Jérôme Orivel

The influence of light, substrate and seed origin on the germination and establishment of an ant-garden bromeliad

Plant germination and development depend upon a seeds successful dispersal into a suitable habitat and its ability to grow and survive within the surrounding biotic and abiotic environment. The seeds of Aechmea mertensii, a tank-bromeliad species, are dispersed by either Camponotus femoratus or Neoponera goeldii, two ant species that initiate ant gardens (AGs). These two mutualistic ant species influence the vegetative and reproductive traits of the bromeliad through their divergent ecological preferences (i.e. light and substrate). We hypothesised that the seeds dispersed by these two ant species have underlying genetic differences affecting germination, growth and survival of A.xa0mertensii seedlings in different ways. To test this, we used an experimental approach consisting of sowing seeds of A.xa0mertensii: (i) taken from the two AG-ant associations (i.e. seed origin), (ii) in two contrasting light conditions, and (iii) on three different substrates. Light and substrate had significant effects on germination, survival and on eight key leaf traits reflecting plant performance. Seed origin had a significant effect only on germination and on two leaf traits (total dry mass and relative growth rate). Overall, this bromeliad performs better (i.e. high growth and survival rates) when growing both in the shade and in the carton nest developed by C.xa0femoratus ants. These results suggest that the plasticity of the tank bromeliad A.xa0mertensii is mainly due to environment but also to genetic differences related to seed origin, as some traits are heritable. Thus, these two ant species may play contrasting roles in shaping plant evolution and speciation.

Isolation and characterization of a structurally unique β-hairpin venom peptide from the predatory ant Anochetus emarginatus.

BACKGROUNDnMost ant venoms consist predominantly of small linear peptides, although some contain disulfide-linked peptides as minor components. However, in striking contrast to other ant species, some Anochetus venoms are composed primarily of disulfide-rich peptides. In this study, we investigated the venom of the ant Anochetus emarginatus with the aim of exploring these novel disulfide-rich peptides.nnnMETHODSnThe venom peptidome was initially investigated using a combination of reversed-phase HPLC and mass spectrometry, then the amino acid sequences of the major peptides were determined using a combination of Edman degradation and de novo MS/MS sequencing. We focused on one of these peptides, U1-PONTX-Ae1a (Ae1a), because of its novel sequence, which we predicted would form a novel 3D fold. Ae1a was chemically synthesized using Fmoc chemistry and its 3D structure was elucidated using NMR spectroscopy. The peptide was then tested for insecticidal activity and its effect on a range of human ion channels.nnnRESULTSnSeven peptides named poneritoxins (PONTXs) were isolated and sequenced. The three-dimensional structure of synthetic Ae1a revealed a novel, compact scaffold in which a C-terminal β-hairpin is connected to the N-terminal region via two disulfide bonds. Synthetic Ae1a reversibly paralyzed blowflies and inhibited human L-type voltage-gated calcium channels (CaV1).nnnCONCLUSIONSnPoneritoxins from Anochetus emarginatus venom are a novel class of toxins that are structurally unique among animal venoms.nnnGENERAL SIGNIFICANCEnThis study demonstrates that Anochetus ant venoms are a rich source of novel ion channel modulating peptides, some of which might be useful leads for the development of biopesticides.

Trade-offs in an ant - plant - fungus mutualism

Species engaged in multiple, simultaneous mutualisms are subject to trade-offs in their mutualistic investment if the traits involved in each interaction are overlapping, which can lead to conflicts and affect the longevity of these associations. We investigate this issue via a tripartite mutualism involving an ant plant, two competing ant species and a fungus the ants cultivate to build galleries under the stems of their host plant to capture insect prey. The use of the galleries represents an innovative prey capture strategy compared with the more typical strategy of foraging on leaves. However, because of a limited worker force in their colonies, the prey capture behaviour of the ants results in a trade-off between plant protection (i.e. the ants patrol the foliage and attack intruders including herbivores) and ambushing prey in the galleries, which has a cascading effect on the fitness of all of the partners. The quantification of partners traits and effects showed that the two ant species differed in their mutualistic investment. Less investment in the galleries (i.e. in fungal cultivation) translated into more benefits for the plant in terms of less herbivory and higher growth rates and vice versa. However, the greater vegetative growth of the plants did not produce a positive fitness effect for the better mutualistic ant species in terms of colony size and production of sexuals nor was the mutualist compensated by the wider dispersal of its queens. As a consequence, although the better ant mutualist is the one that provides more benefits to its host plant, its lower host–plant exploitation does not give this ant species a competitive advantage. The local coexistence of the ant species is thus fleeting and should eventually lead to the exclusion of the less competitive species.

A mimetic nesting association between a timid social wasp and an aggressive arboreal ant

In French Guiana, the arboreal nests of the swarm-founding social wasp Protopolybia emortualis (Polistinae) are generally found near those of the arboreal dolichoderine ant Dolichoderus bidens. These wasp nests are typically protected by an envelope, which in turn is covered by an additional carton shelter with structure resembling the D.xa0bidens nests. A few wasps constantly guard their nest to keep D.xa0bidens workers from approaching. When alarmed by a strong disturbance, the ants invade the host tree foliage whereas the wasps retreat into their nest. Notably, there is no chemical convergence in the cuticular profiles of the wasps and ants sharing a tree. The aggressiveness of D.xa0bidens likely protects the wasps from army ant raids, but the ants do not benefit from the presence of the wasps; therefore, this relationship corresponds to a kind of commensalism.

