Non‐pollinating Fig Wasps Decrease Pollinator and Seed Production in Ficus andicola (Moraceae)

Fig trees ( Ficus spp.) and Agaonine fig‐wasps participate in an obligate mutualism. Fig wasps can only develop within fig inflorescences (syconia) and they are the only organisms capable of pollinating fig flowers. Other non‐pollinating wasps that lay eggs by inserting their ovipositors from the outside can also develop in syconia. These parasitic wasps may be parasitoids of either pollinating or other non‐pollinating wasps, or form galls in fig flowers or other tissues. Depending on this interaction, parasitic wasps may have various effects on the production of pollinating wasps and seeds. Wasps in the genus Idarnes, which parasitize New World figs (subgenus Urostigma), have an effect on wasp production but not on seed production. Heterandrium spp., which have short ovipositors and lay on external flowers, are infrequent and no effect on seed production has been documented. In the Colombian Andes, Idarnes spp. and Heterandrium spp. are the most frequent parasites of the Ficus andicola — Pegoscapus sp. mutualism, affecting 62 and 43 percent of syconia, respectively. Controlling for other factors that influence wasp and seed production, such as number of foundresses, syconium size and tree, we found that Idarnes reduced pollinator production by almost half but did not reduce seed production, whereas Heterandrium reduced seed production by 40 percent, and marginally affected pollinator production. Our results provide the first clear documentation of Heterandrium spp. impact on fig seed production. Whether the relative abundance of this genus is a generalized phenomenon in montane forest remains to be determined.     

Interference Competition and High Temperatures Reduce the Virulence of Fig Wasps and Stabilize a Fig-Wasp Mutualism

Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia (‘figs’) that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can ‘set the rules of the game’ to ensure mutualistic behavior in its symbionts.     

高榕的3类雌花形态及其繁殖特征

榕树(Ficus spp.)及其传粉榕小蜂(Agaonidae)之间经过长期的协同进化, 已形成了高度专一的互惠共生关系。在雌雄同株的榕树中, 同一个榕果内既繁殖种子, 又繁殖榕小蜂, 雌花资源在繁殖种子和榕小蜂之间是怎样分配的?该研究选择广泛分布于西双版纳地区的高榕(F. altissima)及其传粉榕小蜂系统来回答这个问题。高榕果内的雌花柱头形态变异较大, 有3种类型的柱头——球型、弯钩型和火炬型, 它们分别占到雌花总量的54.00%、36.93%和9.07%。3种类型柱头的雌花分别具有不同长度的花柱, 球型柱头雌花的平均花柱长度最短, 火炬型柱头次之, 弯钩型柱头雌花的平均花柱长度最长。在高榕果内, 有传粉者Eupristina altissima和欺骗者Eupristina sp.两类小蜂进入榕果内繁殖, 前者的产卵器长度比96.01%以上的雌花花柱长, 后者的产卵器也要长于85.73%的雌花花柱, 从产卵器长度和雌花花柱长度的匹配情况看, 它们应该可以利用绝大多数雌花产卵繁殖后代。然而, 繁殖榕小蜂的雌花主要是短花柱的雌花, 其中60.64%是球型柱头的雌花; 而繁殖种子的主要是花柱较长的弯钩型柱头和火炬型柱头的雌花。显然, 繁殖榕小蜂和种子的雌花不仅花柱长度有差异, 柱头也分化出了不同的形态, 变异的柱头形状也是调节榕树-榕小蜂繁殖平衡的手段之一。     

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.     

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。     

非传粉小蜂对榕-蜂共生系统的影响

榕-蜂共生系统是桑科榕属(Ficus)植物与传粉榕小蜂专一互惠形成的生态学关系。但是,也有一些非传粉的小蜂出现在这个系统中,对榕-蜂共生系统可能产生较大的影响。西双版纳的聚果榕(Ficus racemosa)树上主要有5种非传粉小蜂,分别在榕果发育的不同阶段从果外向果内产卵。在传粉榕小蜂进果之前的花前期,Platyneura testace、Apocrypta sp.和P. mayri这3种非传粉小蜂先后到果外产卵繁殖后代,对榕-蜂共生系统造成显著影响,尤其是影响传粉榕小蜂的繁殖。在传粉榕小蜂进果之后的间花期,P. mayri、A. westwoodi和P. agraensis这3种非传粉小蜂相继到果外产卵,它们虽然能减少种子形成和传粉榕小蜂繁殖的数量,但最终没有对榕-蜂共生系统造成显著的影响。造瘿类的P. mayri可在花前期和间花期产卵繁殖,在花前期产卵时它主要是影响传粉榕小蜂的繁殖,而在间花期产卵时它则更多地是影响种子的生产。     

