Polymorphic microsatellite loci for the ant-garden ant, Crematogaster levior (Forel)

Throughout Amazonia, the ant Crematogaster levior is known for its participation in a complex ant-garden mutualism with the ant Camponotus femoratus and several species of epiphytic plants for which it plays an important role in seed viability. We isolated nine polymorphic microsatellite loci for C. levior from a genomic library enriched for di-, tri-, and tetra-nucleotide repeats. Two to 14 alleles were detected per locus, with levels of observed heterozygosity ranging from 0.103 to 0.785.     

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     

Differential Recruitment of Camponotus femoratus (Fabricius) Ants in Response to Ant Garden Herbivory

Although several studies have shown that ants can recognize chemical cues from their host plants in ant-plant systems, it is poorly demonstrated in ant gardens (AGs). In this interaction, ant species constantly interact with various epiphyte species. Therefore, it is possible to expect a convergence of chemical signals released by plants that could be acting to ensure that ants are able to recognize and defend epiphyte species frequently associated with AGs. In this study, it was hypothesized that ants recognize and differentiate among chemical stimuli released by AG epiphytes and non-AG epiphytes. We experimentally simulated leaf herbivore damage on three epiphyte species restricted to AGs and a locally abundant understory herb, Piper hispidum, in order to quantify the number of recruited Camponotus femoratus (Fabricius) defenders. When exposed to the AG epiphytes Peperomia macrostachya and Codonanthe uleana leaves, it was observed that the recruitment of C. femoratus workers was, on average, respectively 556% and 246% higher than control. However, the number of ants recruited by the AG epiphyte Markea longiflora or by the non-AG plant did not differ from paper pieces. This indicated that ants could discern between chemicals released by different plants, suggesting that ants can select better plants. These results can be explained by evolutionary process acting on both ants’ capability in discerning plants’ chemical compounds (innate attraction) or by ants’ learning based on the epiphyte frequency in AGs (individual experience). To disentangle an innate behavior, a product of classical coevolutionary process, from an ant’s learned behavior, is a complicated but important subject to understand in the evolution of ant-plant mutualisms.     

Biotic and abiotic determinants of the formation of ant mosaics in primary Neotropical rainforests

1. Ants are widespread in tropical rainforests, including in the canopy where territorially dominant arboreal species represent the main part of the arthropod biomass. 2. By mapping the territories of dominant arboreal ant species and using a null model analysis and a pairwise approach this study was able to show the presence of an ant mosaic on the upper canopy of a primary Neotropical rainforest (c. 1 ha sampled; 157 tall trees from 28 families). Although Neotropical rainforest canopies are frequently irregular, with tree crowns at different heights breaking the continuity of the territories of dominant ants, the latter are preserved via underground galleries or trails laid on the ground. 3. The distribution of the trees influences the structure of the ant mosaic, something related to the attractiveness of tree taxa for certain arboreal ant species rather than others. 4. Small‐scale natural disturbances, most likely strong winds in the area studied (presence of canopy gaps), play a role by favouring the presence of two ant species typical of secondary formations: Camponotus femoratus and Crematogaster levior, which live in parabiosis (i.e. share territories and nests but lodge in different cavities) and build conspicuous ant gardens. In addition, pioneer Cecropia myrmecophytic trees were recorded.     

Disentangling the assembly mechanisms of ant cuticular bacterial communities of two Amazonian ant species sharing a common arboreal nest

Bacteria living on the cuticle of ants are generally studied for their protective role against pathogens, especially in the clade of fungus‐growing ants. However, little is known regarding the diversity of cuticular bacteria in other ant host species, as well as the mechanisms leading to the composition of these communities. Here, we used 16S rRNA gene amplicon sequencing to study the influence of host species, species interactions and the pool of bacteria from the environment on the assembly of cuticular bacterial communities on two phylogenetically distant Amazonian ant species that frequently nest together inside the roots system of epiphytic plants, Camponotus femoratus and Crematogaster levior. Our results show that (a) the vast majority of the bacterial community on the cuticle is shared with the nest, suggesting that most bacteria on the cuticle are acquired through environmental acquisition, (b) 5.2% and 2.0% of operational taxonomic units (OTUs) are respectively specific to Ca. femoratus and Cr. levior, probably representing their respective core cuticular bacterial community, and (c) 3.6% of OTUs are shared between the two ant species. Additionally, mass spectrometry metabolomics analysis of metabolites on the cuticle of ants, which excludes the detection of cuticular hydrocarbons produced by the host, were conducted to evaluate correlations among bacterial OTUs and m/z ion mass. Although some positive and negative correlations are found, the cuticular chemical composition was weakly species‐specific, suggesting that cuticular bacterial communities are prominently environmentally acquired. Overall, our results suggest the environment is the dominant source of bacteria found on the cuticle of ants.     

