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.     

Why do fig wasps actively pollinate monoecious figs?

Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.     

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。     

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.     

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.     

Permeability of receptive fig fruits and its effects on the re‐emergence behaviour of pollinators

1. Figs and pollinating fig wasps provide a model system for studying mutualism. The permeability of the syconium changes during receptivity or between seasons, which may affect the behaviour of pollinators. Fig fruits are permeable during receptivity, and in some species, pollinators can enter and re‐emerge after oviposition/pollination. We studied the relationship between fig permeability and pollinator re‐emergence behaviour with a functional dioecious fig, Ficus hispida and the obligate pollinator Ceratosolen solmsi marchali. 2. The relationship reflects the interaction of figs and pollinators in the mutualism and also the conflicts of interests between the two partners: figs benefit from the enclosed fig fruits which have low permeability, but pollinators benefit from their re‐emergence behaviour, which requires high fig permeability. 3. The results showed that at the end of receptivity, the permeability of fig fruits lowered rapidly with changes to the ostiole structures, and re‐emergence rate was low, with more re‐emerging pollinators trapped in the ostiolar bracts. Our results also showed that in the rainy season, the length of receptivity was shorter and fig permeability was lower. The re‐emergence rates were also lower than those in the dry season. The results elucidated that figs' interests dominated in the conflicts between fig and pollinating wasp. 4. Based on a new criteria which employed the classification of pollinators found dead in the ostiolar bracts and which involved a survey of 6 monoecious and 12 dioecious fig species, we found that re‐emergence behaviour was prevalent among fig species, and was more prevalent in functional dioecious figs than monoecious ones.     

环纹榕传粉榕小蜂的传粉模式

榕小蜂的传粉结构、 传粉行为以及寄主榕树的花药胚珠比是判断榕-蜂互惠系统传粉模式的重要依据。本研究于2010年8月至2011年6月对位于云南西双版纳地区的试验样树环纹榕Ficus annulata进行观察, 对出榕果的环纹榕传粉榕小蜂Deilagaon annulatae进行电镜扫描和室内显微镜下对其进行行为观察。电镜扫描显示： 环纹榕传粉榕小蜂D. annulatae位于胸部的花粉筐消失, 具一片可粘附花粉的毛区, 提示其属于被动传粉的种类。传粉行为观察发现, 该蜂没有主动采集花粉的行为, 显然存在的花粉刷已丧失了主动收集花粉的功能。寄主植物环纹榕F. annulata属于典型的自动散粉让榕小蜂沾附花粉的榕树种类。环纹榕传粉榕小蜂D. annulatae是西双版纳热带地区已知58种传粉榕小蜂中唯一体色为黄色的种类, 该蜂偏爱在低温的夜晚出蜂。除了传粉榕小蜂, 一种金小蜂Lipothymus sp.也在雌花期进入榕果内繁殖, 并且其数量显著高于环纹榕传粉榕小蜂D. annulatae (P<0.0001)。自然单果的繁殖中, 环纹榕传粉榕小蜂的数量显著高于种子数量, 呈现出榕-蜂互惠系统中罕见的传粉榕小蜂主导的局面。综合榕-蜂的传粉特征显示, 环纹榕F. annulata及其传粉榕小蜂D. annulatae互惠系统是被动传粉的模式。     

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.     

Floral reward presentation favored the expression of male function in the pollen‐only flower Melastoma malabathricum

Abstract Animal‐pollinated plant species modulate the presentation of pollinator rewards to maximize reproductive success. In plants providing pollen as the only reward for pollinators, it is usually difficult to unravel the dual roles of reward presentation and the realization of male and female functions (pollen removal and deposition). Exploiting the two types of anther in the androecia of Melastoma malabathricum L., we examined whether the removal of pollen for reward is regulated primarily to favor male function or female function. Pollen removal by carpenter bees from the feeding and pollination anthers, as well as pollen deposition on the stigmas, were quantified during anthesis of M. malabathricum. There was no significant difference in pollen removal rates from the feeding and pollination anthers of M. malabathricum between the onset of anthesis and flower wilting. The stigmatic pollen loads exceeded the ovule number after three sonication bouts, and female function was satisfied earlier than male function. The results support the hypothesis that the presentation of pollination reward in this species is regulated primarily to favor the expression of male function, rather than female function, in agreement with the pollen‐donation hypothesis. A cooperative relationship between the feeding and pollination anthers was demonstrated in heterantherous flowers, which optimizes the balance in investments between pollinator rewards and “functional pollen” for gene transfer.     

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。     

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.     