Seasonal change in the structure of fig-wasp community and its implication for conservation

Figs (Moraceae) and their pollinating wasps (Agaonidae) constitute a famous reciprocal mutualism in which figs provide some female flowers for the development of fig wasp offspring while the fig wasps pollinate fig flowers. However, figs also host many non-pollinating wasps which are either parasitoids or resource competitors of pollinators, and bring no benefit for figs and are detrimental to fig’ fitness. Our data onFicus racemosa in Xishuangbanna showed that the numbers of non-pollinators and the mature syconia without pollinator wasps increase in rainy season, especially in the highly fragmented forest. This might be because of the longer developing time of the syconia and thereby longer oviposition time to non-pollinators in the dry season. The galled flower and the viable seed percentages in dry seasons are also larger than in rainy seasons in both primary forest and fragmented forest, and the development of non-pollinators is mainly at the expense of pollinator wasps. Our results showed that there exists a discriminative seasonal impact of non-pollinators and fragmentation effects on population size of fig’s pollinators. This implies that fig/fig wasp mutualism is more fragile in dry season, and that the critical population size and breeding units of figs in seasonal area might be larger than previously estimated without considering the seasonal change of pollinator population.     

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.     

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。     

寄生垂叶榕的两种非传粉榕小蜂的产卵行为

通过对两种果外产卵非传粉榕小蜂Philotrypesissp.和Sycoscaptersp.产卵行为的详细观察,发现两种小蜂产卵期都集中在榕果发育的间花期,并且只在进过传粉榕小蜂的榕果内产卵。这两种小蜂的产卵行为基本都可以分为寻找产卵位点、刺壁、产卵和回收产卵器等步骤。落在果面上的两种小蜂的繁殖雌蜂都通过触角敲击果面寻找产卵位点。产卵结束后,Philotrypesissp.大多数情况在原位收回产卵针,而Sycoscaptersp.必须向前爬行才能将产卵针从果内收回。为了争夺产卵位点,在同一榕果产卵的Philotrypesissp.繁殖雌蜂之间会进行打斗。而Sycoscaptersp.繁殖雌蜂之间未观察到打斗行为。两种小蜂产卵器长度虽显著长于各自产卵时榕果果壁厚度,但却显著短于其产卵时榕果果壁和子房层的总厚度,说明这两种小蜂采用产卵针直接刺穿小花子房的产卵模式。     

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.     

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.     

西双版纳聚果榕隐头果内小蜂群落结构及种间关系

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

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。     

西双版纳热带雨林对叶榕传粉生物学

研究了西双版纳热带雨林地区雌雄异株植物对叶榕(Ficus hispida L.)的生物学、传粉物候学以及榕小蜂(Ceratosolen solmsi marchali Mayr)的传粉和繁殖行为.研究结果表明:雌雄异株的对叶榕与其他雌雄同株的榕属植物不同,它的种子形成与传粉者有着更为复杂的相互关系.对叶榕一年结隐花果6～8次,结果高峰期4～5次,其中雄性植株仅产生花粉和孕育榕小蜂,而雌性植株(无雄蕊)则需榕小蜂带花粉进入隐花果内,进行传粉授精,使之发育成种子.对叶榕的成熟花粉不能从花药开裂处自行散发出来,必须由榕小蜂采集才能散落.榕小蜂雌蜂羽化、交配后,找到雄花区,用足、触角、口器在推动中采集花粉.雌蜂飞出熟榕果找寻雌株或雄株榕树上的幼嫩隐花果,一般需3～67 min;一部分雌蜂在雄株中寻找幼嫩的隐花果,进去产卵繁殖,另一部分雌蜂则寻找雌株雌花期嫩隐花果进去传粉.雌蜂在雌株榕树的隐花果内传粉时间为15～23 h,在雄株榕树的隐花果内产卵时间为6～9 h.对叶榕小蜂在雌株上进入单个隐花果的数量多少关系到雌花结实率;观察表明,每个隐花果最佳进蜂数为2头;榕小蜂传粉后榕树成熟种子形成率在54.1%～82.5%之间,平均为73.8%;而在雄株上雌蜂进蜂数量则关系到榕小蜂在隐花果内的产卵率,每个隐花果最佳进蜂数为3～4头,产卵率在72.3%～93.8%之间,平均为84.4%.     

