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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:


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

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144 G. GOTTSBERGER

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

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

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146 G. GOTTSBERGER

period. Although during observations in August 1988, no Functional diversification and flower evolution
pollinators arrived, we suspect this species to be polli- in the genera Guatteria and Annona
nated by small flies (G. Gottsberger, unpublished). The
thin, somewhat transparent tissue at the base of the petals As far as pollination is concerned, a genus such as Guatte-
is suggestive of light windows, which are characteristic ria appears to be conservative. With a few exceptions, the
for other myiophilous species with kettle flowers. species studied to date show similar floral characters and
It is suspected that some Sapranthus species and pollination mechanisms. Pollinators of this largest genus
Asimina triloba (L.) Dun. supposedly are pollinated by of the family are mostly fruit-eating nitidulids. Nearly all
carrion or dung flies. Their flowers are of a dark maroon species are uniform with respect to flower biology and
or purple color and exhale an unpleasant odor. Observa- seem to have adapted to the nitidulids as pollinators.
tions, however, are scarce and not well documented (see In contrast, the genus Annona has diversified with
Janzen 1983 for Sapranthus palanga R. E. Fries, on which respect to flower morphology and pollination (Webber
flowers Olesen 1992 detected a few beetles). Therefore, it 1981a, 1981b; Gottsberger 1989a). Examples of the differ-
is not yet clear whether these species are in fact pollinated ent floral rhythms and pollination mechanisms are given
by flies or by beetles, or by both. In North America, below.
Asimina obovata (Willd.) Nash and A. pygmaea (Bartr.) Dun. The large flowers of Annona coriacea Mart. are borne at
are pollinated by Scarabaeidae and Cerambycidae the end of twigs in an inclined, pendulous position. In
(Norman & Clayton 1986). 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
Pollination by beetles, thrips and flies and
cone of the reproductive organs become heated (Fig. 2).
corresponding floral syndromes
The strong fragrance exhaled by the flowers during their
In conclusion, the present state of knowledge indicates heating attracts dynastid scarab beetles. Among them
that cantharophilous species are by far the most frequent Cyclocephala atricapilla Mannerh. is the most common and
in the neotropical Annonaceae, followed by some species most numerous flower visitor within the distribution of
or species groups pollinated by Thysanoptera; only a few A. coriacea (Gottsberger 1989a). The beetles arrive in a zig-
are myiophilous or perhaps even sapromyiophilous (see zag-like flight, alight on the outside of the flower and
Schatz 1987c; Gottsberger 1992, 1993). force their way into the pollination chamber through the
Each of these three main pollination types in the imbricate inner petals. This floral chamber easily shelters
Annonaceae is correlated with some special flower char- up to 10 or 15 beetles. The number of visiting beetles
acters. The beetle-pollinated Annonaceae usually produce varies from flower to flower and from place to place. One
strong fruity, spicy or even offensive floral odors, their to 10 beetles per flower are the rule, but we also have
flowers are often pendulous and the petals are yellowish, noted flowers with 70 individuals. In such overcrowded
greenish or reddish. The Annonaceae pollinated by thrips flowers, the flower chambers were opened and the petals
have white or whitish, mostly commonly erect flowers. were widely spread. Immediately after alighting the
Their stamens are not so densely clustered as those of beetles may copulate. They also start to gnaw at the inner
the cantharophilous Annonaceae and their floral odor basal side of the three inner petals. Each inner petal has
is pleasant and sweet. Supposedly fly-pollinated An- two lateral regions with special food tissue. In these
nonaceae flowers remain open and do not fold their places the visited flowers show two gnawing marks
petals over their reproductive organs. Their floral odors (Gottsberger et al. 1998). During the second evening of
are imperceptible or, in the sapromyophilous species, anthesis, a second temperature elevation takes place
strong and unpleasant (carrion-like). (Fig. 2). The already dehisced stamens detach themselves
That odor compounds may play a major role in polli- from the receptacle and fill up the chamber, together with
nator attraction was suspected long ago (see Gottsberger the released pollen tetrads.
1970; Pellmyr & Thien 1986; Schatz 1987a, 1987b, 1990). The warming of the flower and the scent volatilization
For example, our first results on the identification of floral in the second night attract another crowd of beetles which
odor compounds, e.g. Anaxagorea dolichocarpa Sprague et also enter the floral chamber, and together with the
Sandw., a species with a strong acetonic fruity odor, beetles from the first night, become covered with the
showed a marked prevalence of fruit esters, while Annona released, sticky pollen-grain tetrads. The pollen is now
squamosa L. has a different odor compound profile with the main source of food for the beetles. With the shedding
several monoterpenes and sesquiterpenes, besides esters of the petals, the beetles are released from the flower. The
(G. Gottsberger et al. in preparation). Both species are beetles transfer pollen by flying with their pollen load to
apparently pollinated by nitidulid beetles (Gottsberger warm receptive, first-night flowers, thus guaranteeing
1989b; Webber 1996). pollination.

