# Ficus carica and its pollination

Finn Kjellberg, Annick Lesne

► To cite this version:

Finn Kjellberg, Annick Lesne. Ficus carica and its pollination. Master. France. 2020. hal-02516888

HAL Id: hal-02516888

https://hal.science/hal-02516888

Submitted on 24 Mar 2020

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
*Ficus carica* and its pollination

Finn Kjellberg and Annick Lesne

<figure><img src="image_2.png" /></figure>

Creative Commons Licence CC-BY
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wild *Ficus carica*

*Ficus carica*
typically grows
on rocks

2 meters
wild *Ficus carica*

<figure><img src="image_4.png" /></figure>

fig tree

Ongoing tufa deposition
Hérault, France

<figure><img src="image_5.png" /></figure>

Ia

<figure><img src="image_6.png" /></figure>

I

<figure><img src="image_7.png" /></figure>

Ib

© UPMC Paris, France

I: original tufa concretion

Ia and Ib, *Ficus carica* fossil figs isolated from I

Hérault, France >60.000 years BP

G. Planchon 1864, Paris, France
wild *Ficus carica*

*Ficus carica* (form *Ficus colchica* Grossh.)

This is morphologically the most divergent form of *Ficus carica*

Black Sea coast, Turkey
wild *Ficus carica*

*Ficus carica* (form *Ficus colchica* Grossh.)
Note the gracile branches and flexible leaves
Black Sea coast, Turkey
Ficus palmata

Adıyaman Province, Turkey

Ficus palmata is the sole species closely related to F. carica

It is distributed from Ethiopia to India and Nepal

<figure><img src="image_8.png" /></figure>
<figure><img src="image_9.png" /><figcaption>*Ficus palmata*
Adıyaman Province, Turkey</figcaption></figure>
<figure><img src="image_10.png" /><figcaption>wild *Ficus carica*</figcaption></figure>

ostiole

<figure><img src="image_11.png" /></figure>

immature
male flowers

female flowers

A fig is an urnshaped receptacle. It is closed by an ostiole, the inside is lined by uniovulate female flowers, and male flowers
wild *Ficus carica*

<figure><img src="image_12.png" /></figure>

pollen loaded female *Blastophaga psenes*

Figs are exclusively pollinated by *Blastophaga psenes* wasps that enter the fig through the ostiole to oviposit
wild *Ficus carica*

ovipositing female *Blastophaga psenes*

<figure><img src="image_13.png" /></figure>

Within the fig: *Blastophaga psenes* oviposits in female flowers, transforming them into galls. The ovipositor is inserted through the style of the flower. The egg is laid in the ovule, between the inner integument and the nucellus
*Ficus carica* is a functionally dioecious species

- **Female trees** have long styled female flowers that do not host wasp larvae; their figs produce seeds and no pollen

- **Male trees** have short styled female flowers that host wasp larvae and only very few seeds; their figs produce wasps (pollen vectors) and pollen, i.e. they are functionally male
wild *Ficus carica*

long-styled flower:
turns into seed

<figure><img src="image_14.png" /></figure>

<figure><img src="image_15.png" /></figure>

ovipositor

<figure><img src="image_16.png" /></figure>

short-styled flower:
turns into gall containing wasp larva

<figure><img src="image_17.png" /></figure>

seed

In long styled flowers the ovipositor does not reach the ovule,
no egg is laid, the flower gives a seed. In short styled flowers
an egg is laid and the ovule is transformed into a gall.
wild *Ficus carica*

<figure><img src="image_18.png" /><figcaption>male *Blastophaga psenes*</figcaption></figure>

<figure><img src="image_19.png" /><figcaption>mated female in gall</figcaption></figure>

**Male tree:** males mate females still enclosed in their natal gall

Photo G. Valdeyron
wild *Ficus carica*

male *Blastophaga* searching for galls
containing females

<figure><img src="image_20.png" /></figure>

<figure><img src="image_21.png" /></figure>

galled female flower

Male tree: mated female *Blastophaga* emerging into the fig cavity
from a galled female flower

<figure><img src="image_22.png" /></figure>
wild *Ficus carica*

<figure><img src="image_23.png" /></figure>

Male tree: wasp emerging from the fig cavity through the ostiole

It got abundantly dusted with pollen while emerging

Pollen is largely wasted

The wasp will leave in search of a receptive fig to enter during its short survival outside figs (about 1 day).
wild *Ficus carica*

The year-round cycle of wild *Ficus carica*
in Montpellier, France
Reading a fig branch, in early spring, year N

