Are extrafloral nectaries efficient against herbivores? Herbivory and plant defenses in contrasting tropical species

植物用于防御的资源有限，而那些具有生物防御的物种，其叶片可能会较少地用于其他类型的防御。我们比较了机械防御能力较弱，但具有花外蜜腺的植物，与没有花外蜜腺但叶片更有韧性的植物是否更不容易被取食。我们通过分析文献数据，调查有无花外蜜腺的植物被取食的情况。在巴西南部的热带稀树草原植被中，我们采集了6种热带植物的叶片数据，并测定了被取食情况和比叶面积。我们进一步评估了有无花外蜜腺的物种之间以及植物之间被取食情况和比叶面积的差异。为了检验动物取食与叶片韧性之间的关系，我们对单株平均被取食情况和平均叶片韧性进行了回归。研究结果表明，植物表现出不同程度的叶片损伤，但没有蚂蚁防御的植物因被取食造成的叶面积损失最大。不同植物的机械防御水平也不相同。无花外蜜腺的植株更坚韧，比叶面积值更小。虽然无花外蜜腺的植物有更多的坚硬叶片，但这种机械防御不足以损害和/或减少食草动物的取食，这表明由蚂蚁形成的生物防御可能比用于与叶片适口性相关的机械防御更有效。     

Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores

Many plant species grow extrafloral nectaries and produce nectar to attract carnivore arthropods as defenders against herbivores. Two nectary types that evolved with Populus trichocarpa (Ptr) and Populus tremula × Populus tremuloides (Ptt) were studied from their ecology down to the genes and molecules. Both nectary types strongly differ in morphology, nectar composition and mode of secretion, and defense strategy. In Ptt, nectaries represent constitutive organs with continuous merocrine nectar flow, nectary appearance, nectar production, and flow. In contrast, Ptr nectaries were found to be holocrine and inducible. Neither mechanical wounding nor the application of jasmonic acid, but infestation by sucking insects, induced Ptr nectar secretion. Thus, nectaries of Ptr and Ptt seem to answer the same threat by the use of different mechanisms.     

Extrafloral nectary-bearing plant Mallotus japonicus uses different types of extrafloral nectaries to establish effective defense by ants

Extrafloral nectary (EFN)-bearing plants attract ants to gain protection against herbivores. Some EFN-bearing plants possess different types of EFNs, which might have different effects on ants on the plants. Mallotus japonicus (Thunb.) Muell. Arg. (Euphorbiaceae) bears two types of EFNs, including a pair of large EFNs at the leaf base and many small EFNs along the leaf edge. This study aimed to determine the different roles of the two types of EFNs in biotic defense by ants. A field experiment was conducted to investigate the effect of leaf damage on EFN production and on the distribution pattern of ants. After leaf damage, the number of leaf edge EFNs increased in the leaves first-produced. The number of ants on the leaves also increased, and the foraging area of ants extended from the leaf base to the leaf tip. An EFN-covering field experiment revealed that leaf edge EFNs had a greater effect than leaf base EFNs on ant dispersal on leaves. The extended foraging area of ants resulted in an increase of encounter or attack rate against an experimentally placed herbivore, Spodoptera litura. These results suggest that M. japonicus plants control the foraging area of ants on their leaves using different types of EFNs in response to leaf damage, thus achieving a very effective biotic defense against herbivores by ants.

     

Influence of extrafloral nectary phenology on ant–plant mutualistic networks in a neotropical savanna

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Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities

