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Plant Div. Evol. Vol. 131/4, 263–362 Article
Published online January 19, 2016
© 2016 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de
DOI: 10.1127/pde/2015/0131-0085 1869-6155/2015/0131-0085 $ 25.00
Received June 9, 2015, in revised form September 25, 2015, accepted September 30, 2015
* In memory of the late Prof. Dr. Stefan Vogel, who died in November 5, 2015.
Generalist and specialist pollination in basal
angiosperms (ANITA grade, basal monocots,
magnoliids, Chloranthaceae and Ceratophyllaceae):
what we know now*
By Gerhard Gottsberger
With 3 gures and 2 tables
Abstract
An updated description of the pollination and reproductive biology of basal angiosperms is given to
show their principal associations with pollinating agents. The review considers members of the
ANITA grade, as well as some basal monocots, the magnoliids, Chloranthaceae and Ceratophyllaceae.
Morphological, physiological and behavioral characteristics of owers and their pollinating insects
are evaluated. Based on current evidence, early-divergent angiosperms were and are pollination gen-
eralists, even so there has been early specialization for either ies, beetles, thrips or bees. Although
there are many tendencies for development from generalist owers to specialist ones, there are also
reversals with the development from specialist owers to generalist ones. The earliest specialization
seems to be y pollination. Adaptations to more recently evolved insect groups, such as scarab beetles
or perfume-collecting euglossine bees, demonstrate that several basal angiosperm lines were exible
enough to radiate into modern ecological niches.
Keywords: generalist owers, oral specialization, protogyny, breeding systems, oral scent, ther-
mogenesis, ies, beetles, bees, thrips
Introduction
Phylogenetic studies of angiosperms resulted in the recognition of 413 families
by the Angiosperm Phylogeny Group (Bremer et al. 2009, APG III). Early-divergent
members of owering plants, commonly referred to as the “basal angiosperms”, are
treated in the APG III classication as comprising 28 families, wherein the most
basal grade, called ANITA, consists of the three clades Amborella (Amborellales),
Nymphaeales and Austrobaileyales, and the further clade magnoliids, consist-
ing of the orders Canellales, Piperales, Laurales and Magnoliales. Another order,
Chloranthales, is thought to be sister to the magnoliids. According to estimates by tax-
onomic authors in Kubitzki et al. (1993), the basal angiosperms recognized by APG III
total about 10,000 to perhaps 11,000 extant species. Several of the families have
only one (Amborellaceae, Austrobaileyaceae, Lactoridaceae, Gomortegaceae) or two
(Degeneriaceae, Himantandraceae, Atherospermataceae), probably relictual species,
eschweizerbart_xxx
264 G. Gottsberger, Pollination in basal angiosperms
while others have three to twenty species (Eupomatiaceae, Hydatellaceae, Cabombaceae,
Trimeniaceae, Canellaceae, Hydnoraceae, Saururaceae, Calycanthaceae), and still
others have more than twenty but less than hundred species, namely Nymphaeaceae,
Schisandraceae, Chloranthaceae, Winteraceae and Hernandiaceae. The families
Aristolochiaceae, Siparunaceae, Monimiaceae, Magnoliaceae and Myristicaceae com-
prise between one hundred to several hundreds of species. The three largest families
of the basal angiosperms are the Annonaceae (2300–2500 spp.), Lauraceae (2500–
3500 spp.) and Piperaceae (ca. 3000–3600 spp.).
In recent years, work aimed at resolving deep angiosperm phylogeny has pro-
gressed, and it is currently estimated that after the origin of angiosperms (viz., the
origin of the rst representatives of the ANITA group), the following divergence of
Mesangiospermae probably began several Mry later (e.g. Smith et al. 2010, Zeng
et al. 2014, Beaulieu et al. 2015). According to recent hypotheses, the rst mesan-
giosperm group to diverge were the monocots, followed by the magnoliids, then the
Chloranthaceae and Ceratophyllaceae, and after this the eudicots diverged (Zeng et al.
