Plant Species Biology (1999) 14, 143–152

Pollination and evolution in neotropical Annonaceae

GERHARD GOTTSBERGER
Department of Systematic Botany and Ecology, University of Ulm, Albert-Einstein-Allee 11, D-89081 Ulm, Germany

Abstract

The most prominent pollination mode in neotropical Annonaceae is pollination by

beetles. Flowers are protogynous and have fruity, spicy or unpleasant odors. The floral
chambers, formed by the petals closing over the flower center, emit these specific odors
which entice the beetles to enter the flowers. There, the beetles are sheltered from day-
light and predators and encounter food (tissues and pollen) as well as opportunities for
mating. The amount of food offered, the thickness of the petal tissue and the dimension
of the flowers increases with size, number and voraciousness of the attracted beetles.
Three main groups of beetle-pollinated Annonaceae can be distinguished. Two of them
have relatively small floral chambers, exhibit diurnal and/or nocturnal anthesis and
are visited and pollinated by relatively small beetles (Nitidulidae, Curculionidae,
Chrysomelidae). Large flowers with a large pollination chamber and very thick petals are
associated with nocturnally active, large and voracious dynastid scarab beetles, which are
attracted by strong odors promoted principally by thermogenetic processes of the flowers
during the time of the beetles’ main activity. The dynastid beetle-pollinated species
appear to have the most adapted and most specialized flower characteristics in the
Annonaceae. Some small-flowered Annonaceae are pollinated by thrips and, for a few
species, pollination by flies is suspected. Some genera, such as Guatteria, are uniform
with respect to flower biology and seem to have adapted principally to nitidulids as pol-
linators. In contrast, the genus Annona, basically a group pollinated by dynastid beetles,
is diversified with respect to flower morphology and pollination. The neotropical
Annonaceae as a whole may have started as a group pollinated by sucking and pollen-
eating Thysanoptera and non-destructive beetle groups. Species pollinated by such
Thysanoptera and/or rove beetles (Staphylinidae) still show the laminar, plesiomorphic
stamen type of Annonaceae with a tongue-shaped connective prolongation. The disc-like
sclerified connective shield of the majority of Annonaceae is apparently a secondary and
modified structure, especially prominent in the beetle-pollinated species. The densely
aggregated stamens with their connective shield appear to be a kind of antipredator struc-
ture in Annonaceae adapted to pollination by beetles.
Keywords: flower evolution, neotropical Annonaceae; pollination by beetles, thrips and flies.
Received 1 April 1999; accepted 20 April 1999

Introduction Relevant questions in this context include:

The large family Annonaceae, with approximately 2500
recent species, is still poorly known with regard to its
floral biology. In the present paper a comparison of polli-
nation modes with processes of differentiation and evo-
lution in selected groups of the family in the Neotropics
is attempted.
Email: gerhard.gottsberger@biologie.uni-ulm.de
1. Which are the main insect groups involved in pollina-
tion and do the flowers have typical characters correlated
with these pollinators; in other words, are there pollina-
tion syndromes apparent?
2. Are there genera of Annonaceae being conserva-
tive with respect to pollination? Are there other genera
that have radiated and adapted to several different
pollinators, thereby showing a more active flower
evolution?

© 1999 Society for the Study of Species Biology

144 G. GOTTSBERGER
3. If the Annona–Rollinia group, one of the best studied
entities in respect to flower biology in the family is taken
as an example, what hypothetical evolutionary steps
become apparent if flowering events, rhythms of anthesis
and pollination modes are correlated with geographic dis-
tribution, habitat, habit and chromosomal differentiation?
4. How does the flower biological differentiation and
evolution appear when considering the neotropical rep-
resentatives as a whole?
Floral events and pollinating insect groups
Beetle pollination (cantharophily)
The main pollination mode in neotropical Annonaceae is
cantharophily, pollination by beetles. The beetle-
pollinated species have commonly pendulous, yellowish,
greenish or reddish flowers. The flowers are protogynous
and produce strong fruity, spicy or even unpleasant
odors. One of the most remarkable functional characters
is the floral or pollination chamber formed by the petals
closing over the flower center during anthesis. These
floral chambers emit specific odors that entice the beetles
to enter the flowers. There, the beetles are sheltered from
daylight and predators and encounter food (tissue and
pollen) as well as opportunities for mating. The amount
of food offered and the thickness of the petal tissue
increases with size, number and voraciousness of the
attracted beetles.
The closedness of the flowers serves, to a lesser extent,
to protect the reproductive organs. The floral chamber
mostly serves to select the flower-visiting beetle spectrum
and to retain the beetles inside the flowers while they are
closed (Gottsberger 1970, 1989a).
