microcarpa,A Brief Introduction To The Biology Of dried fig
The distribution of 830 species of Ficus are shown in the green area of above map. Figs occur throughout the Old and New World tropics, extending north to the eastern Mediterranean and China. By far the majority of species are evergreen. The common fig (Ficus carica) is deciduous and grows in colder climates of Turkey and the Middle East. With the exception of the Hawaiian Islands, practically every tropical continent and major island group has one or more species of indigenous fig. In fact, the tiny island of Barro Colorado in the Panama Canal Zone, with an area of only six square miles, has 17 native species. Virtually every species of fig has its own unique species of “in house” wasp pollinator. The wasps are housed throughout the year inside the fig’s hollow syconia, in one of nature’s most remarkable symbiotic relationaships between a tree and an insect. The symbiotic wasps undoubtedly play a major role in the ability of different fig species to grow in the same locality, a phenomenon known as “species packing.”
In the late 1960s, many of the old brick buildings on the campus of Palomar College were covered with creeping fig (Ficus pumila), giving the campus a beautiful ivy-league appearance resembling the Engish ivy (Hedera helix) that covers walls and buildings of universities in the eastern United States. I began studying figs at that time, and after 40 years of teaching botany classes, I have concluded that the figs are the most remarkable trees on earth. The Plant List of Kew and Missoutri Botanical Garden (2011) gives 830 accepted species of Ficus, and they all have their own in-house pollinator wasp. Most species are evergreen and occur in rain forests throughout the tropics. They are a major factor in tropical ecosystems, providing sweet fruits for numerous animals, including parrots, hornbills, toucans and monkeys. Fruit-eating bats commonly disperse the seeds in their excrement, and seedlings often start out as epiphytes on branches high in the rain-soaked canopy. The common edible fig (F. carica) is deciduous and extends north into temperate regions of Europe and the Middle East. The many uses of figs by people is legendary, and there is good evidence that the common fig was one of the earliest cultivated trees. Depending on the reference, there are an estimated 400+ cultivated varieties of the common fig.
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The creeping fig (Ficus pumila) of eastern Asia. There are two distinct types of stem growth: Young, juvenile branches and older, mature branches. The juvenile branches with smaller leaves (top) produce aerial roots that adhere to concrete, stucco, masonry and even glass windows. Without pruning, a single plant can envelop a four-story building. The syconium is lined with all long-style female flowers. Without pollen-bearing male plants and fig wasps, no seeds can be produced and this plant must be propagated by cuttings. In its native habitat there are also male plants (caprifigs) with male flowers and wasp-bearing female flowers. When I began teaching at Palomar College in the late 1960s, this fig covered many of the old brick buildings. The campus truly had an “ivy-league” appearance, except our “ivy” was the creeping fig. The new growth had to be constantly trimmed around windows and doors, and eventually all the plants were removed by the gardening staff.
Creeping fig (Ficus pumila): Close-up view of the aerial roots (red arrow) that develop at the nodes on juvenile branches. The aerial roots secrete a clear, gummy latex that works like rubber cement. The roots adhere to concrete, masonry and glass. This remarkable adhesive was first described in detail by Charles Darwin in his book The Movements and Habits of Climbing Plants (1876). Older, mature branches with larger leaves produce flower-bearing syconia. This species is commonly planted in southern California to cover the monotanous concrete walls of buildings and freeways. In fact, it was been crossed with the edible fig (F. carica) to produce a hybrid vine (F. x pumila-carica). Unfortunately, the hybrid produces inedible syconia and lacks the adhesive aerial root pads. The hybrid is a sprawling vine that can grow on fences but cannot cling to vertical concrete walls like its F. pumila parent (see next image).
Ficus x pumila-carica: A hybrid between the creeping fig (Ficus pumila) and the common edible fig (F. carica). It has leaves and syconia intermediate between the parents; however, the syconia are basically inedible compared with F. carica. In addition, the hybrid lacks the adhesive aerial roots of F. pumila.
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All figs rely on tiny symbiotic wasps for their pollination. Minute male and female fig wasps are borne inside hollow, fleshy, flower-bearing structures called syconia. The syconium is what most people associate with the tasty fruit of a fig, but technically it is not a true fruit. The syconium is lined on the inside with hundreds of tiny male and female flowers. The flowers are greatly reduced and do not have petals. Male flowers consist of pollen-bearing anthers. Female flowers are of two types: Long-style, seed-bearing flowers and short-style flowers that bear fig wasps instead of seeds. Wasp eggs are not laid in the ovaries of long-style flowers because the wasp’s ovipositor cannot reach the ovary.