2014). Thus, all groups treated in the present paper had probably diverged before the
rapid diversication of the eudicots in the later Cretaceous. The monocots are a very
large entity (about 20% of angiosperm species) and much diversied group, and cannot
be treated here in its entirety. Only some data of three families of the early- divergent
monocot orders Acorales and Alismatales are presented, mainly to show some devel-
opments which apparently occurred in parallel in the basal monocots as well as in the
ANITA grade and the magnoliids. Thus, in addition to the 28 families mentioned above,
data on representatives of a further four families, namely the Ceratophyllaceae and the
monocot families Acoraceae, Alismataceae and Araceae are included in this review.
Basal angiosperms pollination and reproductive biology, continues to be a fasci-
nating eld of investigation. With respect to pollination biology, extant basal angio-
sperms exhibit both abiotic (rare) and biotic pollination; the most remarkable diversity
is found among the latter wherein ies, thrips, beetles, moths, cockroaches and even
bees have been found to act as pollen vectors (for reviews see e.g. Gottsberger 1974,
1977, 1988, 2012, Gottsberger et al. 1980, Thien 1980, Thien et al. 1985, 2000, 2009,
Bernhardt & Thien 1987, Endress 1990, 1994, 2010, Bernhardt 2000). Abiotic polli-
nation is rare among basal angiosperms and several members are wind-pollinated or
wind is an additional vehicle complementary to insects.
In this paper, pollination examples are drawn from the literature to nourish a discus-
sion of the principal associations of extant basal angiosperms to pollination agents, as
well as to show likely evolutionary shifts and adaptations. Another goal is to highlight
those groups exhibiting generalist pollination and those having developed specialist
pollination, e.g. by either ies, beetles, thrips or bees, and to evaluate morphological,
physiological and behavioral characteristics of owers and their pollinating insects
associated with the respective phenomena.
In general, pollination mode and pollinator type correspond to ower morphology.
Such characters as color, odor, and the amount of oral resources (commonly called
rewards) probably partly evolved as adaptations to the senses, behavior, and needs
of the pollinating animals. If these oral characters function like a lock and a key, or
nearly so, with respect to the pollinating animal, the oral biology of the plant species
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 265
is considered to be specialized; in the most extreme cases of specialization, owers are
pollinated by a single animal species or a single vector (wind or water). Alternately,
there are plant species that have evolved oral characters which permit pollination by
several animal orders. Such species may be pollinated by ies, bees, butteries and
beetles jointly. They are therefore called generalist or generalized with respect to their
pollination mode. One has to be aware that the above-mentioned two possibilities are
only the extremes of a continuum between broader and more narrow interrelation-
ships of pollinators and their respective owers. One fruitful way to look at it is that
plant species “explore” different niches with respect to pollination. In “generalists” a
broader proportion of the fauna can act as pollinators than in the “specialists”, which
are pollinated only by a few often closely related species of animals or even only by a
single one. For morphological and functional aspects of generalized owers see Frame
(2003a) and Weberling (2007).
One important point to be made is that ower/insect associations, especially in
generalist owers, but also in specialist ones, may have changed over time, and that
former partners of owers have been likely substituted by new ones. “What we observe
on a morphologically generalist ower now as a principal pollinator is not a depend-
able indicator of which insect was the principal pollinator a million or less years ago”
(Frame 2003a). It is also relevant to keep in mind that any ower visitor spectrum,
again particularly in generalist owers, depends on local abundance and presence of
potential pollinators and competition from other owers.
Pollination in the ANITA grade
Analyses of molecular data (e.g. Qiu et al. 1999) and of molecular data combined
with morphological data (e.g. Endress & Doyle 2009) indicated that the ANITA grade
(Amborella, Nymphaeales, Illicium, Trimeniaceae, Austrobaileyaceae) contains the
rst divergent angiosperm lineages.
Amborellaceae (Amborellales) with the single species Amborella trichopoda, is
considered the sister group to all other angiosperms (APG III 2009), followed by
Nymphaeales (Hydatellaceae, Cabombaceae, Nymphaeaceae) and Austrobaileyales
(Austrobaileyaceae, Schisandraceae, Trimeniaceae). Amborella, and especially mem-
bers of Nymphaeales and Austrobaileyales are thus key for reconstructing ancestral
character states and transitions that occurred during the earliest radiation of angio-
sperms (for informations on ower characters, oral biology and pollination of this
and all other groups mentioned in this review see Tables 1 and 2).
