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Diet of Non-pollinating Wasps and Their Impact on the Stability of Fig-pollinator Wasp Mutualism

YANG Cheng-yun,WANG Rui-Wu,ZHAO Gui-Fang,YANG Da-Rong,

动物学研究 , 2005,
Abstract: Ficus (Moraceae) and their species-specific pollinator wasps (Agaonidae) form a remarkable plant-insect obligate mutualism, and non-pollinators are the exploiters of the mutualism. The negative impact of exploiters on the reciprocal mutualists might disrupt the reciprocal mutualism in the process of evolution, but how the exploiters could coexist with the reciprocal mutualsits is not still clear. In this study, the diet of the five species of non-pollinators and relationship among fig wasps were analyzed on Ficus racemosa L. in Xishuangbanna from Dec. 2003 to Apr. 2004. In a controlled experiment pollinators and each species of non-pollinators oviposited and counts of wasps and seeds in mature figs were conducted. The results indicated that only Platyneura testacea Motschulsky and Platyneura mayri Rasplus are gall-makers, which can induce the ovaries into galls; Apocrypta sp., Apocrypta westwoodi Grandi and Platyneura agraensis Joseph are the parasitoids. The gall-makers and the parasitoids of pollinators have negative impacts on pollinators, but the impacts are not significant because of the influence of the ants and parasitoids of gall-makers. Additionally, the experiment excluding non-pollinators oviposition showed that the number of offspring of pollinators and seeds were not significantly different with the natural fruits. Moreover, the analysis on the natural population structure of fig wasps revealed that the pollinators are the dominant species. So in the natural condition, the abundance of gall-makers and parasitoids of pollinators are below the level needed to exclude pollinators, and thus they have a relatively weak impact on the stability of fig-pollinator mutualism and can coexist with the mutualism.
Relation between two non-pollinating wasps oviposition and the fruit abscission on Ficus racemosa

SUN Bao-Fa,WANG Rui-Wu,HU Zhong,LI Yao-Tang,

生态学报 , 2009,
Abstract: In the fig-fig wasp obligate mutualism, parasitic wasps Platyneura testacea and Platyneura mayri coexist with pollinating wasps. Theses non-pollinating wasps only use the seeds of figs or compete with pollinating wasp for floral resources, bring no any benefits to figs. The parasitism of these non-pollinating wasps may result in the disruption of the cooperation between figs and fig wasps. The fruit abscission mechanism of plant is generally considered as one of the key factors maintaining system stability. However, our quantitative experiment and field observations of fig-fig wasp system showed that the figs did not abscise fruits oviposited by Platyneura mayri, but abscised fruits over-ovipisited by P.testacea. The observation showed that tree oviposited by more P. testacea will have higher proportion of abscission. The over-ovipositing of P.testacea is the main reason for selective abscission of syconium. Our results indicate that the plant can only abscise fruits oviposited by parasitic wasps before pollinating wasps in fig-fig wasp mutualism, but do not abscise the fruits parasitized by wasps ovipositing simultaneous or later than pollinating wasps, implying that abscission can not sufficiently maintain the fig-fig wasp mutualism.
The comparison of three fig wasp pollinators and their pollination efficiency on Ficus curtipes