- Close-up view of a male and female fig wasp (Pleistodontes imperialis) that inhabits the syconia of the Australian rustyleaf fig (Ficus rubiginosa). The slender ovipositor on female wasp is too short to penetrate the ovary of long-style flowers; therefore she does not lay eggs in these flowers. The smaller, wingless male has large mandibles and a greatly reduced body which has two primary purposes: (1) Inseminating the female and (2) Chewing exit tunnels through the syconium wall through which the females escape. The “eye” of an ordinary sewing needle is shown for a size comparison. These wasps were collected from trees growing by the old Life Science building. The biology students were always amazed when I brought them into my laboratory classes.
- A non-pollinator “bogus” fig wasp collected from the syconium of the Baja California wild fig (Ficus palmeri, or possibly Ficus brandegeei). The ovipositor is much longer than the symbiotic pollinator wasp. In fact, some non-pollinator wasps can penetrate the entire syconium wall from the outside. Non-pollinators can also lay eggs in long-style fig flowers reserved for fig seeds. Consequently, no seeds are produced in these flowers. In addition, these “bogus” fig wasps do not pollinate fig flowers. Although they do not benefit the fig tree, non-pollinator wasps of the families Torymidae and Eurytomidae are common inhabitants of New World monoecious fig syconia. Their coexistence with natural fig pollinator wasps is a complex and perplexing coevolutionary problem in fig biology.
Fig species have one or more pollinator wasps in the family Agaonidae that enter their syconia through a small opening called an ostiole to pollinate the female flowers inside. Although pollinator wasps are often host specific, one pollinator can have more than one host (J.M. Cook and J.-Y. Rasplus, 2003). In addition, the syconium may contain one or more non-pollinating wasps in a different wasp families. Like the pollinator wasps, the nonpollinators have flattened heads and bodies, and are perfectly adapted to squeeze between the ostiolar bracts of receptive syconia. This is yet another example of convergent evolution. Without the pollinator wasps transferring pollen from one syconium to another, the female flowers inside would not get pollinated and no seeds would be produced (a catastrophe for the fig tree). In the common edible fig (Ficus carica), the female wasp gets covered with pollen as she exits the male caprifig. In many tropical fig species, the wasp packs her pollen baskets (corbiculae) on the underside of her thorax before leaving the syconium. When she enters another receptive syconium, she transfers her load of pollen to the female flowers inside. I have observed this latter scenario many times on rustyleaf figs on campus. Unfortunately, most of these trees were cut down to make room for new buildings. Hopefully, some of these wasps have made their way to the Arboretum.
A 34 million-year-old fossil fig wasp from the Eocene was dicovered in limestone on the Isle of Wight, England (Stephen Compton et al. 2010). It was originally thought to be a tiny winged ant, but was later confirmed to be a female fig wasp because of the pair of pollen baskets (corbiculae) on the underside of its thorax. The corbiculae of this wasp named Ponera minuta even contained Ficus pollen. The previous record for ancient fig wasps was 23 million-year-old Dominican Republic amber from the Miocene. DNA phylogenetic analysis indicates that the fig and fig wasp relationship may extend back more than 65 million years ago to the Cretaceous Period. The Isle of Wight fig wasp is relatively unchanged compared with present-day fig wasps of the family Agaonidae. “No innovations in the relationship are discernible for the last tens of millions of years.” According to Nefdt and Compton (1996) short-style female flowers in moneous figs have longer styles than those in male figs of dioecius species. The shorter ovipositor of Ponera minuta indicates that its symbiotic host was dioecious, an advanced reproductive pattern in fig evolution.
Fossil leaves embedded in 60 million-year-old limestone from the Fort Union Formation near Glendive, Montana have tentatively been identified as Ficus. Fossil fig syconia named Ficus ceratops from the 70 million-year-old Hell Creek Formation in this area have been clearly shown to be a different species, possibly an extinct palm. See Section 17 on this page: Fossil Fig Syconia in Wyoming and Montana.
