Ficus (Moraceae) and fig wasps (Hymenoptera: Chalcidoidea) in Taiwan

Although Ficus-associated wasp fauna have been extensively researched in Australasia, information on these fauna in Taiwan is not well accessible to scientists worldwide. In this study, we compiled records on the Ficus flora of Taiwan and its associated wasp fauna. Initial agronomic research reports on Ficus were published in Japanese in 1917, followed by reports on applied biochemistry, taxonomy, and phenology in Chinese. On the basis of the phenological knowledge of 15 species of the Ficus flora of Taiwan, recent research has examined the pollinating and nonpollinating agaonid and chalcid wasps (Hymenoptera: Chalcidoidea). Updating records according to the current nomenclature revealed that there are 30 taxa (27 species) of native or naturalized Ficus with an unusually high proportion of dioecious species (78%). Four species were observed to exhibit mutualism with more than one pollinating wasp species, and 18 of the 27 Ficus species were reported with nonpollinating wasp species. The number of nonpollinating wasp species associated with specific Ficus species ranges from zero (F. pumila) to 24 (F. microcarpa). Approximately half of the Taiwanese fig tree species have been studied with basic information on phenology and biology described in peer-reviewed journals or theses. This review provides a solid basis for future in-depth comparative studies. This summary of knowledge will encourage and facilitate continuing research on the pollination dynamics of Ficus and the associated insect fauna in Taiwan.


Introduction
The pantropical genus Ficus (Moraceae) is the most speciose genus of woody plants, comprising 735 species known worldwide (Berg and Corner 2005). Ficus is characterized by their unique inflorescences, called figs, or syconia. Due to their essential role in tropical landscapes and their rich ecological relationships with numerous invertebrates and vertebrates, fig trees may be considered as keystone resources of tropical forests (Shanahan et al. 2001;Harrison 2005). Asia contains a wide diversity of Ficus flora, with 130 known species from Borneo (Berg and Corner 2005), 99 from China (Wu et al. 2003) and only 25 species common to the two areas.
The genus has attracted considerable attention among ecologists because of its obligate mutualism with pollinating wasps (Hymenoptera: Agaonidae: Agaoninae, Kradibiinae, Tetrapusiinae) (Cruaud et al. 2010;Heraty et al. 2013). Fig trees have become an essential model for studies on mutualism (Janzen 1979;Frank 1985), sex ratio theory (Herre 1985;Weiblen 2002), and coevolution processes (Anstett et al. 1997;Cook and Rasplus 2003).  (Kjellberg et al. 2001). In contrast, passive pollination requires no specific behavior: The pollen grains simply stick to the wasp body and fertilize ovules when the pollinating wasps enter a fig. Though one Ficus species is associated with only one pollinating wasp species in most of the cases (Janzen 1979), some Ficus species have long been known to host additional pollinating wasp species (Galil and Eisikowitch 1967;Ramírez 1970;Molbo et al. 2003).
In addition to the pollinating wasp species, most of the Ficus species also host nonpollinating wasp species (Kjellberg et al. 2005). These wasps oviposit from the outside of the figs. The number of nonpollinating wasps (NPFW) species varies greatly between Ficus species (Kerdelhué et al. 2000). Their feeding regimes also vary: Some NPFW species gall the ovules similarly to the pollinating species, and some are parasitoids (Compton and van Noort 1992).
Over the past century, extensive research on various characteristics of the fig flora in Taiwan and its associated fauna has been conducted ( Figure 1). Taiwan and its offshore islands are tropical and subtropical. Recently, 26 native and one introduced Ficus species have been reported (Tzeng 2004, in Chinese with English abstract). The first report on the Ficus genus in Taiwan was written in Japanese and focused on the cultivation of Ficus pumila var. awkeotsang (Takao 1917). The first taxonomic monograph was published in 1934 (Sata 1934), followed 10 years later, by a comparison of the fig flora in Taiwan and in the Philippines (Sata 1944). Later on, several studies addressing the biochemistry of an edible jelly produced from the dried seeds of F. pumila var. awkeotsang (Huang and Chen 1979;Huang et al. 1980;Lin et al. 1989;Liu et al. 1989Liu et al. , 1990 were published. This jelly, locally called "aiyu", is a common ingredient of summer beverages in Taiwan. Taxonomic research on the Ficus genus in Taiwan resumed 45 years after Sata's final publication (Liao 1989), which has been recently updated by Tzeng (2004). The research performed by Tzeng (2004) is exhaustive and provides a clear understanding of the Ficus flora and its distribution around Taiwan.