An uneasy alliance: a nesting association between aggressive ants and equally fierce social wasps: An ant-wasp nesting association

Although the Neotropical territorially dominant arboreal ant Azteca chartifex Forel is very aggressive towards any intruder, its populous colonies tolerate the close presence of the fierce polistine wasp Polybia rejecta (F.). In French Guiana, 83.33% of the 48 P. rejecta nests recorded were found side by side with those of A. chartifex. This nesting association results in mutual protection from predators (i.e., the wasps protected from army ants; the ants protected from birds). We conducted field studies, laboratory‐based behavioral experiments and chemical analyses to elucidate the mechanisms allowing the persistence of this association. Due to differences in the cuticular profiles of the two species, we eliminated the possibility of chemical mimicry. Also, analyses of the carton nests did not reveal traces of marking on the envelopes. Because ant forager flows were not perturbed by extracts from the wasps’ Dufours and venom glands, we rejected any hypothetical action of repulsive chemicals. Nevertheless, we noted that the wasps “scraped” the surface of the upper part of their nest envelope using their mandibles, likely removing the ants’ scent trails, and an experiment showed that ant foragers were perturbed by the removal of their scent trails. This leads us to use the term “erasure hypothesis.” Thus, this nesting association persists thanks to a relative tolerance by the ants towards wasp presence and the behavior of the wasps that allows them to “contain” their associated ants through the elimination of their scent trails, direct attacks, “wing‐buzzing” behavior and ejecting the ants.

Land‐use change effects on the taxonomic and morphological trait composition of ant communities in French Guiana

Land‐use changes frequently lead to major changes in the composition and diversity of organisms. A reduction in the range of strategies enabling organisms to survive in a given environment and changes in the average trait values of species may potentially be associated with variations in species’ number and identity. We investigated the variation in ant taxonomic composition and morphological trait diversity along a land‐use gradient in French Guiana. We measured 13 core ant morphological traits on all species sampled. We then selected the set of five traits that best captured changes along the land‐use gradient. Potential effects of the variation in morphological trait diversity and average values were evaluated by examining morphological traits individually as well as in combination. We found that variation in taxonomic diversity was unrelated to the plot‐level morphospace. Conversely, a significant shift in taxonomic composition was accompanied by changes in the average values of community traits along the studied gradient, examined both individually and in combination. We argue that morphological trait values may be related to the success of different species in surviving in a given environment and, therefore, are indicative of the taxonomic turnover in ants along the land‐use gradient. Nevertheless, in contradiction with theoretical expectations, the morphospace is only slightly affected by habitat filtering and loosely impacted by taxonomic changes. Examining the sensitivity of the morphospace to abiotic and biotic factors and how it reflects varying ecological pressures for species is thus of the utmost importance.

Structural adaptations and mechanism of reflex bleeding in the larvae of the myrmecophilous ladybird Diomus thoracicus

Reflex bleeding is an effective defensive mechanism against predators. When attacked, some insects emit hemolymph, which coagulates, quickly entangling their aggressor. Bleeding occurs at weak intersegmental membranes or through dedicated organs, which can be associated or not with glandular cells. Here, we describe the behavior and morphological structures involved in reflex bleeding in the larvae of the ladybird, Diomus thoracicus, which are intranidal parasites of the ant Wasmannia auropunctata. The larvae are tolerated by the ants thanks to odor mimicry, but some rare aggressive ant behaviors were observed that trigger reflex bleeding both at a pair of thoracic tubercles and a pair of posterodorsal abdominal humps. No glandular structure was found in association with these emission points, which suggests that the material emitted was hemolymph only. A 3D reconstruction suggested that reflex bleeding seems to be controlled by muscles whose contraction increases the internal hydrostatic pressure and pushes the hemolymph into a funnel-like structure with an opening to the outside. In D.xa0thoracicus, the morphological structures involved in reflex bleeding are among the most complex and prominent described to date.

Exploring fungus–plant N transfer in a tripartite ant–plant–fungus mutualism

Background and AimsnThe plant Hirtella physophora, the ant Allomerus decemarticulatus and a fungus, Trimmatostroma sp., form a tripartite association. The ants manipulate both the plant trichomes and the fungus to build galleries under the stems of their host plant used to capture prey. In addition to its structural role, the fungus also improves nutrient uptake by the host plant. But it still remains unclear whether the fungus plays an indirect or a direct role in transferring nutrients to the plant. This study aimed to trace the transfer of N from the fungus to the plants stem tissue.nnnMethodsnOptical microscopy and transmission electron microscopy (TEM) were used to investigate the presence of fungal hyphae in the stem tissues. Then, a 15N-labelling experiment was combined with a nanoscale secondary-ion mass spectrometry (NanoSIMS 50) isotopic imaging approach to trace the movement of added 15N from the fungus to plant tissues.nnnKey ResultsnThe TEM images clearly showed hyphae inside the stem tissue in the cellular compartment. Also, fungal hyphae were seen perforating the wall of the parenchyma cell. The 15N provisioning of the fungus in the galleries resulted in significant enrichment of the 15N signature of the plants leaves 1 d after the 15N-labelling solution was deposited on the fungus-bearing trap. Finally, NanoSIMS imaging proved that nitrogen was transferred biotrophically from the fungus to the stem tissue.nnnConclusionsnThis study provides evidence that the fungi are connected endophytically to an ant-plant system and actively transfer nitrogen from 15N-labelling solution to the plants stem tissues. Overall, this study underlines how complex the trophic structure of ant-plant interactions is due to the presence of the fungus and provides insight into the possibly important nutritional aspects and tradeoffs involved in myrmecophyte-ant mutualisms.