Three main groups of beetle-pollinated Annonaceae
can be distinguished. Two of them have relatively small
floral chambers and are visited and pollinated by small
beetles only. The third group has large flowers with large
floral chambers and is visited and pollinated by large
beetles.
Diurnal species pollinated by Nitidulidae. The vast majority
of species of the genera Guatteria and Duguetia have
flowers with relatively small floral chambers. The flowers
attract fruit-inhabiting Nitidulidae (Gottsberger 1970) by
providing an imitation of decaying fruit odors. Usually,
anthesis begins and ends during daytime hours; at the
same time, attraction and release of the beetles takes
place. The pendulous flowers (e.g. Guatteria neglecta R. E.
Fries observed in São Paulo (Gottsberger 1970), become
more or less dish-shaped after opening. Their reproduc-
tive organs, although not yet functional, are exposed.
After weeks of development the flowers enter their sexual
stages of anthesis. The initially hard, greenish petals
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
become softer, yellowish and finally brownish. The three
inner petals fold over the flower center and emit a heavy,
fruit-like odor. The so-formed odoriferous, dark floral
chamber attracts small Nitidulidae (see Fig. 1). The
Nitidulidae enter and may effect pollination of these
protogynous flowers. The beetles stay in the flowers until
the pollen is shed and the petals drop. In some species,
(e.g. Guatteria foliosa Benth. and G. megalophylla Diels;
Webber 1996) small species of Staphylinidae and
Chrysomelidae may constitute additional or even domi-
nant flower-visiting beetles (see also Gottsberger 1970).
The petals of the annonaceous flowers may be heavily
gnawed or even totally consumed by small curculionid
and larger scarabaeid beetles, which, however, normally
do not have any impact on pollination (Gottsberger 1970;
Fig. 1).
Quite similar processes occur in the genera Duguetia
(e.g. D. furfuracea, Gottsberger 1970, 1993, 1994; D.
stelechantha, Webber 1996), Xylopia (e.g. X. benthami R. E.
Fries, X. crinita R. E. Fries, X. excellens R. E. Fries, Webber
& Gottsberger 1994a, 1995a; Webber 1996), and Rollinia
(Webber 1981a, 1992; Murray & Johnson 1987). During
anthesis, the bases of the petals which emit fruit-like
odors also fold over the reproductive organs. Small, flat-
bodied, fruit-eating Nitidulidae or Staphylinidae, or both
are attracted to the flowers.
Species with nocturnal or diurnal anthesis pollinated by
Curculionidae or Chrysomelidae. Some Annonaceae species,
e.g. Annona glabra L. and Tetrameranthus duckei R. E. Fries,
are pollinated by relatively small Chrysomelidae or Cur-
culionidae. These beetles also enter the flowers in the
female stage and leave them when the pollen is shed and
the petals drop.
Anthesis in Annona glabra lasts for approximately 40 h,
is initiated during the daytime and terminates in the
evening hours when the maximum temperature elevation
and emission of fruity odors occurs in the flowers. The
anthers also dehisce in the evening hours. The visitors
observed in Manaus were several species of Chrysomeli-
dae (Webber 1981a; see also Xylopia brasiliensis Spreng.,
observations by Andrade et al. 1996).
The flowers of Tetrameranthus duckei in the female stage
emit musky odors during the night, attracting curculionid
beetles. Anther dehiscence was observed to occur at
midday (Webber 1981a).
Species with nocturnal anthesis pollinated by Dynastinae.
Another beetle group, the Dynastinae, a subfamily of the
Scarabaeidae, is also involved in pollination of neotropi-
cal Annonaceae. The flowers of the species pollinated by
these large beetles are large and have large pollination
chambers (Fig. 1). Such flowers are found in species
of the genera Annona (Webber 1981a; Gottsberger 1986,
 P O L L I N AT I O N A N D E V O L U T I O N I N N E O T R O P I C A L A N N O N A C E A E 145

Fig. 1 Flowers of Annonaceae and adaptation to beetle pollination: Guatteria neglecta with small Nitidulidae as pollinators and
Curculionidae predating the petals. Annona coriaceae and A. crassiflora with large Dynastinae as pollinators and with Curculionidae and
Cerambycidae predating the petals.

1989a; Gottsberger & Silberbauer-Gottsberger 1988), Cym-
bopetalum, Porcelia, Malmea, Cardiopetalum (Schatz 1985,
1987a, 1987b, 1987c; Webber & Gottsberger 1993), and
Duguetia (e.g. D. ulei (Diels) R. E. Fries, D. riparia Hub.,
Webber & Gottsberger 1996; Küchmeister et al. 1998).
