Biased oviposition and biased survival together help resolve a fig–wasp conflict

We report evidence that helps resolve two competing explanations for stability in the mutualism between Ficus racemosa fig trees and the Ceratosolen fusciceps wasps that pollinate them. The wasps lay eggs in the tree's ovules, with each wasp larva developing at the expense of a fig seed. Upon maturity, the female wasps collect pollen and disperse to a new tree, continuing the cycle. Fig fitness is increased by producing both seeds and female wasps, whereas short‐term wasp fitness increases only with more wasps, thereby resulting in a conflict of interests. We show experimentally that wasps exploit the inner layers of ovules first (the biased oviposition explanation), which is consistent with optimal‐foraging theory. As oviposition increases, seeds in the middle layer are replaced on a one‐to‐one basis by pollinator offspring, which is also consistent with biased oviposition. Finally, in the outer layer of ovules, seeds disappear but are only partially replaced by pollinator offspring, which suggests high wasp mortality (the biased survival or ‘unbeatable seeds’ explanation). Our results therefore suggest that both biased oviposition and biased survival ensure seed production, thereby stabilizing the mutualism. We further argue that biased oviposition can maintain biased survival by selecting against wasp traits to overcome fig defenses. Finally, we report evidence suggesting that F. racemosa balances seed and wasp production at the level of the tree. Because figs are probably selected to allocate equally to male and female function, a 1:1 seed:wasp ratio suggests that fig trees are in control of the mutualism.     

Factors Influencing Realized Sex Ratios in Fig Wasps: Double Oviposition and Larval Mortalities

Pollinator fig wasps (Agaonidae) are a model system for studies of sex ratio evolution. They lay their eggs in galled ovules within figs. Only one adult emerges from each gall, suggesting that only one egg is always laid per ovule, but if double oviposition occurs then the assumption that adult (realised) sex ratios of fig wasps are representative of primary sex ratios may be violated. Many galls also fail to produce any wasps. If they initially contained eggs then differential mortality rates may also modify realized sex ratios. We investigated whether Kradibia (= Liporrhopalum) tentacularis foundresses in Ficus montana figs avoid laying in ovules that already contain eggs. Comparisons of oviposition frequencies and wasp emergence frequencies showed that most galls that failed to produce wasps will have had eggs laid in them, but few occupied ovules contained two eggs. Realised sex ratios therefore do not necessarily reflect primary sex ratios in this species, but double oviposition is not responsible.     

Longevity, early emergence and body size in a pollinating fig wasp--implications for stability in a fig-pollinator mutualism

1. Fig trees (Ficus) are pollinated only by agaonid wasps, whose larvae also gall fig ovules. Each ovule develops into either a seed (when pollinated) or a wasp (when an egg is also laid inside) but not both. 2. Ovipositing wasps (foundresses) favour ovules near the centre of the enclosed inflorescence (syconium or 'fig'), leaving ovules near the outer wall to develop into seeds. This spatial stratification of wasps and seeds ensures reproduction in both partners, and thereby enables mutualism persistence. However, the mechanism(s) responsible remain(s) unknown. 3. Theory shows that foundresses will search for increasingly rare inner ovules and ignore outer ovules, as long as ovipositing in outer ovules is sufficiently slow and/or if inner ovules confer greater fitness to wasps. The fig-pollinator mutualism can therefore be stabilized by strong time constraints on foundresses and by offspring fitness gradients over variation in ovule position. 4. Female fig wasps cannot leave their galls without male assistance. We found that females in outer ovules were unlikely to be released. Inner ovules thus have added value to foundresses, because their female offspring are more likely to mate and disperse. 5. For those offspring that did emerge, gall position (inner/outer) and body size did not influence the order in which female pollinators exited syconia, nor did early emerging wasps enjoy increased life spans. 6. We also found that the life spans of female wasps nearly doubled when given access to moisture. We suggest that conflict resolution in the fig-pollinator mutualism may thus be influenced by tropical seasonality, because wasps may be less able to over-exploit ovules in dry periods due to time constraints.     

A role for parasites in stabilising the fig-pollinator mutualism

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their “fruits” (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.     

The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.     

