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1. Species interactions in tightly bound ecological mutualisms often feature highly specialised species' roles in which competitive exclusion may preclude multi‐species coexistence. Among the 800 fig (Ficus) species, it was originally considered that each was pollinated by their own wasp (Agaonidae). However, recent investigations show that this 'one‐to‐one' rule often breaks down, as fig species regularly host multiple agaonids but in ways suggesting that competitive processes still mediate biodiversity outcomes. 2. A phenological survey was conducted of the fig–fig wasp pair, Ficus microcarpa and its associated pollinating wasp, alongside its sister species, the cheating wasp, in Xishuangbanna, China. 3. Reproductive output underwent extreme seasonal variation. Seed and pollinator production fell markedly during cooler, drier months, although high levels of fig production continued. However, this resource was predominantly utilised by the cheater species, which offers no pollination services. Pollinators and cheaters rarely co‐occur, suggesting that temporal coexistence is constrained by competition for access to figs. 4. The overall findings indicate periodic rearrangements of mutualism dynamics, probably resulting from a strongly seasonal environment. Sympatric co‐occurrence may result from a window of opportunity for a functionally divergent agaonid, potentially due to constraints on the main pollinator in adapting to variable year‐round conditions that prevent competitive exclusion. [ABSTRACT FROM AUTHOR]

Most mutualisms are exploited by parasites, which must strike an evolutionary balance between virulence and long‐term persistence. Fig‐associated nematodes, living inside figs and dispersed by fig wasps, are thought to be exploiters of the fig–fig wasp mutualism. The life history of nematodes is synchronized with the fig development and adapted to particular developmental characteristics of figs. We expect host breeding systems (monoecious vs. gynodioecious figs) and seasonality to be central to this adaptation. However, the details of the adaptation are largely unknown. Here, we conducted the first field surveys on the prevalence of nematodes from monoecious Ficus microcarpa L.f. (Moraceae), gynodioecious Ficus hispida L.f., and their pollinating fig wasps in two seasons and two developmental stages of figs in Xishuangbanna, China. We followed this up by quantifying the effects of nematodes on fitness‐related traits on fig wasps (e.g., egg loads, pollen grains, and longevity) and fig trees (seed production) in gynodioecious F. hispida. The magnitude of nematode infection was compared between pre‐ and post‐dispersal pollinators to quantify the probability of nematodes being transported to new hosts. Our results showed that Ficophagus microcarpus (Nematoda: Aphelenchoididae) was the only nematode in F. microcarpa. In F. hispida, Martininema guangzhouensis (Nematoda: Aphelenchoididae) was the dominant nematode species, whereas Ficophagus centerae was rare. For both species of Ficus, rainy season and inter‐floral figs had higher rates of nematode infection than the dry‐hot season and receptive figs. Nematodes did not affect the number of pollen grains or egg loads of female wasps. We did not detect a correlation between seed production and nematode infection. However, carrying nematodes reduced the lifespan and dispersal ability of pollinator wasps, indicating higher rates of post‐emergence mortality in infected fig wasps. Severely infected fig wasps were likely 'filtered out', preventing the overexploitation of figs by wasps and stabilizing the interaction over evolutionary time. [ABSTRACT FROM AUTHOR]

Summary: Interactions between mutualists, competitors, and antagonists have contrasting ecological effects that, sustained over generations, can influence micro‐ and macroevolution. Dissimilar benefits and costs for these interactions should cause contrasting co‐diversification patterns between interacting clades, with prevalent co‐speciation by mutualists, association loss by competitors, and host switching by antagonists.We assessed these expectations for a local assemblage of 26 fig species (Moraceae: Ficus), 26 species of mutualistic (pollinating), and 33 species of parasitic (galling) wasps (Chalcidoidea). Using newly acquired gene sequences, we inferred the phylogenies for all three clades. We then compared the three possible pairs of phylogenies to assess phylogenetic congruence and the relative frequencies of co‐speciation, association duplication, switching, and loss.The paired phylogenies of pollinators with their mutualists and competitors were significantly congruent, unlike that of figs and their parasites. The distributions of macroevolutionary events largely agreed with expectations for mutualists and antagonists. By contrast, that for competitors involved relatively frequent association switching, as expected, but also unexpectedly frequent co‐speciation. The latter result likely reflects the heterogeneous nature of competition among fig wasps.These results illustrate the influence of different interspecific interactions on co‐diversification, while also revealing its dependence on specific characteristics of those interactions. [ABSTRACT FROM AUTHOR]