Whereas the small-flowered nitidulid-, curculionid-, or
chrysomelid-pollinated Annonaceae show tendencies
towards activity in the daytime, the dynastid-scarab
beetle-pollinated species have a distinct nocturnal anthe-
sis, which is in accordance with their night-active visitors.
As far as observed, the flowers of the nocturnal species
show thermogenesis during the evening hours, a phe-
nomenon which seems to be closely coordinated with the
hours of the beetles’ main activity.
Thrips pollination
In some Annonaceae, thrips (order Thysanoptera) func-
tion as exclusive or additional pollinators. Three cases
are mentioned here. One is Bocageopsis multiflora (Mart.)
R. E. Fries, an Amazonian species (Webber & Gottsberger
1995) which bears its flowers in an irregular position,
from erect to pendulous. The flowers of B. multiflora open
by slits at the beginning of the female stage. During
daytime hours their slight rancid-fruity odor attracts the
thrips species which enter the pollination chamber and
cause transmission of the pollen.
Another thrip-pollinated species is Xylopia aromatica
(Lam.) Mart., from Central and South American savannas
and from Amazonia, in which the white flowers are
commonly held in an upright position. The scent of its
flowers, reminiscent of Convallaria flowers, is aromatic
and pleasant. As a rule, X. aromatica is pollinated by
thrips, but some nitidulids are also involved. The insects
become imprisoned by the inner petals which close
tightly over the flower center. Predatory large beetles may
gnaw on the petals but hardly ever destroy the repro-
ductive organs inside the floral chamber (Gottsberger
1994; Webber 1996). Also, the Amazonian X. amazonica is
exclusively thrips-pollinated (Webber 1996).
The protogynous flowers of the Amazonian Oxandra
euneura Diels open in the morning, emit a sweet perfumed
odor during the female stage and are visited by rove
beetles (Staphylinidae) and thrips (Thysanoptera). At
the end of anthesis, the second morning, the bodies of
these flower visitors are covered with pollen (Webber &
Gottsberger 1995).
Fly pollination (myiophylly)
Finally, some Annonaceae are apparently pollinated by
flies. This pollination syndrome is not well documented
in the Neotropics and, in absence of valid observations,
myiophily has been deduced in most cases from the
typical flower character combination of this syndrome.
An as yet undescribed Peruvian Annona species in the A.
ambotay group (W. Morawetz, personal communication,
1988) possesses approximately 1 cm long, erect flowers.
No closed floral chamber is formed. After the unfolding
of the petals, their tips remain open through the whole

© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
146 G. GOTTSBERGER
period. Although during observations in August 1988, no
pollinators arrived, we suspect this species to be polli-
nated by small flies (G. Gottsberger, unpublished). The
thin, somewhat transparent tissue at the base of the petals
is suggestive of light windows, which are characteristic
for other myiophilous species with kettle flowers.
It is suspected that some Sapranthus species and
Asimina triloba (L.) Dun. supposedly are pollinated by
carrion or dung flies. Their flowers are of a dark maroon
or purple color and exhale an unpleasant odor. Observa-
tions, however, are scarce and not well documented (see
Janzen 1983 for Sapranthus palanga R. E. Fries, on which
flowers Olesen 1992 detected a few beetles). Therefore, it
is not yet clear whether these species are in fact pollinated
by flies or by beetles, or by both. In North America,
Asimina obovata (Willd.) Nash and A. pygmaea (Bartr.) Dun.
are pollinated by Scarabaeidae and Cerambycidae
(Norman & Clayton 1986).
Pollination by beetles, thrips and flies and
corresponding floral syndromes
In conclusion, the present state of knowledge indicates
that cantharophilous species are by far the most frequent
in the neotropical Annonaceae, followed by some species
or species groups pollinated by Thysanoptera; only a few
are myiophilous or perhaps even sapromyiophilous (see
Schatz 1987c; Gottsberger 1992, 1993).
Each of these three main pollination types in the
Annonaceae is correlated with some special flower char-
acters. The beetle-pollinated Annonaceae usually produce
strong fruity, spicy or even offensive floral odors, their
flowers are often pendulous and the petals are yellowish,
greenish or reddish. The Annonaceae pollinated by thrips
have white or whitish, mostly commonly erect flowers.
Their stamens are not so densely clustered as those of
the cantharophilous Annonaceae and their floral odor
is pleasant and sweet. Supposedly fly-pollinated An-
nonaceae flowers remain open and do not fold their
petals over their reproductive organs. Their floral odors
are imperceptible or, in the sapromyophilous species,
strong and unpleasant (carrion-like).
