Phenological Adaptations in Ficus tikoua Exhibit Convergence with Unrelated Extra-Tropical Fig Trees

Flowering phenology is central to the ecology and evolution of most flowering plants. In highly-specific nursery pollination systems, such as that involving fig trees (Ficus species) and fig wasps (Agaonidae), any mismatch in timing has serious consequences because the plants must balance seed production with maintenance of their pollinator populations. Most fig trees are found in tropical or subtropical habitats, but the dioecious Chinese Ficus tikoua has a more northerly distribution. We monitored how its fruiting phenology has adapted in response to a highly seasonal environment. Male trees (where fig wasps reproduce) had one to three crops annually, whereas many seed-producing female trees produced only one fig crop. The timing of release of Ceratosolen fig wasps from male figs in late May and June was synchronized with the presence of receptive figs on female trees, at a time when there were few receptive figs on male trees, thereby ensuring seed set while allowing remnant pollinator populations to persist. F. tikoua phenology has converged with those of other (unrelated) northern Ficus species, but there are differences. Unlike F. carica in Europe, all F. tikoua male figs contain male flowers, and unlike F. pumila in China, but like F. carica, it is the second annual generation of adult wasps that pollinate female figs. The phenologies of all three temperate fig trees generate annual bottlenecks in the size of pollinator populations and for female F. tikoua also a shortage of fig wasps that results in many figs failing to be pollinated.     

A comparison of growth and reproduction, under laboratory conditions, of males and females of a dioecious fig tree

The interaction between Ficus spp. (Moraceae) and their pollinating wasps (Chalcidoidae: Agaonidae) is a highly co-evolved mutualism. Approximately half of all fig species are monoecious and produce a mixture of wasps and seeds within the same fig. In functionally dioecious fig trees male and female functions are separate. Figs on male trees produce wasps and pollen, whereas figs borne on female plants produce only seeds. Dioecious fig phenology provides an excellent opportunity to investigate the effect of sexual specialization on the obligate fig?Cfig wasp interaction and the non-pollinators associated with the system. Here we describe laboratory studies of phenological variation between two sexes in terms of vegetative growth and fig production in a dioecious fig tree Ficus montana. We also describe reproductive output in terms of wasp production in males and seeds in females. Intrasexual asynchrony was observed for the plants, with synchrony between the sexes with year-round production of figs. Male plants grew more rapidly, but leaf phenology was very similar. Crop sizes and development times were the same for males and females. Seasonal effects were strong for leaf phenology and fig initiation, but had a very limited effect on fig composition. The results show that the phenological differences described for other dioecious figs do not apply to all species.     

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

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

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.     

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.     

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

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.     

Phenological patterns of <Emphasis Type="Italic">Ficus citrifolia</Emphasis> (Moraceae) in a seasonal humid-subtropical region in Southern Brazil

Year-round flowering is widely reported in fig trees and is necessary for the survival of their short-living, specialized Agaonid pollinators. However, seasonality in both fig and leaf production has been noted in almost all published phenological studies. We have addressed the following questions in the present study: (1) Are reproductive and vegetative phenologies seasonal and, consequently, related to climate? (2) Does Ficus citrifolia produce ripe figs year round? (3) Is the fig development related to climate? And, (4) Are reproductive and vegetative phenologies independent? By investigating these questions with a F. citrifolia population over a two-year period, at the southern edge of the tropical region in Brazil, we detected phenological seasonality that was significantly correlated with climate. Our findings can be summarized as follows: (1) Trees became deciduous during the cold and dry months; (2) The flowering onset was asynchronous among individuals, but with moderate concentration during the hot and rainy months; (3) There was a correlation between the onset of flowering and vegetative phenology, with significantly higher crop initiations in individuals with full-leaf canopy; (4) Fig developmental time was longer in cold months; and (5) Ripe fig production occurred year-round and was not correlated with climate. Our results suggest that there are strong selection pressures that maintain the year-round flowering phenology in figs, for we have observed little seasonality in the phenology of such species despite the strong seasonality in the environment.     

