Species-Specific Seed Dispersal in an Obligate Ant-Plant Mutualism

Throughout lowland Amazonia, arboreal ants collect seeds of specific plants and cultivate them in nutrient-rich nests, forming diverse yet obligate and species-specific symbioses called Neotropical ant-gardens (AGs). The ants depend on their symbiotic plants for nest stability, and the plants depend on AGs for substrate and nutrients. Although the AGs are limited to specific participants, it is unknown at what stage specificity arises, and seed fate pathways in AG epiphytes are undocumented. Here we examine the specificity of the ant-seed interaction by comparing the ant community observed at general food baits to ants attracted to and removing seeds of the AG plant Peperomia macrostachya. We also compare seed removal rates under treatments that excluded vertebrates, arthropods, or both. In the bait study, only three of 70 ant species collected P. macrostachya seeds, and 84% of observed seed removal by ants was attributed to the AG ant Camponotus femoratus. In the exclusion experiment, arthropod exclusion significantly reduced seed removal rates, but vertebrate exclusion did not. We provide the most extensive empirical evidence of species specificity in the AG mutualism and begin to quantify factors that affect seed fate in order to understand conditions that favor its departure from the typical diffuse model of plant-animal mutualism.     

Orchid seed removal by ants in Neotropical ant‐gardens

• Most plants that inhabit ant‐gardens (AGs) are cultivated by the ants. Some orchids occur in AGs; however, it is not known whether their seeds are dispersed by AG ants because most orchid seeds are tiny and dispersed by wind.
• We performed in situ seed removal experiments, in which we simultaneously provided Azteca gnava ants with seeds of three AG orchid species and three other AG epiphyte species (Bromeliaceae, Cactaceae and Gesneriaceae), as well as the non‐AG orchid Catasetum integerrimum.
• The seeds most removed were those of the bromeliad Aechmea tillandsioides and the gesneriad Codonanthe uleana, while seeds of AG orchids Coryanthes picturata, Epidendrum flexuosum and Epidendrum pachyrachis were less removed. The non‐AG orchid was not removed. Removal values were positively correlated with the frequency of the AG epiphytes in the AGs, and seeds of AG orchids were larger than those of non‐AG orchids, which should favour myrmecochory.
• Our data show that Azt. gnava ants discriminate and preferentially remove seeds of the AG epiphytes. We report for the first time the removal of AG orchid seeds by AG ants in Neotropical AGs.

     

Divergent chemical cues elicit seed collecting by ants in an obligate multi-species mutualism in lowland Amazonia

In lowland Amazonian rainforests, specific ants collect seeds of several plant species and cultivate them in arboreal carton nests, forming species-specific symbioses called ant-gardens (AGs). In this obligate mutualism, ants depend on the plants for nest stability and the plants depend on ant nests for substrate and nutrients. AG ants and plants are abundant, dominant members of lowland Amazonian ecosystems, but the cues ants use to recognize the seeds are poorly understood. To address the chemical basis of the ant-seed interaction, we surveyed seed chemistry in nine AG species and eight non-AG congeners. We detected seven phenolic and terpenoid volatiles common to seeds of all or most of the AG species, but a blend of the shared compounds was not attractive to the AG ant Camponotus femoratus. We also analyzed seeds of three AG species (Anthurium gracile, Codonanthe uleana, and Peperomia macrostachya) using behavior-guided fractionation. At least one chromatographic fraction of each seed extract elicited retrieval behavior in C. femoratus, but the active fractions of the three plant species differed in polarity and chemical composition, indicating that shared compounds alone did not explain seed-carrying behavior. We suggest that the various AG seed species must elicit seed-carrying with different chemical cues.     