Moving your sons to safety: galls containing male fig wasps expand into the centre of figs, away from enemies

Figs are the inflorescences of fig trees (Ficus spp., Moraceae). They are shaped like a hollow ball, lined on their inner surface by numerous tiny female flowers. Pollination is carried out by host-specific fig wasps (Agaonidae). Female pollinators enter the figs through a narrow entrance gate and once inside can walk around on a platform generated by the stigmas of the flowers. They lay their eggs into the ovules, via the stigmas and styles, and also gall the flowers, causing the ovules to expand and their pedicels to elongate. A single pollinator larva develops in each galled ovule. Numerous species of non-pollinating fig wasps (NPFW, belonging to other families of Chalcidoidea) also make use of galled ovules in the figs. Some initiate galls, others make use of pollinator-generated galls, killing pollinator larvae. Most NPFW oviposit from the outside of figs, making peripherally-located pollinator larvae more prone to attack. Style length variation is high among monoecious Ficus spp. and pollinators mainly oviposit into more centrally-located ovules, with shorter styles. Style length variation is lower in male (wasp-producing) figs of dioecious Ficus spp., making ovules equally vulnerable to attack by NPFW at the time that pollinators oviposit. We recorded the spatial distributions of galled ovules in mature male figs of the dioecious Ficus hirta in Southern China. The galls contained pollinators and three NPFW that kill them. Pollinators were concentrated in galls located towards the centre of the figs, NPFW towards the periphery. Due to greater pedicel elongation by male galls, male pollinators became located in more central galls than their females, and so were less likely to be attacked. This helps ensure that sufficient males survive, despite strongly female-biased sex ratios, and may be a consequence of the pollinator females laying mostly male eggs at the start of oviposition sequences.     

Measuring the discrepancy between fecundity and lifetime reproductive success in a pollinating fig wasp

Lifetime reproductive success in female insects is often egg‐ or time‐limited. For instance in pro‐ovigenic species, when oviposition sites are abundant, females may quickly become devoid of eggs. Conversely, in the absence of suitable oviposition sites, females may die before laying all of their eggs. In pollinating fig wasps (Hymenoptera: Agaonidae), each species has an obligate mutualism with its host fig tree species [Ficus spp. (Moraceae)]. These pro‐ovigenic wasps oviposit in individual ovaries within the inflorescences of monoecious Ficus (syconia, or ‘figs’), which contain many flowers. Each female flower can thus become a seed or be converted into a wasp gall. The mystery is that the wasps never oviposit in all fig ovaries, even when a fig contains enough wasp females with enough eggs to do so. The failure of all wasps to translate all of their eggs into offspring clearly contributes to mutualism persistence, but the underlying causal mechanisms are unclear. We found in an undescribed Brazilian Pegoscapus wasp population that the lifetime reproductive success of lone foundresses was relatively unaffected by constraints on oviposition. The number of offspring produced by lone foundresses experimentally introduced into receptive figs was generally lower than the numbers of eggs carried, despite the fact that the wasps were able to lay all or most of their eggs. Because we excluded any effects of intraspecific competitors and parasitic non‐pollinating wasps, our data suggest that some pollinators produce few offspring because some of their eggs or larvae are unviable or are victims of plant defences.     

