Disturbance effects on community structure of Ficus tinctoria fig wasps in Xishuangbanna, China: Implications for the fig/fig wasp mutualism

Abstract  Fig trees are important components of tropical forests, because their fruits are eaten by so many vertebrates, but they depend on pollinating fig wasps to produce mature fruits. Disturbance to habitat structure can have a major impact on insect diversity and composition, potentially reducing fruit yields. We investigated the impact of habitat disturbance on the fig wasp community associated with male figs of Ficus tinctoria in Xishuangbanna, China. The community comprised one pollinator species Liporrhopalum gibbosae and six non-pollinating wasp species: Sycoscapter sp.1, Philotrypesis ravii , Philotrypesis sp.1, Neosycophila omeomorpha , Sycophila sp.1, and Walkerella sp.1. More disturbed areas were characterized by higher temperatures, less shade, and more vehicle noise. The response of the fig wasp community was complex, with no simple relationship between intensity of disturbance and pollinator abundance. However, the sex ratios (proportion of male progeny) of pollinators increased significantly in more disturbed areas. We conclude that potential changes in fig wasp community composition brought about by disturbance, are unpredictable, with unclear consequences for tropical rainforest biodiversity.     

Trade-off between reciprocal mutualists: local resource availability-oriented interaction in fig/fig wasp mutualism

1. The mechanisms that prevent competition (conflict) between the recipient and co-operative actor in co-operative systems remain one of the greatest problems for evolutionary biology. Previous hypotheses suggest that self-restraint, dispersal or spatial constraints can prevent direct competition for local resources or any other common resources, thereby maintaining stable co-operation interactions. In this study, we use the obligate fig-fig-wasp mutualism to examine whether the above mechanisms can maintain stable co-operation sufficiently between figs and fig wasps. 2. Our data on obligate co-operation between figs (Ficus racemosa Linn.) and fig wasps (Ceratoslen fusciceps Mayr) show that the number of viable seeds of figs is positively correlated with the number of pollinator offspring when the number of vacant female flowers is high while the foundress number is low (two foundresses). Meanwhile, they are negatively correlated when the number of vacant female flowers is low and the number of foundresses is increased manually (eight foundresses). The correlation coefficient between viable seeds and wasp offspring (galls) depends on vacant female flower availability. 3. Our data suggest that the interaction between figs and fig wasps is conditional, and that they co-operate when local resource availability is plentiful but are in conflict when local resource availability is limited. The self-restraint, dispersal and spatial heterogeneity previously hypothesized in maintaining stable co-operation cannot sufficiently prevent the symbionts from utilizing more local resources at the expense of the recipients. The conflict, which can disrupt the co-operation interaction, exists after the local resource is saturated with symbionts. The repression of symbiont increase, therefore repressing the utilization of local resources in the conflict period, is crucial in the maintenance and evolution of co-operation.     

Diversification in the use of resources by Idarnes species: bypassing functional constraints in the fig–fig wasp interaction

Mutualisms such as the fig–fig wasp mutualism are generally exploited by parasites. We demonstrate that amongst nonpollinating fig wasps (NPFWs) parasitic on Ficus citrifolia, a species of Idarnes galls flowers and another species feeds on galls induced by other wasps killing their larvae. The galling wasp inserts its ovipositor through the fig wall into the fig cavity. The ovipositor then follows a sinuous path and is introduced through the stigma and style of the flower. The egg is deposited between the integument and nucellus, in the exact location where the pollinating mutualistic wasp would have laid its egg. Gall induction is a complex process. In contrast, the path followed by the ovipositor of the other species is straightforward: attacking a larva within a developed gall poses different constraints. Shifts in feeding regime have occurred repeatedly in NPFWs. Monitoring traits associated with such repeated evolutionary shifts may help understand underlying functional constraints. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 114–122.     

Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism

1. Fig pollinating wasps (Agaonidae) enter Ficus inflorescences (figs), oviposit in some of the flowers, and pollinate in the process. Each larva completes its development within a single flower. In most cases, an inflorescence entered by a wasp will represent its only egg‐laying site. The mechanisms that prevent pollinating wasps from exploiting all the flowers inside a fig are not understood. In this study, hypotheses about flower use by pollinating fig wasps were tested by investigating egg deposition patterns in three species. 2. Either one or three wasps were introduced into figs. The figs were then harvested. Serial sections allowed assessment of the presence or absence of a wasp egg in a sample of flowers in each fig. The overall proportion of flowers with eggs and the spatial distribution of eggs were then compared in single wasp figs and three foundress figs. 3. In all species, the proportion of flowers with a wasp egg increased with foundress number but less than three‐fold. 4. In all species, at least in single foundress figs, flowers near the fig cavity were more likely to receive a wasp egg than were flowers near the fig wall. 5. In two species, when the number of foundresses was multiplied by three, there was an increase in the use of flowers near the fig wall, while in the third species, the increase was spread evenly among flowers. 6. Factors affecting wasp egg deposition patterns and the potential of investigating such patterns for studying the stability of the mutualism are discussed.     

Precision of host sanctions in the fig tree–fig wasp mutualism: consequences for uncooperative symbionts

Host sanctions that reduce the relative fitness of uncooperative symbionts provide a mechanism that can limit cheating and thus stabilise mutualisms over evolutionary timescales. Sanctions have been demonstrated empirically in several mutualisms. However, if multiple individual symbionts interact with each host, the precision with which individual cheating symbionts are targeted by host sanctions is critical to their short‐ and long‐term effectiveness. No previous empirical study has directly addressed this issue. Here, we report the precision of host sanctions in the mutualism between fig trees and their pollinating wasps. Using field experiments and molecular parentage analyses, we show that sanctions in Ficus nymphaeifolia act at the level of entire figs (syconia), not at the level of the individual flowers within. Such fig‐level sanctions allow uncooperative wasps, which do not bring pollen, to avoid sanctions in figs to which other wasps bring pollen. We discuss the relevance of sanction precision to other mutualisms.     

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 .     

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.     

Development of 17 microsatellite markers for Ceratosolen constrictus, the pollinating fig wasp of Ficus fistulosa

The obligate mutualism between figs (Ficus) and fig pollinating wasps (Agaonidae) is regarded as a classic example of mutualism. Seventeen polymorphic microsatellite loci were developed for Ceratosolen constrictus, the pollinating wasp of the dioecious fig Ficus fistulosa. The number of alleles per locus ranged from two to 15 and the observed and expected heterozygosities ranged from 0.040 to 0.846 and from 0.040 to 0.916, respectively. These microsatellite loci offer a powerful tool for evolutionary and population genetic studies in C. constrictus, and gene flow of F. fistulosa.     

The dominant exploiters of the fig/pollinator mutualism vary across continents,but their costs fall consistently on the male reproductive function of figs

1. Fig trees (Moraceae: Ficus) are keystone species, whose ecosystem function relies on an obligate mutualism with wasps (Chalcidoidea: Agaonidae) that enter fig syconia to pollinate. Each female flower produces one seed (fig female reproductive function), unless it also receives a wasp egg, in which case it supports a wasp. Fig male reproductive function requires both male flowers and pollinator offspring, which are the only vectors of fig pollen. 2. The mutualism is exploited by other wasps that lay eggs but provide no pollination service. Most of these non‐pollinating fig wasps (NPFWs) do not enter syconia, but lay eggs through the wall with long ovipositors. Some are gall‐makers, while others are parasitoids or lethal inquilines of other wasps. 3. Ficus is pan‐tropical and contains >750 fig species. However, NPFW communities vary across fig lineages and continents and their effects on the mutualism may also vary. This provides a series of natural experiments to investigate how the costs to a keystone mutualism vary geographically. 4. We made the first detailed study of the costs of NPFWs in a fig (Ficus obliqua G. Forst) from the endemic Australasian section Malvanthera. In contrast to the communities associated with section Americana in the New World, wasps from the subfamily Sycoryctinae (Chalcidoidea: Pteromalidae) dominated this community. 5. These sycoryctine wasps have a negative impact on pollinator offspring numbers, but not on seed production. Consequently, while the NPFW fauna varies greatly at high taxonomic levels across continents, we show that the consistent main effect of locally dominant exploiters of the mutualism is to reduce fig male reproductive function.     

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.     