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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 147

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 until the third night. A third group of flowers, after a short
flowering, with a warming-up of its flowers during two female stage in the early hours of the first night, changes
subsequent nights. The temperature peak of approxi- to the male phase as early as the evening or during the
mately 34°C is attained around 21.00 h on the first night. second half of the same night. Such one-day flowers drop
A second peak on the following night is reached approxi- shortly after becoming male-active, either in the evening
mately 1 h earlier, when the petals are shed and the or in the early morning hours. As several flowers enter
pollen-covered beetles fly away (Fig. 2). As the release of their receptive female stage only during the second half
pollen-carrying beetles takes place before younger of their first active night, flowers in male and in female
flowers have reached the peak of their female phase, high stages are present during the whole night. The tem-
effectivity of pollen transfer is achieved. perature elevation during female and male stages is
In contrast, Annona crassiflora Mart. has a distinct one- accompanied by the emission of a fruit-like, pleasant odor
night rhythm of flowering (Gottsberger 1989a). Tempera- which attracts mainly Cyclocephala quatuordecimpunctata
ture elevation occurs during the female phase in the early Mannerh. and, to a lesser extent, also C. atricapilla (in a
evening hours; the odor emission attracts dynastid scarab relation of 10:1).
beetles. From approximately 19.00 h onwards, the first On the second evening of anthesis, the flowers of A.
individuals of Cyclocephala atricapilla alight on the flowers cornifolia show some changes. The floral parts are more
and enter the floral chamber. During the first half of the lax, the petals spread and the floral chamber is quite open;
night, the stigmatic head is usually shed and the dehisced up to 10 beetles were seen sitting and gnawing and
stamens detach and fall into the floral chamber, together copulating in such pendulous flowers. Petals of heavily
with the pollen. In the second half of the same night, the visited flowers had been almost entirely consumed and
petals also detach from the flower receptacle. Annona destroyed.
crassiflora is a gamopetalous species and the six petals are In species with large flowers and large pollination
usually maintained as a unit even when being dropped. chambers the interesting phenomenon of thermogenesis
Most beetles remain inside the fallen ring of petals on the occurs, which is the warming-up of flowers during anthe-
ground. Thus, to leave the flowers on the second evening sis. Annona coriacea (Fig. 2), holds the record for flower
they crawl out of the fallen petals. Covered with sticky, temperature elevation in the Annonaceae to date, attain-
pollen-grain tetrads, they approach newly opened odori- ing as much as 35°C during a short period at dusk, a
ferous flowers in the female stage and pollinate them. temperature 14–15 °C warmer than the surrounding air.
In Annona cornifolia St. Hil. different flowers have dif- Annona montana Macf. with approximately 32°C
ferent flowering rhythms (Gottsberger 1989a). The major- maximum temperature (Webber 1981a) is approximately
ity of the protogynous flowers are active during two or 7 °C warmer than the air. In A. sericea (Webber 1981b), A.
three subsequent nights. Some of them are in the female dioica, A. cornifolia (Gottsberger 1989a), and A. muricata
phase in the first night of anthesis and become male as (Van Tol & Meijdam 1991) temperature elevations of
early as in the second night, while others are female- 6–8∞C have also been measured. By inference, and
active during two nights and do not enter the male stage judging from floral construction, 50–55 of the approxi-

© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
148 G. GOTTSBERGER

mately 110 known Annona species are likely to exhibit the tion barriers between all six species. Different ploidy
phenomenon of floral heating. levels certainly also act as crossing barriers: an example
It was surprising to find that there is little specificity might be A. dioica (diploid) and A. coriacea (hexaploid;
between the dynastid scarab beetle species and the dif- Morawetz 1984a, 1986a), two species which have their
ferent Annona species. This became evident not only in the flowering peaks at approximately the same time and are
cerrado areas (central Brazilian area) where such rela- even pollinated by the same beetle species. However, at
tionships were studied (Gottsberger 1989a), but also in the other sites, hybridization between Annona species does
Amazonian region Manaus, where A. foetida (A. C. seem to occur and we detected such a hybrid swarm, sup-
Webber and G. Gottsberger, unpublished) shares the same posedly as result of mixing of A. coriacea, A. malmeana R.
pollinator, Cyclocephala undata (Olivier), with Cym- E. Fries and A. crotonifolia Mart. in Mato Grosso, Brazil;
bopetalum euneurum N. A. Murray (Webber & Gottsberger Silberbauer-Gottsberger et al. 1997).
1993), Duguetia ulei and D. riparia (Webber & Gottsberger Therefore, the staggered flowering and the alternation
1996). For example, near Indianópolis in the State of of the pollinators seems to be more an adaptation for
Minas Gerais, Brazil, six Annona species belonging to five diminishing competition between the different species.
or six different sections were growing closely together. Pollen flow is not strongly interrupted but is more evenly
Only two dynastid species, namely Cyclocephala atricapilla distributed between different individuals of the same
and C. quatuordecimpunctata, were the main pollinators of Annona species. However, at the end of the flowering
all of them. Cyclocephala atricapilla was the main or exclu- season of one Annona species, the individuals of the same
sive pollinator of A. coriacea, A. crassiflora, A. dioica and A. beetle species gradually intensify visitation of another
monticola, the flowers of which emit a very similar, some- Annona species, being attracted by similar floral odor
what unpleasant odor. However, the flowers of A. tomen- components. In this way the beetles are maintained and
tosa and A. cornifolia, which have a pleasant fruity odor, concentrated at the flowers of a particular Annona species
are visited more intensively by C. quatuordecimpunctata. before they change to another one. For 3–4 months, the
Although all six species flowered in the rainy season beetles find feeding and mating places. This situation, as
from October to January and although there was a broad described for the Minas Gerais site (Brazil), might not
overlapping of flowering periods, flowering was some- be restricted only to the semi-open cerrado savannas.
what staggered with more or less separate peaks (Fig. 3). We studied similar phenomena concerning visitation of
The more interesting fact, however, was that the six Araceae by Cyclocephala in the humid Atlantic rain
species flowered in such a way that predominantly C. forests and restingas of eastern Brazil (Gottsberger,
quatuordecimpunctata-pollinated species were alternating unpublished) and of Annonaceae, Arecaceae, Araceae and
with C. atricapilla-pollinated ones. This arrangement Cyclanthaceae in Central Amazonia (Küchmeister et al.
probably reduces interspecific gene flow. All species are 1998).
members of different systematic groups except for A. In the classification of Annona by Safford (1914) and
crassiflora and A. cornifolia, which probably belong to the Fries (1931, 1959), which is still the only available sys-
same section, Gamopetalum. Although they show a broad tematic treatments of the genus, 17 sections for the New
overlap of flowering periods and in spite of identical and Old World species are recognized. Based on mor-
species of flower visitors permitting some pollen flow phological characters, such as the number of petals, esti-
between two, three or even four Annona species, we did vation of the inner petals, choripetaly or sympetaly, free
not come across any intermediate, presumably hybri- or fused carpels in the flowering stage and others, species
dogenous plants. Apparently there are strong hybridiza- 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.