钝叶榕(Ficus curtipes)非传粉小蜂交配行为

榕树及其传粉榕小蜂繁殖上相互依存,被认为是生物界中协同进化时间最悠久,相互关系最密切的一对生物;在大多数榕树种类的隐头花序内,除了传粉榕小蜂外,还共存着多种非传粉小蜂,它们的繁殖行为直接影响着榕树和传粉榕小蜂的繁殖和互惠稳定。钝叶榕(Ficus curtipes Corner),是一种雌雄同株的绞杀性榕树。研究在西双版纳热带植物园里共收集钝叶榕100个隐头果内的榕小蜂,获得9493号标本;其中,包括1种传粉小蜂和5种非传粉小蜂,钝叶榕传粉小蜂Eupristina sp.占总数的4466%,杨氏榕树金小蜂Diaziella yangi 占46.13%,而其它4种非传粉小蜂（Lipothymus sp., Sycobia sp., Philotrypesis sp.和Sycoscopter sp.）仅占9.20%。前3种榕小蜂雌蜂进到果腔产卵,其余3种在果外产卵。观测23个钝叶榕榕果出蜂情况发现,6种榕小蜂在钝叶榕隐头花序内遵循严格的羽化出蜂顺序,首先是Sycobia sp.,次之是Lipothymus sp.,再次之是杨氏榕树金小蜂,最后是钝叶榕传粉小蜂、Philotrypesis sp.和Sycoscopter sp.。5种非传粉小蜂的交配场所与雄蜂翅型无关,雄蜂有翅型的杨氏榕树金小蜂大部分交配在果内完成,而且它们的雄蜂为争夺交配机会存在激烈的打斗行为;雄蜂无翅型的Lipothymus sp.有部分雄蜂爬出隐头果,在果壁和附近的叶片背面交配;雄蜂有翅型的Sycobia sp.,其所有交配都发生在果外;Philotrypesis sp.和Sycoscopter sp. 雄蜂均无翅,它们的交配全发生在果内。局域配偶竞争使榕小蜂性比偏雌,杨氏榕树金小蜂雄蜂虽然有翅,但大部分交配发生在榕果内,这将影响其最佳的性比率。因此,依赖雄蜂翅型并不能很好地预测榕小蜂的交配场所和性比率。     

高榕雌花期传粉榕小蜂和欺骗性小蜂的繁殖特点

榕树及其专一性传粉榕小蜂组成了动植物界最为经典的协同进化关系,传粉榕小蜂演化出欺骗性是非常罕见的。在雌雄同株的高榕隐头果内,共存着一种传粉榕小蜂Eupristina altissima和一种欺骗性的小蜂Eupristina sp.,两种小蜂在雌花期进入隐头果内繁殖,但有不同的繁殖特点。对比研究了两种小蜂从成虫羽化到产卵和传粉这个阶段的雌蜂个体大小、孕卵量及繁殖差异,结果表明:羽化期两种雌蜂的平均个体小,经飞行小个体的雌蜂易死亡,大个体雌蜂到达接受树,但通过苞片通道,一些个体较大的传粉榕小蜂被夹死导致进入果腔的雌蜂相对小,而欺骗性小蜂易通过苞片以至进入果腔的雌蜂个体较大。两种未产卵雌蜂均表现为个体大者孕卵量较多,但两种雌蜂的平均孕卵量没有差异。即使有充足雌花资源产卵,两种雌蜂均未产完所有卵,产卵后两种雌蜂卵巢中的卵量均显著减少,遗留下的卵量两种小蜂间没有差异。传粉榕小蜂只有部分个体传完所携带花粉,并表现为传粉越成功的雌蜂,产卵越多。存在种内竞争时,两种小蜂的产卵量均减少,传粉榕小蜂的传粉效率也降低。在种间竞争背景下,欺骗性小蜂产卵更成功,传粉榕小蜂的产卵和传粉量均受到极大抑制。研究结果说明雌花期隐头果内传粉榕小蜂只适量利用雌花资源产卵繁殖后代,更有效地传粉繁殖榕树种子,这可能是维持榕-蜂互惠系统稳定共存的重要机制之一;欺骗者稳定存在需降低与传粉者的直接竞争,而欺骗者和传粉者分散在不同果内,甚至是不同的树上繁殖是理想的繁殖策略。     

The dominant exploiters of the fig/pollinator mutualism vary across continents,but their costs fall consistently on the male reproductive function of figs

