Between‐species facilitation by male fig wasps in shared figs

1. Facilitation is recorded from diverse plant–insect interactions, including pollination and herbivory. 2. The significance of facilitation resulting from the behavior of males of multiple fig wasp species inside figs was investigated. Female fig wasps emerge from natal figs via exit holes dug by males, especially male pollinators. When no males are present, the females struggle to escape and may die. 3. Ficus microcarpa L. is a widely‐established invasive fig tree from Southeast Asia. Its pollinator is absent in South Africa, so the tree cannot reproduce, but two Asian non‐pollinating fig wasps (NPFW) Walkerella microcarpae and Odontofroggatia galili occupy its figs. Abundance patterns of the two NPFW and the proportion of male‐free figs in South Africa, Spain (where the pollinator is introduced), and in China, where the native fig wasp community is diverse, were compared to determine the consequences of reduced species richness for insect survival. 4. Female fig wasps in male‐free figs were found to be trapped, and small clutch sizes contributed to the absence of males in both species. The presence of pollinators in Spain allowed most NPFW to develop in figs containing males. Far more male‐free figs were present in South Africa, elevating mortality rates among female NPFW. Facilitation of female release by males of other NPFW species nonetheless benefitted the rarer species. 5. Selection pressures in South Africa currently favour greater aggregation of NPFW offspring and/or less female biased sex ratios.     

Only pollinator fig wasps have males that collaborate to release their females from figs of an Asian fig tree

Male insects rarely collaborate with each other, but pollinator fig wasps (Hymenoptera: Agaonidae) are said to be an exception. Immature fig wasps feed on galled ovules located inside figs, the inflorescences of Ficus species (Moraceae). After mating, adult pollinator males chew communal exit-holes that allow mated females (which are often also their siblings) to escape. Figs also support non-pollinating fig wasps (NPFWs), some of which produce exit-holes independently. We determined whether collaboration between pollinator males (Kradibia tentacularis from Ficus montana) was necessary for the release of their females, and used the relationship between male numbers and likelihood of success to measure the extent of cooperation during exit-hole production. These attributes were then compared with those of an NPFW (Sycoscapter sp.) from the same host plant. Pollinators were more abundant than NPFW, but their more female-biased sex ratio meant male pollinator densities were only slightly higher. Individual males of both species could produce an exit-hole. Single males of the NPFW were just as successful as single male pollinators, but only male pollinators cooperated effectively, becoming more successful as their numbers increased. The lack of cooperation among NPFW may be linked to their earlier period of intense inter-male aggression.     

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.     

Finding hidden females in a crowd: Mate recognition in fig wasps

Multi-species mating aggregations are crowded environments within which mate recognition must occur. Mating aggregations of fig wasps can consist of thousands of individuals of many species that attain sexual maturity simultaneously and mate in the same microenvironment, i.e, in syntopy, within the close confines of an enclosed globular inflorescence called a syconium – a system that has many signalling constraints such as darkness and crowding. All wasps develop within individual galled flowers. Since mating mostly occurs when females are still confined within their galls, male wasps have the additional burden of detecting conspecific females that are “hidden” behind barriers consisting of gall walls. In Ficus racemosa, we investigated signals used by pollinating fig wasp males to differentiate conspecific females from females of other syntopic fig wasp species. Male Ceratosolen fusciceps could detect conspecific females using cues from galls containing females, empty galls, as well as cues from gall volatiles and gall surface hydrocarbons.In many figs, syconia are pollinated by single foundress wasps, leading to high levels of wasp inbreeding due to sibmating. In F. racemosa, as most syconia contain many foundresses, we expected male pollinators to prefer non-sib females to female siblings to reduce inbreeding. We used galls containing females from non-natal figs as a proxy for non-sibs and those from natal figs as a proxy for sibling females. We found that males preferred galls of female pollinators from natal figs. However, males were undecided when given a choice between galls containing non-pollinator females from natal syconia and pollinator females from non-natal syconia, suggesting olfactory imprinting by the natal syconial environment.     