The phenology of Ficus has been extensively studied (Hu et al. 1986;Ho 1987). Phenological research introduced a physiological point of view to the study of fig ecology. However, common fig-wasp interactions have rarely been reported in Taiwan. We here establish a framework for future work on Taiwan Ficus and its associated wasp fauna by providing an updated list of Ficus species and the associated wasp species in Taiwan. These wasp species include specific pollinators or groups of pollinator species (in a few cases) as well as nonpollinating fig wasps.  1979 1980-84 1985-89 1990-94 1995-99 2000-04 2005-  Each Taiwanese article has been classified under a discipline in which the journal they have been published in. The categories are the ones used in the ISI Web of Knowledge SM . Nevertheless 18 of the 24 cited journals were not referenced by ISI Web of Knowledge SM then they have been categorized according to the journal description. For the journals having more than one category, value has been divided in equal parts. For example, a journal categorized in Forestry and Ecology would have counted as 0.5 in the two categories for this graph.
As part of a previous field study (Bain 2012), we collected figs from various sites throughout a lowland forest habitat on Taiwan as well as on Orchid and Green Islands off the southeast coast of Taiwan.
Several species names from the studies of Liao (1989Liao ( , 1995 and Tzeng (2004) were updated according to the recent taxonomic and nomenclatural knowledge. In the subgenus Urostigma, F. subpisocarpa has been subject to two recent revisions. Berg and Corner (2005) reinstated the species from F. superba var. japonica. Subsequently, by incorporating new observations from Thailand, Berg further divided the species into two subspecies: F. subpisocarpa subsp. pubipoda and F. subpisocarpa subsp. subpisocarpa (Berg 2007). Based on this knowledge, the Taiwanese taxon is F. subpisocarpa subsp. subpisocarpa (hereafter called F. subpisocarpa). Several taxonomic questions for this subgenus group remain unanswered. For example, the taxonomic position of F. benjamina var. bracteata is unclear. In 1983, Yamazaki described F. benjamina var. bracteata from Taiwan for the first time; subsequently, Berg and Corner (2005) assigned it a synonym: F. benjamina. In the studies conducted by Berg and Corner (2005) and Corner (1965), the analyzed F. benjamina var. bracteata samples were not obtained from Taiwan. Our observations from southern Taiwan reveal differences between F. benjamina var. benjamina and F. benjamina var. bracteata (Bain and Tzeng, pers. obs.). Despite these differences, until further research provides a new basis for a decision, we continue to list F. benjamina var. bracteata as a variety according to descriptions provided by Tzeng (2004). In addition, F. religiosa was not listed as a native species in the report of Sata (1934), but as introduced to Taiwan. Nevertheless, because the pollinating wasp species of F. religiosa, Platyscapa quadraticeps, has been observed in Taiwan, we consider F. religiosa a naturalized species (Chen and Chou 1997).
Two previously reported species of the subgenus Pharmacosycea from Taiwan have been reported (F. nervosa subsp. nervosa and F. nervosa subsp. pubinervis) have a debatable taxonomic status. Tzeng (2004) considered the aforementioned species as two distinct species whereas Berg and Corner (2005) listed them as subspecies. Both species are allopatric: F. nervosa subsp. nervosa is distributed in southern Taiwan and F. nervosa subsp. pubinervis is distributed only in Orchid Island (the island, located offshore on the Southeast of Taiwan Island, is also called Lanyu, 22°03'N; 121°32'E) (Tzeng 2004). The fact that they are pollinated by different agaonid wasp species (Table 1) provides additional evidence for distinguishing them as different species. According to pollen, pyrena and leaf morphology evidence (Chuang 2000;Tzeng 2004;Tzeng et al. 2009), F. nervosa subsp. nervosa and F. nervosa subsp. pubinervis are phylogenetically close, yet distinct species. Thus, in this study, we refer to F. nervosa subsp. nervosa and F. nervosa subsp. pubinervis as F. nervosa and F. pubinervis, respectively.