1. Fig trees (Moraceae: Ficus) are keystone species, whose ecosystem function relies on an obligate mutualism with wasps (Chalcidoidea: Agaonidae) that enter fig syconia to pollinate. Each female flower produces one seed (fig female reproductive function), unless it also receives a wasp egg, in which case it supports a wasp. Fig male reproductive function requires both male flowers and pollinator offspring, which are the only vectors of fig pollen. 2. The mutualism is exploited by other wasps that lay eggs but provide no pollination service. Most of these non‐pollinating fig wasps (NPFWs) do not enter syconia, but lay eggs through the wall with long ovipositors. Some are gall‐makers, while others are parasitoids or lethal inquilines of other wasps. 3. Ficus is pan‐tropical and contains >750 fig species. However, NPFW communities vary across fig lineages and continents and their effects on the mutualism may also vary. This provides a series of natural experiments to investigate how the costs to a keystone mutualism vary geographically. 4. We made the first detailed study of the costs of NPFWs in a fig (Ficus obliqua G. Forst) from the endemic Australasian section Malvanthera. In contrast to the communities associated with section Americana in the New World, wasps from the subfamily Sycoryctinae (Chalcidoidea: Pteromalidae) dominated this community. 5. These sycoryctine wasps have a negative impact on pollinator offspring numbers, but not on seed production. Consequently, while the NPFW fauna varies greatly at high taxonomic levels across continents, we show that the consistent main effect of locally dominant exploiters of the mutualism is to reduce fig male reproductive function.     

Parasites and mutualism function: measuring enemy‐free space in a fig–pollinator symbiosis

Mutualisms involve cooperation between species and underpin several ecosystem functions. However, there is also conflict between mutualists, because their interests are not perfectly aligned. In addition, most mutualisms are exploited by parasites. Here, we study the interplay between cooperation, conflict and parasitism in the mutualism between fig trees and their pollinator wasps. Conflict occurs because each fig ovary can nurture either one seed or one pollinator offspring and, while fig trees benefit directly from seeds and pollinator offspring (pollen vectors), pollinators only benefit directly from pollinator offspring. The mechanism(s) of conflict resolution is debated, but must explain the widespread observation that pollinators develop in inner, and seeds in outer, layers of fig flowers. We recently suggested a role for non‐pollinating figs wasps (NPFWs) that are natural enemies or competitors of the pollinators and lay their eggs through the fig wall. Most NPFW offspring develop in outer and middle layer flowers, suggesting that inner flowers provide enemy‐free space for pollinator offspring. Here, we test the hypothesis that NPFWs cannot reach inner flowers, by measuring wasp and fig morphology at the species‐specific times of NPFW attack in the field. We found that three species of Sycoscapter and Philotrypesis wasps that parasitise pollinators could reach 34–73%, 75–92% and 82–97% of fig ovaries, respectively. Meanwhile, Eukobelea and Pseudidarnes gall‐formers, despite having shorter ovipositors, can access almost all fig flowers (93–99% and 100%), because they attack smaller (younger) fig fruits. Our mechanistic results from ovipositing wasps support spatial patterns of wasp offspring segregation within figs to suggest that inner ovules provide enemy‐free‐space for pollinators. This may contribute to mutualism stability by helping select for pollinators to avoid laying eggs where they are likely to be parasitised. These outer flowers then remain free to develop as seeds, promoting mutualism persistence.     

榕树-传粉者共生体系的协同进化与系统学研究进展及展望

 榕树-传粉者共生体系是目前植物与昆虫协同进化研究中的典型模式之一。国内外已经开展了大量的相关研究,从不同方面探讨了其特殊的一一对应的共生关系。榕树-传粉者的专一性互惠共生关系中蕴含了与系统发育有关的多因子协同进化的机理,因此,进行系统发育研究将有助于更好地揭示榕树-传粉者的协同进化历史和理解二者的专一性互惠共生关系。本文简单地介绍了目前榕树及其传粉者共生体系的研究状况之后,论述了榕树-传粉者协同进化的系统发育分子生物学研究成果。同时针对国际上在榕属植物的传统的系统与分类研究中存在的一些分歧及榕树传粉者亚科分类不匹配等问题,回顾了榕属的分类研究进展及其与传粉者的关系。最后,结合我国榕树与传粉者共生体系的研究状况对我国榕属的重新分类和系统发育研究作了展望。     

Quantitative tests of interaction between pollinating and non-pollinating fig wasps on dioecious Ficus hispida