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and Psammogenia are generally considered as more odors, which tend to be fruity and attract small Nitiduli-
primitive than, for example, species of the sections dae and Staphylinidae beetles.
Gamopetalum, Oligantha and Atractanthus. Based on a In contrast to the large scarab beetle-pollinated Annona
similar set of morphological characters, species of the sec- species, which function in the evening and during the
tions Atta, Chelenocarpus, Ilama, Saxigena, Annonula and night and attract the beetles basically by odor, the small-
Annonella, with only three petals, quite obviously are even flowered Annona species of section Atta and the species of
more derived. However, there is apparently no linear Rollinia possess flowers which show a tendency to attract
development from Annona species with, for example, six the pollinators during daytime. In addition to odor, they
petals to those with only three petals, or from use visual attractants. The curious, wing-like, enlarged
choripetalous to gamopetalous ones. The presently rec- outer petals of the Rollinia flowers are showy organs. The
ognized sections of Annona represent entities based on nitidulid beetles first alight on them and only afterwards
morphological features which seem to have evolved par- penetrate the small odoriferous pollination chamber
allel from several related groups. This reticulate situation, (Webber 1981a, 1982).
for instance, is shown by the relationships of section Annona is an example of a genus in which a progres-
Annona with Psammogenia; Macrantha with Campicola; sion from large to small flowers has occurred. It is a
Gamopetalum with Pilannona and Rollinia; Oligantha with highly derived genus within the Annonaceae (Fries 1959).
Phelloxylon and Atta, etc. (see Fries 1931). The fact that it is essentially a dynastid scarab beetle-
The genus Annona seems to have evolved and pollinated group may indicate that it is also a relatively
diversified in the forests of the Amazon Basin and adja- recent group. As entomologists have shown, dynastid
cent areas, whereas Central Brazilian cerrados and the scarab beetles apparently are late-comers in the evolution-
West Indies represent secondary centers of diversification ary history of beetles, probably not having evolved before
(Fries 1931). Cytological studies have demonstrated that the Tertiary period (Crowson 1981 and personal com-
a development from diploid Annona species of humid, munication, 1986, Willemstein 1987), whereas most other
forested areas to tetra- or even hexaploid species of flower-visiting beetle groups have existed at least since
open, xeric vegetation types has repeatedly occurred in the Cretaceous period. This is in agreement with the fossil
different sections (Morawetz 1984a,b, 1986a,b; Sauer & record of the Annonaceae. Pollen of the Annona type is
Ehrendorfer 1984). known from the Eocene and Oligocene periods
Many of the more morphologically primitive repre- (Willemstein 1987). The dynastid scarab beetle pollination
sentatives of Annona show pollination by dynastids. As syndrome with nocturnal heating and strong odor
far as we now know, it seems that Annona evolved as a emission of the flowers or inflorescences has evolved in a
genus pollinated by dynastid scarab beetles. As shown by parallel and amazingly similar way in Annona, Duguetia,
the floral ecology (e.g. A. muricata and A. montana; Webber Malmea, Cymbopetalum (Annonaceae); Philodendron, Cala-
1981a), this development had already occurred in the dium, Dieffenbachia (Araceae); Victoria, Nymphaea (Nym-
forest species. phaeaceae); Bactris, Astrocaryum (Arxecaceae); Cyclanthus
Obviously, there was not much change in flower (Cyclanthaceae); and several other genera. Considering
biology when newly differentiated species invaded more the physiological processes involved in thermogenic res-
xeric savanna regions. A stronger competition for the piration and the morphological adaptations of the flowers
same pollinator might have been the reason for the more or inflorescences required for receiving and maintaining
pronounced thermogenesis and odor emission of some such large and voracious visitors without being entirely
savanna species. In contrast, staggered flowering with destroyed or becoming functionally obsolete, the dynas-
alternating attraction of different beetle species tid scarab beetle pollination syndrome has to be regarded
(Gottsberger 1989a) could have reduced this competition. as being highly evolved (Gottsberger 1989b).
All species of the derived sections Oligantha, Atractan- With respect to pollination and evolution in the
thus, Atta, Chelenocarpus, Ilama, Saxigena, Annonula and Annonaceae, more ‘conservative’ and ‘active’ genera may
Annonella possess relatively small flowers with small be distinguished. The genus Guatteria, in which nearly all
floral chambers. Large dynastid scarab beetles are unable species have uniform floral characters and are pollinated
to enter these small pollination chambers. As far as is by fruit-eating nitidulids, may serve as an example for the
known for species of the section Atta, small Nitidulidae former. The Annona–Rollinia group contrasts with Guatte-
are attracted by the fruity odor of the flowers and polli- ria. When the diverse flowering events, rhythms of anthe-
nate them (Wester 1910; Webber 1981a; Gazit et al. 1982). sis and pollination modes of this group are related
In the genus Rollinia, which has probably been derived to distribution, habitat, habit, chromosome numbers
from one of the gamopetalous taxa of Annona, a very and general flower morphology, it seems that the
similar development has apparantly taken place, consist- Annona–Rollinia group has undergone active differentia-
ing of a reduction of the floral chamber and a change of tion and radiation towards pollination by several beetle

© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
150 G. GOTTSBERGER

groups. Annona apparently started with large flowers pol- In the neotropical Annonaceae, most studies demon-
linated by large dynastid beetles; subsequently, its flowers strated the prevalence of beetle pollination. These beetle-
diversified and adapted to smaller nitidulid, staphylinid, pollinated species apparently have specialized flower
chrysomelid and curculionid beetles. In any case, flower characters, such as thick petals, hard connective shields
biology in Annona can be interpreted as an indication that and strong, sticky, resinous stigmatic exudates, which
this group has undergone more active evolutionary radia- appear to protect the reproductive organs against the
tion than Guatteria. 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
Flower biological differentiation and evolution
the laminar stamen type with the so-called, tongue-like
in neotropical Annonaceae
prolongation.
When considering the flower differentiation of Annon- Thysanoptera are small, slender insects with rasping
aceae in the Neotropics, a different evolutionary picture and piercing mouthparts, which often suck on floral
of the family emerges. structures but do not really harm tissues when not
One morphological character of flowers of the appearing in large crowds (d’Araújo & Silva; Jacobs &
Annonaceae which is particularly important in this Renner 1974; Reed 1970; Kirk 1984). In Annonaceae
respect is the stamen. The most remarkable feature of the flowers, thrips were found in Oxandra and Trigynaea
small flowers (e.g. Bocageopsis multiflora and Oxandra species by Schatz (1987a) in Trigynaea guianensis by Van
euneura), is the form of the stamens which have an acute, Tol & Meijdam (1991), in Xylopia aromatica by Gottsberger
tongue-shaped connective prolongation. This connective (1994), and in Bocageopsis multiflora and Oxandra euneura
tongue is found in the genera Stenanona, Oxandra, by Webber & Gottsberger (1995, 1997). Thrips are in-
Deeringothamnus, Bocageopsis, Onychopetalum, Anaxagorea, volved also in the pollination of other primitive angio-
Trigynaea, Bocagea, Tetrameranthus and Cananga (Kessler sperms (Thien 1980; Gottsberger et al. 1980; Kirk 1985;
1993). However, it is often not present in all species of a Pellmyr et al. 1990).
genus and sometimes only in part of the stamens of a The rove beetles (Staphylinidae) are an old beetle
flower. In the supposedly closest relatives of the group, known at least since the Jurassic period (Crowson
Annonaceae, the Myristicaceae, Canellaceae and Eupo- 1981). The species that visit flowers are relatively small
matiaceae (Cronquist 1981) or, following other authors and live on pollen (Costa Lima 1952). The small rove
(Takhtajan 1969; Endress 1980; Kessler 1993), the Eupo- beetle species detected in the Oxandra flowers did not
matiaceae, Magnoliaceae, Myristicaceae and Austrobai- gnaw on tissues but apparently were eating pollen grains
leyaceae, we find stamen structures comparable with only.
those of the annonaceous genera mentioned above. Mag- It needs to be noted that both species studied by
noliaceae, Austrobaileyaceae and Eupomatiaceae show Webber & Gottsberger (1995b), Bocageopsis multiflora, a
the laminar stamen type in which the pollen sacs are thrips-pollinated species; and Oxandra euneura, exhibiting
imbedded adaxially, abaxially or laterally. In these fami- a mixed pollination by thrips and staphylinids, follow a
lies, the laminar stamens do not bear structures that are 2-day rhythm. The attraction of the insects principally
unequivocally identifiable as filament, connective and takes place during the female stage of the flower and their
anther. In such stamens, the sterile laminar part almost release in the male stage after the floral chamber opens
always exceeds the pollen sacs in length. and the flower parts are dropped. This rhythm is essen-
The laminar stamen structure of Bocageopsis, Oxandra tially the same as that of many beetle-pollinated species
and many other Annonaceae is comparable with similar (Webber 1981a, 1981b; Gottsberger 1989a; Webber &
stamen structures in the related Magnoliid families. It Gottsberger 1993, 1994a,b).
seems to represent the plesiomorphic stamen type within The flower-visiting thrips of Bocageopsis and the pre-
the Annonaceae and the disc-like sclerified connective dominant staphilinid beetles in Oxandra are comparable,
shield should then be regarded as a secondary and as both are not really harmful to flower tissues and only
modified structure, which is especially prominent in the suck liquids and/or eat pollen. It is tempting to speculate
beetle-pollinated Annonaceae, in which the stamens that the stamens could maintain their original laminar
with their connective shields form a kind of antipreda- form (see Gottsberger 1992, 1993) because of the low
tor structure (Gottsberger 1988, 1992, 1993). This selection pressure exerted by these non-destructive
advanced character of the sclerified connective shields insects. With attraction of beetle groups with gnawing
has already been recognized by Cronquist (1968): ‘The mouth parts and more destructive habits, an enlargement
prominently exserted connective seen in so many of Annonaceae flowers by thickening of tissues or by pro-
members of the Annonaceae is merely a vestige of the viding excess tissues can be envisioned. Further flower
ancestral lamina’. modifications may also involve the formation of special