Sexual differences in the attractiveness of figs to pollinators: females stay attractive for longer

1. Figs on male dioecious fig trees (Ficus, Moraceae) are breeding sites for pollinator fig wasps (Hymenoptera, Agaonidae), but figs on female plants are traps that produce only seeds. As the short‐lived fig wasps cannot reproduce in female figs, natural selection should favour individuals that avoid them. Several studies have failed to detect such discrimination, a result attributed to inter‐sexual mimicry and ‘selection to rush’ in the wasps, but their experiments failed to explicitly take into account fig age (how long they had been waiting to be pollinated). 2. We compared the relative attraction of male and female figs of known ages of the South East Asian Ficus montana Burm. f. to its pollina tor Liporrhopalum tentacularis Grandi and examined how the reproductive success of the plant and its pollinator change with the age of the figs. 3. Mean retention time for un‐pollinated figs on female plants was 16 days whereas in male figs it was 12 days. Female figs remained attractive for up to 2 weeks, although the wasps were less willing to enter older figs. After pollinator entry, receptivity continued for several days, lasting longer in figs entered by a single wasp. Consistent with abortion rates, attractiveness persisted longer in female figs. Older figs produced fewer fig wasp offspring, but similar numbers of seeds. 4. The sexual differences in floral longevity in F. montana may represent part of a previously un‐recognised reproductive strategy in some fig trees that allows male plants to ‘export’ pollinators while also maintaining a resident fig wasp population.     

Consequences of protecting flowers in a fig: a one-way trip for pollinators?

Abstract. Fig trees ( Ficus ) have closed inflorescences. Closure is an efficient protection of flowers against non-specialist predators and harsh external environmental conditions. Each Ficus species is pollinated by a single insect species, an agaonid wasp, capable of forcing its way through a bract-covered pore, the ostiole, to gain access to the flowers. Figs also provide oviposition sites for the wasps. The fig/pollinator interaction is a classic example of mutualism. It has been widely assumed that, once pollinators have entered a fig, oviposited and pollinated, they die trapped within the fig. In this paper, we present observations under natural conditions and results of field experiments on three very different fig species ( Ficus aurea Nutt., F. carica L. and F. microcarpa L.) showing that some pollinators do exit or try to exit from the fig after pollination and oviposition. Moreover, experimental results demonstrate that in at least one species ( F. carica ), the pollinator is able to oviposit successively in two different figs.
The frequency of re-emergences from figs after pollination varies among species and this may be related to variations in pollination dynamics depending on environmental constraints such as the abundance of trees and tree phenology. Several factors that may favour pollinators that leave figs after pollination and oviposition are discussed. They include competition between pollinators for oviposition sites, and minimising of the risk of vertical transmission of parasites and pathogens.     

Sky islands as foci for divergence of fig trees and their pollinators in southwest China

The dynamics of populations and their divergence over time have shaped current levels of biodiversity and in the case of the “sky islands” of mountainous southwest (SW) China have resulted in an area of exceptional botanical diversity. Ficus tikoua is a prostrate fig tree subendemic to the area that displays unique intraspecific diversity, producing figs typical of different pollination modes in different parts of its range. By combining climate models, genetic variation in populations of the tree's obligate fig wasp pollinators and distributions of the different plant phenotypes, we examined how this unusual situation may have developed. We identified three genetically distinct groups of a single Ceratosolen pollinator species that have largely parapatric distributions. The complex topography of the region contributed to genetic divergence among the pollinators by facilitating geographical isolation and providing refugia. Migration along elevations in response to climate oscillations further enhanced genetic differentiation of the three pollinator groups. Their distributions loosely correspond to the distributions of the functionally significant morphological differences in the male figs of their host plants, but postglacial expansion of one group has not been matched by spread of its associated plant phenotype, possibly due to a major river barrier. The results highlight how interplay between the complex topography of the “sky island” complex and climate change has shaped intraspecies differentiation and relationships between the plant and its pollinator. Similar processes may explain the exceptional botanical diversity of SW China.     

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.     

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.     

Phenological Adaptations in Ficus tikoua Exhibit Convergence with Unrelated Extra-Tropical Fig Trees

Flowering phenology is central to the ecology and evolution of most flowering plants. In highly-specific nursery pollination systems, such as that involving fig trees (Ficus species) and fig wasps (Agaonidae), any mismatch in timing has serious consequences because the plants must balance seed production with maintenance of their pollinator populations. Most fig trees are found in tropical or subtropical habitats, but the dioecious Chinese Ficus tikoua has a more northerly distribution. We monitored how its fruiting phenology has adapted in response to a highly seasonal environment. Male trees (where fig wasps reproduce) had one to three crops annually, whereas many seed-producing female trees produced only one fig crop. The timing of release of Ceratosolen fig wasps from male figs in late May and June was synchronized with the presence of receptive figs on female trees, at a time when there were few receptive figs on male trees, thereby ensuring seed set while allowing remnant pollinator populations to persist. F. tikoua phenology has converged with those of other (unrelated) northern Ficus species, but there are differences. Unlike F. carica in Europe, all F. tikoua male figs contain male flowers, and unlike F. pumila in China, but like F. carica, it is the second annual generation of adult wasps that pollinate female figs. The phenologies of all three temperate fig trees generate annual bottlenecks in the size of pollinator populations and for female F. tikoua also a shortage of fig wasps that results in many figs failing to be pollinated.     

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.     

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.     

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.