Classical biological control agents fail to achieve an impact on their hosts for a variety of reasons and an understanding of why they fail can help shape decisions on subsequent releases. OrnamentalFicus microcarpais a widely planted avenue fig tree that is invasive in countries where its pollinator (Eupristina verticillata) is also introduced. This tree also supports more than 20 species of non-pollinating fig wasps (NPFW) that feed in the figs and have the potential to reduce the plant’s reproduction.Odontofroggatia galili, one of the most widely introduced NPFW, has larvae that develop in galled ovules that might otherwise develop into seeds or support pollinator larvae. We examined the distribution and relative abundance of the pollinator andO. galilionF. microcarpain China, towards the northern limit of the tree’s natural range, and in Italy where the two species have been introduced. Where they co-existed, we also recorded the impact of varying densities ofO. galilionF. microcarpaseed and pollinator production.O. galiliandE. verticillatadisplayed contrasting habitat preferences in China, withO. galilialmost absent from warmer sites.O. galiliabundance and sex ratios varied between the natural and introduced ranges. Figs with moreO. galilicontained fewer seeds and pollinator offspring, but reproduction was rarely inhibited totally. Additional species with a greater impact in the figs they occupy are needed if biocontrol ofF. microcarpais to be effective. [ABSTRACT FROM PUBLISHER]

Floral scents are known as an olfactory signal for attracting pollinators, but why the flowers pollinated by highly specialised pollinators emit scents consisting of mixtures of many compounds and dominated by one or a few compounds is still poorly understood. We supposed that each (especially characteristic) chemical in floral scents may play a specific role in mediating pollinator behaviours and tested this supposition in a fig-fig wasp mutualism.Ficus curtipesis obligately pollinated by an undescribedEupristinaspecies. In the scent ofF.curtipesreceptive figs, over 50 compounds have been identified, and the scent is dominated by two compounds, 6-methyl-5-hepten-2-ol (OL) and 6-methyl-5-hepten-2-one (NE). We therefore tested the roles of the two major chemicals in mediating the pollinator behaviours. Our results show that OL and NE, respectively, act as a long-distance attractant and a fig-entry behaviour stimulant to the obligate pollinator wasp. Namely, OL attracts the wasps to the figs and NE guides the wasps into the figs. This finding on the work division of floral scent compounds partially explains the maintenance mechanism of the fig-fig wasp mutualism and the significance of the chemical diversity of floral scent in plant–pollinator interactions, especially in specialised pollination systems. [ABSTRACT FROM PUBLISHER]

Pollinator fig wasps serve as useful empirical models for studies of sex ratio evolution because females adjust their offspring sex ratios in relation to the number of foundresses that share a fig. Placement of pollinator offspring within figs is not random and more centrally located flowers are more likely to support pollinator development. We compared components of fitness of female fig wasps developing in central and peripheral flowers and whether this influenced the sex ratios of their offspring. We used Ceratosolen solmsi marchali , a pollinator of the Asian dioecious fig tree, Ficus hispida . Mating frequency was determined from the number of mating holes in females' flowers. Most females mated once, but some had the opportunity to mate up to four times and multiple mating opportunities were more frequent among centrally located galls. Body size was not linked to flower location, although the females that mated most were significantly larger than others, and came from significantly larger galls. Females that had multiple mating opportunities produced more daughters but similar numbers of sons, resulting in more female-biased broods. These females are likely to have produced more offspring because of their larger size but may have also benefited from mating with more males. The results demonstrate that differences in the natal locations of foundresses can modify offspring sex ratios and obscure sex ratio adjustment in response to the number of foundresses sharing a fig. [ABSTRACT FROM AUTHOR]