Parasitism <Emphasis Type="Italic">versus</Emphasis> mutualism in the ant-garden parabiosis between <Emphasis Type="Italic">Camponotus femoratus</Emphasis> and <Emphasis Type="Italic">Crematogaster levior</Emphasis>

Ant-gardens represent a special type of association between ants and epiphytes. Frequently, two ant species can share the same nest in a phenomenon known as ‘parabiosis’, but the exact nature (i.e., mutualistic or parasitic) of this interaction is the subject of debate. We thus attempted to clarify the mutual costs and benefits for each partner (ants and plants) in the Crematogaster levior/Camponotus femoratus ant-garden parabiosis. The ants’ response to experimental foliar damage to the epiphytes and to the host tree as well as their behavior and interactions during prey capture were investigated to see if the purported parasitic status of Cr. levior could be demonstrated in either the ant-ant or in the ant-plant interactions. The results show that both species take part in protecting the epiphytes, refuting the role of Cr. levior as a parasite of the ant-garden mutualism. During capture of large prey Ca. femoratus took advantage from the ability of Cr. levior to discover prey; by following Cr. levior trails Ca. femoratus workers discover the prey in turn and usurp them during agonistic interactions. Nevertheless, the trade-off between the costs and benefits of this association seems then to be favorable to both species because it is known that Cr. levior benefits from Ca. femoratus building the common carton nests and furnishing protection from vertebrates. Consequently, parabiosis can then be defined as the only mutualistic association existing between ant species, at least in ant-gardens. Received 31 August 2006 ; revised 8 December 2006 ; accepted 12 December 2006     