西双版纳热带雨林对叶榕传粉生物学(英)

研究了西双版纳热带雨林地区雌雄异株植物对叶榕 (FicushispidaL .)的生物学、传粉物候学以及榕小蜂(CeratosolensolmsimarchaliMayr)的传粉和繁殖行为。研究结果表明 :雌雄异株的对叶榕与其他雌雄同株的榕属植物不同 ,它的种子形成与传粉者有着更为复杂的相互关系。对叶榕一年结隐花果 6～ 8次 ,结果高峰期 4～ 5次 ,其中雄性植株仅产生花粉和孕育榕小蜂 ,而雌性植株 (无雄蕊 )则需榕小蜂带花粉进入隐花果内 ,进行传粉授精 ,使之发育成种子。对叶榕的成熟花粉不能从花药开裂处自行散发出来 ,必须由榕小蜂采集才能散落。榕小蜂雌蜂羽化、交配后 ,找到雄花区 ,用足、触角、口器在推动中采集花粉。雌蜂飞出熟榕果找寻雌株或雄株榕树上的幼嫩隐花果 ,一般需 3～ 6 7min ;一部分雌蜂在雄株中寻找幼嫩的隐花果 ,进去产卵繁殖 ,另一部分雌蜂则寻找雌株雌花期嫩隐花果进去传粉。雌蜂在雌株榕树的隐花果内传粉时间为 15～ 2 3h ,在雄株榕树的隐花果内产卵时间为 6～ 9h。对叶榕小蜂在雌株上进入单个隐花果的数量多少关系到雌花结实率 ;观察表明 ,每个隐花果最佳进蜂数为 2头 ;榕小蜂传粉后榕树成熟种子形成率在 5 4 .1%～ 82 .5 %之间 ,平均为 73.8% ;而在雄株上雌蜂进蜂数量则关系到榕小蜂在隐花果内的产卵率 ,     

Differentiation during fig ontogeny suggests opposing selection by mutualists

Dioecy allows separation of female and male functions and therefore facilitates separate co‐evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower‐stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male (“gall”) figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female (“seed”) figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.     

Evolution of style-length variability in figs and optimization of ovipositor length in their pollinator wasps: A coevolutionary model

Monoecious figs reward their pollinators—agaonid wasps—by allocating a proportion of the flowers for egg laying, and retain the rest for seed production. It has been suggested that these proportions could be regulated by producing short-styled and long-styled flowers such that pollinator wasps could only use the former as their ovipositor does not reach the ovules of the latter. Thus the wasps can lay eggs only in the short-styled flowers and raise their offspring, and the ovules of uninfested, long-styled flowers can develop into seeds. This implied that figs bear dimorphic female flowers, with a bimodal distribution of style length. However, recent studies have shown that style length is distributed normally, with no evidence of bimodality. Therefore the regulation of allocation of flowers to the wasps does not seem to be through the production of two distinct kinds of female flowers. In this article we suggest that two factors govern the proportion of flowers rewarded to the wasps: (i) passive regulation, which is a consequence of the optimization of wasp ovipositor length, and (ii) active regulation, where figs are selected to enhance the variance of style length. We show that these arguments lead to certain predictions about the optimum ovipositor length, the proportion of the flowers available to the wasps, and the coefficient of variation of style length. We also show that data for 18 fig-wasp associations conform well with these predictions. We finally suggest that the regulatory process outlined here can be extended to evolution of style length in dioecious fig species also.     

The style–length of the female florets and their fate in two dioecious species of Xishuangbanna, China

Constraints and evolution are central for the resolution of conflicts between mutualism species and for the stability of mutualisms. Dioecious fig species and their specific pollinators are also in conflict on the use of fig ovaries. Here, our experiments provided some data on the female florets allocation in two dioecious fig trees. The results showed that: (1) there is a bimodal distribution in the style–length of two fig trees’ female florets, moreover, the style–lengths are fairly similar and narrowly distributed in gall figs and more variation seems to occur in seed figs; (2) the styles in seed figs are a little longer than those in gall figs; (3) the pollinator's ovipositor lengths are shorter than the style–lengths in seed figs, but they are very similar to those in gall figs so that pollinators can only lay their eggs into the ovaries of gall figs, but not in seed figs; (4) the stigmas stick together, and the style is curly and flexible in seed syconia of the two fig species studied, so it is very difficult for the pollinators to find suitable ovipositing sites and lay their eggs in seed figs; (5) the variations of style-lengths are bigger in seed figs than gall figs, but they are smaller in dioecious figs than monoecious figs; (6) for Ficus cyrtophylla, about 10% styles are shorter in seed figs than those in gall figs, even shorter than ovipositor. In contrast, about 2% styles in gall figs of Ficus hispida are longer than its corresponding pollinator's ovipositor. In a word, our study suggests that the female floret's fate in these two fig species is mainly dependent on its style–length, but not all. The stigma shape and the floral organization can both also attribute to their fate in the two fig species studied.