Topocentric Pollination: Passive mode where pollen is trapped in intersegmental folds (grooves) as wasps exit the syconium, and is rubbed off as wasps move about on stigmatic platform (synstigma) of new receptive syconium.
Ethodynamic Pollination: Deliberate (purposive) pollen transfer from pollen baskets (corbiculae) to dense stigmas of receptive female flowers (synstigma).
The male & female wasps in above image are Blastophaga psenes from Ficus carica. The exit tunnels were made by male Pleistodontes imperialis in the syconium wall of the rustyleaf fig (F. rubiginosa). Blastophaga males do not cut the exit tunnels through the syconium wall. Instead, the females exit through the ostiole, becoming dusted by pollen from male flowers near the ostiolar end of the syconium.
According to Carole Kerdelhué and Jean-Yves Rasplus (Oikos Vol. 77: 163-166, 1996), monoecious syconia of Ficus sur contain long-style and short-style female flowers densely packed together in a layer that lines the inner cavity of the syconium. Although the styles all form a relatively continuous stigmatic layer called a synstigma (i.e. all stigmas in the same plane) within the syconium, the ovaries may be deep or shallow relative to the synstigma depending on the length of their flower stalks (pedicels). Generally, the deep-seated ovaries (on short pedicels) with long styles each contain a seed, while the shallow ovaries (on long pedicels) with short styles each contain a wasp larva. A pollinator wasp walking on this “bed” of styles (synstigma) can insert her ovipositor down the short style and easily penetrate the ovary where she lays an egg. The deep-seated, long-style ovaries are out of reach for her ovipositor (style longer than her ovipositor), and consequently these ovaries develop seeds rather than wasp larvae. Because of intermediate style lengths (between long and short) and different ovary heights due to the length of flower stalks (pedicels), the ovary position of female flowers in monoecious fig syconia often forms a stratification. There are at least 4 different ovary layers occupied by beneficial (pollinator) and non-beneficial and/or harmful non-pollinator wasps. These layers are shown by different colors in the following illustration according to their position (depth) from the stigmatic surface (synstigma) within the syconial cavity.
According to Kerdelhué and Rasplus (1996), dioecious figs may have evolved from monoecious ancestral fig species due to selection pressure by non-pollinator fig wasps. Although these non-pollinator wasps belong to the same Order Chalcidoidea as pollinators, many of them belong to different families. They do not benefit the fig and may even be harmful–especially when they compete with and/or parasitize the beneficial pollinator wasps.
Heterostyly and four ovary layers (stratification) within the syconium of a monoecious fig (Ficus sur). (1) Yellow: The most shallow ovaries (near surface) with shortest styles which typically contain a pollinator wasp larva; (2) Green and (3) Red: Slightly deeper ovaries that typically contain non-pollinator wasp larvae; (4) Black: The deepest ovaries with longest styles that typically bear mature seeds.
Exception to above illustration: Measurements of styles and pollinator ovipositors show that most
ovules in most monoecious species are within the wasp’s reach (Herre, Andér and Machado, 2008).
Longitudinal section through a caprifig profichi syconium in June showing male flowers.
Left: Caprifig with developing mammoni crop of syconia. Right: F. carica cultivar ‘Calimyrna’ with developing 2nd or main crop of syconia. Both of these syconia form in early summer on new growth. They mature in late summer to early fall. The immature Calimyrna main crop is pollinated (caprified) in June by wasps carrying pollen from the previous profichi crop of caprifigs. Without caprification this main crop will drop from the tree, a trait known as caducous. The mature mammoni syconia will release another generation of female fig wasps who will enter the 3rd or mamme crop of caprifigs in the fall. This crop will overwinter on the tree when all the leaves have fallen.
According to W.B. Storey (1975), there is a dominant mutant allele (P) for persistent syconia and ovule abortion. This allele is egg lethal so it can only be carried in the sperm. In other words, it cannot be passed on from a persistent female tree. The homozygous genotype PP is not possible. A recessive wild type allele (+) results in caducous syconia and normal ovule development. It can be carried by the egg and sperm. Therefore the only possible genotypes for caprifigs and female trees are P+ and ++. Persistent caprifigs and persistent female trees must be heterozygous (P+). Mature pollinated syconia on heterozygous female trees having the allele for persistence (P) may contain hollow drupelets (cenocarps) as well as normal seed-bearing druplets. Although I don’t have a specific reference, I don’t see why the persistent allele (P) could not occur in wild populations of F. carica. This allele does not appear advantageous to the female fig, although if wasp-bearing caprifigs are nearby the syconia are capable of producing seeds.