Potential sources of nitrogen in an ant-garden tank-bromeliad

Epiphytic plants in general and bromeliads in particular live in a water and nutrient-stressed environment often limited in nitrogen. Thus, these plants have developed different ways to survive in such an environment. We focused on Aechmea mertensii (Bromeliaceae), which is both a tank-bromeliad and an ant-garden (AG) epiphyte initiated by either the ants Camponotus femoratus or Pachycondyla goeldii. By combining a study of plant morphology and physiology associated with aquatic insect biology, we demonstrate that the ant species influences the leaf structure of the bromeliad, the structure of the aquatic community in its tank, and nutrient assimilation by the leaves. Based on nitrogen and nitrogen stable isotope measurements of the A. mertensii leaves, the leaf litter inside of the tank and the root-embedded carton nest, we discuss the potential sources of available nitrogen for the plant based on the ant partner. We demonstrate the existence of a complex ant-plant interaction that subsequently affects the biodiversity of a broader range of organisms that are themselves likely to influence nutrient assimilation by the A. mertensii leaves in a kind of plant-invertebrate-plant feedback loop.Key words: Aechmea mertensii, Camponotus femoratus, nitrogen, nitrogen stable isotope, Pachycondyla goeldii, plant-insect interactions, phytotelmataEpiphytes, which belong to numerous phylogenetically distant families, make up more than one-third of the total vascular plant biodiversity of neotropical rainforests.¹ Epiphytism implies physiological consequences and constraints resulting from the lack of access to what are by far the most important sources of water and nutrients for ground-rooting plants.² Epiphytic plants therefore have adapted in various ways to their aerial environment; adaptations for nutrient acquisition include growth forms such as “trash-baskets” (e.g., Asplenium), tanks (tank-bromeliads), specific leaf features such as absorbant trichomes (e.g., Tillandsia) and the velamen radicum in aerial roots (Orchidaceae).^1,3 Potential nitrogen sources for epiphytes may include (1) canopy-derived detritic nitrogen (mineralization of organic material from the canopy) and (2) atmospheric sources (wet and dry deposition, N₂ fixation),⁴ or may involve (3) interactions with animals.⁵ Indeed, some epiphytic species develop symbioses with ants, either by providing chambers (domatia) where ants nest or by rooting in ant gardens⁶ (AGs). By measuring differences in stable isotope composition, Treseder et al. (1995)⁷ estimated that the myrmecophyte Dischidia major (Asclepiadaceae) derives almost 30% of its nitrogen from debris deposited by the ants living in its domatia.Bromeliads are commonly found among the epiphytic species that root in ant-gardens. Their leaves form compartments acting as phytotelmata that hold rainwater and therefore provide habitats for aquatic macro- and microorganisms.^8,9 The detritus (e.g., windborne particulates, faeces, and dead leaves and animals) that enter the tanks constitute a source of nutrients for the aquatic food web, as well as for the bromeliad.¹⁰ Nitrogen is made available through the bacterial decomposition of organic matter, and the presence of arthropod predators in the phytotelmata food web most likely accelerates nitrogen cycling and leaf assimilation.²Recently, we described the complicated interaction that links an epiphytic ant-garden tank-bromeliad, its aquatic micro-ecosystem and the ants with which they are associated in the tropical forest of French Guiana.¹¹ Aechmea mertensii Schult.f. (Bromeliaceae) is an epiphytic tank-bromeliad that roots on AGs initiated either by the ants Camponotus femoratus Fabr. (living in a parabiotic association with Crematogaster levior Forel) or Pachychondyla goeldii Forel.¹² The AGs we studied were situated in tree canopies in pioneer growths along forest edges. By combining ecological studies characterizing the available light for the epiphyte, leaf morpho-anatomy, biochemical studies based on ¹⁵N isotope analysis and the richness of the aquatic communities inside of the tanks, we demonstrate the influence of the ant species on the foliar and aquatic community structures and, subsequently, on nitrogen acquisition by the plant.The ant species either directly or indirectly affects the light incidence, leaf structure, phytotelmata contents and nitrogen content of A. mertensii leaves, which is probably correlated to the plant''s fitness since nitrogen is a limiting factor for epiphytic plants. Pachycondyla goeldii and C. femoratus colonize exposed and partially-shaded areas, respectively. Exposed bromeliads (P. goeldii AGs) are smaller and limit direct light incidence by adopting an amphora-shape, whereas those growing in the shade (C. femoratus AGs) are larger and forage for light by developing a wider canopy. However, the contrast in the leaf mass area (LMA) response to light intensity based on the ant partner seems to support the hypothesis that leaf structure is not primarily controlled by light,^13,14 but rather directly by the ants or by other abiotic factors controlled by the ant partner. The availability of water and leaf debris from the surrounding vegetation may directly influence the diversity of the aquatic organisms in the phytotelmata that are themselves likely to influence nutrient assimilation by A. mertensii leaves in a kind of plant-invertebrate-plant feedback loop.Measurements of the percentage of total nitrogen showed that the carton nest, where the roots are embedded, was characterized by a greater amount of nitrogen compared to the leaf litter inside of the tank for both C. femoratus and P. goeldii AGs (Fig. 1A). While the nitrogen content remained constant for A. mertensii leaves and the leaf litter, the nitrogen content of the carton nest changed with the presence or absence of ants, and according to the ant partner. The carton nests of C. femoratus ants are richer in nitrogen than P. goeldii nests and non-occupied (i.e., abandoned) AGs, which have the lowest nitrogen content. Thus the sources of nitrogen could come from both the carton nest, where the roots are tightly embedded, and the phytotelmata with an average maximum nitrogen content of 2%. Delta ¹⁵N values enable us to estimate that A. mertensii may derive nitrogen from both ant species, but was affected differently depending on the ant partner (Fig. 1B). We demonstrate that A. mertensii—C. femoratus/Cr. levior associations can radically increase the amount of nutrients available to the host. Differences in stable N isotopic composition could reflect the diversity and richness of the macro- and microorganisms¹¹ in the phytotelm and/or the diversity of epiphytic species growing in the AGs,^12,15 and/or variations in the size of the ant colony living in the AGs. Indeed, C. femoratus/Cr. levior AGs are more densely populated than P. goeldii AGs.¹²Open in a separate windowFigure 1(A) Mean (±1 SE) of nitrogen content (%) and (B) δ¹⁵N (%) of Aechmea mertensii leaves (filled circles), root-embedded carton-nest (grey square) and phytotelmata leaf litter (empty triangle) for Camponotus femoratus (N = 10), Pachycondyla goeldii (N = 10) and non-occupied (N = 5) AGs.We have shown that AG ants provide nutrients to their host bromeliad. They either provide nitrogen-rich nutrients by directly or indirectly enhancing the nitrogen uptake of their host plants. Thus ants mediate nutrient uptake as well as phytotelmata contents. Furthermore, the strength of the mutualism appears to be dependent on the ant partner. In contrast to previous studies, our results showed that A. mertensii receives more than twice the amount of nitrogen compared to the myrmecophytic epiphyte Dischidia major⁷ or the epiphytic fern Antrophyum lanceolatum.¹⁶ Such a high level of insect-derived nitrogen could reflect the predominance of a dual nitrogen source derived from animals: one from the phytotelmata-associated organisms and one from the ant-debris (and faeces) in the carton nest. Nevertheless, further research on ¹⁵N enrichment is necessary to properly identify which part of the nitrogen input comes from animal remains and which part comes from the roots and phytotelmata. Moreover, it will enable us to identify which of the two AG ant species represents the greatest direct source of nitrogen for the plant.     