<figure><img src="image_24.png" /></figure>

fig that overwintered as a bud initiated year N-1

scar after a fig that developed directly
on the growth of year N-1

scar after the stipules
that enveloped the terminal bud

shoot of year N-3

scar after a leaf

scar after a fig that developed
at the axil of the leaf

shoot of year N-2

shortened internodes
corresponding to the
resting (August year N-3
to March, year N-2)
terminal bud
<figure><img src="image_25.png" /><figcaption>wild *Ficus carica*</figcaption></figure>

scars after figs that
ripened in August-
September

scars after leaf petioles

Fig buds appear on the shoot of
the year and develop directly into
figs receptive in June-July and
ripe in August-September

winter: **female tree**
wild *Ficus carica*

fig bud from previous growth season, it will resume its
development in spring

<figure><img src="image_26.png" /></figure>

winter: male tree

figs that developped directly
from fig buds on the shoot of
the year and containing last
larval stage *Blastophaga*

fig bud
wild *Ficus carica*

<figure><img src="image_27.png" /></figure>

gall containing a wasp larva

female flowers have short styles,
contain insect larvae and only
very few seeds

winter: male tree
wild *Ficus carica*

fig bud

scars after aborted
unvisited figs that
became receptive
previous summer when
wasps were no longer
available

previous-summer fig containing
wasp larvae

end of winter: **male tree**

Fig buds appear progressively along the shoot of the year from July to September
Their fate depends on wasp visitation at their receptivity and climatic conditions
<figure><img src="image_28.png" /></figure>

wild *Ficus carica*

April: **male tree**, wasps are ready to emerge from the overwintering figs to visit receptive figs on male trees
## Ficus carica sauvage

receptive figs

(attractive to wasps)

fig in which the wasps overwintered

April: male tree, wasps are ready to emerge

from the overwintering figs to visit the receptive,

future polliniferous figs

The receptive figs have grown large, waiting for *Blastophaga* to visit them
wild *Ficus carica*

receptive figs (attractive to wasps)

April: **male tree** without overwintering figs

The receptive figs have grown large, still waiting for *Blastophaga* from another male tree to visit them
wild *Ficus carica*

April: **male tree**, wasps that have just emerged through the ostiole from the fig in which they overwintered.

The wasps are not dusted with pollen as these figs produce no pollen

<figure><img src="image_29.png" /><figcaption>ostiole</figcaption></figure>
wild *Ficus carica*

<figure><img src="image_30.png" /></figure>

April: male tree, a newborn female *Blastophaga psenes* has reached a receptive fig
<figure><img src="image_31.png" /><figcaption>wild *Ficus carica*</figcaption></figure>

April: **male tree**, a female *Blastophaga psenes* close to the ostiole on a receptive fig
wild *Ficus carica*

April: male tree, inside a receptive fig
The styles are short allowing wasp oviposition

<figure><img src="image_32.png" /></figure>
wild *Ficus carica*

<figure><img src="image_33.png" /></figure>

April: male tree, receptive fig

The stigmas form a platform within the fig on which the wasps will walk
wild *Ficus carica*

<figure><img src="image_34.png" /></figure>

April: male tree, *Blastophaga* ovipositing in a receptive fig
wild *Ficus carica*

no ovipositor insertion

elongating flower pedicel

flower style with brown trace of
ovipositor insertion

April: **male tree**, shortly after wasp oviposition

After oviposition into a flower the style turns brown, the pedicel elongates and the ovule begins to swell turning into a gall

swelling galled ovule
containing a pollinator egg
wild *Ficus carica*

<figure><img src="image_35.png" /></figure>

April: **male tree, Philotrypes caricae** - a cleptoparasite of *Blastophaga psenes* - ovipositing into a fig recently entered by *Blastophaga*
wild *Ficus carica*

Photo B. Schatz

April: **male tree, Philotrypes caricae ovipositing into a fig recently entered by**
**Blastophaga**

<figure><img src="image_36.png" /></figure>
wild *Ficus carica*

*Philotrypes* ovipositors

<figure><img src="image_37.png" /></figure>

April: male tree

<figure><img src="image_38.png" /></figure>

ovipositor of *Philotrypes* inserted through the fig wall and entering the flower through the pedicel: the egg is laid beside the *Blastophaga* egg between the inner integument and the nucellus
wild *Ficus carica*

<figure><img src="image_39.png" /></figure>

immature
male flowers

galled female
flowers

April: **male tree**, fig a few days after oviposition

There are many male flowers
<figure><img src="image_40.png" /><figcaption>wild *Ficus carica*</figcaption></figure>

<figure><img src="image_41.png" /></figure>

ostiole

male flowers with pollen

galled female
flowers

June: **male tree**, the female flowers have turned into galls each hosting a wasp larva
Male flowers with pollen are conspicuous
wild *Ficus carica*