Abstract: The interaction between the hundreds of Ficus species and their specific pollinating fig wasps (Agaonidae) presents a striking example of mutualism. Foundress fig wasps pollinate fig flowers, but also lay their eggs in (and gall) some of them. Only two cases of cheating fig wasps (that fail to pollinate) have been reported, from two continents, suggesting that there is a cost to abandoning pollination. Reasons for the rarity of cheating are a major question in fig biology, because persistence of the mutualism depends on fig wasps continuing to pollinate. A cost in terms of reduced reproductive success among cheaters could be one explanation. Here we compare the behavior and reproduction of an undescribed Eupristina sp., a cheater that coexists with the pollinator Eupristina altissima on Ficus altissima in southern China. Adult females of both species fought with conspecifics when they were seeking entry through the ostiole into receptive figs, but there was no fighting with heterospecifics. Despite a similar body size, female pollinators contained more eggs than female cheaters. Pollinators and cheaters produced similar number of galls, and although almost twice as many flowers were galled in figs entered by two compared to one foundress, larval mortality was greatly increased when two foundresses were present. Larval mortality was also significantly higher for cheaters compared to pollinators, independent of the number of foundresses. Ovules galled by the cheater were thus significantly less likely to result in adult offspring, suggesting that there are significant costs associated with abandoning the mutualism. [Copyright &y& Elsevier]

Mutualism can facilitate the colonization, establishment, and spread of invasive species. By modifying interactions with third parties, mutualisms can have cascading community-wide effects. Both native and invasive ants are capable of forming mutualisms with hemipteran insects, preying on non-hemipteran herbivores and indirectly affecting primary production. Comparative research on the effects of both native and invasive ant exclusions on multitrophic interactions is therefore crucial for understanding the invasive potential of ants, along with any ecological consequences that invasions may have. We performed a quantitative review of the multitrophic effects of invasive and native ants on insect–plant food webs. Herbivorous insects are the most common food source for both invasive (comprising 56% of prey species caught) and native ants (55% of the prey species caught), followed by predators (31% for invasive ants, 45% for native ants). Excluding both invasive and native ants significantly reduced hemipteran abundance, and excluding invasive ants had a greater negative impact on hemipteran abundance than native ants. Native ant predation significantly reduced herbivore abundance, but excluding invasive ants had no effect. Cascading effects of native ants on plant fitness were significantly positive, but there was no significant impact of invasive ants. These findings suggest a weak relationship between the presence of invasive ants and non-hemipteran herbivore abundance. We suggest that the hemipteran–ant mutualism could represent a 'symbiotic invasion'. The ecological dominance of invasive ants is often facilitated by hemipteran insects. This association requires invasive ant control strategies to expand beyond ants to consider mutualists. [ABSTRACT FROM AUTHOR]

Plant odours are central for pollinator attraction. This is particularly true in obligate brood site pollination mutualisms. However, we know little about the evolution of olfactory signalling in these mutualisms. Here, we investigate geographic variation of floral odour in the obligate host-specific brood site pollination mutualism between Ficus hirta and its specialised pollinators. Floral scent samples from nine locations in China were collected using head-space adsorption and were analysed by gas chromatography-mass spectrometry. We evidence progressive geographic divergence of floral odours. The pattern of variation fits plant genetic structure for neutral genes but differs from pollinating insect structuring into species and populations. In our study system, the geographic variation of receptive floral odour presents a pattern that is not distinguishable from neutral drift. The variation is not canalised by the insects. We propose that this pattern characterises obligate brood site pollination mutualisms in which pollinators are host specific and dispersal of plant and insect is limited. Insects with their short generation times and large population sizes rapidly track any chance variation in host receptive inflorescence odours. Plants are the drivers and insects the followers. The source of the geographic variation in floral odours can be genetic or phenotypic in response to local conditions. Strict sense plant-insect co-evolution is not involved. In contrast, previous results on another Ficus -pollinating wasp association suggest that stabilising selection could be at work in more dispersive systems. • Here, we investigate the geographic variation of floral odour in the obligate host-specific brood site pollination mutualism between Ficus hirta and its specialised pollinators. We evidence that floral odours vary geographically in accordance to plant genetic variation but not to pollinating wasp structure, suggesting that plants are the drivers of geographic variation of floral odours in brood site pollination mutualisms. [ABSTRACT FROM AUTHOR]