Amborella trichopoda (Amborellaceae, Amborellales)
This woody species from New Caledonia has attracted wide attention as it is thought to
be the sole living representative of a lineage that seems to have emerged at the base of
the owering plants. The owers of this dioecious species are far from what decades of
botanists have postulated and expected to be characteristic of a most basal angiosperm
representative. Its owers with several cream-colored tepals are borne in inorescences
and are small, 4–5 mm in diameter in staminate and 3–4 mm in diameter in pistillate
owers. Floral phyllotaxis is spiral and also appears partly whorled (Buzgo et al. 2004).
eschweizerbart_xxx
266 G. Gottsberger, Pollination in basal angiosperms
Table 1. Flower characters of basal angiosperms
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
ANITA
Amborellales
AMBORELLACEAE
Amborella trichopoda di nr 0.3–0.5 spir whorl cream 3–5 t 6–15 st 11–21 4–7
Nymphaeales
HYDATELLACEAE
Trithuria spp. bi uni mo di protogyn 0.1–0.2 greenish st 1 up to 19
CABOMBACEAE
Cabomba caroliniana bi protogyn c. 2.5 whorl white
yellow
pink
2 t 3+3 st 3–6 1–4
Brasenia schreberi bi protogyn c. 2 whorl purple-red 2 t 3+3 st 18–36 4–18
NYMPHAEACEAE
Nuphar spp.bi protogyn 2.5–4 spir-whorl yellow c. 5 ou t 5–14
in t many st many 5–23
Euryale ferox bi protogyn 1–3 spir-whorl blue violet 2–3 ou t 4
in t 20–35 st 78–92 8–16
Barclaya spp. bi protogyn 3–6 spir-whorl pink red ou t 4–5
in t 8–20 st many 8–14
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 267
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Nymphaea ondinea (former
Ondinea)bi protogyn c. 4 spir-whorl purple 3 ou t 4
in t 0–4 st many 5–23
Nymphaea subgen.
Nymphaea, Brachyceras,
Anecphya
bi protogyn up to 14 spir-whorl white
yellow
pink red
blue
2–4 ou t 3–5
in t 8–40 st many 8–35
N. subgen. Hydrocallis,
Lotos bi protogyn up to 20 spir-whorl white 2–5 ou t and
in t 16–30 st many up to 40
Victoria bi protogyn 25–30 spir-whorl white 2 out t 4
in t 50–70 st 150–200
ou sto 20
in sto 25
30–40
Austrobaileyales
AUSTROBAILEYACEAE
Austrobaileya scandens bi protogyn 5–6 spir yellow
brown
green
t 19–24 st 7–11
in sto 9–16 10–13
SCHISANDRACEAE
Schisandra glabra uni mo nr 1.3 spir green
yellow
crimson
t 8–13 st 4–7 25–30
S. henryi uni di nr 1–2 spir yellow
orange 2.5–4.5 t 6–10 st 14–40 50–60
S. sphenanthera uni di nr 1.6–1.7 spir yellow red up to 4 t 6–7
eschweizerbart_xxx
268 G. Gottsberger, Pollination in basal angiosperms
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Kadsura longipedunculata uni mo nr 1.5–2.6 spir red yellow 1–2.6 t c. 10 st c. 36 20–60
Illicium oridanum bi protogyn 3 spir red purple 12–14 t 24–28 st 30–39 c. 13
I. dunnianum bi protogyn c. 1 3–4 st 12–29 8
I. tsangii bi protogyn 0.8 2 st 7–10
TRIMENIACEAE
Trimenia moorei andmo protogyn 1.3 spir cream 2–5 t 2–38 st 7–25 1–2
BASAL MONOCOTS
Acorales
ACORACEAE
Acorus spp.bi protogyn c. 0.2 whorl greenish 3–5 t 3+3 st 3+3 2–3
Alismatales
ALISMATACEAE spp. bi uni mo di
poly protogyn
homo
