Bertrand Schatz

Floral scents: their roles in nursery pollination mutualisms

Mutualisms are interspecies interactions in which each participant gains net benefits from interacting with its partner. In nursery pollination mutualisms, pollinators reproduce within the inflorescence they pollinate. In these systems, each partner depends directly on the other for its reproduction. Therefore, the signal responsible for partner encounter is crucial in these horizontally transmitted mutualisms, in which the association between specific partners must be renewed at each generation. As in many other interspecies interactions, chemical signals are suspected to be important in the functioning of these mutualisms. We synthesized and compared the published data available on the role of floral scents in the functioning of the 16 known independently evolved nursery pollination mutualisms. So far, attraction of pollinators to their specific hosts has been investigated in only seven of these systems, and the majority of the studies have been conducted on one of them, fig/fig wasp interactions. While such unevenness of the information limits the potential for meta-analysis, some patterns emerge from this review concerning the role of flower volatiles in maintaining the specificity of pollinator attraction, in signaling the appropriate phenological stage for pollinator visit, in attracting the pollinator toward the rewardless sex in dioecious plant species and in aiding the location and exploitation of resources by parasites and predators associated with these mutualisms. Finally, we highlight new perspectives on the evolution of signals in these diversified systems depending on the age and the degree of specificity of the interaction, and on the effect of phylogenetic inertia on the evolutionary dynamics of plant signals.

Graded recruitment and hunting strategies linked to prey weight and size in the ponerine ant Ectatomma ruidum

Abstract According to the weight and size of their prey, Ectatomma ruidum workers can employ different recruitment systems (solitary hunting, cooperative hunting and group hunting with recruitment) when mastering and retrieving prey items from short distances from the nest. Prey size determined the backwards entry typically adopted by this species, while prey weight determined the predatory strategy selected. After a common initial sequence (search for prey, detection, localization), predatory sequences varied in terms of the type of approach, the site of seizure, the reaction after stinging and the type of transport. Nevertheless, irrespective of prey weight and size, seizure was preferentially oriented towards the head and prey were always stung. Short-range recruitment and mass recruitment without trail laying were elicited by a large range of heavy prey (> 2.5 times the weight of an individual worker). According to the mortality risk associated with each prey, hunters exhibited a “prudent” stinging posture associated with an increase in the duration of the subsequent phase of waiting for prey immobilization. The overall time of capture was positively correlated with the weight of the prey. When collective hunting strategies were involved, E. ruidum colonies matched the number of recruited hunters to the size and weight of the prey. Compared to solitary hunting strategies, for short food–nest distances, this graded recruitment appeared to enhance the energetic benefits derived by this species from the use of recruitment systems: the higher the number of workers involved in the recruitment process, the greater the energetic benefits obtained. The exhibition or absence of trail laying behavior in the recruitment responses displayed by E. ruidum workers is discussed in relation to their involvement in scavenging or predatory behavior.

Can chemical signals, responsible for mutualistic partner encounter, promote the specific exploitation of nursery pollination mutualisms? – The case of figs and fig wasps

In nursery pollination mutualisms, where pollinators reproduce within the inflorescence they pollinate, floral scents often play a major role in advertizing host location and rewards for the pollinator. However, chemical messages emitted by the plant that are responsible for the encounter of mutualist partners can also be used by parasites of these mutualisms to locate their host. Each species of Ficus (Moraceae) is involved in an obligatory nursery pollination mutualism with usually one pollinating fig wasp (Hymenoptera: Chalcidoidea: Agaonidae). In this interaction, volatile compounds emitted by receptive figs are responsible for the attraction of their specific pollinator. However, a large and diverse community of non‐pollinating chalcidoid wasps can also parasitize this mutualism. We investigated whether the chemical message emitted by figs to attract their pollinator can promote the host specificity of non‐pollinating fig wasps. We analysed the volatile compounds emitted by receptive figs of three sympatric Ficus species, namely, Ficus hispida L., Ficus racemosa L., and Ficus tinctoria G. Forster, and tested the attraction of the pollinator of F. hispida (Ceratosolen solmsi marchali Mayr), and of one species of non‐pollinating fig wasp [Philotrypesis pilosa Mayr (Hymenoptera: Chalcidoidea: Pteromalidae)] to scents emitted by receptive figs of these three Ficus species. Analysis of the volatile compounds emitted by receptive figs revealed that the three Ficus species could be clearly distinguished by their chemical composition. Behavioural bioassays performed in a Y‐tube olfactometer showed that both pollinator and parasite were attracted only by the specific odour of F. hispida. These results suggest that the use by non‐pollinating fig wasps of a specific chemical message produced by figs could limit host shifts by non‐pollinating fig wasps.