In the subgenus Sycidium, F. tinctoria subsp. swinhoei has been synonymized under F. tinctoria subsp. tinctoria (Berg and Corner 2005). The distribution of the former taxon is limited to southern Taiwan and Orchid Island, whereas F. tinctoria is widely distributed throughout Australasia (Berg and Corner 2005). Moreover, these two subspecies have different pollinators (J-Y Rasplus, pers. obs.). Therefore, on the basis of the study by Tzeng (2004), we continue to list F. tinctoria subsp. swinhoei as separated from F. tinctoria subsp. tinctoria. Ficus tinctoria and F. virgata are two species that require further taxonomic investigation. After solely studying herbarium samples, Berg and Corner (2005) could not clearly distinguish between Taiwanese F. tinctoria and F. virgata. However, according to local field observations, F. virgata can be clearly and unambiguously distinguished from other Ficus species (Liao 1989(Liao , 1995Tzeng 2004). Thus, Taiwanese F. virgata and F. tinctoria subsp. swinhoei are here considered distinct species.
Furthermore, in the subgenus Ficus, F. esquiroliana has been synonymized under F. triloba subsp. triloba (Berg 2007). We support this decision because we found morphologically similar trees in Yunnan, China, and Taiwan (Bain and Tzeng, pers. obs.).

Phenology, ecology, and biology of figs and fig wasps
Ficus ecology, particularly the interspecific mutualism between Ficus and fig wasps, began to receive attention in the early 1990s. Since then, several studies on this interspecific mutualism have been conducted (see Kjellberg et al. 2005 for review). Prior knowledge of phenology is essential for studies on mutualism. Ficus trees differ from most of other tree species: the figs they produced host their mutualistic pollinators. Thus the Ficus reproductive phenology is not constant as other tree species (Bain et al. 2014a) that are, for example, bound to seasons (spring bloom). Numerous phenological studies of Ficus trees have been conducted in Taiwan. The subgenus Urostigma includes monoecious taxa, whereas all other subgenera in Taiwan are dioecious, having separate male and female trees. The latter produce only seeds whereas the figs of the former produce both pollen and pollen dispersers (pollinating fig wasp). Among the six subgenera in Taiwan, phenological data on all subgenera, except for the subgenus Pharmacosycea, have been collected. Finally, among the 30 Ficus taxa, only half of them have seen their phenology examined. The most studied taxon is F. erecta var. beecheyana, which has been described in six reports. In Taiwan, most phenological research has been undertaken as a part of graduate thesis work, and, therefore, is found mainly in Chinese language theses and remains unpublished in peer-reviewed journals. Nevertheless, data from this phenological research provides a strong basis for further study.
The monoecious F. microcarpa has been a study subject of four theses in Taiwan (Hsieh 1992;Chen 1994;Chen 2001;Yang 2011). Ficus microcarpa is the most studied species worldwide because of its common occurrence in cities and campuses, and its invasive status in several continents (Beardsley 1998 (Hsieh 1992;Yang et al. 2013) and some years, no figs were observed on the trees (Chen et al. 2004). In all of the aforementioned studies, the fig yield was the lowest in the winter season. Moreover, the number of crops per year varied greatly from zero to four. In addition, fig bearing in the F. microcarpa population was highly asynchronous as no distinct seasonal or annual pattern was identified in any of the studies. However, the genetic diversity seems to determinate the phenological diversity of the F. microcarpa trees (Yang et al. 2014).
In addition to F. erecta, numerous dioecious species have been surveyed to determine fig production patterns (Tzeng et al. 2003(Tzeng et al. , 2005a2006b;Bain et al. 2014a). In northern Taiwan, dioecious species were found to have similar phenological patterns across the genus. First, male trees consistently began bearing figs at the beginning of spring every year; female trees began their fig productiona few weeks later. Second, a noticeable second production peak occurred in September and October. Third, rarer winter figs have a longer maturation period. Similar to the F. microcarpa population, other fig tree populations produced figs asynchronously. Although there was a peak production period, the production of figs was not simultaneous. The production of some trees can be delayed for a few weeks (Yao 1998;Bain et al. 2014a). After the spring crop, the populations bore a low number of figs until autumn, when the male trees again preceded the female trees with a production few weeks earlier. Finally, in winter, the trees were barest throughout Taiwan (Ho 1991;Chen 1998;Yao 1998;Chang 2003;Huang 2007;Ho et al. 2011;Chen 2012;Chiu 2012;Bain et al. 2014a).