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Life cycle of the common fig (Ficus carica). Style length is genetically determined and it is vital that syconia on seed-bearing female trees have styles longer than the female wasp’s ovipositor. Unable to reach the ovaries of these flowers, she does not lay eggs (oviposit). Therefore, a seed develops inside the ovary rather than a hungry wasp larva. She can only oviposit in the short-style female flowers on “male” trees called caprifigs. Caprifig trees produce pollen and the crucial pollinator wasps (Blastophaga psenes). In some common figs termed “caducous” or early deciduous, the immature female syconium drops from the tree if the flowers inside are not pollinated. There are many cultivated “parthenocarpic” varities of the common fig in which the syconia develop on female trees wthout wasp pollination (caprification). The ripe syconia are fleshy and edible; however, the numerous ovaries (drupelets) inside are hollow and seedless.
- Some Definitions Used In Fig Biology
Style Length-Ovipositor Length Hypothesis: This refers to oviposition through style of female flower by pollinator wasp. Wasp ovipositor can penetrate ovary of short-style flower where egg is deposited. Ovipositor is too short to penetrate ovary of long-style flower. Consequently, wasp larvae occupy ovaries of short-style flowers while seeds develop in ovaries of long-style flowers. This mechanism limits seed predation in dioecious figs, but may not hold true in most monoecious figs.
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Hypotheses For Limiting Seed Predation In Monoecious Figs:
Stigma morphology controlling preferential oviposition.
Aborting syconia with too many parasitized seeds.
Limiting number of pollen-bearing wasps through ostiole.
More ovaries in syconium than wasp can oviposit in.
Short life span of pollen-bearing female wasps (foundresses).
Gall Flower = Short-style Female Flower: Oviposition and the presence of a wasp larva initiates the development of endosperm tissue that the larva feeds on. Since pollination is not required, the developing wasp-bearing ovary is called a gall. This relationship is clearly seen in the ovaries of Ficus sycomorus inhabited by the nonpollinator wasp Sycophaga sycomori. It is also seen in the overwintering mamme crop of F. carica caprifigs where developing wasp larvae feed on endosperm tissue from unpollinated flowers in the previous mammoni crop. According to some fig biologists, since the normal course of events is to abort unpollinated syconia in caducous figs, the entire syconium could be viewed as a gall occupied by nonpollinator wasps. [Some fig biologists also state that the short-style flower is pollinated and the larva feeds on the endosperm of developing seed.] According to Storey (1977) the term “gall flower” is a misomer because it is fully capable of producing normal seed-bearing drupelets if pollinated, and in this respect are no different from long-style flowers.
Gall Flowers In Figs
Foundress: Gravid, pollen-bearing female pollinator wasp that enters ostiole of specific syconium during receptive stage.
Parthenocarpy: Development of the ovary of a flower without pollination and fertilization. In figs, this refers to the hollow, seedless druplets (cenocarps). In figs the outer syconium also develops.
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Stimulative Parthenocarpy: Development of the drupelet by the oviposition and habitation of wasp larva. Since the egg and embryo sac is destroyed in the process, the nutritive nucellar and endosperm tissue that the larva feeds on develops without fertilization. The resulting druplet is a hollow psenocarp bearing a wasp larva.
Vegetative Parthenocarpy: Development of drupelets and syconium without pollination, fertilization or any known stimulus. The druplets are hollow cenocarps. This is characteristic of common figs with the persistent gene. These figs do not require pollination by a fig wasp (caprification); however, they are fully capable of producing seed-bearing drupelets if they are pollinated and fertilized.
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Parthenogenesis: Development of the egg into an embryo without fertilization. This also applies to the development of endosperm tissue without fertilization of the two polar nuclei within the binucleate endosperm mother cell. Parthenogenetic endosperm tissue in figs has the same chromosome number as sporophtye tissue (2n = 26) according to Saleeb (1965).
Apomixis: Parthenogenesis & Agamospermy
Syconium: An inside-out inflorescence composed of a hollow, fleshy structure (peduncular tissue) lined on the inside with hundreds of tiny unisexual, apetalous flowers. Some authors state that it is composed of receptacle tissue, but Storey (1977) states that this is incorrect. Some authors refer to the syconium as a compound or multiple fruit because it contains many ripened ovaries derivied from many separate flowers. The actual fruits of a fig are the one-seeded drupelets that form inside wasp-pollinated syconia.
Drupelet: The actual fruit from the ovary of a long-style female flower, composed of a sclerified endocarp surrounding the seed. It is erroneously called an “achene.” An empty druplet which develops parthenocarpically (without fertilization) is called a Cenocarp. A wasp-bearing drupe in the caprifig is called a Psenocarp.
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Protogynous: Female flowers are receptive before male flowers mature and shed pollen. This strategy favors cross pollination and is typical of monoecious fig syconia and “male” syconia of dioecious figs.