ZHANG Feng-Ping,PENG Yan-Qiong,YANG Da-Rong,

生态学报 , 2009,
Abstract: Figs and fig-pollination wasps (Agaonidae) are highly coevolved mutualists that depend completely on each other for continued reproduction. A few non-agaonid wasps can enter figs to oviposit and effectively pollinate their fig hosts. However, there are few studies that compare the pollination efficiency of agaonid and non-agaonid wasps. In Xishuangbanna, Ficus curtipes is monoecious, and is typically pollinated by agaonid Eupristina sp. Two species of non-agaonid wasps Diaziella yangi and Lipothymus sp. also enter the fig to oviposit and can effect pollination. These wasps are specific and strictly dependent on the fig for their development. The pollination efficiencies of the three species of fig wasps were compared in this study. We collected the data from natural populations and combined these with introduction experiments of the three species of fig wasps. We compared the contribution of three fig wasps to the seed production of F. curtipes. The results showed that the number of three fig wasps trapped in the fig cavity was usually one. However, as the number of conspecific foundresses per fruit increased, the number of seeds produced increased. Sometimes the pollination efficiency of D. yangi and Lipothymus sp. was even higher than that of Eupristina sp. When one Eupristina sp. and one non-agaonid wasp were introduced to enter a fig at the same time, the seed production did not significantly increase and the number of seeds was close to that when only one foundress of Eupristina sp. entered. This implied that D. yangi or Lipothymus sp. did not increase the pollination efficiency. When comparing the pollination efficiency of three fig wasps in one- and two-foundress broods, in two-foundress brood the average pollination efficiency of Eupristina sp. and Lipothymus sp. decreased, but that of D. yangi increased. The differences of pollination efficiency possibly result from different interactions between three fig wasps and the host Ficus. The results will be useful for further studying the mutualism origin of the fig-fig wasp interaction.
Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism
Michael J McLeish, Simon van Noort
BMC Evolutionary Biology , 2012, DOI: 10.1186/1471-2148-12-1
Abstract: Statistical parsimony and AMOVA revealed deep divergences at the COI locus within several pollinating fig wasp species that persist on the same host Ficus species. Changes in branching patterns estimated using the generalized mixed Yule coalescent test indicated lineage duplication on the same Ficus species. Conversely, Elisabethiella and Alfonsiella fig wasp species are able to reproduce on multiple, but closely related host fig species. Tree reconciliation tests indicate significant codiversification as well as significant incongruence between fig wasp and Ficus phylogenies.The findings demonstrate more relaxed pollinating fig wasp host specificity than previously appreciated. Evolutionarily conservative host associations have been tempered by horizontal transfer and lineage duplication among closely related Ficus species. Independent and asynchronistic diversification of pollinating fig wasps is best explained by a combination of both sympatric and allopatric models of speciation. Pollinator host preference constraints permit reproduction on closely related Ficus species, but uncertainty of the frequency and duration of these associations requires better resolution.Several lines of theory have been proposed to account for the enormous diversity of phytophagous insects. Diversification conceivably ensues by ecological opportunity and adaptation to the exploitation of previously unattainable resources [1,2]; by restricted gene flow through allopatric means [3,4]; and disruptive selection and sympatric speciation [5,6]. In order to discern among potential mechanisms driving speciation, both historical pattern and ecological scale processes are important to consider [7-10]. Comparative phylogenetic approaches that test congruence between host and associate populations can contribute to greater resolution in unravelling ecological scale processes [11-14]. Here we interpret the codiversification between Ficus host species and populations of a group of African fig wasp
The mating behaviors of the non-pollinating fig wasps of Ficus curtipes
钝叶榕(Ficus curtipes)非传粉小蜂交配行为