Geographic variation of floral scent in a highly specialized pollination mutualism

Floral scents are important signals for communication between plants and pollinators. Several studies have focused on interspecific variation of these signals, but little is known about intraspecific variation in flower scent, particularly for species with wide geographic distributions. In the highly specific mutualism between Ficus species and their pollinating wasps, chemical mediation is crucial for partner encounter. Several studies show that scents, i.e. blends of volatiles, are species-specific, but no studies address interpopulation variation of scents in fig pollination mutualisms, which often have broad geographic distributions. In this study, using absorption/desorption headspace techniques, we analyzed variation in floral scent composition among three populations of each of two widely distributed Asian Ficus species. We identified more than 100 different volatile organic compounds, predominantly terpenes. In both species, significant differences were found between scent bouquets of East Asian and Indian populations. These differences are discussed in relation to geographical barriers that could disrupt gene exchange between these two areas, thereby isolating Indian populations from those of Eastern Asia.

Interactions of the ant Crematogaster scutellaris with the fig/fig wasp mutualism

Abstract. 1. A classical example of specialised pollination mutualisms is the relationship between fig trees and their pollinating wasps, in which each partner depends completely on the other for its reproduction; however the fig/fig wasp association is also the target of a great diversity of other species, ranging from specialised parasites to opportunistic foragers, among them ants.

The learning of a sequence of visual patterns by the ant Cataglyphis cursor

We used a maze to explore the ability of Cataglyphis cursor to store multiple visual patterns presented in a fixed sequence. Ants were trained individually to negotiate a linear maze that consisted of four boxes connected by tunnels and through which an ant travelled from a sucrose feeder back to its nest. Each box had one entrance and two possible exits. One exit led to a blocked tunnel and the other to an open tunnel leading to the entrance of the next box. The open and closed exits in each box were labelled by different solid, black shapes that were specific to each box. Ants learnt to negotiate the maze using the shapes for guidance rather than a fixed motor strategy. Trained ants could not only discriminate positive from negative shapes, but had also learnt which positive shape belonged to which box. For example, when the positive shape appropriate to box 1 (1+) was pitted against that appropriate to box 3 (3+), ants preferred 1+ to 3+ in box 1, but chose 3+ over 1+ in box 3. We conclude that ants can identify individual positive shapes and expect to encounter them in the correct order independently of extra-maze cues.

Evidence for intersexual chemical mimicry in a dioecious plant.

The dioecious Mediterranean fig, Ficus carica, displays a unique phenology in which males sometimes bloom synchronously with females (in summer), and sometimes not (in spring). Ficus carica is engaged in an obligatory mutualism with a specific pollinating wasp, which reproduces only within figs, localising them by their specific scents. We show that scents emitted by male figs show seasonal variation within individual trees. Scents of summer male figs resemble those of the co-flowering females, and are different from those of the same male trees in spring, when female figs are absent. These differences hold even if only compounds electrophysiologically active for pollinators are considered. The similar scents of summer males and females may explain why the rewardless females are still pollinated. These results offer a tractable model for future studies of intersexual chemical mimicry in mutualistic pollination interactions.