Are ontogenetic shifts in foliar structure and resource acquisition spatially conditioned in tank‐bromeliads?

The phenotypic plasticity of plants has been explored as a function of either ontogeny (apparent plasticity) or environment (adaptive plasticity), although few studies have analyzed these factors together. In the present study, we take advantage of the dispersal of Aechmea mertensii bromeliads by Camponotus femoratus or Pachycondyla goeldii ants in shaded and sunny environments, respectively, to quantify ontogenetic changes in morphological, foliar, and functional traits, and to analyze ontogenetic and ant species effects on 14 traits. Most of the morphological (plant height, number of leaves), foliar (leaf thickness, leaf mass area, total water content, trichome density), and functional (leaf δ¹³C) traits differed as a function of ontogeny. Conversely, only leaf δ¹⁵N showed an adaptive phenotypic plasticity. On the other hand, plant width, tank width, longest leaf length, stomatal density, and leaf C concentration showed an adaptation to local environment with ontogeny. The exception was leaf N concentration, which showed no trend at all. Aechmea mertensii did not show an abrupt morphological modification such as in heteroblastic bromeliads, although it was characterized by strong, size‐related functional modifications for CO₂ acquisition. The adaptive phenotypic variation found between the two ant species indicates the spatially conditioned plasticity of A. mertensii in the context of insect‐assisted dispersal. However, ant‐mediated effects on phenotypic plasticity in A. mertensii are not obvious because ant species and light environment are confounding variables. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175 , 299–312.     

Ant species identity mediates reproductive traits and allocation in an ant-garden bromeliad

Background and Aims

Determining the sources of variation in floral morphology is crucial to understanding the mechanisms underlying Angiosperm evolution. The selection of floral and reproductive traits is influenced by the plant''s abiotic environment, florivores and pollinators. However, evidence that variations in floral traits result from mutualistic interactions with insects other than pollinators is lacking in the published literature and has rarely been investigated. We aimed to determine whether the association with either Camponotus femoratus or Pachycondyla goeldii (both involved in seed dispersal and plant protection) mediates the reproductive traits and allocation of Aechmea mertensii, an obligatory ant-garden tank-bromeliad, differently.

Methods

Floral and reproductive traits were compared between the two A. mertensii ant-gardens. The nitrogen flux from the ants to the bromeliads was investigated through experimental enrichments with stable isotopes (¹⁵N).

Key Results

Camponotus femoratus-associated bromeliads produced inflorescences up to four times longer than did P. goeldii-associated bromeliads. Also, the numbers of flowers and fruits were close to four times higher, and the number of seeds and their mass per fruit were close to 1·5 times higher in C. femoratus than in P. goeldii-associated bromeliads. Furthermore, the ¹⁵N-enrichment experiment showed that C. femoratus-associated bromeliads received more nitrogen from ants than did P. goeldii-associated bromeliads, with subsequent positive repercussions on floral development. Greater benefits were conferred to A. mertensii by the association with C. femoratus compared with P. goeldii ants.

Conclusions

We show for the first time that mutualistic associations with ants can result in an enhanced reproductive allocation for the bromeliad A. mertensii. Nevertheless, the strength and direction of the selection of floral and fruit traits change based on the ant species and were not related to light exposure. The different activities and ecological preferences of the ants may play a contrasting role in shaping plant evolution and speciation.     

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.     

Cuticular hydrocarbons as potential mediators of cryptic species divergence in a mutualistic ant association

Upon advances in sequencing techniques, more and more morphologically identical organisms are identified as cryptic species. Often, mutualistic interactions are proposed as drivers of diversification. Species of the neotropical parabiotic ant association between Crematogaster levior and Camponotus femoratus are known for highly diverse cuticular hydrocarbon (CHC) profiles, which in insects serve as desiccation barrier but also as communication cues. In the present study, we investigated the association of the ants’ CHC profiles with genotypes and morphological traits, and discovered cryptic species pairs in both genera. To assess putative niche differentiation between the cryptic species, we conducted an environmental association study that included various climate variables, canopy cover, and mutualistic plant species. Although mostly sympatric, the two Camponotus species seem to prefer different climate niches. However in the two Crematogaster species, we could not detect any differences in niche preference. The strong differentiation in the CHC profiles may thus suggest a possible role during speciation itself either by inducing assortative mating or by reinforcing sexual selection after the speciation event. We did not detect any further niche differences in the environmental parameters tested. Thus, it remains open how the cryptic species avoid competitive exclusion, with scope for further investigations.     