SONG Bo,PENG Yan-Qiong,YANG Zhao-Xiong,YANG Da-Rong,

生态学报 , 2008,
Abstract: Ficus and their species-specific pollinator wasps (Agaonidae) exhibit a remarkable obligate mutualism. Fig trees are typically pollinated only by female agaonids, whose offspring feed on the ovules of the plant. Figs also shelter numerous other, unrelated, fig wasps that usually exploit the fig pollinator mutualism. Ficus curtipes Corner is a monoecious strangler fig tree. At Xishuangbanna Tropical Botanical Garden, 9493 individual fig wasps were reared from 100 figs (syconia). They included one species of agaonid wasp and five unrelated fig wasps. The agaonid Eupristina sp. was represented by 45% of the individuals, Diaziella yangi van Noort & Rasplus by 46% and the remaining 9% by Lipothymus sp., Philotrypesis sp., Sycobia sp. and Sycoscopter sp. Females of the first three species enter the figs to oviposit whereas the others lay their eggs from the outside of the figs. In this study, the order of emergence of the fig wasps from their natal figs and their mating behavior were recorded. They followed a strict sequence of emergence, with Sycobia sp. emerging first, then Lipothymus sp., followed by Diaziella yangi. Eupristina sp., Philotrypesis sp. and Sycoscopter sp. emerged last. Contrary to expectations, the mating sites of the five species of non-agaonid fig wasps were not always linked to the presence or absence of wings in the males. D. yangi (with winged males) mated mostly inside the figs and its males engaged in fatal fights for mating opportunities. Male Lipothymus sp. (with wingless males), mated both inside and outside the figs whereas male Sycobia sp. (with winged males) only mated outside. Males of Philotrypesis sp. and Sycoscopter sp. (both with wingless males), only mated inside the figs. Fig wasps often display highly female-biased sex ratios linked to local mate competition. D. yangi, despite having winged males, mated mainly inside the figs, which is likely to influence its optimal sex ratio. The presence of wings in male fig wasps is therefore not a good predictor of mating sites, nor sex ratio.
Host-Plant Species Conservatism and Ecology of a Parasitoid Fig Wasp Genus (Chalcidoidea; Sycoryctinae; Arachonia)  [PDF]
Michael J. McLeish, Gary Beukman, Simon van Noort, Theresa C. Wossler
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0044804
Abstract: Parasitoid diversity in terrestrial ecosystems is enormous. However, ecological processes underpinning their evolutionary diversification in association with other trophic groups are still unclear. Specialisation and interdependencies among chalcid wasps that reproduce on Ficus presents an opportunity to investigate the ecology of a multi-trophic system that includes parasitoids. Here we estimate the host-plant species specificity of a parasitoid fig wasp genus that attacks the galls of non-pollinating pteromalid and pollinating agaonid fig wasps. We discuss the interactions between parasitoids and the Ficus species present in a forest patch of Uganda in context with populations in Southern Africa. Haplotype networks are inferred to examine intraspecific mitochondrial DNA divergences and phylogenetic approaches used to infer putative species relationships. Taxonomic appraisal and putative species delimitation by molecular and morphological techniques are compared. Results demonstrate that a parasitoid fig wasp population is able to reproduce on at least four Ficus species present in a patch. This suggests that parasitoid fig wasps have relatively broad host-Ficus species ranges compared to fig wasps that oviposit internally. Parasitoid fig wasps did not recruit on all available host plants present in the forest census area and suggests an important ecological consequence in mitigating fitness trade-offs between pollinator and Ficus reproduction. The extent to which parasitoid fig wasps exert influence on the pollination mutualism must consider the fitness consequences imposed by the ability to interact with phenotypes of multiple Ficus and fig wasps species, but not equally across space and time.
Spatial Stratification of Internally and Externally Non-Pollinating Fig Wasps and Their Effects on Pollinator and Seed Abundance in Ficus burkei  [PDF]
Sarah Al-Beidh,Derek W. Dunn,James M. Cook
ISRN Zoology , 2012, DOI: 10.5402/2012/908560
Abstract: Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms. 1. Introduction Mutualisms are reciprocally beneficial interspecific interactions [1, 2], and a well-known system is that between fig trees (Ficus spp.) and their agaonid wasp pollinators [3–6]. In return for pollination, the wasps gall some fig ovules, which are then eaten by the larvae. About half (300+) of Ficus species are monoecious, where both male flowers and ovules are present in the same syconium (enclosed inflorescence or “fig”). Within monoecious syconia, ovules are highly variable in length [7–10]. Long (inner) ovules have short styles and mature near the centre of the syconium, whereas short (outer), long-styled ovules mature nearer the outer wall (see Figure 1). Female pollinating wasps (foundresses) lay their eggs by inserting their ovipositors down the flower styles. At maturation, wasp galls are clustered at the syconium’s centre [4, 6, 9–13] with seeds at the outer wall. This spatial stratification of pollinating wasps and seeds enables mutualism stability, although the mechanisms preventing the wasps from galling all ovules are unclear. Figure 1: Variation in style and pedicel length in female flowers of monoecious Ficus (adapted from Dunn et al. [ 13]). Mechanisms proposed to
Chemical attraction of fig volatiles to their pollinating fig wasps