This is a complicated subject when discussing the biology of Ficus carica. In general, unpollinated parthenocarpic cultivars with the persistent gene must be propagated by cuttings because the druplets in their syconia are hollow cenocarps without seeds. These cultivars have been grown and selected for flavorful “figs” and, like many other excellent fruit cultivars, must be propagated asexually in order to obtain clones. Cultivars such as the ‘Verte’ are valuable because they are absolutely delicious and do not require wasp pollination in order to set fruit. If these parthenocarpic cultivars are pollinated by a nearby caprifig they can produce seed-bearing druplets in addition to hollow druplets (cenocarps). The remains of female F. carica syconia have been discovered in archaeological sites of the Jordon Valley that date back 11,400 years. They are clearly persistent, parthenocarpic syconia containing hollow druplets (cenocarps). When M.E. Kislev concluded they were planted by cuttings and possibly represented the first known domesticated plants, perhaps he assumed that the trait for persistent syconia was unique to seedless fig cultivars. According to Storey (1975), this gene can occur in both female trees and caprifigs. It is passed to female progeny in the sperm of caprifig pollen parents. Female parthenocarpic trees with the persistent gene can produce seeds if they are pollinated by fig wasps. The ancient syconia of the Jordon Valley with hollow cenocarps could have come from unpollinated female trees that grew from seeds.
Note: In fig crosses where you would like the persistent gene (P) in your offspring, the pollen parent must be a persistent, heterozygous caprifig (P+). The persistent gene (P) cannot come from female parent even if it is persistent; therefore, the persistent caprifig cannot be homozygous (PP). Persistent caprifigs have been used in crosses to develop a possible persistent Calimyrna with quality syconia that don’t require caprification. What I don’t understand here is that pollinator wasps are responsible for fruit set and viable seeds in caducous Calimyrna figs which impart a superior nutty flavor to these delicious figs. Persistent figs are seedless without pollination unless there is a caprifig with fig wasps nearby.
According to Neeman and Galil (1978), caprifigs can produce seeds if the ovaries of short-style female flowers within the syconium are pollinated by fig wasps, but not inhabited by wasp larvae. The seed-bearing endocarps will sink in water. A true heterozygous, persistent caprifig that has never been caprified (pollinated) by fig wasps would not produce viable seeds that sink in water.
Seed-bearing endocarps of Ficus carica variety ‘Verte’ at the bottom of a dish of water. Although this cultivar is parthenocarpic, it has been pollinated by fig wasps from a nearby caprifig. Endocarps with mature, viable seeds typically sink in water. These are the actual fruits of a fig. They are the sclerified inner layer of tiny, ovule-bearing ovaries after the thin, fleshy, outer pericarp layer has been removed. Hollow (seedless) drupelets produced without pollination and fertilization are called cenocarps. If the endocarps contain wasp larvae they are called psenocarps.
According to Ira Condit’s monograph on fig varieties (1955), the caprifig of this species has a distinctive profichi syconium that is purple-black in color with a long, slender stalk (peduncle). In his classic volume The Fig (1947), Condit describes the syconium as smaller than other varieties of F. carica. In Ficus: The Exotic Species (1969), Condit describes the twigs of F. pseudocarica as velvety pubescent and the twigs of F. carica as glabrous or only slightly puberulent when young. F. pseudocarica is listed as a synonym of F. palmata (Punjab fig) in the Kew List Of Plant Species (2011). It is listed as naturalized in California (under F. palmata) in the Calflora Database and USDA Plant Database. According to the revised Jepson Manual (2011), reports of F. pseudocarica and F. palmata are based on misidentified specimens of F. carica (A.T. Whittemore, 2006, Sida 22: 769-775).
According to Condit (1955), Ficus pseudocarica is native to Eritrea and Abyssinia, while F. palmata is indigenous to Pakistan, northern India and Afghanistan. He states that F. pseudocarica was introduced into Santa Barbara, California in 1902, and like F. palmata, was used for hybridizing with F. carica. In fact, the edible ‘Brawley’ caprifig cultivar is a hybrid between F. carica var. ‘kadota’ and a F. pseudocarica caprifig (Storey et al. 1977). Ficus palmata is commonly used in modern floras, with F. pseudocarica listed as a synonym. Alan Whittemore (2006) has studied herbarium collections of F. palmata (F. pseudocarica) from California and has concluded that they are misidentified and should be labeled F. carica. He compared 4 collections of “F. palmata” by H.M. Pollard from Cold Spring Canyon, Santa Barbara Co. during the 1950s with 31 sheets of F. palmata from India, Nepal, Pakistan, Saudi Arabia, Yemen, Eritrea and Ethiopia and 70 sheets of cultivated F. carica worldwide. [Interestingly enough, Pollard’s 1950 collections at Rancho Santa Ana Botanic Garden are labeled F. pseudocaria.] Whittemore used 14 characteristics in his analysis of Pollard’s sheets, 10 of which matched F. carica better than F. palmata. According to Whittemore, F. palmata (F. pseudocarica) was occasionally grown horticulturally in California, but there is no evidence that it ever escaped from cultivation.