Les « jardins de fourmis,une association plantes-fourmis originale

The ant gardens of tropical America constitute one of the most unique forms of plant-insect associations. The ants that initiate these gardens belong to a limited number of species disparate from a phylogenetic point of view, but having the following two behavioural characteristics: (1) the capacity to build an arboreal nest rich in humus; and (2) an attraction towards the fruits and/or seeds of epiphytes that they retrieve to the nest and incorporate into its walls. The seeds then germinate, and produce a root system that reinforces the nest structure. The demographic growth of the ant colony is accompanied by an increase in the size of the nest which is the result of (1) the constant provisioning of diverse materials and seeds, and (2) the growth of the root system. Moreover, the volume of the ant garden increases as the host tree grows. An ant garden is an association which benefits both the ants and the epiphytes. In addition to the structural role played by their roots, the epiphytes often provide nourishment to the ants living in the ant gardens through fruits and extra-floral nectaries. In return, the ants disseminate the epiphyte seeds and protect the epiphytes from eventual defoliators. Different ant species can be found in the same garden. Such cohabitation can be the result of parabiosis, but, in the oldest gardens, certain ants are the secondary residents that partially or entirely excluded the ants that initiated the garden. An ant garden constitutes a relatively stable nesting site, something rather rare in this environment, such that different parts of the garden can be occupied by numerous Arthropods (including other social insects such as stingless-bees) on the condition that these insects can cohabit with the ants. As such, an ant garden can constitute a veritable microecosystem. While it is not possible to demonstrate a strict or obligate interspecific relationship between ant and plant species, only several rare species among the numerous neotropical epiphytes are involved and a certain number of preferences can be underlined. We present here in detail the characteristics of the ant gardens initiated in French Guiana by the parabiotic associations Crematogaster limata parabiotica/Camponotusfemoratus, and by the ants Pachycondyla goeldii and Odontomachus mayi.     

An ant–plant mutualism induces shifts in the protist community structure of a tank-bromeliad

Although ants may induce community-wide effects via changes in physical habitats in terrestrial environments, their influence on aquatic communities living in plant-held waters remains largely underexplored. The neotropical tank-bromeliad Aechmea mertensii (Bromeliaceae) occurs along forest edges in ant-gardens initiated by Camponotus femoratus or by Pachycondyla goeldii. Its leaves form wells that hold rainwater and provide suitable habitats for many aquatic organisms. We postulated that these ant–plant mutualisms indirectly affect the microbial community structure via changes in the environmental conditions experienced by the plants. To test this hypothesis, we analyzed the protist communities from 63 tank-bromeliads associated with either C. femoratus or P. goeldii (hereafter Cf-Aechmea and Pg-Aechmea) along a forest edge in French Guiana. For each plant, a large number of environmental variables (including habitat structure, food resources, incident radiation and the presence of aquatic invertebrates) were quantified to determine their relative importance in driving any observed differences across ant-associated plants. Pg-Aechmea are located in sun-exposed areas and hold low volumes of water and low amounts of detritus, whereas Cf-Aechmea are located in partially shaded areas and accumulate higher amounts of water and detritus. Protists (i.e., protozoa and algae) inhabiting Cf-Aechmea exhibit greater richness and abundances than those in Pg-Aechmea. Variations in detritus content, number of leaves, incident radiation, and the epiphyte richness of the ant-garden were the main factors explaining the variation in protist richness. A shift in the functional group composition of protists between bromeliads tended by different ant species suggested that mutualistic ants indirectly mediate changes in the microbial food web.     