Caprification: Pollination of a female fig (Ficus carica) by fig wasps in order to produce mature seed-bearing syconia. Without pollination, Smyrna-type (caducous) syconia will fall from the tree without ripening.
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Monoecious: Fig species with pollen-bearing male flowers, short-style female flowers and long-style female flowers in the same syconia. This includes about half of the world’s fig species, the other half being dioecious with separate male and female trees. Measurements of styles and pollinator ovipositors show that most ovules in most monoecious species are within the wasp’s reach (Herre, andér and Macado, 2008). This significant revelation indicates that other mechanisms are involved in the determination of seed-bearing and wasp-bearing ovaries. This is quite different from Ficus carica and other dioecious species. Monoecious figs are considered to be the ancestral breeding system, dating back at least to late Cretaceous (70 million years ago) to the time of T-Rex. Again, it is extremely difficult to generalize about fig biology because of all the exceptions.
Gynodioecious: Fig species with male and female trees in the population. Male trees (caprifigs) bear “male” syconia containing pollen-bearing male flowers and short-style female flowers. The ovaries of short-style female flowers often contain a male or female wasp larva if eggs were oviposited inside them. Female trees only bear female syconia containing seed-bearing long-style female flowers and no male flowers. About half the world’s 830 fig species are gynodioecious, the other half being monoecious with male flowers, short-style and long-style female flowers in the same syconium (i.e. without separate male and female trees).
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Pollen Basket (Pollen Pocket) = Corbicula: A specially-adapted cavity often surrounded by fringe of hairs on underside of thorax or base of leg on female wasps where pollen is purposely deposited before exiting the syconium of monoecious and gynodioecious figs.
Coxal Comb: A specially-adapted fringe of hairs on the fore coxae (base of front legs) on female wasps. It is used to actively (purposely) gather pollen from within the syconium and store it in thoracic pockets (pollen pockets). According to Cook, et al. 2004, the presence of coxal combs always indicate active (purposive) pollination behavior, whereas pollen pockets provide a good but imperfect index. Active pollination includes serveral identifiable components: Wasps must collect pollen from anthers, place it into pockets, and deposit it onto receptive flowers. To accomplish this they require coxal combs and pollen pockets. The following paragraph from Cook, et al (2004) illustrates the complexity of pollination behavior, especially Pleistodontes froggatti in the Moreton Bay fig (Ficus macrophylla):
“Kjellberg et al. (2001) observed pollen deposition behaviour for several species from various fig wasp genera and identified a morphological trait (presence of coxal combs) that always indicated active pollination. This trait is easy to observe and allows inference of behaviour for a much wider set of species than can be observed in the act of pollination. The presence of pollen pockets also generally indicates active pollination, but there are exceptions involving passive species in a genus that is primarily active (Kjellberg et al., 2001). The genus Pleistodontes contains the only species highlighted as a possible exception to the striking general pattern of fig pollinator coadaptation. Ficus macrophylla Desf. ex Pers. has a high anther/ovule ratio, typical of a passively pollinated fig. However, its pollinator, Pleistodontes froggatti Mayr, although lacking coxal combs (suggesting passive pollination), has pollen pockets that can contain concentrated pollen (suggesting active pollination). On balance, this species has been considered an active pollinator in two previous studies (Kjellberg et al., 2001; Jousselin et al., 2003).”
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A deceased female fig wasp (Pleistodontes imperialis) extracted from the ostiole of Ficus rubiginosa. Note the coxal comb at the base of front leg that it used to actively gather pollen from syconium and store it in ventral thoracic pocket (pollen pocket). Inset (left): SEM from Kjellberg, F., Jousselin, E., Bronstein, J.L., Patel, A., Yokoyama, J., and J.-Y. Rasplus. 2001. “Pollination Mode in Fig Wasps: The Predictive Power of Correlated Traits.” Proceedings of the Royal Society of London 268: 1113-1121.
Syconium of Moreton Bay fig (Ficus macrocarpa) in Palomar College Arboretum. Palomar College horticulturist Tony Rangel grew viable seeds from this tree, so I suspected that the pollinator wasp (Pleistodontes froggatti) must be present.