Infestation by a Common Parasite is Correlated with Ant Symbiont Identity in a Plant‐Ant Mutualism

In East Africa, up to four symbiotic ant species associate with the obligate myrmecophyte Acacia drepanolobium. These ant species differ in the extent to which they defend their host trees from both vertebrate and invertebrate herbivores, but other potential roles of ants in tree defense have not been studied. We investigate the distribution of a new species of parasitic midge targeting A. drepanolobium in a region where A. drepanolobium is inhabited almost exclusively by two ant species—Crematogaster nigriceps and C. mimosae. We find that the frequency of infestation correlates strongly with the identity of the ant occupant: trees inhabited by C. nigriceps are significantly less likely to be infested with parasitic midges. Although the two ant species responded similarly to simulated large herbivore disturbances, trees inhabited by C. nigriceps also had a lower invertebrate load than trees inhabited by C. mimosae. We suggest that differences in defensive behavior towards invertebrates could be one explanation of the observed differences in infestation of A. drepanolobium by parasitic midges.     

Chemo–ecological interactions in Antarctic bryozoans

The role of bioactive metabolites in ecological interactions involving Antarctic bryozoans has been scarcely studied. Bryozoans are one of the most abundant and diverse members of the Antarctic benthos and are preyed upon by diverse kinds of predators. They seem to be casual food items of the common Antarctic sea urchin Sterechinus neumayeri and the ubiquitous omnivorous amphipod Cheirimedon femoratus. In this study, the cytotoxic activity against embryos and sperm of the sea urchin S. neumayeri and the substrate preferences of the amphipod C. femoratus were assessed using organic extracts from Antarctic bryozoans, in order to determine the presence of chemical defenses. New adapted protocols were designed using a solidifying gel for simulating bryozoans’ surface. We analyzed 32 organic extracts from 16 samples that belonged to 13 different bryozoan species. No cytotoxicity was detected against embryos of S. neumayeri, while 12 of the 13 bryozoan species were cytotoxic to sperm at natural concentrations. In the substrate preference assays, the amphipod C. femoratus was repelled by ten species. The variable bioactivities found in both types of organic partitions of extracts indicated the presence of both lipophilic and hydrophilic defenses. Inter- and intraspecific variability of chemical defenses was detected also, suggesting environmental-induced responses, symbiotic production, and/or genetic variability. Possible alternative defensive mechanisms are also discussed for species with low or no chemical defense. Our results clearly support the fact that chemically mediated bioactivity in Antarctic bryozoans is common, and there is a likely ecological role of cytotoxic and repellent compounds for their protection.     

Effects of an Epiphytic Orchid on Arboreal Ant Community Structure in Panama

Epiphytes are conspicuous structural elements of tropical forest canopies. Individual tree crowns in lowland forests may support more than 30 ant species, yet we know little about the effects of epiphytes on ant diversity. We examined the composition of arboreal ant communities on Annona glabra trees and their interactions with the epiphytic orchid Caularthron bilamellatum in Panama. We surveyed the ants on 73 trees (45 with C. bilamellatum and 28 lacking epiphytes) and recorded their nest sites and behavioral dominance at baits. We found a total of 49 ant species (in 20 genera), ranging 1–9 species per tree. Trees with C. bilamellatum had higher average (±SD) ant species richness (4.2±2.28) than trees without epiphytes (2.7±1.21). Hollow pseudobulbs (PBs) of C. bilamellatum were used as nest sites by 32 ant species, but only 43 percent of suitable PBs were occupied. Ant species richness increased with PB abundance in trees, but nest sites did not appear to be a limiting resource on A. glabra. We detected no close association between ants and the orchid. We conclude that higher ant species richness in the presence of the orchid is due to bottom‐up effects, especially the year‐round supply of extrafloral nectar. The structure of ant communities on A. glabra partly reflects interference competition among behaviorally dominant species and stochastic factors, as observed in other forests.     

Female beetles facilitate leaf feeding for males on toxic plants

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Ants on swollen-thorn acacias: species coexistence in a simple system

 On the black cotton soils of the Laikipia ecosystem in Kenya, two swollen-thorn acacia species support nine ant species, four of which are apparently obligate plant-ants. Among the ants, there are five species of Crematogaster, two species of Camponotus, and one each of Tetraponera and Lepisota. Acacia drepanolobium is host to four ant species that are both common and mutually exclusive. These four ant species, and an additional non-exclusive ant species, tend to occur on trees of different sizes, implying a succession of ant occupants. Nonetheless, all four exclusive species occur in substantial proportions on trees of intermediate size. There is direct evidence that an early successional ant species (Tetraponera penzigi) is actively evicted by two late successional ant species in the genus Crematogaster. There was also some evidence of height differentiation among ant species resident on A. seyal. Different acacia-ant species had different direct effects on A. drepanolobium. Extrafloral nectaries were eaten and destroyed only on trees inhabited by Tetraponera. Axillary shoots were eaten only on trees inhabited by C. nigriceps (potentially another early successional ant). This was associated with more new terminal shoots and healthier leaves than other trees, but also the virtual elimination of flowering and fruiting. Different resident acacia-ant species also had characteristic relationships with other insects. Among the four mutually exclusive ant species, only Crematogaster sjostedti was associated with two species of Camponotus, at least one of which (C. rufoglaucus) appears to be a foraging non-resident. A. drepanolobium trees occupied by C. sjostedti were also far more heavily infested with leaf galls than were trees occupied by other ant species. A. drepanolobium trees occupied by C. mimosae and C. sjostedti uniquely had tended adult scale insects. This diversity of ant inhabitants, and their strikingly different relationships with their hosts and other insect species, are examples of coexisting diversity on an apparently uniform resource. Received: 13 November 1995 / Accepted: 16 May 1996     

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.     