Spatial patterns of the ant Crematogaster scutellaris in a model ecosystem

1. The spatial arrangement of individuals and populations may have deep influences on all the biotic interactions within a community. 2. The spatial distribution of nests of the ant Crematogaster scutellaris Olivier was analysed in an olive orchard in central Italy. As this species nests inside tree trunks, the regular structure of this simplified ecosystem may help to reduce the confounding effect of habitat heterogeneity on the spatial distribution of nests. In total, 531 trees were mapped and their shape (size and structure of the trunk) recorded. The presence of C. scutellaris nests in each tree was assessed in spring–summer and autumn 2006 and 2007. 3. The number of occupied trees changed in time, from a maximum of 129 (summer 2006) to a minimum of 60 (autumn 2007). Occupancy of tree was related to its shape, with larger trees being more frequently and more steadily occupied than smaller ones. 4. Nests were spatially aggregated, forming well‐defined clusters, but aggregation was not explained by a corresponding clumping of larger trees. Nests belonging to the same cluster were usually not aggressive to each other, whereas aggression was more common between nests belonging to different clusters. The dynamic nature of the system coupled with the clustered distribution of nests, is consistent with a hypothesis of seasonal polydomy, and suggest that whereas some trees are steadily occupied (core) others are opportunistically colonised when new resources are discovered (satellites). 5. Clusters size distribution was shown to follow a truncated power‐law, a finding consistent with the idea that clusters are self‐organised structures dependent on local interactions. These results suggest that spatial self‐organisation in ant colonies may in principle be more common than previously thought, although the mechanisms generating these patterns still need to be clarified.     

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。     

Why mutualist partners vary in quality: mutation–selection balance and incentives to cheat in the fig tree–fig wasp mutualism

Mutualisms between species are ecologically ubiquitous but evolutionarily puzzling. Host discrimination mechanisms that reduce the fitness of uncooperative symbionts can stabilise mutualism against collapse, but also present a paradox – if discrimination is effective, why do uncooperative symbionts persist? Here, we test whether mutations or fitness benefits of cheating best explain the prevalence of uncooperative wasps in the fig tree–fig wasp mutualism. By combining theory with field‐collected data we demonstrate that the proportions of pollen‐free wasps of strongly discriminating hosts are reached with reasonable mutation rates. In contrast, in weakly discriminating hosts, the required mutation rates, assuming a single locus, are untenably high, but the required cheater advantages fall within expected ranges. We propose that when discrimination is weak, uncooperative symbionts proliferate until they reach the equilibrium proportion that balances costs and benefits of cheating. Our results suggest that mechanisms that resolve the paradox of uncooperative symbionts differ among host species.     

蚂蚁-紫胶虫兼性互利关系对蚂蚁群落多样性的影响

为了探讨蚂蚁-紫胶虫兼性互利关系对树冠上蚂蚁群落多样性的影响,作者于2009年12月至2010年5月,采用目光搜寻的方法调查了不同紫胶虫数量样地(样地Ⅰ有效枝条寄生率为60％、样地Ⅱ为30％、样地Ⅲ为10％、样地Ⅳ不放养紫胶虫)中钝叶黄檀(Dalbergia obtusifolia)树冠蚂蚁群落的多样性.结果显示,兼性互利关系能够显著提高树冠蚂蚁群落多度及物种丰富度,改变树冠上蚂蚁的群落结构;由紫胶虫数量高低导致的蜜露产量的多寡对树冠上蚂蚁的多度和群落结构均具有显著影响,但对物种丰富度无显著影响;同时紫胶虫的个体发育阶段也是影响树冠上蚂蚁多度的重要因素.本研究证明,紫胶虫对于提高树冠上蚂蚁的多样性具有显著的正面影响,紫胶林对蚂蚁多样性保护有利.     

