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.     

Extremely high proportions of male flowers and geographic variation in floral ratios within male figs of Ficus tikoua despite pollinators displaying active pollen collection

Most plants are pollinated passively, but active pollination has evolved among insects that depend on ovule fertilization for larval development. Anther‐to‐ovule ratios (A/O ratios, a coarse indicator of pollen‐to‐ovule ratios) are strong indicators of pollination mode in fig trees and are consistent within most species. However, unusually high values and high variation of A/O ratios (0.096–10.0) were detected among male plants from 41 natural populations of Ficus tikoua in China. Higher proportions of male (staminate) flowers were associated with a change in their distribution within the figs, from circum‐ostiolar to scattered. Plants bearing figs with ostiolar or scattered male flowers were geographically separated, with scattered male flowers found mainly on the Yungui Plateau in the southwest of our sample area. The A/O ratios of most F. tikoua figs were indicative of passive pollination, but its Ceratosolen fig wasp pollinator actively loads pollen into its pollen pockets. Additional pollen was also carried on their body surface and pollinators emerging from scattered‐flower figs had more surface pollen. Large amounts of pollen grains on the insects' body surface are usually indicative of a passive pollinator. This is the first recorded case of an actively pollinated Ficus species producing large amounts of pollen. Overall high A/O ratios, particularly in some populations, in combination with actively pollinating pollinators, may reflect a response by the plant to insufficient quantities of pollen transported in the wasps’ pollen pockets, together with geographic variation in this pollen limitation. This suggests an unstable scenario that could lead to eventual loss of wasp active pollination behavior.     

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。     

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.     

Has Pollination Mode Shaped the Evolution of Ficus Pollen?

Background

The extent to which co-evolutionary processes shape morphological traits is one of the most fascinating topics in evolutionary biology. Both passive and active pollination modes coexist in the fig tree (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) mutualism. This classic obligate relationship that is about 75 million years old provides an ideal system to consider the role of pollination mode shifts on pollen evolution.

Methods and Main Findings

Twenty-five fig species, which cover all six Ficus subgenera, and are native to the Xishuangbanna region of southwest China, were used to investigate pollen morphology with scanning electron microscope (SEM). Pollination mode was identified by the Anther/Ovule ratio in each species. Phylogenetic free regression and a correlated evolution test between binary traits were conducted based on a strong phylogenetic tree. Seventeen of the 25 fig species were actively pollinated and eight species were passively pollinated. Three pollen shape types and three kinds of exine ornamentation were recognized among these species. Pollen grains with ellipsoid shape and rugulate ornamentation were dominant. Ellipsoid pollen occurred in all 17 species of actively pollinated figs, while for the passively pollinated species, two obtuse end shapes were identified: cylinder and sphere shapes were identified in six of the eight species. All passively pollinated figs presented rugulate ornamentation, while for actively pollinated species, the smoother types - psilate and granulate-rugulate ornamentations - accounted for just five and two among the 17 species, respectively. The relationship between pollen shape and pollination mode was shown by both the phylogenetic free regression and the correlated evolution tests.

Conclusions

Three pollen shape and ornamentation types were found in Ficus, which show characteristics related to passive or active pollination mode. Thus, the pollen shape is very likely shaped by pollination mode in this unique obligate mutualism.     

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.     

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。     

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.     