Nevertheless, some inter-and intraspecific variations were observed. The duration of the spring crop and the The pollinating wasps are noted with a superscripted p whereas the wasp species not yet observed in Taiwan but reported elsewhere for these fig taxa are noted with an asterisk (*). The last column displays the references of the description, the name modifications of the given species and/or the observations on these species.
proportion of male trees producing figs between the two crop peaks differed between species. Also the synchrony between male and female tree peaks of fig production varied greatly. Throughout most of the island of Taiwan, Ficus tree populations were found to crop during a long period in spring. A considerable proportion of male trees produce figs throughout the year (Ho 1991;Chen 1998;Yao 1998;Chang 2003;Huang 2007;Ho et al. 2011;Chen 2012;Chiu 2012;Bain et al. 2014a). At low altitudes in the extreme north, male trees have shorter spring crops than those in the south. The percentage of male trees producing figs between the two peak seasons is lower in the north than that in the south of Taiwan (Bain et al. 2014a). Finally, at higher altitudes, the production peaks of male trees during spring are extremely short and are synchronous within a population, with few male trees bearing figs between the two seasonal peaks (Wu 1996;Tzeng et al. 2003Tzeng et al. , 2006bBain et al. 2014a).
The general island-wide pattern suggests that phenology has been shaped by environmental factors but constrained by mutualism: In Taiwan, biochemical studies on Ficus have centered on F. pumila var. awkeotsang, which produces an edible jelly, and the two varieties (var. pumila and var. awkeotsang) with morphological features have drawn research attention. The two varieties are morphologically close Tzeng 2004). Because of the economic interest in the edible jelly produced from the dried seeds of F. pumila var. awkeotsang, the biochemical and nutritional composition of the jelly has been established (Huang and Chen 1979). Later, the compounds responsible for the jelly have been identified ). The vegetative reproduction characteristics of this species have also been reported ).

Pollinating fig wasps (Hymenoptera: Agaonidae)
According to the phylogenetic nomenclature of Cruaud et al. (2010), we have noticed two changes in the former Taiwanese fig wasp nomenclature. First, the wasps belonging to the genus Blastophaga subgenus Valisia have been listed under the new genus Valisia. Therefore, pollinators of F. triloba and F. ruficaulis are now known as Valisia esquirolianae and V. filippina. Second, the genus Liporrhopalum has been synonymized under the genus Krabidia. Thus, all Agaonidae wasps pollinating the Ficus species from the subgenus Sycidium have been moved to the genus Krabidia (Table 1).
The study by Chen and Chou (1997) was one of the few studies that attempted to describe all pollinating wasp species from Taiwan. In their study, 24 species (seven newly described species) from eight genera were observed in Taiwan (Chen and Chou 1997). Their study still observed the 1:1 species specificity rule between fig trees and pollinating wasps. However, recently, a genetic study on the pollinating wasp species of Ficus septica concluded that it has three pollinator species with different distributions in Taiwan (Lin et al. 2011). One species was strictly limited to Orchid Island and the extreme south of Taiwan. The second species was limited only to Orchid Island and was considered rare. The third species was widely observed throughout Taiwan. Furthermore, genetic results showed weak differentiation among the fig wasp populations on the island, suggesting that the gene flow is high within the F. septica population in Taiwan (Lin et al. 2008). This trend was previously observed in other Ficus species, fig wasps, and other locations (Compton et al. 2000;Harrison and Rasplus 2006;Ahmed et al. 2009;Kobmoo et al. 2010). In addition, Wiebesia pumilae and Wiebesia sp., the pollinators of F. pumila var. pumila and F. pumila var. awkeotsang, were morphologically and genetically distinct (Lee 2009;Jiang 2011). These two wasp species have been observed in the figs of both varieties of F. pumila (Lu et al. 1987;Jiang 2011).
In addition to taxonomic studies, since the late 1990s, studies on the population dynamics of pollinators associated with Ficus phenology have been conducted (Chen et al. 2004). The most recent phenological study on F. microcarpa in Taipei City provided data on the size of the pollinating wasp population (Yang et al. 2013). The population size varied greatly during a year. During winter, the pollination rate of figs was low whereas in summer the size of the pollinating wasp population was great and the number of foundresses could reach 19 in one single fig. These data have been used to estimate the total population of female wasps living around the studied group of F. microcarpa trees in Taipei (Yang et al. 2013). Yang et al. (2013) showed marked variation in the dynamics of the foundress population size from 0 to 40,000 within one season for the 29 studied trees. Although there was a winter trough in the number of pollinators, the pollinator population could exhibit a high recovery rate in the spring season and still reach the peak during the summer-fall season.