That odor compounds may play a major role in polli-
nator attraction was suspected long ago (see Gottsberger
1970; Pellmyr & Thien 1986; Schatz 1987a, 1987b, 1990).
For example, our first results on the identification of floral
odor compounds, e.g. Anaxagorea dolichocarpa Sprague et
Sandw., a species with a strong acetonic fruity odor,
showed a marked prevalence of fruit esters, while Annona
squamosa L. has a different odor compound profile with
several monoterpenes and sesquiterpenes, besides esters
(G. Gottsberger et al. in preparation). Both species are
apparently pollinated by nitidulid beetles (Gottsberger
1989b; Webber 1996).
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
Functional diversification and flower evolution
in the genera Guatteria and Annona
As far as pollination is concerned, a genus such as Guatte-
ria appears to be conservative. With a few exceptions, the
species studied to date show similar floral characters and
pollination mechanisms. Pollinators of this largest genus
of the family are mostly fruit-eating nitidulids. Nearly all
species are uniform with respect to flower biology and
seem to have adapted to the nitidulids as pollinators.
In contrast, the genus Annona has diversified with
respect to flower morphology and pollination (Webber
1981a, 1981b; Gottsberger 1989a). Examples of the differ-
ent floral rhythms and pollination mechanisms are given
below.
The large flowers of Annona coriacea Mart. are borne at
the end of twigs in an inclined, pendulous position. In
bud, and even during anthesis, the reproductive organs
remain completely covered by the internal, imbricate
petals (Fig. 1). During evening hours the petals and the
cone of the reproductive organs become heated (Fig. 2).
The strong fragrance exhaled by the flowers during their
heating attracts dynastid scarab beetles. Among them
Cyclocephala atricapilla Mannerh. is the most common and
most numerous flower visitor within the distribution of
A. coriacea (Gottsberger 1989a). The beetles arrive in a zig-
zag-like flight, alight on the outside of the flower and
force their way into the pollination chamber through the
imbricate inner petals. This floral chamber easily shelters
up to 10 or 15 beetles. The number of visiting beetles
varies from flower to flower and from place to place. One
to 10 beetles per flower are the rule, but we also have
noted flowers with 70 individuals. In such overcrowded
flowers, the flower chambers were opened and the petals
were widely spread. Immediately after alighting the
beetles may copulate. They also start to gnaw at the inner
basal side of the three inner petals. Each inner petal has
two lateral regions with special food tissue. In these
places the visited flowers show two gnawing marks
(Gottsberger et al. 1998). During the second evening of
anthesis, a second temperature elevation takes place
(Fig. 2). The already dehisced stamens detach themselves
from the receptacle and fill up the chamber, together with
the released pollen tetrads.
The warming of the flower and the scent volatilization
in the second night attract another crowd of beetles which
also enter the floral chamber, and together with the
beetles from the first night, become covered with the
released, sticky pollen-grain tetrads. The pollen is now
the main source of food for the beetles. With the shedding
of the petals, the beetles are released from the flower. The
beetles transfer pollen by flying with their pollen load to
warm receptive, first-night flowers, thus guaranteeing
pollination.
 P O L L I N AT I O N A N D E V O L U T I O N I N N E O T R O P I C A L A N N O N A C E A E
Fig. 2 Rhythm of flower heating in Annona
coriacea and visitation by beetles during
two subsequent nights (observed in
1986). (—) Flower temperature; (---) and
(– . – .) air temperature.
Annona coriacea has a clear, two-night rhythm of
flowering, with a warming-up of its flowers during two
subsequent nights. The temperature peak of approxi-
mately 34°C is attained around 21.00 h on the first night.
A second peak on the following night is reached approxi-
mately 1 h earlier, when the petals are shed and the
pollen-covered beetles fly away (Fig. 2). As the release of
pollen-carrying beetles takes place before younger
flowers have reached the peak of their female phase, high
effectivity of pollen transfer is achieved.
In contrast, Annona crassiflora Mart. has a distinct one-
night rhythm of flowering (Gottsberger 1989a). Tempera-
ture elevation occurs during the female phase in the early
evening hours; the odor emission attracts dynastid scarab
beetles. From approximately 19.00 h onwards, the first
individuals of Cyclocephala atricapilla alight on the flowers
and enter the floral chamber. During the first half of the
night, the stigmatic head is usually shed and the dehisced
stamens detach and fall into the floral chamber, together
with the pollen. In the second half of the same night, the
petals also detach from the flower receptacle. Annona
crassiflora is a gamopetalous species and the six petals are
usually maintained as a unit even when being dropped.