Phenology of Ficus variegata in a seasonal wet tropical forest at Cape Tribulation, Australia

Abstract. We studied the phenology of 198 mature trees of the dioecious fig Ficus variegata Blume (Moraceae) in a seasonally wet tropical rain forest at Cape Tribulation, Australia, from March 1988 to February 1993. Leaf production was highly seasonal and correlated with rainfall. Trees were annually deciduous, with a pronounced leaf drop and a pulse of new growth during the August-September drought. At the population level, figs were produced continually throughout the study but there were pronounced annual cycles in fig abundance. Figs were least abundant during the early dry period (June-September) and most abundant from the late dry season (October-November) through the wet season (December-April). The annual peak in reproduction actually reflected two staggered peaks arising from gender differences in fig phenology. In this dioecious species, female and male trees initiated their maximal fig crops at different times and flowering was to some extent synchronized within sexes. Fig production in the female (seed-producing) trees was typically confined to the wet season. Male (wasp-producing) trees were less synchronized than female trees but reached a peak level of fig production in the months prior to the onset of female fig production. Male trees were also more likely to produce figs continually. Asynchrony among male fig crops during the dry season could maintain the pollinator population under adverse conditions through within- and among-tree wasp transfers.     

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.     

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.     

Evidence for intersexual chemical mimicry in a dioecious plant

The dioecious Mediterranean fig, Ficus carica, displays a unique phenology in which males sometimes bloom synchronously with females (in summer), and sometimes not (in spring). Ficus carica is engaged in an obligatory mutualism with a specific pollinating wasp, which reproduces only within figs, localising them by their specific scents. We show that scents emitted by male figs show seasonal variation within individual trees. Scents of summer male figs resemble those of the co-flowering females, and are different from those of the same male trees in spring, when female figs are absent. These differences hold even if only compounds electrophysiologically active for pollinators are considered. The similar scents of summer males and females may explain why the rewardless females are still pollinated. These results offer a tractable model for future studies of intersexual chemical mimicry in mutualistic pollination interactions.     

Few figs for frugivores: Riparian fig trees in Zimbabwe may not be a dry season keystone resource

Most plants flower and fruit at times of year when probabilities of pollination and seedling establishment are high. Fig trees (Ficus spp.) are often considered as keystone resources for vertebrate frugivores, in part because of year-round fig production. This unusual fruiting phenology results in the maintenance of fig wasp populations, but in seasonal environments this means fruiting occurs during periods when the chances of seedling establishment are low. Under these circumstances, selection is expected to favour any individuals that reduce or eliminate fruiting at these times. Here, we describe a large-scale survey of the extent of dry season fruiting by three riparian Ficus species in Gonarezhou National Park, Zimbabwe. Few trees of two monoecious species, F. sycomorus and F. abutilifolia, had figs, and most crops of F. sycomorus were far smaller than the trees were capable of producing. Large stands of the dioecious F. capreifolia were present, but fig densities were low and no mature female (seed containing) figs were recorded. Even though fig trees may have been the only species bearing fruit, the consequences of the low investment in reproduction by the three Ficus species were clear—there were too few figs for a landscape-scale keystone role.     

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.     

鸡嗉子榕隐头果雌花期特征对传粉榕小蜂选择的影响

为了探讨榕树隐头果的发育期、性别、大小等外部特征对传粉榕小蜂选择的影响,采取人为控制雌花期的方法,对鸡嗉子榕(Ficus sermicordata)及其传粉榕小蜂(Ceratosolen gravelyi)的选择行为进行研究。结果表明,在隐头花序发育到雌花期后,如果阻止传粉小蜂进入,隐头果会继续生长。直径较小的雌果和雄果的进蜂量较多,且在雌雄果同时存在时,小蜂仍然会选择进入雌果,但进蜂量显著低于雄果。小蜂优先选择进入雌花期前期的隐头花序,雌雄果皆有此特点。对于相同发育期的隐头果,果径和进蜂量呈正相关关系,说明对于相同发育期的隐头果,小蜂更倾向于进入较大的隐头果。因此,真正控制小蜂行为的是隐头花序所处的发育期,以及不同发育期所产生的化学挥发物,而非隐头果直径大小。这为进一步研究榕-蜂系统的稳定机制提供依据。     

