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.     

Molecular phylogenies of figs and their pollinator wasps

Abstract. We collected and analysed nucleotide sequence and protein electrophoretic data in order to estimate phylogenies of figs and fig-pollinating wasps at several taxonomic scales. The relatively conserved chloroplast gene coding rbCl allowed the estimation of the taxonomic position of Ficus relative to other genera within the Moraceae. Further, in conjunction with chloroplast tRNA spacer genes, rbcL sequences allowed the partial resolution of the phylogenetic associations of fig species from different parts of the world with representatives from all the recognized subgenera of Ficus . The phylogeny of the corresponding wasp species that pollinate most of those taxa was estimated using mitochondrial COI-COII and 12S ribosomal genes. At a fine scale, the phylogenies of species within two subgenera of figs growing in Panama ( Urostigma , and Pharmacosycea) were estimated by using protein electrophoretic data. The phylogeny of the corresponding pollinator wasp species was estimated using COII sequence data. Although we need to extend the taxa sampled and augment the molecular database, the host and pollinator phylogenies show a high degree of congruence and the results support the predominance of strict-sense co-evolution between figs and their pollinator wasps at both global and fine scales.     

垂叶榕上16种榕小蜂的种群动态

传粉榕小蜂和榕树的互利共生是传粉昆虫与植物间协同进化的典范。在榕果(榕树的隐头状花序)内,还生活着多种非传粉榕小蜂。这些生活在密闭榕果内由传粉榕小蜂和非传粉榕小蜂组成的群落对研究群落生态学有很大价值。然而,对生存在单一榕树的榕果内的所有榕小蜂的种群动态了解很少,特别是缺少相对长期的连续数据。通过野外近3a观察和采样,研究了垂叶榕榕小蜂群落结构和榕小蜂的种群动态。共记录榕小蜂16种;各种榕小蜂根据发生规律可分为常见种和偶见种,Eupristina koningsbergeri,Philotrypesis sp.1,Philotrypesis sp.4,Philotrypesis sp.5,Sycoscapter sp.1,Walkerella benjamini,Walkerella sp.1,Sycophila sp.2,Sycobia sp.2为常见种;Sycobia sp.1,Acophila sp.1,Sycophila sp.1,Ormyrus sp.1等为偶见种。每种榕小蜂在单果上的数量随季节呈波动变化,季节对榕小蜂群落的多样性和均匀性无显著影响。除了传粉榕小蜂外,Sycoscapter sp.1也是优势种类之一。传粉榕小蜂的数量与非传粉榕小蜂总数间呈显著负相关。传粉榕小蜂与非传粉榕小蜂几乎都呈负相关,而与Walkerella sp.1在数量上呈显著正相关。Sycobia sp.2与Sycophila sp.2在同一瘿中出现,数量上呈显著正相关。但其它非传粉榕小蜂种类在数量上的相关性较为复杂,可能是造成各种榕小蜂数量波动的一个原因。     

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.     

Host-specificity and coevolution among pollinating and nonpollinating New World fig wasps

Figs (Ficus spp., Moraceae) and their pollinating wasps (Hymenoptera, Agaonidae, Chalcidoidea) constitute a classic example of an obligate plant-pollinator mutualism, and have become an ideal system for addressing questions on coevolution, speciation, and the maintenance of mutualisms. In addition to pollinating wasps, figs host several types of nonpollinating, parasitic wasps from a diverse array of Chalcid subfamilies with varied natural histories and ecological strategies (e.g. competitors, gallers, and parasitoids). Although a few recent studies have addressed the question of codivergence between specific genera of pollinating and nonpollinating fig wasps, no study has addressed the history of divergence of a fig wasp community comprised of multiple genera of wasps associated with a large number of sympatric fig hosts. Here, we conduct phylogenetic analyses of mitochondrial DNA sequences (COI) using 411 individuals from 69 pollinating and nonpollinating fig wasp species to assess relationships within and between five genera of fig wasps (Pegoscapus, Idarnes, Heterandrium, Aepocerus, Physothorax) associated with 17 species of New World Urostigma figs from section Americana. We show that host-switching and multiple wasp species per host are ubiquitous across Neotropical nonpollinating wasp genera. In spite of these findings, cophylogenetic analyses (TREEMAP 1.0, TREEMAP 2.02beta, and parafit) reveal evidence of codivergence among fig wasps from different ecological guilds. Our findings further challenge the classical notion of strict-sense coevolution between figs and their associated wasps, and mirror conclusions from detailed molecular studies of other mutualisms that have revealed common patterns of diffuse coevolution and asymmetric specialization among the participants.     

Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig–fig wasp interaction

Like other mutualisms, pollination mutualisms attract parasites, as well as opportunistic and specialist predators of the pollinators and parasites. These associated species influence the evolutionary dynamics of pairwise mutualisms. Predatory ants are frequent associates of pollination mutualisms, but their effects on the complex interactions between plants, pollinators and parasites have not yet been clearly established, even in the case of the well-described obligate interaction between figs and fig wasps. We attempted to quantify such effects for ants associated with three fig species, two dioecious ( Ficus condensa [Bruneï], F . carica [France]) and one monoecious ( F . racemosa [India]). In all these cases, ant presence on a fig tree strongly reduced the number of parasitic wasps on the figs. Experimental exclusion of ants resulted in an increase in the number of non-pollinating fig wasps on F . condensa and F . racemosa . Experimental ant supplementation led to a decrease in the number of non-pollinating fig wasps on F . carica . Moreover, on F . condensa , the level of reduction of the number of parasitic wasps depended on the number and identity of the ants. On F . carica , non-pollinating fig wasps even avoided trees occupied by the dominant predatory ant. The consistency of the effect of ants in these three cases, representing a geographically, ecologically, and taxonomically broad sample of figs, argues for the generality of the effect we observed. Because reduction of parasitism benefits the pollinator, ants may be considered as indirect mutualists of plants and pollinators in the network of complex interactions supported by fig trees.     

Restructuring of a mutualism following introduction of Australian fig trees and pollinating wasps to Europe and the USA

Figs and fig-pollinating wasps are obligate mutualists that require each other to complete sexual reproduction. However, landscapers can establish populations of fig trees outside their native ranges by propagation through exported seeds, seedlings or cuttings. Once mature, these trees could be colonized by pollinating wasps and/or various non-pollinating wasps that also develop in figs. In recent decades, the Australian endemic Ficus rubiginosa has been planted widely in the Mediterranean region and in parts of the USA. Observation of ripe fruit production suggested that a pollination mutualism has been re-established by pollinating wasps colonizing trees in the plant’s introduced range. We therefore used sampling of pollinators from mainland Spain, Tenerife and California (USA) and molecular studies to characterize the restructured mutualism and compare it with the native range. In the native range, the plant is pollinated by five wasp species that form the Pleistodontes imperialis complex. However, all wasps in the introduced ranges belonged to just one of these species (P. imperialis sp. 1). Moreover, their mtDNA diversity was close to zero and the sequences clearly link them with the native southern population of this species. None of the?>?20 non-pollinating wasp species from the native range were found in the introduced ranges. In summary, the restructured mutualism has been dramatically simplified, lacking all non-pollinating wasps and all but one pollinator species from the native range. Moreover, the one pollinator species to establish successfully shows a drastic reduction in genetic diversity relative to its source population.     