Nonpollinating fig wasps (Hymenoptera)
Nonpollinating fig wasps (NPFWs) are categorized in three trophic categories: the gallers that induce a gall from the plant tissue, their larva feeds on the growing gall tissue; the parasitoids that lay their eggs on other larvae which feed on the host larva; and the kleptoparasites that kill galler larvae to feed on the induced gall tissues.
The NPFWs belong to three families (Eurytomidae, Ormyridae, and Torymidae) and seven subfamilies (Colotrechninae, Epichrysomallinae, Otitesellinae, Pteromalinae, Sycoecinae, Sycophaginae, and Sycoryctinae). The recent molecular phylogeny of the superfamily Chalcidoidea (Munro et al. 2011), which includes all of the aforementioned groups, has shown that four groups are monophyletic (Agaonidae, Epichrysomallinae, Pteromalinae, and Sycophaginae), whereas the other groups are paraphyletic. In addition, phylogenies of the subfamilies Sycophaginae  and Sycoryctinae (Segar et al. 2012) have been established. As we previously modified the names of pollinating wasp species, we here display the names of the Taiwanese species on the basis of the recent updates Segar et al. 2012). First, the genus Apocryptophagus forms a single taxon with the genus Sycophaga, and consequently, it has been considered a junior synonym of Sycophaga and then synonymized under the genus Sycophaga . Therefore, the former Apocryptophagus wasps are currently named Sycophaga. Second, the Sycoscapter wasps once formed a group that was synonymized by Bouček (1988), all of the former names were reinstated by Segar et al. (2012): Sycoscapter, Sycoryctes, Arachonia, Sycoscapteridea, and Sycorycteridea. Nevertheless, some Sycoscapter wasps listed in Table 1 and cited from other studies may be still grouped under Sycoscapter sensu Bouček (1988).
The first and only taxonomic publication on Taiwanese NPFW addressed the F. microcarpa wasp community (Chen et al. 1999). Studies examining NPFWs have been ecological studies, such as a study of the feeding regime (galler or parasitoid) of some Sycoscapter larvae (Tzeng et al. 2008). Conversely, the ecology of Taiwanese NPFW has been thoroughly studied. First, regarding F. microcarpa, to determine whether some NPFW are galler species (gallers produce plant galls that contain a growth of tissue to feed their larvae), the fig ostiole (i.e., the only entry of the fig) was sealed to avoid the entry of the pollinating wasps . Without the agaonid wasps, two NPFW species laid eggs inside the fig ovules from the outside: Odontofroggatia sp. (Epichrysomallinae) and Walkerella kurandensis (Otitesellinae). Chen et al. (2001) showed that these two species were undoubtedly gallers. Second, regarding F. formosana, the exclusion of the two Sycoscapter species showed that they had a negative effect on the pollinating wasp population (Tzeng et al. 2008). In another study, Tzeng et al. (2014) showed that the fig wall thickness is a factor affecting the NPFW oviposition. Moreover, the timing of oviposition of these NPFW clearly indicated that the wasps were parasitoids.
Recent observations have shown that the NPFW species occurring on F. pedunculosa var. mearnsii belong to the genus Apocrypta (Bain, unpublished data). This genus was reported to feed on the larvae of pollinating wasps from the genus Ceratosolen (Ulenberg 1985), all pollinators of the fig subgenus Sycomorus (Rønsted et al. 2005). However, F. pedunculosa var. mearnsii belongs to the subgenus Ficus and is pollinated by Blastophaga wasps, but not by Ceratosolen wasps. Therefore, this observation is unexpected and should be further confirmed by studying more trees and by covering a larger area.
Finally, NPFWs are the prey of numerous ant species (Formicidae). Such ant species have been observed foraging inside figs of F. tinctoria subsp. swinhoei, F. septica, F. benguetensis, and F. subpisocarpa (Bain et al. 2014b). Ants enlarged the wasp exit hole and entered inside the figs to prey on the remaining fig wasps. On F. subpisocarpa, ants live more closely on the tree nesting inside the living branches of the tree . In these nests, numerous bodies of nonpollinating and pollinating wasps have been collected. Nevertheless, the foraging and hunting behaviors of the ants seem to be species dependent as wasp bodies have not been found in the nests of every ant species .

Conclusion
This paper presents and organizes the abundant and previously difficult-to-access research data on Ficus species and fig wasps in Taiwan. This paper compiles data from internationally accessible English language journal articles as well as local theses and dissertations, mostly in Chinese. In addition, this paper includes data from recent research conducted by the authors of this paper and presents an elaborate picture of the insect com-