Abstract.  1. The interaction between Ficus species and their pollinating wasps (Agaonidae) represents a striking example of a mutualism. Figs also shelter numerous non-pollinating chalcids that exploit the fig–pollinator mutualism.
2. Previous studies showed a weak negative correlation between numbers of pollinating and non-pollinating adults emerging from the same fruit. Little is known about the patterns and intensities of interactions between fig wasps. In the Xishuangbanna tropical rainforests of China, the dioecious Ficus hispida L. is pollinated by Ceratosolen solmsi marchali Mayr and is also exploited by the non-pollinators Philotrypesis pilosa Mayr, Philotrypesis sp., and Apocrypta bakeri Joseph. Here, the interaction of pollinator and non-pollinators on F. hispida is studied quantitatively.
3. The exact time of oviposition was determined for each species of fig wasp. Based on observational and experimental work it is suggested that (i) the relationship between pollinator and non-pollinators is a positive one, and that the genus Philotrypesis appears to have no significant impact on the pollinator population, whereas Apocrypta has a significant effect on both Philotrypesis and Ceratosolen ; (ii) gall numbers do not always increase with increasing number of foundresses, but developmental mortality of larvae correlates positively with the number of foundresses; and (iii) there is a positive correlation between non-pollinator numbers and their rates of parasitism, but the three species of non-pollinators differed in their rates of parasitism and show different effects on pollinator production.
4. The rates of parasitism when combined with the coexistent percentage and developmental mortality, underpin the way non-pollinating fig wasps successfully exploit and coexist stably in a fig–pollinator mutualism.     

Interference Competition and High Temperatures Reduce the Virulence of Fig Wasps and Stabilize a Fig-Wasp Mutualism

Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia (‘figs’) that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can ‘set the rules of the game’ to ensure mutualistic behavior in its symbionts.     

聚果榕传粉榕小蜂传粉与产卵之间的权衡

【目的】榕树(Ficus)依赖专性榕小蜂(Agaonidae)传粉,同时为传粉榕小蜂提供繁衍后代的场所,两者形成动植物间经典的协同进化关系。在雌花期果内,榕小蜂需在有限的存活时间内完成传粉和产卵,而传粉榕小蜂如何在传粉与产卵之间进行权衡仍然是悬而未解的问题。本研究旨在明确传粉榕小蜂——一种栉颚榕小蜂Ceratosolen sp.在雌雄同株的聚果榕Ficus racemosa雌花期果内的行为活动及繁殖模式。【方法】借助测微尺测量聚果榕榕果雌花花柱长度与传粉榕小蜂(Ceratosolen sp.)产卵器长度,通过显微视频记录传粉榕小蜂在雌花期果内搜索、传粉及产卵行为;结合单果控制性引蜂试验,测定不同阶段榕小蜂个体大小、孕卵量、携粉量,以及雄花期最终繁殖的榕小蜂后代和榕果种子数量。【结果】聚果榕雌花花柱长度存在树间变异,榕小蜂产卵器长度比绝大多数的雌花花柱长,说明该小蜂可以产卵于大部分的雌花子房里。通常个体大的榕小蜂孕卵量更多,但个体大小与携粉量之间相关性不显著。观察发现,榕小蜂进入雌花期榕果内,前6 h集中产卵,可产下孕卵量的95%,平均搜索用时27 s,产卵用时46 s,此期间传粉行为少见,花粉筐中携带花粉量亦无明显变化;榕小蜂进果后6-24 h,主要执行传粉,其行为主动,连贯高效,单次传粉用时平均为2 s,最终可传完携粉量的80%。控制引蜂试验也证实榕小蜂进入榕果内前6 h主要执行产卵繁殖后代,之后6-24 h主要执行传粉以繁殖榕树种子。【结论】在雌雄同株的聚果榕雌花期榕果内,榕小蜂先产卵、后传粉。本研究首次展示了传粉榕小蜂在聚果榕雌花期榕果内的产卵和传粉行为,并获得与行为相匹配的产卵量和传粉繁殖量,反映了具主动传粉行为的榕小蜂在传粉和产卵之间存在时间和数量上的权衡。     