Most beetles remain inside the fallen ring of petals on the
ground. Thus, to leave the flowers on the second evening
they crawl out of the fallen petals. Covered with sticky,
pollen-grain tetrads, they approach newly opened odori-
ferous flowers in the female stage and pollinate them.
In Annona cornifolia St. Hil. different flowers have dif-
ferent flowering rhythms (Gottsberger 1989a). The major-
ity of the protogynous flowers are active during two or
three subsequent nights. Some of them are in the female
phase in the first night of anthesis and become male as
early as in the second night, while others are female-
active during two nights and do not enter the male stage
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
147
until the third night. A third group of flowers, after a short
female stage in the early hours of the first night, changes
to the male phase as early as the evening or during the
second half of the same night. Such one-day flowers drop
shortly after becoming male-active, either in the evening
or in the early morning hours. As several flowers enter
their receptive female stage only during the second half
of their first active night, flowers in male and in female
stages are present during the whole night. The tem-
perature elevation during female and male stages is
accompanied by the emission of a fruit-like, pleasant odor
which attracts mainly Cyclocephala quatuordecimpunctata
Mannerh. and, to a lesser extent, also C. atricapilla (in a
relation of 10:1).
On the second evening of anthesis, the flowers of A.
cornifolia show some changes. The floral parts are more
lax, the petals spread and the floral chamber is quite open;
up to 10 beetles were seen sitting and gnawing and
copulating in such pendulous flowers. Petals of heavily
visited flowers had been almost entirely consumed and
destroyed.
In species with large flowers and large pollination
chambers the interesting phenomenon of thermogenesis
occurs, which is the warming-up of flowers during anthe-
sis. Annona coriacea (Fig. 2), holds the record for flower
temperature elevation in the Annonaceae to date, attain-
ing as much as 35°C during a short period at dusk, a
temperature 14–15 °C warmer than the surrounding air.
Annona montana Macf. with approximately 32°C
maximum temperature (Webber 1981a) is approximately
7 °C warmer than the air. In A. sericea (Webber 1981b), A.
dioica, A. cornifolia (Gottsberger 1989a), and A. muricata
(Van Tol & Meijdam 1991) temperature elevations of
6–8∞C have also been measured. By inference, and
judging from floral construction, 50–55 of the approxi-
148 G. GOTTSBERGER
mately 110 known Annona species are likely to exhibit the
phenomenon of floral heating.
It was surprising to find that there is little specificity
between the dynastid scarab beetle species and the dif-
ferent Annona species. This became evident not only in the
cerrado areas (central Brazilian area) where such rela-
tionships were studied (Gottsberger 1989a), but also in the
Amazonian region Manaus, where A. foetida (A. C.
Webber and G. Gottsberger, unpublished) shares the same
pollinator, Cyclocephala undata (Olivier), with Cym-
bopetalum euneurum N. A. Murray (Webber & Gottsberger
1993), Duguetia ulei and D. riparia (Webber & Gottsberger
1996). For example, near Indianópolis in the State of
Minas Gerais, Brazil, six Annona species belonging to five
or six different sections were growing closely together.
Only two dynastid species, namely Cyclocephala atricapilla
and C. quatuordecimpunctata, were the main pollinators of
all of them. Cyclocephala atricapilla was the main or exclu-
sive pollinator of A. coriacea, A. crassiflora, A. dioica and A.
monticola, the flowers of which emit a very similar, some-
what unpleasant odor. However, the flowers of A. tomen-
tosa and A. cornifolia, which have a pleasant fruity odor,
are visited more intensively by C. quatuordecimpunctata.
Although all six species flowered in the rainy season
from October to January and although there was a broad
overlapping of flowering periods, flowering was some-
what staggered with more or less separate peaks (Fig. 3).
The more interesting fact, however, was that the six
species flowered in such a way that predominantly C.
quatuordecimpunctata-pollinated species were alternating
with C. atricapilla-pollinated ones. This arrangement
probably reduces interspecific gene flow. All species are
members of different systematic groups except for A.
crassiflora and A. cornifolia, which probably belong to the
same section, Gamopetalum. Although they show a broad
overlap of flowering periods and in spite of identical
species of flower visitors permitting some pollen flow
between two, three or even four Annona species, we did
not come across any intermediate, presumably hybri-
dogenous plants. Apparently there are strong hybridiza-
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
tion barriers between all six species. Different ploidy
levels certainly also act as crossing barriers: an example
might be A. dioica (diploid) and A. coriacea (hexaploid;
Morawetz 1984a, 1986a), two species which have their
flowering peaks at approximately the same time and are
even pollinated by the same beetle species. However, at
other sites, hybridization between Annona species does
seem to occur and we detected such a hybrid swarm, sup-
posedly as result of mixing of A. coriacea, A. malmeana R.