Ant dominance in tropical ecosystems can be explained by a capacity to exploit liquid foods such as extrafloral nectaries (EFNs) and secretions from honeydew-producing hemipterans (HPHs). Such nutritious exudates may determine ant distribution in space and shape specialization in ant–plant interactions. We provide a first assessment of how EFNs and HPHs mediate the structure of ant assemblages, ant visitation intensity, and characteristics of ant–plant interaction networks across space in Brazilian “cerrado” savanna. We used arboreal pitfall traps to sample visiting ants in four cerrado localities and recorded the presence of lepidopteran larvae to determine their possible response to ant visitation. Ant species composition and richness did not differ regardless of the presence of liquid rewards on plants, and most network patterns did not show consistent differences. However, in two of the four sites, ant densities were higher on plants with HPHs or EFNs due to increased activity by Camponotus and Pseudomyrmex ants. At these two sites, plants with liquid food sources had a more specific ant assemblage (higher specialization d′) than did plants without resources, and caterpillars were more frequently found on plants with fewer workers of Camponotus and Pseudomyrmex. Plants with HPHs had increased ant visitation and accumulated more ant species than did plants with EFNs or without liquid foods. Ant response to such food sources may thus depend on local conditions and identity of ant species, and may determine how ant assemblages are structured. Results highlight how different patterns of ant visitation to liquid resources can produce distinctive effects on herbivore infestation.     

Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae)

1. This study examines the anti-herbivore effect of ants visiting the extrafloral nectaries (EFNs) of Opuntia stricta (Cactaceae) and its possible influence on the plant's reproductive output in Mexican coastal sand dunes. Opuntia 's EFNs are located in the areoles of the developing tissue of emerging cladodes and flower buds.
2. Ants visited the EFNs of O . stricta on a round-the-clock basis. The associated ant assemblage was formed by nine species distributed in four subfamilies, and the species composition of the principal ant visitors changed markedly from day to night period.
3. Cladodes of control (ants present) and treatment (ants excluded) plants of Opuntia were equally infested by sucking bugs and mining dipterans. Damage to buds by a pyralid moth, however, was significantly higher on treatment than on control plants. Ant visitation to Opuntia 's EFNs translated into a 50% increase in the plant's reproductive output, as expressed by the number of fruits produced by experimental control and treatment branches. Moreover, fruit production by ant-visited branches was positively and significantly associated with the mean monthly rate of ant visitation to EFNs.
4. This is the first demonstration of ant protection leading to increased fruit set in the Cactaceae under natural conditions. Although the consequences of damage by sucking and mining insects remain unclear for Opuntia , the results show how the association of EFNs with vulnerable reproductive plant organs can result in a direct ant-derived benefit to plant fitness.     

Morphological characterization of extrafloral nectaries and associated ants in tropical vegetation of Los Tuxtlas,Mexico

Extrafloral nectaries (EFNs) are glands that produce sugary exudates and can be located in any vegetative or reproductive structure of the plant. The EFNs occur in different locations on the leaves, stems, inflorescences and flowers (but are not directly involved with pollination). Occurrence of EFNs on plants of coastal vegetation, tropical rain forest and cloud forest in southern Mexico was studied within Los Tuxtlas Biosphere Reserve, Veracruz. We focused on determining the identity and species richness of plants with EFNs, and describing EFNs morphologies. We found 50 species of plants with EFNs (16 families, 31 genera), which corresponds to approximately 5% of the flora reported for the field site (943 species). Trees were the life form with the greatest representation of EFNs while shrubs and epiphytes had the least representation. EFN-bearing plants were particularly well represented in the families Fabaceae, Euphorbiaceae, Convolvulaceae, Bignoniaceae, Malpighiaceae, Passifloraceae, Costaceae, Tiliaceae, while eight other families had only one species. We found six different types of EFNs according to their morphological structure. Dissimilarity analyses between plants and ant species showed that the forest in the Los Tuxtlas region has a rich array of ant species associated with EFNs, with a low niche overlap of ant species. This diversification in ant use of EFNs is of particular interest from an ecological and evolutionary perspective (potential mutualisms with adaptative value), but this deserves still further studies in detail. The present study shall provide basic information for future research in these fields of plant–animal interactions in neotropical vegetation.     