非传粉小蜂的食性及其对榕树-传粉小蜂系统稳定性的影响

榕树与其传粉小蜂形成了高度专一的互惠共生系统。非传粉小蜂则是该系统的资源掠夺者,但它与该系统共存的机制仍不清楚。于2003年12月-2004年4月在西双版纳以聚果榕（Ficus racemosa L．）为材料,研究了寄生在聚果榕榕果内的5种非传粉小蜂的食性及相互关系,以探讨非传粉小蜂与榕树-传粉小蜂系统共存的机制。结果表明：寄生在聚果榕榕果内的5种非传粉小蜂中,仅Platyneura testacea Motschulsky和Platyneura,mayri Rasplus能刺激子房发育成瘿花,是造瘿者;Apocrypta sp．,Apocrypta westwoodi Grandi和Platyneura agraensis Joseph不能刺激子房发育成瘿花,是拟寄生者。传粉小蜂的拟寄生者和造瘿者对传粉小蜂有负的影响。但在蚂蚁和造瘿者的拟寄生蜂作用下,这种负面影响并不显著,而且它们对榕树繁殖没有显著影响。对小蜂自然种群的分析表明,传粉小蜂处于优势地位。说明在自然情况下传粉小蜂的拟寄生者和造瘿者的种群维持在一个较低水平,对榕树一传粉小蜂系统稳定性影响较小,故能与之长期共存。     

Different Stimuli Reduce Attraction to Pollinators in Male and Female Figs in the Dioecious Fig Ficus hispida

Fig trees ( Ficus ) and their obligate pollinating wasps (Hymenoptera, Chalcidoidea, Agaonidae) are a classic example of a coevolved mutualism. Pollinating wasps are attracted to figs only when figs are receptive. It has been shown that figs will lose their attraction to pollinators sooner in monoecious and male dioecious figs when multiple pollinators have entered the enclosed inflorescence. However, little is known about the nature of the stimulus inducing the loss of attraction. By conducting experiments on the functionally dioecious fig, Ficus hispida , we show that (1) different stimuli induce the loss of attraction in each sex, pollination in female figs, and oviposition in male figs; and (2) foundress number affects the loss of attraction in both sexes only when the prerequisites ( i.e ., pollination in female figs and oviposition in male figs) have been satisfied. In general, the more foundresses that enter, the earlier the fig will lose its receptivity. We argue that the stimuli in male and female figs are adaptations to the fulfillment of its respective reproduction.     

非传粉小蜂对榕-蜂共生系统的影响

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。     

Foundress Fig Wasps are More Likely to Re-emerge From Older Figs

The mutualistic interaction between Ficus spp. and their pollinating fig wasps (Agaonidae) centres on the plants’ unique inflorescences—their figs. Each Ficus species is pollinated by foundresses of host-specific fig wasps which enter figs to lay eggs in the female flowers. Most foundresses are trapped in the first figs they enter, but in some species wingless foundresses can re-emerge and subsequently enter and oviposit into further figs. We investigated whether number of potential oviposition sites, age of the fig and age of the wasp influence the likelihood of re-emergence of lone foundresses of the Asian fig wasp Kradibia (=Liporrhopalum) tentacularis from previously un-entered figs of Ficus montana. Likelihood of re-emergence was not influenced by wasp age or flower numbers (resource abundance), but was more frequent from older figs that had waited longer to be pollinated. Laying eggs in several figs offers clear advantages, but foundresses often failed to re-emerge despite being unable to lay all their eggs. Resource quality not quantity appears to be the main influence on the fig wasp’s oviposition decisions. The physical difficulty that the wasps experience when trying to re-emerge may prevent it, even when re-emergence would be advantageous for both the insect and its host plant, but older fig wasps were not detectably ‘weaker’ than younger individuals.     

粗叶榕—爪哇榕小蜂共生体系的研究

粗叶榕是榕属灌木或小乔木 ,雌雄异株。一年到头皆有不同发育阶段的花序 ,序内开花同步 ,株内开花异步。雌花序有长柱雌花平均为 641 .2枚 ,雄花序中有短柱雌花 (瘿花 )平均为 488.2枚 ,自然状态下结实率和成虫率分别为 5 1 .3 7%和 3 6.1 1 %。榕小蜂科的爪哇榕小蜂是粗叶榕的传粉者 ,是共生体系的真正的互惠共生伙伴。二者在形态结构、生理功能上高度互适 ,粗叶榕必须依靠爪哇榕小蜂的传粉才能获得有性生殖 ;而爪哇榕小蜂又必须依赖粗叶榕的短柱头雌花作为繁殖后代的场所 ,才能获得种群的繁衍。