E. Fries and A. crotonifolia Mart. in Mato Grosso, Brazil;
Silberbauer-Gottsberger et al. 1997).
Therefore, the staggered flowering and the alternation
of the pollinators seems to be more an adaptation for
diminishing competition between the different species.
Pollen flow is not strongly interrupted but is more evenly
distributed between different individuals of the same
Annona species. However, at the end of the flowering
season of one Annona species, the individuals of the same
beetle species gradually intensify visitation of another
Annona species, being attracted by similar floral odor
components. In this way the beetles are maintained and
concentrated at the flowers of a particular Annona species
before they change to another one. For 3–4 months, the
beetles find feeding and mating places. This situation, as
described for the Minas Gerais site (Brazil), might not
be restricted only to the semi-open cerrado savannas.
We studied similar phenomena concerning visitation of
Araceae by Cyclocephala in the humid Atlantic rain
forests and restingas of eastern Brazil (Gottsberger,
unpublished) and of Annonaceae, Arecaceae, Araceae and
Cyclanthaceae in Central Amazonia (Küchmeister et al.
1998).
In the classification of Annona by Safford (1914) and
Fries (1931, 1959), which is still the only available sys-
tematic treatments of the genus, 17 sections for the New
and Old World species are recognized. Based on mor-
phological characters, such as the number of petals, esti-
vation of the inner petals, choripetaly or sympetaly, free
or fused carpels in the flowering stage and others, species
of the sections Annona, Macrantha, Ulocarpus, Campicola
Fig. 3 Staggered flowering peri-
ods of six co-occurring Annona
spp. and their main pollinating
Cyclocephala species, observed
at Indianópolis, Minas Gerais,
Brazil, from October 1986 to
January 1987. C. qu. punctata = C.
quatuordecimpunctata.
 P O L L I N AT I O N A N D E V O L U T I O N I N N E O T R O P I C A L A N N O N A C E A E
and Psammogenia are generally considered as more
primitive than, for example, species of the sections
Gamopetalum, Oligantha and Atractanthus. Based on a
similar set of morphological characters, species of the sec-
tions Atta, Chelenocarpus, Ilama, Saxigena, Annonula and
Annonella, with only three petals, quite obviously are even
more derived. However, there is apparently no linear
development from Annona species with, for example, six
petals to those with only three petals, or from
choripetalous to gamopetalous ones. The presently rec-
ognized sections of Annona represent entities based on
morphological features which seem to have evolved par-
allel from several related groups. This reticulate situation,
for instance, is shown by the relationships of section
Annona with Psammogenia; Macrantha with Campicola;
Gamopetalum with Pilannona and Rollinia; Oligantha with
Phelloxylon and Atta, etc. (see Fries 1931).
The genus Annona seems to have evolved and
diversified in the forests of the Amazon Basin and adja-
cent areas, whereas Central Brazilian cerrados and the
West Indies represent secondary centers of diversification
(Fries 1931). Cytological studies have demonstrated that
a development from diploid Annona species of humid,
forested areas to tetra- or even hexaploid species of
open, xeric vegetation types has repeatedly occurred in
different sections (Morawetz 1984a,b, 1986a,b; Sauer &
Ehrendorfer 1984).
Many of the more morphologically primitive repre-
sentatives of Annona show pollination by dynastids. As
far as we now know, it seems that Annona evolved as a
genus pollinated by dynastid scarab beetles. As shown by
the floral ecology (e.g. A. muricata and A. montana; Webber
1981a), this development had already occurred in the
forest species.
Obviously, there was not much change in flower
biology when newly differentiated species invaded more
xeric savanna regions. A stronger competition for the
same pollinator might have been the reason for the more
pronounced thermogenesis and odor emission of some
savanna species. In contrast, staggered flowering with
alternating attraction of different beetle species
(Gottsberger 1989a) could have reduced this competition.
All species of the derived sections Oligantha, Atractan-
thus, Atta, Chelenocarpus, Ilama, Saxigena, Annonula and
Annonella possess relatively small flowers with small
floral chambers. Large dynastid scarab beetles are unable
to enter these small pollination chambers. As far as is
known for species of the section Atta, small Nitidulidae
are attracted by the fruity odor of the flowers and polli-
nate them (Wester 1910; Webber 1981a; Gazit et al. 1982).
In the genus Rollinia, which has probably been derived
from one of the gamopetalous taxa of Annona, a very
similar development has apparantly taken place, consist-
ing of a reduction of the floral chamber and a change of
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
149
odors, which tend to be fruity and attract small Nitiduli-
dae and Staphylinidae beetles.