Rare white‐flowered morphs increase the reproductive success of common purple morphs in a food‐deceptive orchid

How floral colour polymorphism can be maintained in evolutionary time is still debated. In rewardless orchids, it is unknown whether rare white-flowered morphs differ in scent chemistry from pigmented morphs, and whether such intraspecific variation in floral signals may have an impact on reproductive success. We compared the chemical composition of floral volatiles emitted by white- and purple-flowered morphs of Orchis mascula, and recorded the fruit set of both colour morphs. We also used white ping-pong balls to mimic white-flowered morphs in field bioassays. We found that colour polymorphism was not associated with floral odour polymorphism. Surprisingly, when populations of purple-flowered plants included a few white-flowered individuals, the fruit set of the purple morph increased significantly (from 6 to 27%), while that of the white morph remained low. We obtained the same fourfold increase in fruit set when using ping-pong balls as visual lures, demonstrating the association between colour variation and fruit set, and the key role of visual signals in pollinator attraction. Our results are incompatible with negative frequency-dependent selection, a hypothesis invoked to explain colour polymorphism in other rewardless orchids. We propose several hypotheses to explain the maintenance of white morphs in O. mascula.

Ambush predation by the ponerine ant Ectatomma ruidum roger (Formicidae) on a sweat bee Lasioglossum umbripenne (Halictidae), in Panama

An individual ambush predation is used by huntresses of the ponerine ant Ectatomma ruidum to capture halictid bees (Lasioglossum umbripenne) in the Panamanian mountains. Workers, which use this strategy and originated from a colony (A) situated within a nest aggregation of halictid bees, capture almost four times more prey than colony (B) with a foraging area which does not include this type of bees nest. Forty-eight percent of the prey of colony (A) are halictid bees, demonstrating the local importance of this predatory strategy in E. ruidum. A close examination of the behavioral sequence of predation shows that ambush is successful in only 4.8% of cases, a very low success rate in comparison to other predatory strategies described in this species. Nevertheless, due to the high repetition (16.1 ± 5.9 times on average) of very short waiting phases (6.3 ± 1.9 s), the true success rate (i.e., according to the number of individual trips) can reach up to 80%. A review of ambush predation among ant species allows us to distinguish approaches between jumping, long stealth approaches, and true ambushes. Implications of learning and expectation processes are also discussed.

Floral scent variation in two Antirrhinum majus subspecies influences the choice of naïve bumblebees

Two wild subspecies of snapdragon, Antirrhinum majus, subspecies pseudomajus and striatum, differ in floral color and can be visually discriminated by insect visitors. The extent to which olfactory cues derived from floral scents contribute to discrimination between snapdragon subspecies is however unknown. We tested whether these two subspecies differ in floral scent and whether these olfactory differences are used by bumblebees (Bombus terrestris) to discriminate between them. We grew individuals of both subspecies, collected from a total of seven wild populations, under controlled conditions. We quantified the volatile organic compounds (VOCs) emitted by the flowers using gas-chromatography/mass-spectrometry/flame-ionization-detection. We studied antennal detection of VOCs by bumblebees, by means of electroantennogram study (EAG). We also performed behavioral experiments in a Y-maze to determine the innate response of bumblebees to the main floral VOCs emitted by our snapdragon subspecies. The floral scent of Antirrhinum majus pseudomajus contained three volatile benzenoids absent in the floral scent of Antirrhinum majus striatum. One of them, acetophenone, contributed over 69% of the absolute emissions of A. majus pseudomajus. These benzenoids elicited a significantly higher EAG response compared with other VOCs. In the Y-maze, bumblebees were significantly less attracted by acetophenone, suggesting an aversive effect of this VOC. Our findings indicate that bumblebees are able to discriminate between the two Antirrhinum majus subspecies. Differences in flower scent between these subspecies and olfactory bumblebee preferences are discussed in the light of biochemical constraints on VOCs synthesis and of the role of flower scent in the evolutionary ecology of A. majus.