<figure><img src="image_42.png" /></figure>

June-July: **male tree**, *Blastophaga* emerging through the ostiole from a polliniferous fig, covered with pollen before cleaning themselves. Some pollen remains caught in the intersegment pleura
<figure><img src="image_43.png" /></figure>

wild *Ficus carica*

June-July: male tree, *Blastophaga* emerging from a polliniferous fig
## Two wild *Ficus carica*

June-July

**Female tree:** a recently pollinated fig
two receptive figs

At that period, there are no receptive figs on male trees
The wasps can only go from male figs to figs on female trees

**Male tree:** polliniferous figs at the stage of *Blastophaga* emergence
wild *Ficus carica*

<figure><img src="image_44.png" /></figure>

wasps trying to enter fig

pre-receptive fig

very recently pollinated figs

June-July: **female tree**
wild *Ficus carica*

<figure><img src="image_45.png" /><figcaption>July: female tree, pollen-bearing wasp trying to enter a fig</figcaption></figure>
<figure><img src="image_46.png" /></figure>

wild *Ficus carica*

elongate stigmas that will brush the body of the wasp,
collecting pollen and ensuring seed set

July: **female tree**, receptive fig
wild *Ficus carica*

flower ovule

long style, the wasp cannot oviposit

elongate stigmas with papillae on which pollen will stick

July: **female tree**, receptive fig
<figure><img src="image_47.png" /></figure>

wild *Ficus carica*

figs from which the wasps have already emerged

young fig buds

Late July: **male tree**, the very earliest young figs are visited by the wasps emerging from the very latest polliniferous figs. This sensitive point in the yearly cycle of the wasps is present throughout the wild range of *Ficus carica*
<figure><img src="image_48.png" /></figure>

wild *Ficus carica*

September: **female tree**, ripe seed-containing figs
wild *Ficus carica*

<figure><img src="image_49.png" /></figure>

September: **female tree**, ripe seed-containing figs

The climacteric ripening involves nutriment transfer, ethylene production and
respiratory peak

Ripening can be artificially sped up by depositing a drip of olive oil on the ostiole
wild *Ficus carica*

<figure><img src="image_50.png" /></figure>

September: fig seed dispersal by a mammal
wild *Ficus carica*, in man-made habitat

<figure><img src="image_51.png" /></figure>

fig tree

Valleraugue, Hérault, France
<figure><img src="image_52.png" /></figure>

wild *Ficus carica*, in man-made habitat

Church of Saint Simeon the Stylite, Syria
wild *Ficus carica*, in man-made habitat

<figure><img src="image_53.png" /></figure>

Wild-germinated *Ficus carica*, outside the range of the pollinator, Britany, France

Photo G. Valdeyon
Fig cultivation and domestication
From wild to cultivated

<figure><img src="image_54.png" /></figure>

Wild figs are as good as domesticated ones
<figure><img src="image_55.png" /></figure>

fig cultivation

<caption>cultivated wild-germinated fig tree
Montpeyroux, Hérault, France</caption>

Photo G. Valdeyron
fig cultivation

<figure><img src="image_56.png" /></figure>

Fig plantation, Syria
fig cultivation

Fig plantation,
Meander valley, Turkey

<figure><img src="image_57.png" /></figure>
fig cultivation

<figure><img src="image_58.png" /></figure>

Figs of the cultivars producing the best dry figs abort if not pollinated
How is pollination achieved in large fig plantations?
Turkey, Meander valley
fig cultivation

June: **female tree**, receptive figs of the second crop (= the crop present on wild female trees), requiring pollination

This phenotype is very similar to typical wild female trees
Turkey, Meander valley
fig cultivation

<figure><img src="image_59.png" /></figure>

Fig plantation for dry fig production with caprifig trees
(male trees) planted upwind of the female trees so
wasps are blown towards the receptive figs
Idlib governorate, Syria

Photo G. Valdeyron
<figure><img src="image_60.png" /><figcaption>fig cultivation</figcaption></figure>

June: **caprification=profichi** (polliniferous figs of male trees)
are suspended in female trees to ensure pollination
Greece, Kalamata
fig cultivation

June: tying profichi (polliniferous figs from male trees) together to suspend in female trees. Kalamata, Greece

<figure><img src="image_61.png" /></figure>
fig cultivation

female tree

fresh profichi

older profichi

June: weeding is neglected, but caprification is still performed

With caprification many female trees can be pollinated with figs from few distant

caprifig trees

Greece, Kalamata
<figure><img src="image_62.png" /></figure>

fig cultivation

second crop receptive figs

a pair of profichi
tied together

June: caprification of **female tree** for dried fig production
Idlib governorate, Syria
fig cultivation

<figure><img src="image_63.png" /><figcaption>Preparing profichi for caprification in a village of dried fig producers, Meander valley, Turkey</figcaption></figure>
fig cultivation

A village specialized in profichi cultivation for sale at the market in the city
Meander valley, Turkey