歪叶榕非传粉小蜂的繁殖策略及其对榕-蜂共生系统的影响

2004年8月至2005年8月在西双版纳热带植物园内,通过广泛收集歪叶榕榕小蜂标本、非传粉小蜂产卵行为学观察和阻止传粉者入果等实验方法,研究了我国西双版纳热带雨林下的一种榕树——歪叶榕Ficus cyrtophylla的榕小蜂群落组成结构、非传粉小蜂的繁殖策略以及它们对榕-蜂共生系统的影响。结果表明,歪叶榕中除了具有唯一传粉榕小蜂Blastophag sp.以外,还具有3种非传粉小蜂Platyneura sp.、Philotrypesis sp.和Sycoscapter sp.。在歪叶榕榕小蜂群落中,传粉榕小蜂占整个群落总数的92.21%,是群落的最主要组成者;主要的非传粉小蜂是Sycoscaptersp.,占5.78%; 其次是Philotrypesissp.,占1.84%,而Platyneurasp.仅占群落总数的0.17%。歪叶榕中的非传粉小蜂通过各自产卵时间和食性分化的策略来利用榕果中的资源繁殖后代。非传粉小蜂寄生使传粉榕小蜂的总数和其雌蜂数量都显著地降低,但是对传粉小蜂雄蜂数量没有显著影响,从而导致传粉榕小蜂的雄性性比显著地增加。这说明非传粉小蜂在选择寄居宿主时具有明显的倾向性,而且更多地将卵产于含有雌性传粉小蜂的瘿花之中。因此,非传粉小蜂通过减少雌性传粉小蜂的数量而降低了榕树的雄性适合度,从而在一定程度上对榕 蜂共生系统的稳定存在和发展产生了负面影响。     

鸡嗉果榕榕小蜂产卵时序与种群数量分析

榕树与传粉榕小蜂的互惠共生体系被多种非传粉榕小蜂利用。在同一个榕果中,具有较高种群密度的传粉榕小蜂和多种非传粉榕小蜂生存在一起并相互作用。通过野外观察和采样分析的方法,对鸡嗉果榕内5种榕小蜂（传粉榕小蜂Ceratosolen gravelyi;非传粉榕小蜂Apocrypta sp., Philotrypesis dunia, Platyneura cunia和Sycoscaptertr ifemmensis）的产卵行为进行了研究。结果证明,鸡嗉果榕内生活的各种榕小蜂通过比较严格的产卵时序在榕果内产卵以占领不同的生态位,这反映了这些榕小蜂各自的生物学特性。自然种群数量分析表明,单个非传粉榕小蜂物种的种群数量几乎不与传粉榕小蜂种群数量呈负相关,而所有非传粉榕小蜂物种的种群个体总量与传粉榕小蜂的种群个体数呈正相关,这可能是多个物种共存于单个榕果内的进化适应。     

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.     

Secondary galling: a novel feeding strategy among ‘non‐pollinating’ fig wasps from Ficus curtipes

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How to be a fig wasp down under: The diversity and structure of an Australian fig wasp community

Endophytic insects and their parasitoids provide valuable models for community ecology. The wasp communities in inflorescences of fig trees have great potential for comparative studies, but we must first describe individual communities. Here, we add to the few detailed studies of such communities by describing the one associated with Ficus rubiginosa in Australia. First, we describe community composition, using two different sampling procedures. Overall, we identified 14 species of non-pollinating fig wasp (NPFW) that fall into two size classes. Small wasps, including pollinators, gallers and their parasitoids, were more abundant than large wasps (both galler and parasitoid species). We show that in figs where wasps emerge naturally, the presence of large wasps may partly explain the low emergence of small wasps. During fig development, large gallers oviposit first, before and around the time of pollination, while parasitoids lay eggs after pollination. We further show that parasitoids in the subfamily Sycoryctinae, which comprise the majority of all individual NPFWs, segregate temporally by laying eggs at different stages of fig development. We discuss our results in terms of species co-existence and community structure and compare our findings to those from fig wasp communities on other continents.     