Plasticity and diversity of the phenology of dioecious Ficus species in Taiwan

While Ficus present a series of traits often associated with dioecy, the prevalence of dioecy in Ficus is atypical. In Asian floras, dioecious Ficus species generally outnumber monoecious ones. Further this is also true in relatively northerly locations for Ficus such as the island of Taiwan. Ficus are pollinated by species-specific wasps that use fig flowers as breeding sites. In dioecious fig species, pollinators develop only in the inflorescences of male fig trees. In this study, we investigated the reproductive phenology of four dioecious Ficus species with distinct ecologies in several locations in northern and southern Taiwan. The two first species (Ficus erecta and Ficus septica) were investigated in four locations. Reproductive phenology was quite different among sites, even within a single species. For example, F. erecta presented well-defined crops at the population level in its usual high-elevation habitat but continuous fig production at low elevations, especially in South Taiwan. The two other fig species (Ficus pedunculosa var. mearnsii and Ficus tinctoria subsp. swinhoei), are shrubs growing together along seashores in exposed locations on coral reef remnants. These two species presented quite different traits allowing the survival of pollinating wasp populations. Ficus pedunculosa var. mearnsii produced figs continuously so that fresh receptive figs were always available for the pollinating wasps while F. tinctoria subsp. swinhoei extended the period of receptivity of its figs, so that receptive figs that had been waiting for pollinating wasps were almost always available. In summary, dioecious figs in Taiwan showed remarkable variation in their phenology, within species among locations or among species within location. Nevertheless, despite this variation, the phenology of the trees always allowed survival of pollinating wasp populations. Dioecious figs seem to have adopted a differentiated set of strategies which result in high resilience of pollinator populations. This resilience could help explain the atypical prevalence of dioecy in Ficus.     

Stigma development and receptivity in almond (Prunus dulcis)

BACKGROUND AND AIMS: Fertilization is essential in almond production, and pollination can be limiting in production areas. This study investigated stigma receptivity under defined developmental stages to clarify the relationship between stigma morphology, pollen germination, tube growth and fruit set. METHODS: Light and scanning electron microscopy were employed to examine stigma development at seven stages of flower development ranging from buds that were swollen to flowers in which petals were abscising. Flowers at different stages were hand pollinated and pollen germination and tube growth assessed. Artificial pollinations in the field were conducted to determine the effect of flower age on fruit set. KEY RESULTS: Later stages of flower development exhibited greater stigma receptivity, i.e. higher percentages of pollen germination and more extensive tube growth occurred in older (those opened to the flat petal stage or exhibiting petal fall) than younger flowers. Enhanced stigma receptivity was associated with elongation of stigmatic papillae and increased amounts of stigmatic exudate that inundated papillae at later developmental stages. Field pollinations indicated that the stigma was still receptive and nut set was maintained in older flowers. CONCLUSIONS: Stigma receptivity in almond does not become optimal until flowers are past the fully open stage. The stigma is still receptive and fruit set is maintained in flowers even at the stage when petals are abscising. Strategies to enhance pollination and crop yield, including the timing and placement of honey bees, should consider the effectiveness of developmentally advanced flowers.     

Reproductive biology of Nymphaea capensis Thunb. var. zanxibariensis (Casp.) Verdc. (Nymphaeaceae)

Anthesis in Nymphaea capensis var. zanzibariensis is diurnal with flowers opening and closing for three consecutive days. On the first day of anthesis, the stigmatic papillae secrete fluid and the outermost anthers are dehiscent. On the second day of anthesis the stamens form a cone above the dry stigmatic cup. The middle stamens open and turn outward. On the third day of flowering, all the stamens open and the dry stigmatic cup is exposed. The flowers are homogamous and not protogynous as the other Nymphaea. The gynoecium of the self-compatible N. capensis var. zanzibariensis , is characterized by a wet papillate stigma, a short hollow style, and secretory cells on the ventral surface of the ovary. The pollen is released on the receptive stigma. Following initial growth in intercellular spaces in the transmitting tract of the stigma, pollen tubes travel through the stylar canal and into the ovary.     