Effects of within-tree flowering asynchrony on the dynamics of seed and wasp production in an Australian fig species

Abstract. Within-tree flowering asynchrony in figs, which may allow pollinating wasps to avoid the risks of dispersal in inclement conditions, has been predicted as a trait to be favoured in highly seasonal environments. Comparisons of such asynchronous figs with better-known species that exhibit within-tree synchrony might also be expected to reveal differences in the outcome of the conflict between pollinator wasp and fig seed production, and the dynamics of non-pollinating wasps. This paper presents data on wasp and seed production in Ficus rubiginosa Desf. ex Vent., an asynchronous species that occurs in the highly seasonal environment of south-eastern Australia. In contrast to recent studies of figs showing within-tree flowering synchrony, syconium size was the main determinant of wasp and seed production in F. rubiginosa . Non-pollinating wasps were highly prevalent but occurred in low numbers and appeared to have relatively little impact on pollinator wasp or fig seed production. Data on flower positions revealed that non-pollinating wasps occurred almost exclusively in the outer layer of flowers, while pollinators were more abundant in the inner flower layer, which may represent an area of enemy-free space. The ratio of seeds to female pollinator wasps, an index of fig sex allocation, was more seed-biased than in several New World fig species that exhibit within-tree synchrony. This last result supports the idea that within-tree fruiting asynchrony permits a degree of self-pollination in F. rubiginosa .     

歪叶榕非传粉小蜂的繁殖策略及其对榕-蜂共生系统的影响

2004年8月至2005年8月在西双版纳热带植物园内,通过广泛收集歪叶榕榕小蜂标本、非传粉小蜂产卵行为学观察和阻止传粉者入果等实验方法,研究了我国西双版纳热带雨林下的一种榕树——歪叶榕Ficus cyrtophylla的榕小蜂群落组成结构、非传粉小蜂的繁殖策略以及它们对榕-蜂共生系统的影响。结果表明,歪叶榕中除了具有唯一传粉榕小蜂Blastophag sp.以外,还具有3种非传粉小蜂Platyneura sp.、Philotrypesis sp.和Sycoscapter sp.。在歪叶榕榕小蜂群落中,传粉榕小蜂占整个群落总数的92.21%,是群落的最主要组成者;主要的非传粉小蜂是Sycoscaptersp.,占5.78%; 其次是Philotrypesissp.,占1.84%,而Platyneurasp.仅占群落总数的0.17%。歪叶榕中的非传粉小蜂通过各自产卵时间和食性分化的策略来利用榕果中的资源繁殖后代。非传粉小蜂寄生使传粉榕小蜂的总数和其雌蜂数量都显著地降低,但是对传粉小蜂雄蜂数量没有显著影响,从而导致传粉榕小蜂的雄性性比显著地增加。这说明非传粉小蜂在选择寄居宿主时具有明显的倾向性,而且更多地将卵产于含有雌性传粉小蜂的瘿花之中。因此,非传粉小蜂通过减少雌性传粉小蜂的数量而降低了榕树的雄性适合度,从而在一定程度上对榕 蜂共生系统的稳定存在和发展产生了负面影响。     

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.     

Fig wasp dispersal and the stability of a keystone plant resource in Borneo

The stability of interactions in remaining rainforest fragments is an issue of considerable concern for conservation. Figs are a pre-eminent tropical keystone resource because of their importance for wildlife, but are dependent on tiny (1-2 mm) species-specific wasps for pollination. To investigate fig wasp dispersal I trapped insects at various heights (5-75 m) in an isolated fragment (ca. 4500 ha) of Bornean rain forest. Fig wasps constituted the majority of captures above the canopy (pollinators 47%, non-pollinators 5%). However, genera were not evenly represented. There were 50% more species of monoecious fig pollinator than there were host species in the fragment, indicating some must have arrived from forests with different assemblages of figs at least 30 km away. Dioecious fig pollinators were poorly represented suggesting more limited dispersal, which could account for higher endemism and vulnerability to catastrophic disturbance in these figs. Diurnal activity and flight height also varied among genera. Most non-pollinating fig wasps were very rare.     