Food source availability and interspecific dominance as structural mechanisms of ant-plant-hemipteran multitrophic networks

Extrafloral nectar of plants and honeydew of hemipterans is a food source extensively explored by ants. Although basically a sugary liquid food, nectar and honeydew are composed of different nutrients and offered in distinct ways; thus, ants must interact differently with plants and hemipterans. In this study we assessed the availability and dominance of nectar of extrafloral nectaries and honeydew of sap-sucking hemipterans (i.e., sugar-based resources) as mechanisms regulating interaction frequency and structuring ant-plant-hemipteran networks. We studied 12 plant species (240 shrubs, 20 per species) and 12 hemipteran species (240 aggregations, 20 per species) that interacted with 26 ant species in an area of Rupestrian Fields (Rocky Montane Savannah), Brazil. We observed that the 7 ant species that collected honeydew were a subset of the 25 ant species feeding on nectar, but the highly interacted species Camponotus crassus was the same for both subnetworks. The ant-plant subnetwork exhibited a nested pattern of interaction with a low degree of specialization, while the ant-hemipteran subnetwork exhibited lower nestedness but higher specialization. We found a positive relationship between the offer of EFNs and the number of interactions with ants, probably resulting from reduced competition in plants with high availability of EFNs. However, hemipteran species that were most abundant did not interact with more species of ants, probably because of the numerical dominance of the species tending all hemipteran aggregations, regardless of size. However, segregation between ant species was higher than expected by chance for both plants and hemipterans, confirming a deterministic factor (i.e., competition between ant species) regulating the frequency of interactions. In summary, the availability of ENFs seems to be an important mechanism regulating ant-plant interactions, while numerical dominance seems to be an important mechanism structuring ant-hemipteran interactions.     

A castration parasite of an ant-plant mutualism

Exploring the factors governing the maintenance and breakdown of cooperation between mutualists is an intriguing and enduring problem for evolutionary ecology, and symbioses between ants and plants can provide useful experimental models for such studies. Hundreds of tropical plant species have evolved structures to house and feed ants, and these ant–plant symbioses have long been considered classic examples of mutualism. Here, we report that the primary ant symbiont, Allomerus cf. demerarae, of the most abundant ant-plant found in south-east Peru, Cordia nodosa Lam., castrates its host plant. Allomerus workers protect new leaves and their associated domatia from herbivory, but destroy flowers, reducing fruit production to zero in most host plants. Castrated plants occupied by Allomerus provide more domatia for their associated ants than plants occupied by three species of Azteca ants that do not castrate their hosts. Allomerus colonies in larger plants have higher fecundity. As a consequence, Allomerus appears to benefit from its castration behaviour, to the detriment of C. nodosa. The C. nodosa–ant system exhibits none of the retaliatory or filtering mechanisms shown to stabilize cheating in other cooperative systems, and appears to persist because some of the plants, albeit a small minority, are inhabited by the three species of truly mutualistic Azteca ants.     

A bromeliad species reveals invasive ant presence in urban areas of French Guiana

Tank bromeliads, frequently associated with ants, are considered ‘biodiversity amplifiers’ for both aquatic and terrestrial organisms, and thus have a high ecological value. The focal species of this study, Aechmea aquilega, sheltered the colonies of 12 ant species in a Guianese rural habitat where Odontomachus haematodus, associated with 60% of these plants, was the most frequent. Unexpectedly, the ant species richness was higher in a compared urban habitat with 21 species, but two synanthropic and four invasive ants were noted among them. Consequently, we conducted baiting surveys (on the ground, on trees and on trees bearing A. aquilega) as well as complementary surveys using different sampling modes in urban areas to test if A. aquilega is a surrogate revealing the presence of certain invasive ants. During the baiting survey, we recorded four Neotropical and eight introduced invasive ants out of a total of 69 species. Of these 12 invasive species, five were noted by baiting A. aquilega (including two only noted in this way). A bootstrap simulation permitted us to conclude that A. aquilega significantly concentrates certain species of invasive ants. This was confirmed by complementary surveys, where we did not record further species. We conclude that baiting on trees bearing large epiphytes in human-modified, Neotropical areas is a relevant complement to the early detection of invasive ants.     

