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.     

Pollinator sharing in dioecious figs (Ficus: Moraceae)

As one of the most specialized pollination syndromes, the fig (Ficus)–fig wasp (Agaonidae) mutualism can shed light on how pollinator behaviour and specificity affect plant diversification through processes such as reproductive isolation and hybridization. Pollinator sharing among species has important implications for Ficus species delimitation and the evolutionary history of the mutualism. Although agaonid wasp pollinators are known to visit more than one host species in monoecious figs, pollinator sharing has yet to be documented in dioecious figs. The present study investigated the frequency of pollinator sharing among sympatric, closely‐related dioecious figs in Ficus sections Sycocarpus and Sycidium. Molecular and morphological species identification established the associations between pollinating agaonid wasp species and host fig species. Cytochrome oxidase I was sequenced from 372 Ceratosolen pollinators of Ficus section Sycocarpus and 210 Kradibia pollinators of Ficus section Sycidium. The association between fig species and morphologically distinct clades of pollinator haplotypes was predominantly one‐to‐one. In Ceratosolen, six of 372 pollinators (1.5%) visited fig species other than the predominant host. No pollinator sharing was detected between the two Sycidium host species, although a rare hybrid shared Kradibia pollinators with both parental species. These findings point to low rates of pollinator sharing among closely‐related dioecious fig species in sympatry, and perhaps lower rates than among monoecious figs. Such rare events could be evolutionarily important as mechanisms for gene flow among fig species. Differences in rates of pollinator sharing among fig lineages might explain the conflicting phylogenetic patterns inferred among monoecious figs, dioecious figs, and their respective pollinators. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 546–558.     

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.     

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.     

Pollination and parasitism in functionally dioecious figs

Fig wasps (Agaonidae: Hymenoptera) are seed predators and their interactions with Ficus species (Moraceae) range from mutualism to parasitism. Recently considerable attention has been paid to conflicts of interest between the mutualists and how they are resolved in monoecious fig species. However, despite the fact that different conflicts can arise, little is known about the factors that influence the persistence of the mutualism in functionally dioecious Ficus. We studied the fig pollinator mutualism in 14 functionally dioecious fig species and one monoecious species from tropical lowland rainforests near Madang, Papua New Guinea. Observations and experiments suggest that (i) pollinating wasps are monophagous and attracted to a particular host species; (ii) pollinating and non-pollinating wasps are equally attracted to gall (male) figs and seed (female) figs in functionally dioecious species; (iii) differing style lengths between gall figs and seed figs may explain why pollinators do not develop in the latter; (iv) negative density dependence may stabilize the interaction between pollinating wasps and their parasitoids; and (v) seed figs may reduce the search efficiency of non-pollinators. This increased pollinator production without a corresponding decrease in seed production could provide an advantage for dioecy in conditions where pollinators are limiting.     

不同繁育系统的榕树雌花的花柱长度和繁殖率比较

多年来, 不同繁育系统的榕树(Ficus spp.)的进化问题引起生物学家们极大的兴趣。前人通过对不同繁育系统榕树雌花的花柱长度、传粉榕小蜂产卵器长度和繁殖率的比较, 推测榕树的雌雄异株是由雌雄同株进化而来的。为验证这一推论, 选取雌雄同株的垂叶榕(Ficus benjamina)和钝叶榕(F. curtipes)以及雌雄异株的斜叶榕(F. tinctoria)和鸡嗉子榕(F. semicordata), 进行了雌花花柱长度、传粉榕小蜂产卵器长度及繁殖率的比较。研究结果显示: 1)两种雌雄同株榕树的传粉榕小蜂(Eupristina koningsbergeri和Eupristina sp.)的产卵器长度, 显著长于两种雌雄异株榕树的传粉榕小蜂(Liporrhopalum gibbosae和Ceratosolen gravelyi)产卵器的长度, 且雌雄同株榕树雌花花柱长度的变异大于雌雄异株雌花花柱长度的变异; 2)两种雌雄同株榕树的雌花花柱长度呈单峰分布, 且花柱长度的变异大于传粉榕小蜂产卵器长度的变异; 两种雌雄异株榕树花序的雌花花柱长度呈双峰分布, 雌花花柱长度的变异也大于传粉榕小蜂产卵器的长度变异; 3)两种雌雄同株榕树的传粉榕小蜂产卵器长度能到达雌花子房的比例更高, 可更有效地产生瘿花, 而雌雄异株榕树产生种子的优势更强。研究表明: 在传粉榕小蜂产卵器长度及花序雌花花柱分布方面, 雌雄异株榕树有着明显的优势, 但在繁殖率方面没有绝对优势。因此, 前人从雌花花柱分布及繁殖率比较而做出榕树进化的推测并不正确。要真正解决榕树的进化问题, 需要多学科、多指标的综合分析和深入研究。     

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.     