In contrast to the large scarab beetle-pollinated Annona
species, which function in the evening and during the
night and attract the beetles basically by odor, the small-
flowered Annona species of section Atta and the species of
Rollinia possess flowers which show a tendency to attract
the pollinators during daytime. In addition to odor, they
use visual attractants. The curious, wing-like, enlarged
outer petals of the Rollinia flowers are showy organs. The
nitidulid beetles first alight on them and only afterwards
penetrate the small odoriferous pollination chamber
(Webber 1981a, 1982).
Annona is an example of a genus in which a progres-
sion from large to small flowers has occurred. It is a
highly derived genus within the Annonaceae (Fries 1959).
The fact that it is essentially a dynastid scarab beetle-
pollinated group may indicate that it is also a relatively
recent group. As entomologists have shown, dynastid
scarab beetles apparently are late-comers in the evolution-
ary history of beetles, probably not having evolved before
the Tertiary period (Crowson 1981 and personal com-
munication, 1986, Willemstein 1987), whereas most other
flower-visiting beetle groups have existed at least since
the Cretaceous period. This is in agreement with the fossil
record of the Annonaceae. Pollen of the Annona type is
known from the Eocene and Oligocene periods
(Willemstein 1987). The dynastid scarab beetle pollination
syndrome with nocturnal heating and strong odor
emission of the flowers or inflorescences has evolved in a
parallel and amazingly similar way in Annona, Duguetia,
Malmea, Cymbopetalum (Annonaceae); Philodendron, Cala-
dium, Dieffenbachia (Araceae); Victoria, Nymphaea (Nym-
phaeaceae); Bactris, Astrocaryum (Arxecaceae); Cyclanthus
(Cyclanthaceae); and several other genera. Considering
the physiological processes involved in thermogenic res-
piration and the morphological adaptations of the flowers
or inflorescences required for receiving and maintaining
such large and voracious visitors without being entirely
destroyed or becoming functionally obsolete, the dynas-
tid scarab beetle pollination syndrome has to be regarded
as being highly evolved (Gottsberger 1989b).
With respect to pollination and evolution in the
Annonaceae, more ‘conservative’ and ‘active’ genera may
be distinguished. The genus Guatteria, in which nearly all
species have uniform floral characters and are pollinated
by fruit-eating nitidulids, may serve as an example for the
former. The Annona–Rollinia group contrasts with Guatte-
ria. When the diverse flowering events, rhythms of anthe-
sis and pollination modes of this group are related
to distribution, habitat, habit, chromosome numbers
and general flower morphology, it seems that the
Annona–Rollinia group has undergone active differentia-
tion and radiation towards pollination by several beetle
150 G. GOTTSBERGER
groups. Annona apparently started with large flowers pol-
linated by large dynastid beetles; subsequently, its flowers
diversified and adapted to smaller nitidulid, staphylinid,
chrysomelid and curculionid beetles. In any case, flower
biology in Annona can be interpreted as an indication that
this group has undergone more active evolutionary radia-
tion than Guatteria.
Flower biological differentiation and evolution
in neotropical Annonaceae
When considering the flower differentiation of Annon-
aceae in the Neotropics, a different evolutionary picture
of the family emerges.
One morphological character of flowers of the
Annonaceae which is particularly important in this
respect is the stamen. The most remarkable feature of the
small flowers (e.g. Bocageopsis multiflora and Oxandra
euneura), is the form of the stamens which have an acute,
tongue-shaped connective prolongation. This connective
tongue is found in the genera Stenanona, Oxandra,
Deeringothamnus, Bocageopsis, Onychopetalum, Anaxagorea,
Trigynaea, Bocagea, Tetrameranthus and Cananga (Kessler
1993). However, it is often not present in all species of a
genus and sometimes only in part of the stamens of a
flower. In the supposedly closest relatives of the
Annonaceae, the Myristicaceae, Canellaceae and Eupo-
matiaceae (Cronquist 1981) or, following other authors
(Takhtajan 1969; Endress 1980; Kessler 1993), the Eupo-
matiaceae, Magnoliaceae, Myristicaceae and Austrobai-
leyaceae, we find stamen structures comparable with
those of the annonaceous genera mentioned above. Mag-
noliaceae, Austrobaileyaceae and Eupomatiaceae show
the laminar stamen type in which the pollen sacs are
imbedded adaxially, abaxially or laterally. In these fami-
lies, the laminar stamens do not bear structures that are
unequivocally identifiable as filament, connective and
anther. In such stamens, the sterile laminar part almost
always exceeds the pollen sacs in length.