Although in Moraceae the presence of laticifers is considered to be a synapomorphy, little is known about the distribution and morphology of this type of secretory structure in the reproductive organs of its species. Ficus , the largest genus of Moraceae, is characterized by an inflorescence known as syconium and by an obligate mutualistic interaction with pollinating wasps. The objectives of the present study were to evaluate the distribution and morphology of laticifers in syconia of 36 species belonging to different Ficus sections and to survey traits of taxonomic and adaptive value for the group. Syconia containing flowers in a receptive state were collected, fixed and processed for anatomical analysis. All species studied have branched laticifers distributed in the syconium receptacle, in the ostiolar bracts and in the pedicel of staminate flowers. Almost all species show laticifers in the pedicel of shorter-styled flowers. Laticifers also occur in the pedicel of longer-styled flowers in most Ficus sections, except F. curtipes ( Conosycea section) and more than 75% of the studied species of the Americanae section. Laticifers are observed in the sepals of 25 of the 36 species studied and occasionally in the pistil. The presence of laticifers in the pedicel of shorter-style flowers and its absence in the pistil suggest that the distribution of this secretory structure in the fig flower was selected by pressures imposed by the fig-fig wasp mutualism. The laticifers in the pedicel of shorter-styled flowers may confer protection to the developing wasp larvae against natural enemies. However, the absence of laticifers in the pistil of most Ficus species studied was probably selected by the mutualistic relationship with the agaonid pollinating wasps since the latex could interfere with oviposition through the style, with the larval development of the pollinating fig wasps, and the emergence of pollinator offspring from their galls. [ABSTRACT FROM AUTHOR]

Abstract: Fig pollinating wasps and most non-pollinator wasps apply secretions from their poison sacs into oviposited flowers that appear necessary to the formation of the galls that their developing offspring consume. Thus, both eggs and poison sac secretions appear to be essential for wasp reproduction, but the relative investment in each is unknown. We measured relative investment in poison sac and egg production in pollinating and non-pollinating wasps associated with seven species of monoecious Panamanian figs representing both active and passive pollination syndromes. We then collected similar data for four fig hosts in China, where some wasp species in the genus Eupristina have lost the ability to pollinate (“cheaters”). All wasps examined possessed large poison sacs, and we found a strong positive correlation between poison sac size and absolute egg production. In the Panamanian species, the relative poison sac to egg investment was highest in the externally ovipositing non-pollinator wasps, followed by active pollinators, then by passive pollinators. Further, pollinator wasps of fig species with demonstrated host sanctions against “cheating” wasps showed higher investment in the poison sac than wasps of species without sanctions. In the Chinese samples, relative investment in the poison sac was indistinguishable between pollinators and “cheaters” associated with the same fig species. We suggest that higher relative investment in poison sac across fig wasp species reflects higher relative difficulty in initiating formation of galls and subsequently obtaining resources from the fig. We discuss the implications for the stability of the fig–wasp mutualism, and for the ability of non-pollinators to exploit this mutualism. [Copyright &y& Elsevier]