Spatial distribution patterns of three fig wasps on Ficus semicordata: How non-pollinators affect pollinator’s sex ratio

Sex ratio theory is one of the most productive fields in research on evolutionary biology. Pollinating fig wasps, due to their particular natural life history, are considered to be a valuable model for the study of sex ratio evolution. A great deal of research concerning the factors that affect pollinator fig wasp (Agaonidae) progeny sex ratio has been done, and at present three main factors (haplodiploidy, local mate competition and inbreeding) are found to be important at the population level. However, there still exists variation between empirical data and model predictions. Another factor to which little thought has been given before is the effect of non-pollinating fig wasps (NPFWs) which parasitize in the larvae gall of pollinator thus kill pollinators and exploit the fig/fig pollinator mutualistic systems. In this study, we focus on why and how non-pollinating fig wasps distort pollinator fig wasp’s original sex ratio. Through controlling the number of ovipositing foundresses inside a fig, combined with the observation of ovipositing behavior and sequence, we studied three species of wasp in the figs of a dioecious fig Ficus semicordata including the pollinator Ceratosolen gravely and NPFWs Platyneura cunia, Sycoscapter trifemmensis in tropical area of Xishuangbanna from September to December 2009. First, we observed the timing of oviposition of all fig wasps utilizing F. semicordata and found differences when compared to previous studies. Such as P. cunia is the fourth rather then the secondary fig wasps to oviposit on the syconia approximately 10 days after the pollinator. S. trifemmensis oviposits much earlier than previously thought, 14–32 days after the pollinators. We examined the spatial location of male and female progeny of the pollinator. We found foundresses of pollinator prefer to use innermost ovules first. Only at high offspring numbers were the outer ovules used. More male pollinator offspring were developed near the fig cavity, while female pollinator offspring were more evenly distributed among ovule layers. As pollinator offspring numbers increased, this phenomenon became more pronounced. This pattern of segregation of male larvae gall in inner ovules and female larvae gall in outer ovules suggests that female offspring might be more vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Experiments later demonstrated that NPFWs are restricted by their ovipositor length and they prefer to or can only lay their eggs into ovules near the fig wall. Then we examined the spatial location of NPFWs and compared this with the spatial location of male/female progeny of pollinator. NPFWs had a high probability of parasitizing female pollinator larvae. Thus, NPFWs have a substantial effect on the sex ratio of the pollinator, as parasitism risk decreases towards the center of the syconium, where inner ovules provide enemy-free space for most of male pollinator offspring. Partial correlation analyse shows that sex ratio of pollinator progeny has a positive relationship with the number of NPFWs. We suggest that the resulting gradient in offspring viability between male and female contributes to selection on pollinators’ for a less femalebiased sex ratio. When the affect of NPFWs was excluded, the pollinator sex ratio was not in good agreement with local mate competition theory, although it was still female-biased. In addition, the average number of offspring per foundress decreased with increasing foundress number, but pollinator sex ratio was positively related to brood size. Thus, pollinator females do not appear to adjust their sex ratio to foundress density directly, but use brood size and foundress density simultaneously as cues to assess potential LMC.     

Some pollinators are more equal than others: Factors influencing pollen loads and seed set capacity of two actively and passively pollinating fig wasps

The nursery pollination system of fig trees (Ficus) results in the plants providing resources for pollinator fig wasp larvae as part of their male reproductive investment, with selection determining relative investment into pollinating wasps and the pollen they carry. The small size of Ficus pollen suggests that the quantities of pollen transported by individual wasps often limits male reproductive success. We assessed variation in fig wasp pollen loads and its influence on seed production in actively pollinated (Ficus montana) and passively pollinated (Ficus carica) dioecious fig trees.The ratios of number of male flowers on number of female flowers in a glasshouse-maintained F. montana population were highly variable. When fig wasps were introduced into receptive female figs, the resulting seed numbers were strongly linked to the numbers of pollinators that had been seeking access to pollen, relative to the number of anthers in their natal figs. In F. carica estimates of the amounts of pollen produced per fig and the quantities of pollen carried by emerging fig wasps suggest that less than 10% of the pollen is transported. Pollinators of F. carica that emerged earlier from figs carried more pollen, and also generated more seeds when introduced into receptive female figs.We show here that all pollinators are not equally valuable and producing more pollinators is not necessarily a good option in terms of Ficus male fitness. Previous results on F. montana figs showed that only around half of the flowers where pollinators lay eggs produced adult offspring. The amount of pollen collected by young female fig wasps may be a major determinant of their reproductive success.     