Unlike the similar P. imperialis of rustyleaf figs (F. rubiginosa), P. froggatti does not have a coxal comb at the base of its front legs. According to Cook, J.M. et al. (2004), the lack coxal combs indicates passive rather than active (purposive) pollination; however, they also state that “pollen pockets provide a good but imperfect index.” In Table 1 of their article they state that pollination by P. froggatti is passive. Prior to my discovery of P. froggatti in the Moreton Bay fig at Palomar College (December 2011), the only fig wasps I have documented on campus are P. imperialis on rustyleaf figs and Eupristina verticillata on the Indian laurel fig (Ficus microcarpa).
Pleistodontes froggatti from Moreton Bay fig syconium in Palomar College Arboretum.
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Eupristina (Parapristina) verticillata from Indian laurel fig (Ficus microcarpa) syconia on Palomar College campus. One wasp is squeezing through an exit tunnel cut by male wasps (white arrow). Another Fig/Fig Wasp Discrepancy: J.T. Otero and J.D. Ackerman (2002) statistically analyzed the style length of native F. citrifolia and introduced F. microcarpa in Puerto Rico. They found no correlation between style length and seed predation in syconia of these trees: “Neither Ficus species showed significant differences in style length between flowers with wasps and flowers with seeds, as expected under the short-ovipositor-length hypothesis.”
It is interesting to speculate on how these symbiotic wasp species were introduced at Palomar College. Were wasp-bearing syconia already present on the original plantings, or were wasps carried here by the wind from trees in neighboring cities? The Moreton Bay fig is native to eastern Australia where it grows in the rain forest and often starts out as an epiphytic vine that develops into a strangler fig. Eventually it shades out and kills its host, becoming a massive tree with a buttressed trunk and huge spreading surface roots. In Hawaii and northern New Zealand it has become naturalized because of the introduction of its pollinator wasp (Pleistodontes froggatti). In Hawaii the wasp was deliberately introduced in 1921. In New Zealand it was first recorded in 1993, having apparently arrived by long-distance dispersal from Australia, a 3,000 km (1900 mile) journey. According to R.O. Gardner and J.W. Early (1996), adult female wasps usually live 2-3 days; there are an average of 21 days over the course of a year during which the wasps could make this trip in 1-3 days on air currents. Fig wasps have been caught in light traps aboard ships up to 99 km (60 miles) offshore in the Pacific (J.C. Harrell and E. Holzapfel, 1966). Ahmed, at al. (2009) reported pollen transfer by the African fig wasp Ceratostolen arabicus between known host trees of Ficus sycomorus separated by a distance of 160 km (100 miles). Based on these records for long distance dispersal, reaching Palomar College in San Marcos from known wasp-bearing trees in coastal San Diego County is certainly plausible. Once in the vicinity of host trees, they are attracted to the correct syconia by mixtures of species-specific chemical attractants, including volatile terpenoids. For example, receptive syconia of F. hispida release blends of three fragrant monoterpenes, including linalool (major constituent), limonene and pinene (C. Chen and Q. Song, 2008).
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A single large monoecious fig tree or gynodioecious “male” tree produces several crops of syconia per year. Depending on the species, one crop may consist of hundreds or even thousands of syconia, each bearing a hundred or more pollinator wasps. A large tree, such as the Moreton Bay fig could theoretically release thousands of pollinator wasps into the wind. In fact, during wasp exodus season in Balboa Park, hundreds of fig wasps from nearby trees collect in windows at the San Diego Natural History Museum!
The introduction of symbiotic fig wasps poses a serious problem of invasive strangler figs in tropical regions because of the prolific production of syconia and viable seeds. According to Jennifer Possley, Field Biologist at Fairchild Tropical Botanic Garden, five species of strangler and banyan figs are naturalized in southern Florida, including Ficus altissima, F. benghalensis, F. benjamina, F. microcarpa and F. religiosa. Throughout Key West, seeds of the Indian laurel fig (F. microcarpa) germinate readily in cracks and crevices of old buildings, gradually sending a weblike mass of aerial roots down the walls to the ground. Some residents of the Coral Gables area consider the Asiatic banyan-type figs to be a nuisance and potential menace. The massive, spreading roots of these enormous trees buckle pavement and concrete swimming pools, plug drainage and sewer lines, and pose a serious threat to underground utilities. In other parts of the world alien figs can also invade native rain forest and other plant communities. It should also be noted here that southern Florida and the Caribbean region also have native strangler figs, including F. aurea and F. citrifolia.
Naturalized figs in the Florida Keys. Strangler figs and banyans need viable seeds and a moist climate to be naturalized. Viable seeds require pollinator wasps in their syconia.
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