The occurrence of fig wasps in the fruits of female gynodioecious fig trees

Fig trees are pollinated by wasp mutualists, whose larvae consume some of the plant's ovaries. Many fig species (350+) are gynodioecious, whereby pollinators generally develop in the figs of ‘male’ trees and seeds generally in the ‘females.’ Pollinators usually cannot reproduce in ‘female’ figs at all because their ovipositors cannot penetrate the long flower styles to gall the ovaries. Many non-pollinating fig wasp (NPFW) species also only reproduce in figs. These wasps can be either phytophagous gallers or parasites of other wasps. The lack of pollinators in female figs may thus constrain or benefit different NPFWs through host absence or relaxed competition. To determine the rates of wasp occurrence and abundance we surveyed 11 dioecious fig species on Hainan Island, China, and performed subsequent experiments with Ficus tinctoria subsp. gibbosa to identify the trophic relationships between NPFWs that enable development in female syconia. We found NPFWs naturally occurring in the females of Ficus auriculata, Ficus hainanensis and F. tinctoria subsp. gibbosa. Because pollinators occurred only in male syconia, when NPFWs also occurred in female syconia, overall there were more wasps in male than in female figs. Species occurrence concurred with experimental data, which showed that at least one phytophagous galler NPFW is essential to enable multiple wasp species to coexist within a female fig. Individuals of galler NPFW species present in both male and female figs of the same fig species were more abundant in females than in males, consistent with relaxed competition due to the absence of pollinator. However, these wasps replaced pollinators on a fewer than one-to-one basis, inferring that other unknown mechanisms prevent the widespread exploitation by wasps of female figs. Because some NPFW species may use the holes chewed by pollinator males to escape from their natal fig, we suggest that dispersal factors could be involved.     

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.     

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.     

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。     

Variation in inflorescence size in a dioecious fig tree and its consequences for the plant and its pollinator fig wasp

The host-specific relationship between fig trees (Ficus) and their pollinator wasps (Agaonidae) is a classic case of obligate mutualism. Pollinators reproduce within highly specialised inflorescences (figs) of fig trees that depend on the pollinator offspring for the dispersal of their pollen. About half of all fig trees are functionally dioecious, with separate male and female plants responsible for separate sexual functions. Pollen and the fig wasps that disperse it are produced within male figs, whereas female figs produce only seeds. Figs vary greatly in size between different species, with female flower numbers varying from tens to many thousands. Within species, the number of female flowers present in each fig is potentially a major determinant of the numbers of pollinator offspring and seeds produced. We recorded variation in female flower numbers within male and female figs of the dioecious Ficus montana growing under controlled conditions, and assessed the sources and consequences of inflorescence size variation for the reproductive success of the plants and their pollinator (Kradibia tentacularis). Female flower numbers varied greatly within and between plants, as did the reproductive success of the plants, and their pollinators. The numbers of pollinator offspring in male figs and seeds in female figs were positively correlated with female flower numbers, but the numbers of male flowers and a parasitoid of the pollinator were not. The significant variation in flower number among figs produced by different individuals growing under uniform conditions indicates that there is a genetic influence on inflorescence size and that this character may be subject to selection.     

Parasitism of a pollinator fig wasp: mortalities are higher in figs with more pollinators,but are not related to local densities of figs

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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.     

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.     

First record of an apparently rare fig wasp feeding strategy: obligate seed predation

1. Fig trees require host‐specific agaonid fig wasps for pollination, but their figs also support numerous non‐pollinating fig wasps (NPFW) that gall fig tissues or develop as parasitoids. 2. Ficus microcarpa L. is widely naturalised outside its native range and the most invasive fig tree species. Seed predators are widely used for the biological control of invasive plants, but no obligate seed predatory (as opposed to ovule or fig wall galling) NPFW have been recorded previously from any fig trees. 3. Philotrypesis NPFW are usually regarded as parasitoids or ‘inquilines’ (parasitoids that also eat plant material) of pollinator fig wasps, but the present study provides evidence that Philotrypesis taiwanensis, a NPFW associated with F. microcarpa, is an obligate seed predator: (i) adults emerge from seeds of typical appearance, with a surrounding elaiosome; (ii) it shows no preference for figs occupied by fig wasp species, other than the pollinator; (iii) it only develops in figs that contain pollinated ovules, avoiding figs occupied by an agaonid that fails to pollinate; (iv) larvae are distributed in layers where seeds are concentrated and (v) it has a negative impact on seed but not pollinator offspring numbers. 4. Philotrypesis is a large genus, and further species are likely to be seed predators.     