© 1999 Society for the Study of Species Biology, Plant Species Biology, 14, 143–152
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 151

nutritious tissues (Gottsberger et al. 1998) to deviate Endress P. K. (1994b) Shapes, sizes and evolutionary trends in
beetles from other structures. stamens of Magnoliidae. Botany Jahrb Syst 115: 429–460.
The need for better protection of the reproductive Fries R. E. (1931) Revision der Arten einiger Annonaceen-
Gattungen. Acta Horticultura Bergiani 10: 129–341, tables 1–
organs against beetles caused a modification of the
27.
loosely packed laminar stamens into an androeceum with Fries R. E. (1959) Annonaceae. In: Die Natürlichen Pflanzenfami-
tightly packed, narrowly oblong stamens and the forma- lien, 2nd edn (ed. H. Melchior), Band 17a II, pp. 1–171.
tion of hard, sclerified connective shields, as well as Duncker & Humblot, Berlin.
copious resinous stigmatic exudates. A development from Gazit S., Galon I. & Podoler H. (1982) The role of nitidulid beetles
small flowers with relatively few reproductive organs and in natural pollination of Annona in Israel. Journal of the
with stamens lacking an elaborate sterile connective part American Society of Horticultural Science 107: 849–852.
Gottsberger G. (1970) Beiträge zur Biologie von Annonaceen-
to larger flowers with more numerous reproductive
Blüten. Österreichische Botanische Zeitschrift, 118, 237–279.
organs and a better protection against beetles was also Gottsberger G. (1986) Some pollination strategies in neotropical
recently considered by Endress (1994a,b; see also Deroin savannas and forests. Plant Systematics and Evolution 152:
& Le Thomas 1989). The strong influence of beetle polli- 29–45.
nation upon flower structures, at least in neotropical Gottsberger G. (1988) The reproductive biology of primitive
Annonaceae, seems quite obvious (Gottsberger 1989a,b, angiosperms. Taxon 37: 630–643.
1992, 1993). However, the supposed evolutionary steps Gottsberger G. (1989a) Beetle pollination and flowering rhythm
of Annona spp. (Annonaceae) in Brazil. Plant Systematics and
from unspecialized to more specialized pollination and
Evolution 167: 165–187.
the morphological and physiological correlates are only Gottsberger G. (1989b) Comments on flower evolution and beetle
vaguely understood at present. pollination in the genera Annona and Rollinia (Annonaceae).
Plant Systematics and Evolution 167: 189–194.
Gottsberger G. (1992) Blütenbiologische Differenzierung bei
Acknowledgements Annonaceae. Botanikertagung September 1992, Berlin,
Tagungsband: 155–156.
This paper benefited from comments and linguistic Gottsberger G. (1993) Flower biological differentiation in
improvements by the late Karl Cramer, Zürich and Sigrid neotropical Annonaceae. Annonaceae Newsletter 9: 29–33.
Liede, Bayreuth. Field work was supported by the Gottsberger G. (1994) As Anonáceas do cerrado e a sua poliniza-
German Research Council (DFG). ção. Revista Brasileira de Biologia 54: 391–402.
Gottsberger G. & Silberbauer-Gottsberger I. (1988) Pollination
strategies of Annona species from the cerrado vegetation in
Brazil. Lagascalia 15: 665–672.
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