The laminar stamen structure of Bocageopsis, Oxandra
and many other Annonaceae is comparable with similar
stamen structures in the related Magnoliid families. It
seems to represent the plesiomorphic stamen type within
the Annonaceae and the disc-like sclerified connective
shield should then be regarded as a secondary and
modified structure, which is especially prominent in the
beetle-pollinated Annonaceae, in which the stamens
with their connective shields form a kind of antipreda-
tor structure (Gottsberger 1988, 1992, 1993). This
advanced character of the sclerified connective shields
has already been recognized by Cronquist (1968): ‘The
prominently exserted connective seen in so many
members of the Annonaceae is merely a vestige of the
ancestral lamina’.
© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
In the neotropical Annonaceae, most studies demon-
strated the prevalence of beetle pollination. These beetle-
pollinated species apparently have specialized flower
characters, such as thick petals, hard connective shields
and strong, sticky, resinous stigmatic exudates, which
appear to protect the reproductive organs against the
gnawing beetle species. In contrast, species visited only
by Thysanoptera or small, pollen-eating non-destructive
beetles which do not gnaw on flower tissues, often bear
the laminar stamen type with the so-called, tongue-like
prolongation.
Thysanoptera are small, slender insects with rasping
and piercing mouthparts, which often suck on floral
structures but do not really harm tissues when not
appearing in large crowds (d’Araújo & Silva; Jacobs &
Renner 1974; Reed 1970; Kirk 1984). In Annonaceae
flowers, thrips were found in Oxandra and Trigynaea
species by Schatz (1987a) in Trigynaea guianensis by Van
Tol & Meijdam (1991), in Xylopia aromatica by Gottsberger
(1994), and in Bocageopsis multiflora and Oxandra euneura
by Webber & Gottsberger (1995, 1997). Thrips are in-
volved also in the pollination of other primitive angio-
sperms (Thien 1980; Gottsberger et al. 1980; Kirk 1985;
Pellmyr et al. 1990).
The rove beetles (Staphylinidae) are an old beetle
group, known at least since the Jurassic period (Crowson
1981). The species that visit flowers are relatively small
and live on pollen (Costa Lima 1952). The small rove
beetle species detected in the Oxandra flowers did not
gnaw on tissues but apparently were eating pollen grains
only.
It needs to be noted that both species studied by
Webber & Gottsberger (1995b), Bocageopsis multiflora, a
thrips-pollinated species; and Oxandra euneura, exhibiting
a mixed pollination by thrips and staphylinids, follow a
2-day rhythm. The attraction of the insects principally
takes place during the female stage of the flower and their
release in the male stage after the floral chamber opens
and the flower parts are dropped. This rhythm is essen-
tially the same as that of many beetle-pollinated species
(Webber 1981a, 1981b; Gottsberger 1989a; Webber &
Gottsberger 1993, 1994a,b).
The flower-visiting thrips of Bocageopsis and the pre-
dominant staphilinid beetles in Oxandra are comparable,
as both are not really harmful to flower tissues and only
suck liquids and/or eat pollen. It is tempting to speculate
that the stamens could maintain their original laminar
form (see Gottsberger 1992, 1993) because of the low
selection pressure exerted by these non-destructive
insects. With attraction of beetle groups with gnawing
mouth parts and more destructive habits, an enlargement
of Annonaceae flowers by thickening of tissues or by pro-
viding excess tissues can be envisioned. Further flower
modifications may also involve the formation of special
 P O L L I N AT I O N A N D E V O L U T I O N I N N E O T R O P I C A L A N N O N A C E A E
nutritious tissues (Gottsberger et al. 1998) to deviate
beetles from other structures.
The need for better protection of the reproductive
organs against beetles caused a modification of the
loosely packed laminar stamens into an androeceum with
tightly packed, narrowly oblong stamens and the forma-
tion of hard, sclerified connective shields, as well as
copious resinous stigmatic exudates. A development from
small flowers with relatively few reproductive organs and
with stamens lacking an elaborate sterile connective part
to larger flowers with more numerous reproductive
organs and a better protection against beetles was also
recently considered by Endress (1994a,b; see also Deroin
& Le Thomas 1989). The strong influence of beetle polli-
nation upon flower structures, at least in neotropical
Annonaceae, seems quite obvious (Gottsberger 1989a,b,
1992, 1993). However, the supposed evolutionary steps
from unspecialized to more specialized pollination and
the morphological and physiological correlates are only
vaguely understood at present.
Acknowledgements
This paper benefited from comments and linguistic
improvements by the late Karl Cramer, Zürich and Sigrid
Liede, Bayreuth. Field work was supported by the
German Research Council (DFG).
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