Behavioural traits mediating effects of two plant-ants on their specific myrmecophyte host

Summary. Symbiotic ant species vary in their effects on the same host plant, and some ant species are exploiters. These can destabilise the interaction. The behavioural repertoire of ant associates should be important in determining their effects on the host. We examined several traits of foraging behaviour of two ant species associated with the African understorey tree Leonardoxa africana africana – the protective mutualist Petalomyrmex phylax and the parasite Cataulacus mckeyi – to examine the mechanistic basis of the difference in their effects on the plant. These two ant species displayed significant differences not only in activity rhythms, P. phylax patrolling leaves day and night while C. mckeyi was strictly diurnal, but also in their predatory behaviour (P. phylax killed more herbivores) and recruitment dynamics (C. mckeyi recruited at a lower level). For all traits examined, C. mckeyi expressed behaviours reflecting an opportunistic exploitation of the nectar produced by the host plant, whereas those displayed by P. phylax contribute to conferring effective protection of the host plant. Our results suggest that prey capture may be important as a source of food for Petalomyrmex, in addition to its function in increasing plant-provided resources through protection.Received 27 August 2004; revised 11 November 2004; accepted 16 November 2004.     

Community level impacts of an ant invader and food mediated coexistence

Ant invasions exert a range of effects on recipient communities, from displacement of particular species to more complex community disruption. While species loss has been recorded for a number of invasion events, a little examined aspect of these invasions is the mechanisms for coexistence with resident ant species.The yellow crazy ant, Anoplolepis gracilipes (Smith), is considered one of the world’s worst ant invaders and has recently undergone rapid population growth in Tokelau. We surveyed the ground-dwelling ant fauna in two plots on each of five invaded and three uninvaded islands across two atolls in Tokelau to examine community characteristics of the ant fauna in areas with and without yellow crazy ants. We also used three types of food bait (tuna, jam and peanut butter) to experimentally test if species are able to coexist by consuming different food resources. Anoplolepis gracilipes was found to coexist with two to six other ant species at any one site, and coexisted with a total of 11 ant species. Four species never co-occurred with A. gracilipes. Non-metric multidimensional scaling showed significant differences in community composition and the relative abundance of species between areas that had, and had not, been invaded by A. gracilipes. The number of other ant species was significantly lower in communities invaded by the yellow crazy ant, but did not decline with increasing A. gracilipes abundance, indicating that impacts were independent of population density. The yellow crazy ant dominated all tuna and jam baits, but had a low attendance on peanut butter, allowing four other ant species to access this resource. Our results demonstrate community level impacts of an ant invader on a tropical oceanic atoll and suggest that differing use of food resources can facilitate coexistence in ant communities. Received 11 September 2006; revised 15 January 2007; accepted 22 February 2007.     

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.     

The effect of manipulated shading on the colony abundance of two species of ants,Formica aserva and Leptothorax muscorum,in dead wood

Ants (Hymenoptera: Formicidae) are known to be a thermophilic group with fewer species at higher latitudes. They are ubiquitous in the sub‐boreal forests of west‐central British Columbia (Canada) in the early seral ages of forest succession, nesting almost exclusively in woody debris. Individual species begin to disappear with advancing seral ages as the canopy closes, suggesting the hypothesis that heat gain from insolation is critical to many species. We experimentally manipulated shading of two wood‐nesting ant species –Leptothorax muscorum (Nylander) and Formica aserva Forel – to emulate advancing seral age, in an environment documented to support their normal habitation. Shaded down woody debris (DWD) was found to be ca. 2 °C cooler than unshaded DWD, whereas stumps were ca. 1.5 °C cooler when shaded than when unshaded. We found significantly fewer colonies of both L. muscorum and F. aserva in shaded wood, as compared to unshaded, in a pattern consistent with how each species has been observed to respond to advancing seral age. Temperature monitoring during the experiment indicated that soil was cooler than either stumps or DWD, possibly explaining the absence of soil‐nesting ant species in these forests. The species‐specific differences in ant colony abundance in response to small temperature differences, found in this study, support other research on the significance of temperature in structuring ant assemblages.