Culture-Free Survey Reveals Diverse and Distinctive Fungal Communities Associated with Developing Figs (Ficus spp.) in Panama

The ancient association of figs (Ficus spp.) and their pollinating wasps (fig wasps; Chalcidoidea, Hymenoptera) is one of the most interdependent plant–insect mutualisms known. In addition to pollinating wasps, a diverse community of organisms develops within the microcosm of the fig inflorescence and fruit. To better understand the multipartite context of the fig–fig wasp association, we used a culture-free approach to examine fungal communities associated with syconia of six species of Ficus and their pollinating wasps in lowland Panama. Diverse fungi were recovered from surface-sterilized flowers of all Ficus species, including gall- and seed flowers at four developmental stages. Fungal communities in syconia and on pollinating wasps were similar, dominated by diverse and previously unknown Saccharomycotina, and distinct from leaf- and stem endophyte communities in the same region. Before pollination, fungal communities were similar between gall- and seed flowers and among Ficus species. However, fungal communities differed significantly in flowers after pollination vs. before pollination, and between anciently diverged lineages of Ficus with active vs. passive pollination syndromes. Within groups of relatively closely related figs, there was little evidence for strict-sense host specificity between figs and particular fungal species. Instead, mixing of fungal communities among related figs, coupled with evidence for possible transfer by pollinating wasps, is consistent with recent suggestions of pollinator mixing within syconia. In turn, changes in fungal communities during fig development and ripening suggest an unexplored role of yeasts in the context of the fig–pollinator wasp mutualism.     

Living on the edge: Fig tree phenology at the northern range limit of monoecious Ficus in China

Fig trees (Ficus) are a species-rich group of mainly tropical and subtropical plants that are of ecological importance because of the large numbers of vertebrates that utilise their figs for food. Factors limiting their distributions to warmer regions are still poorly understood, but are likely to include factors linked to their specialised pollination biology, because each Ficus species is dependent on one or a small number of host-specific fig wasps (Agaonidae) for pollination. Adult fig wasps are short-lived, but some species are capable of dispersing extremely long distances to pollinate their hosts. Close to its northern range limit we investigated the phenology of Ficus virens, the monoecious fig tree that reaches furthest north in China. Relatively few trees produced any figs, and very few retained figs throughout the winter. Despite this, new crops produced in spring were pollinated, with seasonally migrant pollinators from plants growing further south the most likely pollen vectors. An inability to initiate new crops at low temperatures may limit the distribution of monoecious fig trees to warmer areas.     

Can fine-scale post-pollination variation of fig volatile compounds explain some steps of the temporal succession of fig wasps associated with Ficus racemosa?

Volatile organic compounds (VOCs) emitted by flowers play an essential role in mediating the attraction of pollinators. However, they also attract other species exploiting resources associated with flowers. For instance, VOCs emitted by figs play a major role in encounters between Ficus spp., their mutualistic pollinating wasps, and all the members of the community of non-pollinating fig wasps (NPFWs) that exploit the mutualistic interaction. Because pollinators might be in limited supply for a tree bearing many inflorescences, the plant might maximize its individual reproductive success by reducing the attractiveness of inflorescences once they are pollinated, so that pollinators orient only towards the tree's unpollinated figs. Changes in VOCs emission that bring this about could represent an important cue for NPFWs that exploit particular stages of fig development. In this study, by monitoring precisely the presence of fig-associated wasps on figs of F. racemosa, a common widespread fig species, we demonstrated that 4–5 days and 15 days following pollination represent two critical transitional steps in the succession of different wasp species. Then, focusing on the first one of these transitional steps, by investigating the composition of fig VOCs at receptivity and from 1 to 5 days following pollination, we detected progressive quantitative and qualitative variation of floral scent following pollination. These changes are significant at 5 days following pollination. The qualitative changes are mainly due to an increase in the relative proportions of two monoterpenes (α-pinene and limonene). These variations of the floral VOCs following pollination could explain why pollinating wasps stop visiting figs very shortly after the first pollinators enter receptive figs. They also possibly explain the succession of non-pollinating wasps on the figs following pollination.     

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.     