A comparison was performed of the antennal sensilla of females of four chalcid wasp species Ceratosolen emarginatus Mayr, 1906, Sycophaga sp., Philotrypesis longicaudata Mayr, 1906, and Sycoscapter roxburghi Joseph, 1957, which are specific and obligatory associated with Ficus auriculata (Lour, 1790). The four species exhibit different oviposition strategies in the fig ovules where their offspring hatch and develop. Antennal sensilla morphology was evaluated using scanning electron microscopy. Females of the four species present 11 morphologically similar types of sensilla: trichoid sensilla, sensilla obscura, chaetica sensilla 1 and 2, which all have mechanosensory functions; uniporous basiconic sensilla, which are presumably contact chemosensilla; basiconic capitate peg sensilla, coeloconic sensilla 1, multiporous basiconic and placoid sensilla, which may be regarded as olfactory sensilla, and coeloconic sensilla 2 and 3, which are presumed to be proprioreceptors or pressure receptors. The four species have significant differences in the abundance and arrangement of trichoid sensilla and chaetica sensilla 1 on the flagellum. The coeloconic sensilla and sensilla obscura only occur on the antennae of C. emarginatus that enter figs. The chemosensilla which are presumably involved in host discrimination, i.e., basiconic sensilla, multiporous placoid sensilla and basiconic capitate peg sensilla, are similar in shape and configuration, although they present some differences in abundance. These findings provide practical information on the adaptations of fig wasps and the relationship between multisensory antennae and functions in fig wasp behaviour. [ABSTRACT FROM AUTHOR]

• In male figs agaonid wasps deposit a single pollen grain each time they oviposit. • Stigma shape and pollen transfer to the hypopygium ensure very precise pollination. • In female figs wasp behaviour is less precise than in male figs. • In female figs exposed stigmatic papillae and synstigma ensure efficient seed set. • Plant morphology stabilises the mutualism. Active pollination has evolved four times in brood site pollination mutualisms. When pollination is active, the pollinator's behaviour specifically evolves to ensure flower fertilisation. In functionally dioecious Ficus species, the male figs host pollinating wasp larvae, while wasps cannot breed in the female figs because the styles are longer than the wasp ovipositor. Here we investigate the dioecious Ficus hispida. We show that in male figs, every time the wasp has laid an egg into a pistillate flower, it removes one pollen grain from its pollen pockets and places it on the hypopygium. When the wasp inserts its ovipositor into the next flower, the pollen grain is deposited deep within the style. Each ovipositor insertion results in flower pollination and insect oviposition. Because of systematic pollination of the flowers into which the eggs are laid, the wasp larvae benefit from feeding on fertilised endosperm while no seed are produced. In female figs, after probing a flower, the wasp presents pollination behaviour only every five visits. However, if it does occur, this behaviour lasts longer than in male figs and results in the deposition of on average 10 pollen grains on the hypopygium. The exposed sticky papillae on the stigmatic surface collect pollen from the hypopygium and pollen tubes may grow to neighbouring stigmas, ensuring secondary dispersal and efficient ovule fertilisation. Overall, our study demonstrates that the floral morphology of male figs facilitates precise pollen deposition, beneficial for the wasp progeny, while the floral morphology of female figs compensates for wasp pollination behaviour that is not selected in those figs. We conclude that the morphology of the arena in which interactions with its pollinator are played out is the result of selection on the plant to maximize its male and female fitness. Incidentally, this morphology stabilises the mutualistic interaction. [ABSTRACT FROM AUTHOR]

Abstract: Fig trees (Ficus spp.) are popular ornamental trees that are entirely dependent on a mutalistic association with host-specific pollinating fig wasps for reproduction. They can become naturalized and invasive in countries where the associated pollinator is also established. Figs (syconia) are also also utilized by a diverse community of organisms that are potentially detrimental to the pollinators or seed production. Ficus benjamina is a widely-planted fig tree with the ability to establish outside its native range. We examined the impact of an undescribed gall midge species associated with F. benjamina within the plant’s natural range in Xishuangbanna, south-western China. Observations on the levels of abundance of the midge together with fig abortion and seed germination rates showed that the gall midge had a strong negative effect on reproduction. The gall midge reduced pollinator survival and at high densities eliminated all pollinators, due primarily to premature abortion of figs. Seed numbers were only reduced at high gall midge densities, but seed quality, as measured by germination success and root growth rates, was greatly reduced whenever the gall midge was present. Within its presumed natural range the gall midge appears to be host specific, and given its dramatic impact on host reproductive success, is a potential candidate for the biological control of F. benjamina. [Copyright &y& Elsevier]