Quantitative tests of interaction between pollinating and non-pollinating fig wasps on dioecious Ficus hispida

Abstract.  1. The interaction between Ficus species and their pollinating wasps (Agaonidae) represents a striking example of a mutualism. Figs also shelter numerous non-pollinating chalcids that exploit the fig–pollinator mutualism.
2. Previous studies showed a weak negative correlation between numbers of pollinating and non-pollinating adults emerging from the same fruit. Little is known about the patterns and intensities of interactions between fig wasps. In the Xishuangbanna tropical rainforests of China, the dioecious Ficus hispida L. is pollinated by Ceratosolen solmsi marchali Mayr and is also exploited by the non-pollinators Philotrypesis pilosa Mayr, Philotrypesis sp., and Apocrypta bakeri Joseph. Here, the interaction of pollinator and non-pollinators on F. hispida is studied quantitatively.
3. The exact time of oviposition was determined for each species of fig wasp. Based on observational and experimental work it is suggested that (i) the relationship between pollinator and non-pollinators is a positive one, and that the genus Philotrypesis appears to have no significant impact on the pollinator population, whereas Apocrypta has a significant effect on both Philotrypesis and Ceratosolen ; (ii) gall numbers do not always increase with increasing number of foundresses, but developmental mortality of larvae correlates positively with the number of foundresses; and (iii) there is a positive correlation between non-pollinator numbers and their rates of parasitism, but the three species of non-pollinators differed in their rates of parasitism and show different effects on pollinator production.
4. The rates of parasitism when combined with the coexistent percentage and developmental mortality, underpin the way non-pollinating fig wasps successfully exploit and coexist stably in a fig–pollinator mutualism.     

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。     

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.     

Non-pollinating wasps distort the sex ratio of pollinating fig wasps

In fig wasps, mating occurs among the offspring of one or a few foundress mothers within the fig, from which the mated females disperse to found new broods. Under these conditions, males will compete with each other for mating, and such local mate competition can result in female-biased sex ratios. In addition to pollinating wasps, non-pollinating wasp species are also associated with figs and develop in flower ovaries or parasitize the larvae of primary galling wasps. While studying the fig wasp Pegoscapus tonduzi , which pollinates Ficus citrifolia in Brazil, we examined the influence of non-pollinating fig wasps on the sex ratio of species that pollinate F. citrifolia to determine whether the presence of non-pollinating wasps resulted in a distorted sex ratio. There was a positive relationship between the sex ratio of P. tonduzi and the number of non-pollinating wasps that was independent of the number of foundresses and brood size. In addition, the number of non-pollinating wasps correlated negatively with the number of pollinating females, but was not significantly related to the number of pollinating males. This finding suggested that non-pollinating wasps had a direct effect in distorting the sex ratio of P. tonduzi broods. Our results indicate that the secondary sex ratio may not precisely reflect the primary sex ratio when there is a high infestation of non-pollinating fig wasps.     

Relative investment in egg load and poison sac in fig wasps: Implications for physiological mechanisms underlying seed and wasp production in figs

Fig pollinating wasps and most non-pollinator wasps apply secretions from their poison sacs into oviposited flowers that appear necessary to the formation of the galls that their developing offspring consume. Thus, both eggs and poison sac secretions appear to be essential for wasp reproduction, but the relative investment in each is unknown. We measured relative investment in poison sac and egg production in pollinating and non-pollinating wasps associated with seven species of monoecious Panamanian figs representing both active and passive pollination syndromes. We then collected similar data for four fig hosts in China, where some wasp species in the genus Eupristina have lost the ability to pollinate (“cheaters”). All wasps examined possessed large poison sacs, and we found a strong positive correlation between poison sac size and absolute egg production. In the Panamanian species, the relative poison sac to egg investment was highest in the externally ovipositing non-pollinator wasps, followed by active pollinators, then by passive pollinators. Further, pollinator wasps of fig species with demonstrated host sanctions against “cheating” wasps showed higher investment in the poison sac than wasps of species without sanctions. In the Chinese samples, relative investment in the poison sac was indistinguishable between pollinators and “cheaters” associated with the same fig species. We suggest that higher relative investment in poison sac across fig wasp species reflects higher relative difficulty in initiating formation of galls and subsequently obtaining resources from the fig. We discuss the implications for the stability of the fig–wasp mutualism, and for the ability of non-pollinators to exploit this mutualism.     