On the inability of ants to protect their plant partners and the effect of herbivores on different stages of plant reproduction

Ants co‐occur with herbivorous thrips in several tropical plants, but their interactions are largely unexplored. Should thrips be deterred by ants, a positive effect of ants on plant fitness might be expected. Here, by using an experimental study design with ant‐present and ant‐excluded treatments, we investigated the influence of Camponotus blandus on Pseudophilothrips obscuricornis abundance and herbivory in three extrafloral nectaried species: Banisteriopsis malifolia, B. laevifolia and B. stellaris. In addition, we examined the effect of thrips herbivory on flower set and fruit development and dispersion. Thrips abundance and herbivory were higher on ant‐present stems of B. malifolia and B. laevifolia, where thrips managed to escape from ants by hiding in between clusters of flower buds (thygmotaxis behaviour). In B. stellaris the results were the opposite, as flower bud clusters did not offer hiding places, so thrips were unable to hide from ants; thus both thrips abundance and herbivory were lower on ant‐present stems. Thrips herbivory had no significant effect on flower and fruit set, but samaras (V‐shaped winged fruits of Malpighiaceae) attacked by thrips presented severe distortions and asymmetries. This caused damaged fruits to be dispersed closer to the mother plant, whereas uninjured fruits were dispersed further away. This study is evidence that ant–plant–herbivore systems have variable outcomes depending on the species involved, their behaviour and the plant structure under consideration. Unlike other herbivores, thrips negatively influence the very last stage of plant reproduction. The minute and furtive herbivorous thrips have long been ignored in natural systems, but because of their wide host range, they may be important herbivores even in extrafloral nectaried plants, which are usually fiercely protected by ants.     

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     

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.     

Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna

Studies of ant–plant relationships elucidate how top-down effects of the third trophic level can affect the biomass, richness, and/or species composition of plants. Although widespread in the neotropics, few studies have so far examined the direct effects of ants on plant fitness. Here, through experimental manipulation (ant-exclusion) under natural conditions, we examined the effect of ant visitation to extrafloral nectaries on leaf herbivory and fruit set in Chamaecrista debilis in the Brazilian savanna. As opposed to other Chamaecrista species, our results showed that visiting ants (15 species) significantly reduce herbivory and increase fruit set by more than 50% compared to plants from which ants were excluded. This mutualistic system is facultative in nature, and corroborates the potential beneficial role of exudate-feeding ants as anti-herbivore agents of tropical plants.     

Fire affects the occurrence of small mammals at distinct spatial scales in a neotropical savanna

Fire is a major disturbance event that affects biomes worldwide, altering vegetation structure and flora and fauna assemblages. Here, we investigated the effects of an extensive wildfire (~?6240 ha) on small mammal assemblages in savanna woodland (cerradão) at two spatial scales (meso- and macrohabitat) in a neotropical savanna (Brazilian Cerrado). At each spatial scale, we assessed relationships between habitat structure and small mammal species composition and abundance before and after the fire in four natural patches (one burned, three unburned) using partial redundancy analysis. From July 2009 to October 2013, we captured 1319 individuals belonging to 14 species. Our results showed that the fire had consequences for small mammal assemblage at both scales. After the fire, the burned patch differed from the other patches in vegetation attributes and species composition. At a fine scale, fire increased the herbaceous layer and decreased the litter layer and understory obstruction. On a larger scale, the main consequences of fire on vegetation structure were increased variation in litter depth, tree diameter, and distance to the nearest tree. We observed a relationship between mesohabitat structure and the abundance of species with different habitat requirements during the post-fire succession. Fire favored the invasion of generalist species from open Cerrado habitats (rodents Calomys tener, Calomys expulsus, Cerradomys scotti, and Necromys lasiurus) at the expense of more specialized forest species. Our results reinforce the relevance of incorporating multi-scale habitat heterogeneity in future studies assessing the effects of fire on wildlife.     

Insights into a novel three-partner interaction between ants,coreids (Hemiptera: Coreidae) and extrafloral nectaries: implications for the study of protective mutualisms