Food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions in an arid environment

In this study, we conducted a series of experiments in a population of Vachellia constricta (Fabaceae) in the arid Tehuacan-Cuicatláan valley, Mexico, in order to evaluate if the food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions. Using an experiment with artificial nectaries, we observed that ants foraging on food sources with higher concentration of sugar are quicker in finding and attacking potential herbivorous insects. More specifically, we found that the same ant species may increase their defence effectiveness according to the quality of food available. These findings indicate that ant effectiveness in plant protection is context-dependent and may vary according to specific individual characteristics of plants. In addition, we showed that competitively superior ant species tend to dominate plants in periods with high nectar activity, emphasizing the role of the dominance hierarchy structuring ant-plant interactions. However, when high sugar food sources were experimentally available ad libitum, the nocturnal and competitively superior ant species, Camponotus atriceps, did not dominate the artificial nectaries during the day possibly due to limitation of its thermal tolerance. Therefore, temporal niche partitioning may be allowing the coexistence of two dominant ant species (Camponotus rubritorax during the day and C. atriceps at night) on V. constricta. Our findings indicate that the quality of the food source, and temporal shifts in ant dominance are key factors which structure the biotic plant defences in an arid environment.     

Recognition in a Social Symbiosis: Chemical Phenotypes and Nestmate Recognition Behaviors of Neotropical Parabiotic Ants

Social organisms rank among the most abundant and ecologically dominant species on Earth, in part due to exclusive recognition systems that allow cooperators to be distinguished from exploiters. Exploiters, such as social parasites, manipulate their hosts’ recognition systems, whereas cooperators are expected to minimize interference with their partner’s recognition abilities. Despite our wealth of knowledge about recognition in single-species social nests, less is known of the recognition systems in multi-species nests, particularly involving cooperators. One uncommon type of nesting symbiosis, called parabiosis, involves two species of ants sharing a nest and foraging trails in ostensible cooperation. Here, we investigated recognition cues (cuticular hydrocarbons) and recognition behaviors in the parabiotic mixed-species ant nests of Camponotus femoratus and Crematogaster levior in North-Eastern Amazonia. We found two sympatric, cryptic Cr. levior chemotypes in the population, with one type in each parabiotic colony. Although they share a nest, very few hydrocarbons were shared between Ca. femoratus and either Cr. levior chemotype. The Ca. femoratus hydrocarbons were also unusually long–chained branched alkenes and dienes, compounds not commonly found amongst ants. Despite minimal overlap in hydrocarbon profile, there was evidence of potential interspecific nestmate recognition –Cr. levior ants were more aggressive toward Ca. femoratus non-nestmates than Ca. femoratus nestmates. In contrast to the prediction that sharing a nest could weaken conspecific recognition, each parabiotic species also maintains its own aggressive recognition behaviors to exclude conspecific non-nestmates. This suggests that, despite cohabitation, parabiotic ants maintain their own species-specific colony odors and recognition mechanisms. It is possible that such social symbioses are enabled by the two species each using their own separate recognition cues, and that interspecific nestmate recognition may enable this multi-species cooperative nesting.     

Leaf volatile compounds and the distribution of ant patrollingin an ant-plant protection mutualism: Preliminary results onLeonardoxa (Fabaceae: Caesalpinioideae) andPetalomyrmex(Formicidae: Formicinae)

While observations suggest that plant chemicals could be important in maintaining the specificity and permitting the functioning of ant-plant symbioses, they have been little studied. We report here the strongest evidence yet for chemical signalling between ants and plants in a specific ant-plant protection symbiosis. In the mutualism between Leonardoxa africana subsp. africana and Petalomyrmex phylax, ants continuously patrol young leaves, which are vulnerable to attacks by phytophagous insects. We provide experimental evidence for chemical mediation of ant attraction to young leaves in this system. By a comparative analysis of the related non-myrmecophytic tree L. africana subsp. gracilicaulis, we identify likely candidates for attractant molecules, and suggest they may function not only as signals but also as resources. We also propose hypotheses on the evolutionary origin of these plant volatiles, and of the responses to them by mutualistic ants.     