Shift to mutualism in parasitic lineages of the fig/fig wasp interaction

The interaction between Ficus and their pollinating wasps (Chalcidoidea, Agaonidae) represents a striking example of mutualism. Figs also host numerous non-pollinating wasps belonging to other chalcidoid families. We show that six species of Ficus that are passively pollinated by the agaonid genus Waterstoniella also host specific wasps belonging to the chalcidoid genera Diaziella (Sycoecinae) and Lipothymus (Otitesellinae). Both belong to lineages that are considered as parasites of the fig/fig wasp mutualism. We show that these wasps are efficient pollinators of their hosts. Pollen counts on wasps of a species of Diaziella hosted by Ficus paracamptophylla show that Diaziella sp. transports more pollen than the associated pollinator when emerging from its natal fig. Further, the number of pollinated flowers in receptive figs is best explained by the number of Diaziella plus the number of Waterstoniella that had entered it. Figs that were colonised by Diaziella always produced seeds: Diaziella does not overexploit its host. Similarly, figs of Ficus consociata that were colonised solely by a species of Lipothymus produced as many seeds as figs that were colonised only by the legitimate pollinator Waterstoniella malayana . Diaziella sp. and Lipothymus sp. seem to pollinate their host fig as efficiently as do the associated agaonid wasps. Previous studies, on actively pollinated Ficus species, have found that internally ovipositing non-agaonid wasps are parasites of such Ficus species. Hence, mode of pollination of the legitimate pollinator conditions the outcome of the interaction between internally ovipositing parasites and their host.     

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

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.     

Complementary fruiting phenologies facilitate sharing of one pollinator fig wasp by two fig trees

Aims Most pollinator fig wasps are host plant specific, with each species only breeding in the figs of one fig tree species, but increasing numbers of species are known to be pollinated by more than one fig wasp, and in rare instances host switching can result in Ficus species sharing pollinators. In this study, we examined factors facilitating observed host switching at Xishuangbanna in Southwestern (SW) China, where Ficus squamosa is at the northern edge of its range and lacks the fig wasps that pollinate it elsewhere, and its figs are colonized by a Ceratosolen pollinator that routinely breeds in figs of F. heterostyla .Methods We recorded the habitat preferences of F. squamosa and F. heterostyla at Xishuangbanna, and compared characteristics such as fig size, location and colour at receptive phase. Furthermore, the vegetative and reproductive phenologies in the populations of F. squamosa and F. heterostyla were recorded weekly at Xishuangbanna Tropical Botanical Garden for 1 year.Important findings Ficus squamosa is a shrub found near fast-flowing rivers, F. heterostyla is a small tree of disturbed forest edges. Although preferring different habitats, they can be found growing close together. Both species have figs located at or near ground level, but they differ in size when pollinated. Fig production in F. squamosa was concentrated in the colder months. F. heterostyla produced more figs in summer but had some throughout the year. The absence of its normal pollinators, in combination with similarly located figs and partially complementary fruiting patterns appear to have facilitated colonization of F. squamosa by the routine pollinator of F. heterostyla. The figs probably also share similar attractant volatiles. This host switching suggests one mechanism whereby fig trees can acquire new pollinators and emphasizes the likely significance of edges of ranges in the genesis of novel fig tree–fig wasp relationships.     

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.     

Disturbance effects on community structure of Ficus tinctoria fig wasps in Xishuangbanna, China: Implications for the fig/fig wasp mutualism

Abstract  Fig trees are important components of tropical forests, because their fruits are eaten by so many vertebrates, but they depend on pollinating fig wasps to produce mature fruits. Disturbance to habitat structure can have a major impact on insect diversity and composition, potentially reducing fruit yields. We investigated the impact of habitat disturbance on the fig wasp community associated with male figs of Ficus tinctoria in Xishuangbanna, China. The community comprised one pollinator species Liporrhopalum gibbosae and six non-pollinating wasp species: Sycoscapter sp.1, Philotrypesis ravii , Philotrypesis sp.1, Neosycophila omeomorpha , Sycophila sp.1, and Walkerella sp.1. More disturbed areas were characterized by higher temperatures, less shade, and more vehicle noise. The response of the fig wasp community was complex, with no simple relationship between intensity of disturbance and pollinator abundance. However, the sex ratios (proportion of male progeny) of pollinators increased significantly in more disturbed areas. We conclude that potential changes in fig wasp community composition brought about by disturbance, are unpredictable, with unclear consequences for tropical rainforest biodiversity.     

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。     

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.     

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。     

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.     

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

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