垂叶榕隐头果内小蜂群落结构与生境关系的初步研究

垂叶榕(Ficusbenjamina)是一种世界上广泛栽培的绿化树种,但是关于其隐头果内小蜂群落结构的研究国内外很少涉及。我们根据植被覆盖度和干扰程度差异在西双版纳州勐仑镇选择了3块不同的样地,采集垂叶榕隐头果180个,统计其中的榕小蜂种类和数量。结果表明:共鉴定出榕小蜂13种,隶属于膜翅目小蜂总科中的8个属,其中Eupristinakoningsbergeri为传粉榕小蜂,其余12种为非传粉小蜂;3个样地中的小蜂群落多样性指数、丰富度存在显著差异,植被覆盖度高、干扰小的样地内小蜂群落多样性指数、丰富度显著高于其他样地;非传粉小蜂在产卵时更倾向于选择植被覆盖度高、干扰相对小的生境,且非传粉小蜂的存在对传粉榕小蜂的繁殖有着显著的负面影响。     

The ecology and evolution of the New World non-pollinating fig wasp communities

Abstract. We present data on several previously undescribed species from six genera of New World non-pollinating fig wasps. We show that many of these species have a negative effect on the reproductive success of both the pollinator wasps and the host figs. Our results suggest that the two most abundant genera of non-pollinating wasps, the Idarnes and the Critogaster , compete for the same pool of female flowers as the pollinating wasps in the Urostigma and Pharmacosycea figs, respectively. Wasps from the genus Aepocerus induce and develop within large galls, in the Urostigma figs. By draining resources from the fruit these wasps may have a detrimental effect on the production of pollinator wasps and viable seeds. Some of the species investigated are parasitoids of other non-pollinating species. We examine the importance of the various forms of spatial heterogeneity in the parasitism rate that can act to stabilise the host-parasitoid interaction. Finally, we discuss the factors underlying the large variation in the abundance and diversity of the non-pollinating wasps both among and within fruit crops.     

Molecular phylogenies of fig pollinating and non-pollinating wasps and the implications for the origin and evolution of the fig-fig wasp mutualism

Abstract. Figs host three ecologically distinct groups of wasps: pollinators, non-pollinators (parasitic wasps) and parasitoids. Both pollinators and non-pollinators complete their life cycles using fig tissue, while parasitoids appear to attack some groups of non-pollinators. We used nucleotide sequence data to address a series of questions concerning genealogical associations, host specificities and degree of strict-sense co-evolution exhibited by members of these groups. We used the relatively conserved 12S rRNA gene of the mitochondria to estimate high level relationships among pollinator, parasitic and parasitoid taxa by sampling species collected from host figs representing five sections (three subgenera) from Asia, Africa, Europe and Central America. We found that all pollinators formed a clear monophyletic group. However, we could not resolve whether or not all of the non-parasitoid wasps associated with figs (Agaonidae, sensu Bouček) formed a single monophyletic group. Further, we used the more variable COII mitochondrial gene to attempt to determine relationships among closely related species of pollinators within two New World genera. Using sequences from the same gene we estimated the phylogenetic relationships among the parasites collected from the same New World host fig species and compared them with those of the pollinators. At fine taxonomic scale, we found that for both pollinator and parasites, species were generally specific to a given fig host. Moreover, the phylogenies of the non-pollinators are largely congruent with those of the pollinators, suggesting the predominance of strict-sense co-evolution on shared host fig species. The implications of these findings and opportunities for future research are discussed.     

Ant mutualists alter the composition and attack rate of the parasitoid community for the gall wasp Disholcaspis eldoradensis (Cynipidae)

Abstract.  1. The strength or density dependence of pairwise species interactions can depend on the presence or absence of other species, especially potential mutualists.
2. The gall wasp Disholcaspis eldoradensis induces plant galls that secrete a sweet honeydew from their top surfaces while the wasp larvae are active. These galls are actively tended by Argentine ants, which collect the honeydew and drive off parasitoids attempting to attack the gall wasp.
3. When ants were excluded, the total rate of parasitism by seven species of parasitoids increased by 36%, and the rate of gall-wasp emergence decreased by 54%.
4. The total percentage parasitism was affected by gall density when ants were excluded but not when ants were unmanipulated, suggesting a change in parasitoid functional responses due to ant tending.
5. In addition, excluding ants significantly altered the proportions of different parasitoid species that emerged from galls; one parasitoid species increased from 1% to 34%, and another decreased from 46% to 19%.
6. The invasive Argentine ants studied are capable of maintaining the mutualism with the gall wasps that evolved in the presence of different ant species and also act as a selective filter for the local community of generalist parasitoids trying to attack this gall species.