CHEN Chun,

生态学报 , 2004,
Abstract: The specificity of the relationship between fig species and their particular agaonine pollinators (Hymenoptera: Chalcidoidea Agaonidae) has long been regarded as the extreme example of co-evolution. The maintenance of the fig-fig wasp mutualism system is strongly dependent on the chemical orientation of pollinating fig wasps using fig volatiles. The pollinating fig wasps trace the fig volatiles of their particular host and enter the figs at receptive phase (female flower phase) only, where they oviposit for themselves or pollinate for their partners.Field assay and olfactometry experiments were designed to examine the chemical basis of the species-specific mutualism and the difference between receptive fig volatiles and non-receptive ones in attracting pollinators. Three tropical fig species: Ficus hispida, F.auriculata and F.semicordata, and their corresponding pollinating fig wasps Ceratosolen solmsi marchali, (C. emarginatus) and C.gravelyi were chosen for tests. Fig volatiles including 12 info-chemicals and 3 dichloromethane extracts of figs in receptive and inter-floral phases were tested. The field experiments were conducted in Xishuangbanna Tropical Botanical Garden in Yunnan province of China. Sticky traps with cotton balls contained 0.5ml solvent or fig volatile compounds were set near fig trees of F. hispida and (F. auriculata) in male phase. Every day at 12:00 and 18:00, the numbers of fig wasps in each trap were recorded. Each observation lasted 2 weeks. Data were analyzed by the Mann-Whitney U test. The results showed that geraniol was significantly attractive to C. solmsi marchali (p<0.05), while vanillin and linalool were attractive in lesser degrees only (p<0.10). Linalool and the extract of receptive figs of F. auriculata were significantly attractive to C. emarginatus, but the number of the wasps trapped by the inter-floral fig extract was even lower than the control. Furthermore, a four-arm olfactometer was used to test the responses of the pollinating fig wasps to 12 fig volatile compounds. The wasps trapped in the arm treated with volatile compound and in the control arm were recorded respectively. Data were analyzed by a paired t-test. The results showed that C. gravelyi were significantly attracted by geraniol and terpineol (p<0.05). The responses of C.solmsi marchali and C.gravelyi to 12 info-chemicals were different, but they both preferred geraniol, linalool, farnesol, vanillin and terpineol to other compounds. C.emarginatus showed greater preference for the receptive fig extracts than the inter-floral ones.The results suggest that the fig-fig wasp specificity might result from the specific combination of several major fig volatile compounds and some particular minor volatile compounds. The results also indicate that pollinating fig wasps have preferences for receptive figs.
Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp
Eleanor R Haine, Joanne Martin, James M Cook
BMC Evolutionary Biology , 2006, DOI: 10.1186/1471-2148-6-83
Abstract: We studied variation in 71 fig-pollinating wasps from across the large geographic range of Ficus rubiginosa in Australia. All wasps sampled belong to one morphological species (Pleistodontes imperialis), but we found four deep mtDNA clades that differed from each other by 9–17% nucleotides. As these genetic distances exceed those normally found within species and overlap those (10–26%) found between morphologically distinct Pleistodontes species, they strongly suggest cryptic fig wasp species. mtDNA clade diversity declines from all four present in Northern Queensland to just one in Sydney, near the southern range limit. However, at most sites multiple clades coexist and can be found in the same tree or even the same fig fruit and there is no evidence for parallel sub-division of the host fig species. Both mtDNA data and sequences from two nuclear genes support the monophyly of the "P. imperialis complex" relative to other Pleistodontes species, suggesting that fig wasp divergence has occurred without any host plant shift. Wasps in clade 3 were infected by a single strain (W1) of Wolbachia bacteria, while those in other clades carried a double infection (W2+W3) of two other strains.Our study indicates that cryptic fig-pollinating wasp species have developed on a single host plant species, without the involvement of host plant shifts, or parallel host plant divergence. Despite extensive evidence for coevolution between figs and fig wasps, wasp speciation may not always be linked strongly with fig speciation.Hosts and their symbionts often have major effects on each other's evolution. Indeed, many symbioses show coevolution of key traits, such as parasite virulence and host resistance and, in some cases, may also manifest cospeciation. A classic example of a coevolved mutualism is provided by the obligate relationship between fig trees (Ficus species) and fig-pollinating wasps (Hymenoptera:Agaonidae). Female wasps enter receptive fig syconia (inflorescences) via a nar

XU Fa-Jian,CHEN Guo-Hua,PENG Yan-Qiong,XIE Xiao-Bo,YANG Da-Rong,

植物生态学报 , 2007,
Abstract: 榕-蜂共生系统是桑科榕属(Ficus)植物与传粉榕小蜂专一互惠形成的生态学关系。但是,也有一些非传粉的小蜂出现在这个系统中,对榕-蜂共生系统可能产生较大的影响。西双版纳的聚果榕(Ficus racemosa)树上主要有5种非传粉小蜂,分别在榕果发育的不同阶段从果外向果内产卵。在传粉榕小蜂进果之前的花前期,Platyneura testace、Apocrypta sp.和P.mayri这3种非传粉小蜂先后到果外产卵繁殖后代,对榕-蜂共生系统造成显著影响,尤其是影响传粉榕小蜂的繁殖。在传粉榕小蜂进果之后的间花期,P.mayri、A.westwoodi和P.agraensis这3种非传粉小蜂相继到果外产卵,它们虽然能减少种子形成和传粉榕小蜂繁殖的数量,但最终没有对榕-蜂共生系统造成显著的影响。造瘿类的P.mayri可在花前期和间花期产卵繁殖,在花前期产卵时它主要是影响传粉榕小蜂的繁殖,而在间花期产卵时它则更多地是影响种子的生产。
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