Extrafloral nectar of plants and honeydew of hemipterans are the common mediators of facultative interactions that involve ants as a mobile strategy of defence. The outcome of these interactions can vary from mutualistic to commensalistic or even antagonistic, depending on the ecological context and the interacting species. Here, we explore a novel, three-partner interaction involving ants, the coreid Dersagrena subfoveolata (Hemiptera) and the extrafloral nectaries (EFNs) bearing plant Senna aphylla (Fabaceae) in semi-arid Northwest Argentina. We surveyed natural areas and conducted ant exclusion experiments, to understand how each pairwise interaction influences the overall outcome among the three interacting parts. The outcome of the interactions was assessed for experimental plants as the reproductive output and herbivore abundances and for coreids as predator abundances. We found that the coreids occurred exclusively on S. aphylla plants and that at least nine ant species interacted with the EFNs as well as with the coreids. Coreid occurrence and abundance depended on ant densities, which in turn, was determined by the presence of actively secreting EFNs. Coreid and ant presence did not influence plant reproductive success, and ants provided to coreids some biotic defence, mainly against vespid wasp predators, but had no effect on non-coreid herbivores. We conclude that the interaction outcome is commensalistic between ants and plants (assuming that EF nectar is not costly for the plant), antagonistic between coreids and plants, and mutualistic between coreids and ants. The sum of all outcomes is net positive effect for ants and coreids, and net slightly negative to neutral for plants.     

Aggressiveness of ants attracted to the extrafloral nectary‐bearing plant,Mallotus japonicus,and temporal fluctuations in their abundance

Many plants that bear extrafloral nectaries (EFNs) attract various ant species that can exclude herbivores. The aggressiveness of the attracted ants and their temporal activity patterns are important factors that can affect the efficiency of herbivore exclusion from the plant. However, the characteristics of this mutualistic relationship between EFN‐bearing plants and ants have not been sufficiently elucidated. We investigated the aggressiveness of six ant species against the common armyworm, Spodoptera litura Fabr., and temporal fluctuations in the abundance of four aggressive ant species on an EFN‐bearing plant, Mallotus japonicus (L.f.) Müll. Arg. Workers of Crematogaster teranishii Santschi, Pheidole noda Smith, Pristomyrmex punctatus Smith and Formica japonica Motschoulsky were observed to be highly aggressive. In contrast, workers of Camponotus vitiosus Smith showed low aggressiveness. Paratrechina flavipes Smith workers did not attack the herbivore. The activity patterns of the four aggressive ant species greatly differed. Crematogaster teranishii and Ph. noda workers were constantly active throughout the day and night. In contrast, F. japonica was diurnal. Pristomyrmex punctatus was principally nocturnal. Formica japonica workers foraged solitarily, whereas workers of the other three species foraged in a group or recruited nestmates. Our results suggest that the efficacy of the indirect defense in M. japonicus depends principally on the attracted ant species.     

Ecological interactions among insect herbivores,ants and the host plant Baccharis dracunculifolia in a Brazilian mountain ecosystem

Insect–plant interactions occur in several ways and have considerable environmental and ecological importance. Many feeding strategies have evolved among herbivorous insects, with host–herbivore systems likely being influenced by trophobionts with ants. We investigated how these interactions vary across elevation gradients by evaluating the structure of the herbivorous insect community and ants associated with Baccharis dracunculifolia at three distinct elevations (800, 1100, and 1400 m a.s.l.) on a mountain in southeastern Brazil. Moreover, we evaluated the diversity and specialisation of interactions between herbivores and host plants along the elevational gradient. We sampled herbivores and ants on 60 plants at each elevation (totalling 180 plant individuals). Herbivore species composition differed among elevations, as did interaction diversity and specialisation. Richness and abundance of chewing insects increased with elevation, while β‐diversity among patches of the host plant was higher at the lowest elevation, probably due to the patchy occurrence of B. dracunculifolia. Richness and abundance of sap‐sucking insects were higher at the intermediate elevation, possibly due to local environmental conditions. We observed a positive relationship between ant and herbivore trophobiont richness on B. dracunculifolia. We found that interactions were more specialised and less diverse at higher elevations compared to the lowest elevation. Changes in vegetation and environmental variables shaped species distributions and their ecological interactions along the elevation gradient. Our study demonstrates that increased elevation changes the structure and patterns of interactions of the herbivore insect guilds associated with the host plant B. dracunculifolia. Ant effects depend on the context, the environment, and the species of ants involved, and are essential for the presence of insect trophobionts.     