Mallikarjuna Aradhya et al. (2010) studied 194 fig accessions maintained at the USDA National Clonal Germplasm Repository, Davis, California. Their extensive DNA cladogram shows F. pseudocarica on a sister clade with the ‘Hacin’ cultivar of F. carica, between clades of the popular F. carica cultivars ‘Zidi’ and ‘Roeding.’ All of these varieties were derived from the ancestral F. pumila. Under “Materials and Methods,” Aradhya et al. cite the single accession of F. pseudocarica as a synonym of F. palmata. Dna cladograms by Nina Rønsted et al. (2005 and 2006) show F. palmata in a clade far away from F. pumila and certainly not derived from F. pumila. In another cladogram by Rønsted et al. (2008), Ficus pumila (Subsection Frutescentiae) is placed close to F. palmata (Subsection Ficus). In the latter cladogram, the sister clade of F. palmata is F. johannis, another closely-related deciduous fig in the Ficus carica-F. palmata complex. F. pumila has been artificially crossed with F. carica, indicating a close genetic relationship. It is unfortunate that F. carica was not included in these phylogenetic trees.
The leaves of F. palmata are quite distinctive and match illustrations and photos of the tree in its native habitat from Ethiopia to India; however, according to Condit (1969) the leaves can also be deeply lobed. Condit lists Blastophaga psenes as the symbiotic pollinator wasp for F. palmata, the same species found in F. carica. K.J. Joseph (1954) reported B. vaidi for F. palmata in India, but Wiebes and Compton (1990) consider this species of wasp questionable because it is so similar morphologically to B. psenes. The nonpollinator wasps Sycoscapter forsteni and Philotrypesis palmata are also reported for F. palmata in India (S. van Noort and A. van Harten, 2006). Although the obligate mutualism between pollinating fig wasps and their host fig trees has historically been a one-to-one relationship, more than one species of pollinator wasp can be associated with a single host and, conversely, a single pollinator can be associated with more than one host fig species (van Noort and van Harten, 2006; van Noort and Rasplus, 2010).
Ficus pseudocarica is an enigma. In the DNA cladogram of Aradhya et al. (2010), the clade of a specimen identified as F. pseudocarica is embedded within clades of F. carica cultivars and yet it is considered synonymous with F. palmata. It seems reasonable to assume that if F. pseudocarica is synonymous with F. palmata and if F. palmata is a valid species, it should be in a clade separate from F. carica. These discrepencies suggest that perhaps some collections identified as F. pseudocarica in California are varieties of F. carica.
During the past two decades, a number of additional fig collections have been made in southern California by reputable botanists who concluded the species was Ficus palmata rather than F. carica. Eight of these are listed by the Consortium of California Herbaria at Rancho Santa Ana Botanic Garden and University of California, Riverside. DNA evidence strongly suggests that these two species are closely related; however, major herbaria such as Kew and Missouri Botanical Garden recognize them as distinct species. Although my 1986 caprifig collection from Vista, California (RSA381641) has some characteristics matching Condit’s description of F. pseudocarica, it is perhaps best treated as a variety of Ficus carica.
In Ficus: The Exotic Species (1969) Condit discusses the difficulty in separating Ficus palmata from F. pseudocarica. In fact, in his Key To Ficus, the two species are not separated. Even the separation between these two species and Ficus carica is only based on the degree of pubescence of young stems. Ficus carica twigs are glabrous or only slightly puberulent, while those of F. pseudocarica and F. palmata are velvety pubescent. Other characteristics, such as leaf shape and size, venation, and the size, shape and color of fruit are so variable that it is difficult to make a positive identification from the key. Under his description of Ficus palmata, Condit cites George King who studied these species in the late 1800s: “I have a strong suspicion that all may be but forms of F. carica Linn.” According to the extensive fig website FigWeb (2011), fig biologists Simon van Noort and Jean-Yves Rasplus state that F. palmata and F. carica are probably conspecific. The Principle of Parsimony (Occam’s Razor) states that the least complex explanation for an oberservation is probably the best explanation. If F. pseudocarica, F. palmata and F. carica are all taxonomic varieties or subspecies of one species complex, the above discrepencies between DNA analysis and disputed California collections of these species might be resolved!