Ecology of a fig ant–plant

Mutualistic interactions are embedded in networks of interactions that affect the benefits accruing to the mutualistic partners. Figs and their pollinating wasps are engaged in an obligate mutualism in which the fig is dependent on the fig pollinator for pollination services and the pollinator is dependent on fig ovules for brood sites. This mutualism is exploited by non-pollinating fig wasps that utilise the same ovules, but do not provide a pollination service. Most non-pollinating wasps oviposit from outside the inflorescence (syconium), where they are vulnerable to ant predation. Ficus schwarzii is exposed to high densities of non-pollinating wasps, but Philidris sp. ants patrolling the syconia prevent them from ovipositing. Philidris rarely catch wasps, but the fig encourages the patrolling by providing a reward through extra-floral nectaries on the surface of syconia. Moreover, the reward is apparently only produced during the phase when parasitoids are ovipositing. An ant-exclusion experiment demonstrated that, in the absence of ants, syconia were heavily attacked and many aborted as a consequence. Philidris was normally rare on the figs during the receptive phase or at the time of day when wasp offspring are emerging, so predation on pollinators was limited. However, Myrmicaria sp. ants, which only occurred on three trees, preyed substantially on pollinating as well as non-pollinating wasps. F. schwarzii occurs in small clusters of trees and has an exceptionally rapid crop turnover. These factors appear to promote high densities of non-pollinating wasps and, as a consequence, may have led to both a high incidence of ants on trees and increased selective pressure on fig traits that increase the payoffs of the fig–ant interaction for the fig. The fig receives no direct benefit from the reward it provides, but protects pollinating wasps that will disperse its pollen.     

Only pollinator fig wasps have males that collaborate to release their females from figs of an Asian fig tree

Male insects rarely collaborate with each other, but pollinator fig wasps (Hymenoptera: Agaonidae) are said to be an exception. Immature fig wasps feed on galled ovules located inside figs, the inflorescences of Ficus species (Moraceae). After mating, adult pollinator males chew communal exit-holes that allow mated females (which are often also their siblings) to escape. Figs also support non-pollinating fig wasps (NPFWs), some of which produce exit-holes independently. We determined whether collaboration between pollinator males (Kradibia tentacularis from Ficus montana) was necessary for the release of their females, and used the relationship between male numbers and likelihood of success to measure the extent of cooperation during exit-hole production. These attributes were then compared with those of an NPFW (Sycoscapter sp.) from the same host plant. Pollinators were more abundant than NPFW, but their more female-biased sex ratio meant male pollinator densities were only slightly higher. Individual males of both species could produce an exit-hole. Single males of the NPFW were just as successful as single male pollinators, but only male pollinators cooperated effectively, becoming more successful as their numbers increased. The lack of cooperation among NPFW may be linked to their earlier period of intense inter-male aggression.     

聚果榕两种非传粉小蜂产卵与果实脱落的关系

在聚果榕与其传粉榕小蜂Ceratosolen fusciceps组成的互利共生系统中,与传粉榕小蜂共存的还有榕树的寄生性小蜂Platyneura testacea和Platyneura mayri.这些寄生性小蜂由于不能给榕树带来任何收益而只是利用榕树的种子或与传粉小蜂竞争植物的雌花资源,因而可能导致榕树与榕小蜂之间合作系统的崩溃.植物果实的脱落机制普遍被认为是维持系统稳定的关键因素之一.然而,定量实验和野外观测发现P. mayri产卵并不会引起果实脱落,只有P. testacea产卵会使果实大量脱落.通过对3株样树进行比较发现:当产卵时的P. testacea数量越多时,它产生的瘿花数就越多,榕果发生脱落的比例越高.P. testacea的过度产卵是导致榕果选择性脱落的主要原因.结果表明:脱落机制并不能完全阻止非传粉小蜂的寄生,榕树只能选择性地脱落掉先于传粉小蜂产卵的榕果.这也同时表明维持榕树与榕小蜂互利共存的机制不仅仅只有榕果的脱落机制,可能还存在其它未被发现的机制.     

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.