薜荔榕小蜂对薜荔和爱玉子雌花期榕果挥发物的行为反应

薜荔和爱玉子均属雌雄异株桑科榕属植物,两者互为原变种与变种的关系,分别与薜荔传粉小蜂和爱玉子传粉小蜂(二者互为隐存种)建立了专性共生关系,榕树榕果挥发物在维系传粉小蜂与其寄主的共生关系上起着重要作用。利用Y型嗅觉仪测定薜荔榕小蜂(薜荔和爱玉子的传粉小蜂)对薜荔和爱玉子雌花期榕果挥发物的行为反应。结果表明:(1)雌花期果型的大小对薜荔榕小蜂行为反应无显著影响,薜荔大、小果型雌花期雌(雄)榕果挥发物对其传粉小蜂均具有强烈的吸引作用;(2)榕果挥发物浓度影响薜荔榕小蜂行为反应,薜荔、爱玉子雌花期雌(雄)榕果挥发物对其传粉小蜂的吸引作用均可能存在阈值反应,即榕果挥发物浓度未超过阈值时,雌花期榕果挥发物对传粉小蜂的吸引作用与挥发物浓度成正相关关系,而一旦超过阈值,榕果挥发物对传粉蜂的吸引作用显著下降,表明寄主榕果挥发物浓度影响传粉小蜂的寄主定位;(3)薜荔传粉小蜂对低浓度爱玉子雌花期雌(雄)榕果挥发物、爱玉子传粉小蜂对低浓度薜荔雌花期雌(雄)榕果挥发物均既无趋向也无驱避行为;薜荔传粉小蜂对高浓度的爱玉子雌花期雌(雄)榕果挥发物表现为显著的驱避行为,而爱玉子传粉小蜂对高浓度薜荔雌(雄)雌花期榕果挥发物表现为显著的趋向行为,因此,薜荔传粉小蜂与爱玉子传粉小蜂存在寄主专一性不对称现象,爱玉子传粉小蜂进入薜荔雌(雄)果内传粉或产卵的可能性较大,而福州地区的薜荔传粉小蜂可能难以进入爱玉子雌(雄)果内传粉或产卵。本研究结果将为榕-蜂共生体系的化学生态学理论研究以及爱玉子栽培提供科学依据。     

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.     

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

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

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.     

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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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.     

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.     

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.     

Ability to gall: the ultimate basis of host specificity in fig wasps?

1. Fig trees (Ficus spp.) and their host‐specific pollinator fig wasps (Agaonidae) are partners in an obligate mutualism. Receptive phase figs release specific volatiles to attract their pollinators, and this is generally effective in preventing pollinator species from entering figs of the wrong hosts. 2. If entry is attempted into atypical host figs, then ostiole size and shape and style length may also prevent reproduction. In spite of these barriers, there is increasing evidence that fig wasps enter atypical hosts, and that this can result in hybrid seed and fig wasp offspring. 3. This study examines the basis of pollinator specificity in two dioecious fig species from different geographical areas. Kradibia tentacularis pollinates Ficus montana in Asia. Ficus asperifolia from East Africa is closely related but is pollinated by a different species of Kradibia. 4. In glasshouses, K. tentacularis was attracted to its normal host, F1s and backcrosses, but only rarely entered figs of F. asperifolia. Foundresses were able to lay eggs in hybrids, backcrosses, and F. asperifolia, although flower occupancy was lowest in F. asperifolia figs and intermediate in hybrids. 5. The fig wasp failed to reproduce in female F. montana, male F. asperifolia, and male F1s, and most but not all backcrosses to F. montana. This was a result of the failure to initiate gall production. 6. Host specificity in this fig wasp is strongly influenced by host volatiles, but the ability to gall may be the ultimate determinant of whether it can reproduce.     

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.     

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.     

Can chemical signals,responsible for mutualistic partner encounter,promote the specific exploitation of nursery pollination mutualisms? – The case of figs and fig wasps

In nursery pollination mutualisms, where pollinators reproduce within the inflorescence they pollinate, floral scents often play a major role in advertizing host location and rewards for the pollinator. However, chemical messages emitted by the plant that are responsible for the encounter of mutualist partners can also be used by parasites of these mutualisms to locate their host. Each species of Ficus (Moraceae) is involved in an obligatory nursery pollination mutualism with usually one pollinating fig wasp (Hymenoptera: Chalcidoidea: Agaonidae). In this interaction, volatile compounds emitted by receptive figs are responsible for the attraction of their specific pollinator. However, a large and diverse community of non-pollinating chalcidoid wasps can also parasitize this mutualism. We investigated whether the chemical message emitted by figs to attract their pollinator can promote the host specificity of non-pollinating fig wasps. We analysed the volatile compounds emitted by receptive figs of three sympatric Ficus species, namely, Ficus hispida L., Ficus racemosa L., and Ficus tinctoria G. Forster, and tested the attraction of the pollinator of F. hispida ( Ceratosolen solmsi marchali Mayr), and of one species of non-pollinating fig wasp [ Philotrypesis pilosa Mayr (Hymenoptera: Chalcidoidea: Pteromalidae)] to scents emitted by receptive figs of these three Ficus species. Analysis of the volatile compounds emitted by receptive figs revealed that the three Ficus species could be clearly distinguished by their chemical composition. Behavioural bioassays performed in a Y-tube olfactometer showed that both pollinator and parasite were attracted only by the specific odour of F. hispida . These results suggest that the use by non-pollinating fig wasps of a specific chemical message produced by figs could limit host shifts by non-pollinating fig wasps.     

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。