Assembling a mutualism: ant symbionts locate their host plants by detecting volatile chemicals

In most mutualisms, partners disperse independently of each other. For instance, in ant-plant symbioses, plants disperse as seeds, and ants disperse as winged queens. For an ant-plant mutualism to persist, therefore, queens must be able to locate and colonise host plant saplings. It has been suggested that host plants emit volatile chemical cues that attract dispersing queens, but this has never been demonstrated experimentally. We used a Y-tube olfactometry protocol to test this hypothesis in the tropical understorey antplant Cordia nodosa Lam. (Boraginaceae), which associates with two genera of ants, Azteca (Dolichoderinae) and Allomerus (Myrmicinae). Both genera show significant attraction to the volatiles of C. nodosa over control understorey plant species that do not associate with ants. These results support the hypothesis that ants are attracted to volatiles emitted by their host plant and suggest a key preadaptation that promoted the evolution of ant-plant symbioses. Received 1 July 2005; revised 2 November 2005; accepted 8 November 2005.     

Epiphytes on the rocky intertidal red alga RhodomelaLarix (Turner) C. Agardh: Negative effects on the host and food for herbivores?

The diversity of epiflora and fauna associated with a dominant turf-forming alga was examined in intertidal communities on the central Oregon coast. Epiphytes associated with the red alga, Rhodomelalarix (Turner) C. Agardh, were examined by surveying intertidal areas for the presence of epiphytes, and by following changes in epiphyte cover in marked quadrats of R. larix. The alga is host for at least 17 species of sessile plants and animals. To determine the role of some of the larger epiphytes in the community, Rhodomela plants were marked and monitored and herbivore feeding was examined. Data suggest that epiphytes decrease the growth rate of their host, increase the probability of axis breakage and decrease reproductive output. Epiphytes provide food for littorine snails and gammarid amphipods that live in the beds of the plant. Amphipods were found to decrease epiphyte cover on R. larix in laboratory tanks, suggesting that these herbivores may have beneficial effects on the host plant.     

Floral volatiles play a key role in specialized ant pollination

Chemical signals emitted by plants are crucial to understand the ecology and evolution of plant–animal interactions. Scent is an important component of floral phenotype and represents a decisive communication channel between plants and floral visitors. Floral volatiles promote attraction of mutualistic pollinators and, in some cases, serve to prevent flower visitation by antagonists such as ants. Despite ant visits to flowers have been suggested to be detrimental to plant fitness, in recent years there has been a growing recognition of the positive role of ants in pollination. Nevertheless, the question of whether floral volatiles mediate mutualisms between ants and ant-pollinated plants still remains largely unexplored. Here we review the documented cases of ant pollination and investigate the chemical composition of the floral scent in the ant-pollinated plant Cytinus hypocistis. By using chemical-electrophysiological analyses and field behavioural assays, we examine the importance of olfactory cues for ants, identify compounds that stimulate antennal responses, and evaluate whether these compounds elicit behavioural responses. Our findings reveal that floral scent plays a crucial role in this mutualistic ant–flower interaction, and that only ant species that provide pollination services and not others occurring in the habitat are efficiently attracted by floral volatiles. 4-oxoisophorone, (E)-cinnamaldehyde, and (E)-cinnamyl alcohol were the most abundant compounds in Cytinus flowers, and ant antennae responded to all of them. Four ant pollinator species were significantly attracted to volatiles emitted by Cytinus inflorescences as well as to synthetic mixtures and single antennal-active compounds. The small amount of available data so far suggest that there is broad interspecific variation in floral scent composition among ant-pollinated plants, which could reflect differential responses and olfactory preferences among different ant species. Many exciting discoveries will be made as we enter into further research on chemical communication between ants and plants.     

Indirect effects of granivory by harvester ants: plant species composition and reproductive increase near ant nests

Summary Of 36 plant species surveyed, 6 were significantly associated with nests of the desert seed-harvester ant Veromessor pergandei or Pogonomyrmex rugosus; two other plant species were significantly absent from ant nests. Seeds of two common desert annuals, Schismus arabicus and Plantago insularis, realize a 15.6 and 6.5 fold increase (respectively) in number of fruits or seeds produced per plant growing in ant nest refuse piles compared to nearby controls. Mass of individual S. arabicus seed produced by plants growing in refuse piles also increased significantly. Schismus arabicus, P. insularis and other plants associated with ant nests do not have seeds with obvious appendages attractive to ants. Dispersal and reproductive increase of such seeds may represent a relatively primitive form of ant-plant dispersal devoid of seed morphological specializations. Alternatively, evolution of specialized seed structures for dispersal may be precluded by the assemblage of North American seed-harvester ants whose workers are significantly larger than those ants normally associated with elaiosome-attached seed dispersal. Large worker size may permit consumption of elaiosome and seed.     