Adaptive phenology of Ficus subpisocarpa and Ficus caulocarpa in Taipei,Taiwan

Insect pollination is the main strategy used by Angiosperm plants to transport pollen to another individual. The interaction between entomophilous plants and their pollinators is often mutualistic, with many species pairs being interdependent. In obligate pollination mutualism, the plant relies on its partner for pollination, whereas the pollen vector relies on plant resources. In the mutualism between Ficus (Moraceae) and the fig wasps (Hymenoptera, Agaonidae), the plant provides oviposition sites to its exclusive pollinator, which has an extremely short lifespan (a maximum lifespan of few days). This study examined how fig trees maintain their associated pollinator populations by conducting a 45-month phenological survey of 27 and 64 trees belonging to the species Ficus caulocarpa and F. subpisocarpa in Taipei, Taiwan. The observations indicated that the trees produce figs year-round with no clear seasonal pattern, and are not affected by meteorological factors. On average, about 30% of the trees of both species were bearing figs during the survey. The duration of the fig development was longer during the winter-spring period than during the summer-fall period. The trees displayed strong asynchrony among trees in the population but each crop was synchronous within a tree. However, after wasp emergence, crops lost their synchrony with part of the figs ripening within few days whereas some figs only ripened eight weeks later for F. subpisocarpa and four weeks later for F. caulocarpa. This study also discusses the implications of fig frugivory and mutualism.     

The reproductive success of Ficus altissima and its pollinator in a strongly seasonal environment: Xishuangbanna, Southwestern China

Fig trees (Ficus spp.) are of great ecological significance, producing fruits that are fed on by more birds and mammals than any other plants in the tropics. They are pollinated by host-specific pollinator fig wasps (Hymenoptera, Agaonidae), and their fruit phenology and reproductive success are, therefore, modulated by symbiotic fig wasps. However, there are few studies focusing on the variation of Ficus reproductive success in strongly seasonal environments. We examined the phenology and reproductive success of Ficus altissima growing in a highly seasonal climate towards the northern limit of the range of fig trees in Xishuangbanna, China. Leaf production occurred at irregular intervals throughout the year, with new leaves and syconia initiated together, producing between three and seven crops over a 3-year period. Syconia were produced in synchronous crops with asynchrony between trees. The syconia produced more seeds than pollinators, and those syconia with more seeds also produced more pollinators. Reproductive success (measured as the number of seeds and pollen-carrying agaonid females produced by each syconium) varied greatly between seasons. It was highest for crops that matured during the cooler, relatively dry periods from February to March and October to November, and was lowest during the summer months from April to August. This variation corresponded to small differences in the number of flowers in the syconia, but was mainly driven by large seasonal differences in the relative abundance of non-pollinating fig wasps.     

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

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

CAUSES AND CONSEQUENCES OF WITHIN-TREE PHENOLOGICAL PATTERNS IN THE FLORIDA STRANGLING FIG,FICUS AUREA (MORACEAE)

The obligate pollinators of figs (Ficus, Moraceae), species-specific agaonid wasps, benefit figs only by transporting pollen between trees; larvae are seed predators. But given the high risk of mortality in flight between trees, adult wasps should prefer to pollinate and oviposit within inflorescences (syconia) at the same tree at which they developed. Flowering within individuals is tightly synchronous in most species, while different trees flower out of phase with each other, suggesting that fig phenology has evolved to assure outcrossing. However, some fig species show distinct within-tree flowering asynchrony. It has been suggested that such asynchrony is an adaptation by which figs in seasonal environments can reduce pollinator mortality, by permitting wasps to persist on individual trees at times when flight would be impossible. We have evaluated and rejected the validity of this Seasonality Hypothesis for the Florida strangling fig, Ficus aurea, near its northern range limit. Crops of individual trees were most, not least, synchronous during the coldest, driest months of 2 years. Maximum asynchrony occurred in seasons that were probably most favorable for wasp transit between trees. However, temporal overlap of the phenological stages that permit wasps to remain on their natal trees was always very rare, implying that consecutive cohorts of developing syconia may be spaced in time to limit this occurrence. We suggest alternative costs and benefits for these phenological traits, as well as the proximate mechanisms that might produce them.