Fire effects on insect herbivores in an oak savanna: the role of light and nutrients

Abstract.  1. Environmental heterogeneity created by prescribed burning provided the context for testing whether the distribution of an oak specialist (the lace bug, Corythuca arcuata ) could be explained by stoichiometric mismatches between herbivore and host plant composition.
2. Field observations showed that lace bug density was seven-fold higher in frequently burned than in unburned units.
3. Lace bug density did not increase with leaf nutrient concentrations, but was instead associated with higher light levels, higher concentrations of leaf carbon (C), lignin and total phenolics, and lower levels of cellulose. In addition, lace bugs reared on high-light leaves had higher levels of survivorship than those fed on low-light leaves.
4. Sampling restricted to full-sun leaves was used to test whether fire-related changes in leaf nitrogen (N) and phosphorus (P) concentrations have a secondary influence on lace bug success. This sampling provided only limited evidence for nutrient limitation, as decreases in leaf N and P were associated with an increase in lace bug mass but a decrease in density.
5. It is concluded that burning probably promotes lace bug population growth by increasing canopy openness, light penetration, and the availability of C-based metabolites, and thus simple stoichoimetric mismatches between herbivores and host plants are not of primary importance in this system.     

Behavioral strategy of a lycaenid (Lepidoptera) caterpillar against aggressive ants in a Brazilian savanna

Myrmecophily is widespread in lycaenid butterflies, in which ants receive food resources and, in turn, protect caterpillars against natural enemies. This interaction ranges from obligate myrmecophily, in which immatures are invariably associated with ants and are dependent on ants for survival, and facultative myrmecophily, in which larvae are not dependent on ants for survival, but the presence of the latter may increase larvae survival. Lycaenids also include non-myrmecophilous butterflies, which do not have positive associations with ants and have developed strategies to avoid being attacked or preyed upon by them. In this study, we examined the relationship between the lycaenid Michaelus ira and two ant species associated with Distictella elongata (Bignoniaceae). This plant has extrafloral nectaries and is patrolled by Camponotus crassus and Ectatomma tuberculatum. Morphological analyses revealed that M. ira larvae have ant organs, such as dorsal nectary organs and perforated cupolas, structures associated with myrmecophily. We performed larval exposure experiments in the field, predicting that, in the absence of myrmecophily, the butterfly larva would present strategies to avoid ant attack. Results showed that larvae were attacked by both ant species. To escape ant molestation, larvae lived and fed inside silk-sealed D. elongata flower buds. We concluded that the M. ira bud-sheltering behavior was a defensive strategy against these ant species, while the dorsal nectary organs were apparently nonfunctional. Nonetheless, myrmecophily, in general, cannot be excluded in M. ira since relationships with other ant species may exist.     

Leaf nutrient content and host plant selection by leaf-cutter ants, Atta laevigata, in a Neotropical savanna

The selection of nutrient-rich leaves by leaf-cutter ants ( Atta spp.) is thought to be of indirect benefit to these ants by promoting the growth of their symbiotic fungus. However, relatively few studies have analyzed the influence of leaf nutrient content on host plant selection by leaf-cutter ants, and conflicting results have been found. We compared the content of eight nutritional elements plus the non-nutrient aluminum between leaves harvested by colonies of Atta laevigata (Smith) (Hymenoptera: Formicidae: Attini) and leaves collected randomly within their foraging areas. In addition, we evaluated whether leaf nutrient content explained the frequency with which these ants attacked and defoliated some of the tree species found in the study area. For 2 years, we monitored 17–26 trees from 15 species and determined the number of times each plant was attacked and the amount and type of foliage removed. Leaves harvested by A. laevigata presented significantly higher concentrations of N, P, K, Zn, and Cu than those collected randomly. This result is likely to reflect the foraging pattern presented by these ants, which were selective both in terms of the plant species and age of leaves most commonly attacked. Young leaves were the only or the main leaf type exploited in many species, and in comparison to mature leaves these presented significantly higher concentrations of P and K. Large differences in the mean number of ant attacks on the tree species studied were also observed, and those presenting more leaf N tended to be the most frequently attacked.