Age at pollination modifies relative male and female reproductive success in a monoecious fig tree

Plants that depend on a single species of insect pollinator must often contend with infrequent and unpredictable visitation. Prolongation of floral receptivity comes at the cost of reduced male and/or female reproductive success among older flowers. Fig trees (Ficus spp.) have a highly specific pollination symbiosis and individual inflorescences (syconia) that remain receptive for days or weeks. Reproductive success in monoecious fig trees involves production of both seeds and fig wasp offspring. We assessed whether the reproductive output of individual syconia changes with the length of time they waited for pollination, and whether the relative female and male reproductive success also changes. A pollination experiment was conducted in an SE Asian monoecious fig tree Ficus curtipes, in which receptive syconia were covered with mesh bags to exclude wasps and pollinated by single pollinators of this fig tree at their different receptive ages. When the syconia matured their size and contents were recorded. Seed quality was also assessed. The results showed that pollinators entered syconia that had been waiting for up to 36?days. The frequencies of abortions among syconia pollinated at different ages were low throughout. The number of un-utilised flowers increased progressively in older syconia. Seed production was highest in syconia entered on the first day of receptivity, whereas pollinator production peaked in syconia pollinated on day 12, then declined in older syconia. Consequently, overall reproductive efficiency declined with syconium age and floral sex allocation became more male-biased in older syconia. Older syconia also produced lighter seeds. These results suggest that un-pollinated syconia of F. curtipes can remain receptive for several weeks. This makes pollination of each syconium more likely, but at the cost of reduced productivity and with more ovules allocated to male function. However, the prolongation of floral receptivity has significance for the co-adaptation between syconia and fig wasps and for the evolution of the fig tree-fig wasp symbiosis.     

影响对叶榕及其传粉者繁殖的生态学因素

在西双版纳,分别统计了对叶榕(Ficus hispida)雌花期雌雄果的进蜂量和花后期雌雄果繁殖的多个特征值,以此来探讨自然条件下,影响对叶榕及其传粉榕小蜂(Ceratosolen solmsi marchali)繁殖的因素。结果表明:单果内有效进蜂数量是影响种子生产和传粉榕小蜂繁殖的首要因素,而雌花期进果的传粉榕小蜂并不是都能全部进入果腔传粉或产卵,大部分蜂还未进到果腔就被夹死在顶生苞片层的通道里,能进入雌果内传粉的榕小蜂为(2.72±2.04)只·果^-1,约占总进蜂量的52%;而在雄果里,能进入果腔的蜂量只有(2.08±1.65)只·果^-1,占35%左右。由于雌果内的雌花显著比雄果内的雌花多,结合单果进蜂量雌多雄少的格局,最终单果生产的种子数量 (1 891.63 ± 471.53)比传粉榕小蜂的数量 (367.20 ± 208.02) 多5倍有余。在雌果里,供给传粉的雌花数量与所生产的种子数量之间呈显著的正相关,而没有接受到花粉或不能正常受精的雌花数量与种子数量呈显著的负相关。雄果不仅生产花粉,也是传粉榕小蜂繁殖的场所,在相关于传粉榕小蜂自身繁殖力的因子中,传粉榕小蜂产卵制造的瘿花数量对其种群数量有最大的影响;影响次之的是发育过程中死亡的个体数量,它可降低30%左右的传粉榕小蜂数量;影响排在第三位的是寄主的雌花数量。此外,3类非传粉者的存在,单果内平均可减少30多只传粉小蜂。     

Making the most of your pollinators: An epiphytic fig tree encourages its pollinators to roam between figs

