshy fruits. Higher production of initial fruits by ant-visited shrubs would be neutralized by competition among developing fruits and subsequent abortion.
6. Possible ant-derived benefits to C. brasiliense include: protection of vegetative tissues during plant growth, larger floral display and increased attractiveness to bat pollinators, increased male contribution to fitness through pollen donation and selective abortion of genetically inferior progeny as the maternal investment is adjusted to match available resources.