Utilisation of chemical signals by inquiline wasps in entering their host figs

The fig tree, Ficus curtipes, hosts an obligate pollinating wasp, an undescribed Eupristina sp., but can also be pollinated by two inquiline (living in the burrow, nest, gall, or other habitation of another animal) wasps, Diaziella yangi and an undescribed Lipothymus sp. The two inquilines are unable to independently induce galls and depend on the galls induced by the obligate pollinator for reproduction and, therefore, normally enter receptive F. curtipes figs colonised by the obligate pollinators. However, sometimes the inquilines also enter figs that are not colonised by the pollinators, despite consequent reproductive failure. It is still unknown which signal(s) the inquilines use in entering the colonised and non-colonised figs. We conducted behavioural experiments to investigate several possible signals utilised by the inquilines in entering their host receptive figs. Our investigation showed that both inquiline species enter the receptive F. curtipes figs in response to the body odours of the obligate wasps and one of the main compounds emitted by the figs, 6-methyl-5-hepten-2-one. The compound was not found in the pollinator body odours, suggesting that the two inquiline wasps can utilise two signals to enter their host figs, which is significant for the evolution of the fig-fig wasp system. These inquilines could evolve to become mutualists of the figs if they evolve the ability to independently gall fig flowers; there is, however, another possibility that a monoecious Ficus species hosting such inquilines may evolve into a dioecious one if these inquilines cannot evolve the above-mentioned ability. Additionally, this finding provides evidence for the evolution of chemical communication between plants and insects.     

The pollination biology of Sauroglossum elatum Lindl. (Orchidaceae: Spiranthinae): moth-pollination and protandry in neotropical Spiranthinae

The pollination biology of Sauroglossum elatum Lindl (Orchidaceae: Spiranthinae) was studied in the State of São Paulo, south-eastern Brazil. This orchid is protandrous and almost fully self-compatible, but pollinator-dependent. Thus, pollinators are required for the plants to set fruits and seeds. The flowers are pollinated by moths of the family Noctuidae. Pollinia are dislodged when the moths probe flowers in the male phase. At this stage the stigmatic surface is inaccessible, so that the flowers can act only as pollen-donors. Flowers in the female phase present their stigmatic surfaces well exposed and dry viscidia; at this stage the flowers act as pollen receivers. Pollinarium-bearing moths, when visiting a flower in the female phase, will brush the pollinarium against the stigmatic surface, thus effecting the pollination. Moth-pollination is reported here for the first time for the orchid subtribe Spiranthinae. Protandry also occurs in a few additional Brazilian Spiranthinae. Based on the evidence presented in this work, protandry in Spiranthinae is not necessarily linked to bumblebee pollination, as currently accepted. It is suggested that the occurrence of protandry in Spiranthinae and in the closely related subtribes Prescottinae and Goodyerinae may also be a feature encompassing ecological and phylogenetic implications. Anecdotal ex-situ observations are briefly discussed. Cultivated specimens were actively visited by Tetragonisca angustula (Meliponini) bees. which broke the pollinaria, collected the pollen and eventually performed pollination by leaving small fragments of the pollinia on the stigmatic surface. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 138 , 9–16.     

The control of incompatibility in distylous Pulmonaria affinis Jordan (Boraginaceae)

In P. affinis, pin pollen is shorter on average than thrum pollen. Pins have more coronal hooks on stigmatic papillae than thrums, but gaps between papillae are relatively smaller for thrums. Pin stigmas receive more pollen than thrum stigmas. Thrum stigmas receive more (dissortive) pin pollen, but pin stigmas are assortively pollinated. Pollen only germinates when trapped below papilla coronas. On thrum stigmas, most trapped pollen is pin. Pollen germination is better on thrum stigmas than pin stigmas, and thrum stigmas show a close relationship between numbers of legitimate pollen grains, numbers of germinating grains, and numbers of pollen tubes in the style. There is no inhibition of illegitimate pollen germination. Illegitimate pollen tubes are inhibited in the style. Incompatibility operates by a combination of dissortive pollination, dissortive pollen trapping, and stylar pollen tube inhibition. All heteromorphic features differing between pins and thrums are implicated in the inhibition of within-morph fertilization in thrums.     

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。     

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.