Ficus species are characterized by their unusual enclosed inflorescences (figs) and their relationship with obligate pollinator fig wasps (Agaonidae). Fig trees have a variety of growth forms, but true epiphytes are rare, and one example is Ficus deltoidea of Southeast Asia. Presumably as an adaptation to epiphytism, inflorescence design in this species is exceptional, with very few flowers in female (seed‐producing) figs and unusually large seeds. Figs on male (pollinator offspring‐generating) trees have many more flowers. Many fig wasps pollinate one fig each, but because of the low number of flowers per fig, efficient utilization by F. deltoidea''s pollinators depends on pollinators entering several female figs. We hypothesized that it is in the interest of the plants to allow pollinators to re‐emerge from figs on both male and female trees and that selection favors pollinator roaming because it increases their own reproductive success. Our manipulations of Blastophaga sp. pollinators in a Malaysian oil palm plantation confirmed that individual pollinators do routinely enter several figs of both sexes. Entering additional figs generated more seeds per pollinator on female trees and more pollinator offspring on male trees. Offspring sex ratios in subsequently entered figs were often less female‐biased than in the first figs they entered, which reduced their immediate value to male trees because only female offspring carry their pollen. Small numbers of large seeds in female figs of epiphytic F. deltoidea may reflect constraints on overall female fig size, because pollinator exploitation depends on mutual mimicry between male and female figs.     

Interactions between pollinator and non‐pollinator fig wasps: correlations between their numbers can be misleading

Ficus and their species–specific pollinator fig wasps represent an obligate plant–insect mutualism, but figs also support a community of non‐pollinating fig wasps (NPFWs) that consist of phytophages and parasitoids or inquilines. We studied interactions between Kradibia tentacularis, the pollinator of a dioecious fig tree species Ficus montana, and an undescribed NPFW Sycoscapter sp. Members of Sycoscapter sp. oviposited 2–4 weeks after pollinator oviposition, when host larvae were present in the figs. No negative correlation was found between the numbers of the two wasp species emerging from figs in a semi‐natural population. However, in experiments where the numbers of pollinator foundresses entering a fig were controlled, Sycoscapter sp. significantly reduced the numbers of pollinator offspring. Consequently, it can be concluded that Sycoscapter sp. is a parasitoid of K. tentacularis (which may also feed on plant tissue). Sycoscapter females concentrate their oviposition in figs that contain more potential hosts, rendering invalid conclusions based on simple correlations of host and natural enemy numbers.     

笔管榕榕小蜂的群落结构与物种多样性

笔管榕为桑科榕属落叶乔木,雌雄同株,为福建地区的常见树种。笔管榕榕果内生活着多种榕小蜂,它们与笔管榕共同构成了榕树-榕小蜂共生体系。通过全年(2011年7月至2012年7月间)对福州地区不同样地的30株笔管榕进行的定时、定点、定株观察与采集,在15批次830个榕果中,共收集到50817头榕小蜂。笔管榕榕果内有7种小蜂,隶属于小蜂总科中的6个科(亚科)7个属,其中榕小蜂科的Platyscapa ishiiana为传粉小蜂,其余6种为非传粉小蜂,分别属于金小蜂科、广肩小蜂科、姬小蜂科及隐针榕小蜂亚科。非传粉小蜂中的Philotrypesis sp.、Acophila mikii、Otitesella ako、Sycophila sp.和Sycobiomorpha sp.小蜂几乎在全年的每个月都可采集到,属常见种。Aprostocetus sp.全年仅收集到2头,为偶见种。笔管榕榕果内的榕小蜂种类在不同月份、不同季节没有明显变化,但不同种类榕小蜂的数量变化明显。在笔管榕榕小蜂群落结构中,全年有9个月均是传粉小蜂占优势,但在1月、9月和11月的采集批次中,非传粉小蜂占优势。非传粉小蜂(Acophila mikii、Sycophila sp.、Philotrypesis sp.和Otitesella ako)常呈爆发性发生,每批次中往往是1-2种的非传粉小蜂数量较多,但不同批次,数量较多的非传粉小蜂种类往往不同,因此在小蜂群落结构中未见某种非传粉小蜂占明显优势。福州地区笔管榕榕果内小蜂群落的的多样性指数为0.72,均匀度指数为0.37,丰富度指数为0.55,优势集中性指数为0.68。分析了6种小蜂的性比,结果表明:传粉小蜂的性比极度偏雌,非传粉小蜂虽然也偏性,但均高于传粉小蜂,推测榕小蜂性比与雄蜂的翅型和交配场所有关。非传粉小蜂的数量和传粉小蜂总数、雌蜂数和雄蜂数均呈极显著负相关,和性比呈极显著正相关关系,说明非传粉小蜂对传粉小蜂的雌、雄蜂都有负面影响,且传粉小蜂雌蜂减少的幅度大于传粉小蜂雄蜂,从而导致其性比升高。非传粉小蜂中Acophila mikii、Sycobiomorpha sp.、Otitesella ako Ishii为造瘿类群,Philotrypesis sp.、Sycophila sp.属于寄居者或寄生者类群,非传粉小蜂中的寄生或寄居类群与造瘿类群相比,对传粉小蜂的负面影响更大。研究结果为榕-蜂协同进化研究,以及城市绿化和生物多样性保护提供科学依据。     