How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew

Ant-plant interactions in the canopy of a lowland Amazonian rainforest of the upper Orinoco, Venezuela, were studied using a modified commercial crane on rails (Surumoni project). Our observations show a strong correlation between plant sap exudates and both abundance of ants and co-occurrence of ant species in tree canopies. Two types of plant sap sources were compared: extrafloral nectaries (EFNs) and honeydew secretions by homopterans. EFNs were a frequent food source for ants on epiphytes (Philodendron spp., Araceae) and lianas (Dioclea, Fabaceae), but rare on canopy trees in the study area, whereas the majority of trees were host to aggregations of homopterans tended by honeydew-seeking ants (on 62% of the trees examined). These aggregations rarely occurred on epiphytes. Baited ant traps were installed on plants with EFNs and in the crowns of trees from three common genera, including trees with and without ant-tended homopterans: Goupia glabra (Celastraceae), Vochysia spp. (Vochysiaceae), and Xylopia spp. (Annonaceae). The number of ant workers per trap was significantly higher on plants offering one of the two plant sap sources than on trees without such resources. Extrafloral nectaries were used by a much broader spectrum of ant species and genera than honeydew, and co-occurrence of ant species (in traps) was significantly higher on plants bearing EFNs than on trees. Homopteran honeydew (Coccidae and Membracidae), on the other hand, was mostly monopolised by a single ant colony per tree. Homopteran-tending ants were generally among the most dominant ants in the canopy. The most prominent genera were Azteca, Dolichoderus (both Dolichoderinae), Cephalotes, Pheidole, Crematogaster (all Myrmicinae), and Ectatomma (Ponerinae). Potential preferences were recorded between ant and homopteran species, and also between ant-homopteran associations and tree genera. We hypothesize that the high availability of homopteran honeydew provides a key resource for ant mosaics, where dominant ant colonies and species maintain mutually exclusive territories on trees. In turn, we propose that for nourishment of numerous ants of lower competitive capacity, Philodendron and other sources of EFNs might be particularly important.     

Cropping Systems and Cultural Practices Determine the Rhizoctonia Anastomosis Groups Associated with Brassica spp. in Vietnam

Ninety seven Rhizoctonia isolates were collected from different Brassica species with typical Rhizoctonia symptoms in different provinces of Vietnam. The isolates were identified using staining of nuclei and sequencing of the rDNA-ITS barcoding gene. The majority of the isolates were multinucleate R. solani and four isolates were binucleate Rhizoctonia belonging to anastomosis groups (AGs) AG-A and a new subgroup of A-F that we introduce here as AG-Fc on the basis of differences in rDNA-ITS sequence. The most prevalent multinucleate AG was AG 1-IA (45.4% of isolates), followed by AG 1-ID (17.5%), AG 1-IB (13.4%), AG 4-HGI (12.4%), AG 2-2 (5.2%), AG 7 (1.0%) and an unknown AG related to AG 1-IA and AG 1-IE that we introduce here as AG 1-IG (1.0%) on the basis of differences in rDNA-ITS sequence. AG 1-IA and AG 1-ID have not been reported before on Brassica spp. Pathogenicity tests revealed that isolates from all AGs, except AG-A, induced symptoms on detached leaves of several cabbage species. In in vitro tests on white cabbage and Chinese cabbage, both hosts were severely infected by AG 1-IB, AG 2-2, AG 4-HGI, AG 1-IG and AG-Fc isolates, while under greenhouse conditions, only AG 4-HGI, AG 2-2 and AG-Fc isolates could cause severe disease symptoms. The occurrence of the different AGs seems to be correlated with the cropping systems and cultural practices in different sampling areas suggesting that agricultural practices determine the AGs associated with Brassica plants in Vietnam.