<figure><img src="image_64.png" /></figure>
<figure><img src="image_65.png" /></figure>

June: caprifig cultivar from a village specialised in profichi production
Pollinator reproduction is facilitated by the early development of the next generation
of figs on the shoot of the year.
Meander valley, Turkey
fig cultivation

A caprifig cultivar from the Meander valley

On this phenotype wasps visit figs on the same tree instead of ensuring pollen
transfer to female trees, and the reproduction of the male tree

This phenotype is counterselected in the wild

<figure><img src="image_66.png" /></figure>

numerous wasps attracted to a receptive fig
on the same tree

<figure><img src="image_67.png" /></figure>

just emerged wasp on natal fig

<figure><img src="image_68.png" /></figure>

June: **caprifig** cultivar with early receptive figs selected in the
villages specialised in profichi production, Meander valley, Turkey
fig cultivation

under insular conditions, overwintering figs containing wasps
may lack in spring: wasps are brought from the continent

profichi

mamme (=overwintering fig on male tree)
picked on the continent and used to ensure
wasp colonization of profichi figs

Photo G. Valdeyron
fig cultivation

diseases spread by
pollinating wasps

<figure><img src="image_69.png" /></figure>

*Fusarium* growing in a mamme fig

California, USA

Photo Themis Michailides UC Davis
fig cultivation

diseases spread by
pollinating wasps

*Fusarium moniliforme* on *Blastophaga*

California, USA

Photo Themis Michailides UC Davis
fig cultivation

diseases spread by
pollinating wasps

second crop figs, *Endosepsis* caused by *Fusarium*

<figure><img src="image_70.png" /><figcaption>Photo Themis Michailides UC Davis</figcaption></figure>
fig cultivation

diseases spread by
pollinating wasps

<figure><img src="image_71.png" /></figure>

Smut
*Aspergillus niger*

Endosepsis
*Fusarium spp.*

Alternaria rot
*Alternaria, Ulocladium*

*Aspergillus japonicus*

*Aspergillus carbonarius*

Photo Themis Michailides UC Davis
fig cultivation

controlling diseases spread by pollinating wasps

a caprifig plantation, preparation to collect mamme for sanitation
California, USA

Photo Themis Michailides UC Davis
fig cultivation

profichi collected in specialised orchard, before sanitation
California, USA

Photo Themis Michailides UC Davis
fig cultivation

<caption>Profichi collected in specialized orchard before sanitation
California, USA</caption>

Photo Themis Michailides UC Davis
fig cultivation

sanitation with fungicide of profichi figs split open, just before wasp emergence
California

Photo Themis Michailides UC Davis
<figure><img src="image_72.png" /><figcaption>fig cultivation</figcaption></figure>

<caption>sanitation of profichi figs split open
California</caption>

Photo Themis Michailides UC Davis

Packaging of profichi sanitised just before wasp emergence, ready for use in caprification
fig cultivation

second crop figs (typical crop present in
wild female trees) on the shoot of the year

<figure><img src="image_73.png" /></figure>

First crop fig (equivalent of profichi on
female trees) on the shoot of previous
year

June: **female tree**, biferous cultivar (=2 crops, the typical one of wild female trees, and the one corresponding to the generation of profichi figs, only present in cultivars )

Mamme figs do not produce pollen so that first crop figs are never pollinated

First crop figs develop without pollination, they are parthenocarpic

The second crop is also parthenocarpic in some cultivars
fig cultivation

<figure><img src="image_74.png" /><figcaption>Winter: **female tree**, biferous cultivar</figcaption></figure>
fig cultivation

Receptive female fig, first crop

First crop figs are larger and have a thicker wall, the flowers are less densely packed and the styles are shorter than in second crop figs

The overwintering first crop fig bud presented differentiated flower primordia

Morphological differences with second crop figs are induced during winter
fig cultivation

Receptive female fig, first crop

The stigmas will never be pollinated as mamme do not produce pollen

First crop figs artificially pollinated with preserved pollen produce seeds
<figure><img src="image_75.png" /></figure>

枝蔓伸展

buds that will give ripe first
crop figs next August

<figure><img src="image_76.png" /></figure>

at the northern limit:
second crop figs that will never ripen
March, Normandy, France
fig cultivation

Croisic, a caprifig cultivar cultivated outside the range the fig wasp

It produces edible figs

Britany, France

Photo G. Valdeyron
## Other-fig cultivation

<figure><img src="image_77.png" /></figure>

<figure><img src="image_78.png" /><figcaption>Jelly fig
(*Ficus pumila* var *awkeotsang*)
Taiwan</figcaption></figure>

<figure><img src="image_79.png" /></figure>
<figure><img src="image_80.png" /></figure>

<figure><img src="image_81.png" /></figure>

<figure><img src="image_82.png" /></figure>