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.     

Pollinators entering female dioecious figs: why commit suicide?

In the dioecious fig/pollinator mutualism, the female wasps that pollinate figs on female trees die without reproducing, whereas wasps that pollinate figs on male trees produce offspring. Selection should strongly favour wasps that avoid female figs and enter only male figs. Consequently, fig trees would not be pollinated and fig seed production would ultimately cease, leading to extinction of both wasp and fig. We experimentally presented pollinators in the wild (southern India) with a choice between male and female figs of a dioecious fig species, Ficus hispida L. Our results show that wasps do not systematically discriminate between sexes of F. hispida. We propose four hypotheses to explain why wasp choice has not evolved, and how a mutualism is thus maintained in which all wasps that pollinate female figs have zero fitness.     

西双版纳聚果榕隐头果内小蜂群落结构及种间关系

聚果榕Ficus racemosa Linn.是雌雄同株榕树,它是西双版纳热带雨林生态系统中的一个常见种群。聚果榕必须依靠聚果榕小蜂Ceratosolen fusciceps Mayr传粉才能获得有性繁殖,而聚果榕小蜂又必须依靠聚果榕隐头果内短柱花繁衍后代,两者间形成了种间专一的互惠共生体系。同时,在其隐头果内还存在一个复杂的非传粉小蜂功能群,它们主要是榕树种子和传粉榕小蜂的寄生者。在云南省西双版纳自治州勐腊县勐仑镇选取了5个样地,对聚果榕单果内小蜂群落组成和种间相互关系进行研究。在不同时间段采集聚果榕单果242个,共收集小蜂366660头。聚果榕隐头果内有6种小蜂,隶属小蜂总科Chalcidoidae中的榕小蜂科Agaonidae、长尾小蜂科Caliimomidae、金小蜂科Pteromalidae,其中榕小蜂科中的C．fusciceps是聚果榕唯一的传粉者。金小蜂科中的Apocryta westwoodi Grandi和Apocryta sp.两个种是榕小蜂的寄生者,它们的寄生是传粉榕小蜂的种群数量减少因素之一。长尾小蜂科中Platyneura agraensis Joseph,Platyneura mayri Rasplus和Platyneura testacea Motschulsky3个种是寄生榕树种子或与榕小蜂争夺食物(瘿花)资源的小蜂类群,它们的出现与发生,致使聚果榕正在发育成种子的长柱小花形成瘿花,同时一部分种类把卵寄生在已被榕小蜂产卵的短柱小花子房中与榕小蜂争夺食物资源,致使榕小蜂食物资源的匮乏而死亡,对传粉小蜂种群有明显的影响。传粉小蜂从花托口钻入隐头果内,在隐头果内的长柱小花传粉和短柱小花子房中产卵,5种非传粉小蜂从隐头果外部把产卵器刺穿果肉把卵产在小花子房上。通过对5块样地隐头果内小蜂群落的综合分析发现,传粉榕小蜂为优势种群,而Apocryta sp.种的数量最少。在传粉及非传粉小蜂自然群体中各种类性比明显具有偏雌现象。小蜂群落表现异常的是聚果榕孤立株的样地,该样地传粉小蜂个体数量明显下降,非传粉小蜂个体数量则增加,各小蜂种群之间竞争激烈,出现C．fusciceps和P．mayri两个优势种。