protand
1–3 whorl-spir white pink
purple 1–2 s 3 p 3 st 3-many 3-many
ARACEAE spp. bi uni protogyn 0.1–0.3 whorl white
yellow
green
purple
1–4 t 3+3
2+2–9 st 3+3
2+2–8 3–1
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 269
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
MAGNOLIIDS
Canellales
CANELLACEAE spp. bi protogyn
WINTERACEAE
Takhtajania perrieri bi protogyn
Tasmannia piperita di bi white 10–12
Drimys brasiliensis bi protogyn c. 2 spir-whorl white 7–11 s 2 p
8–20 st 20–50 3–13
Pseudowintera colorata bi protogyn 1–1.3 spir-whorl greenish-
white 13–20 p 4–9 st 7–23 1–4
Zygogynum crassifolium,
Z. pancheri, Z. pauciorum bi protogyn 5–6 spir-whorl pale-
yellow
white
4–5 p c. 15 st c. 20 6–7
Z. baillonii, Z. pomiferum,
Z. stipitatum bi protogyn 3–5.5 spir-whorl yellow
orange
green
white
2 p 4–12 st 20–25 4–6
Piperales
ARISTOLOCHIACEAE
Saruma henryi bi protogyn whorl yellow s 3 p 3 st 12 6
Asarum europaeum bi protogyn c. 1 whorl dark-
purple 8–20 t 3 st 12 6
eschweizerbart_xxx
270 G. Gottsberger, Pollination in basal angiosperms
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Asarum caudatum and
other spp. bi protogyn 8–12 whorl dark-
maroon-
red
7–10 t 3 st 12 6
Aristolochia spp. bi protogyn 1–100 whorl brown
yellow
purple
green
2–9 t 3 st 6 6
LACTORIDACEAE
Lactoris fernandeziana gynmo protogyn 0.35 whorl green 1–2 t 3 st 6 3
HYDNORACEAE
Hydnora spp. bi protogyn 5.5–11 whorl pink red
purple 2–5-
more t 2–5 staminal
structure
3–5
3–5
Prosopanche americana
and spp. bi protogyn whorl t 3 3
PIPERACEAE
Piper spp., Pothomorphe
spp. and Peperomia spp. bi uni di mo
gynmo
andmo
protogyn
(protand) 0.1 whorl green
cream
yellow
white
6 -more 0 st 2–6 1–4
SAURURACEAE
Saururus cernuus bi protogyn c. 2.5 whorl white 0 st 6 4
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 271
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Laurales
CALYCANTHACEAE
Idiospermum australe bi uni
andmo protogyn c. 3.5 spir cream
white to
dull-
purple
3–4 t 32–52 st 10–20
in sto 8–10 1–5
Chimonanthus praecox bi protogyn 2.5–3 spir cream
yellow
dull-
purple
3–7 t 15–25 st 5–10 5–15
Calycanthus occidentalis
and C. oridus bi protogyn 4–8 spir red-brown
marroon 1–2 t 15–30 st 10–20
in sto 10–25 15–35
Calycanthus chinensis bi protogyn 4–7 spir whitish
pale-
yellow
t 21–34 st 18–19
sto 11–12 11–12
SIPARUNACEAE
Siparuna spp. uni mo di nr 0.3–1 whorl-spir cream
yellow
orange
9–24
(1–30) t 3–6 st 5–9
(1–100) 3–35
GOMORTEGACEAE
Gormortega keule bi protogyn 0.4–0.5 spir-whorl white t 7–10 st 7–13 2–5
ATHEROSPERMATACEAE
spp. bi protogyn
eschweizerbart_xxx
272 G. Gottsberger, Pollination in basal angiosperms
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
HERNANDIACEAE
Hernandia nymphaeifolia uni mo heterodi-
chogamie c. 1.5 whorl white 1 t 6–8 st 3 1
Sparattanthelium
botocudorum bi c. 0.5 whorl cream 1 t 4–5 st 4–5 1
MONIMIACEAE
Mollinedia spp. uni di nr 0.4–0.5 whorl-spir green
yellow up to 14 t 4 st many many
Wilkiea huegeliana uni mo nr 0.4 whorl-spir green
yellow 2–17 t 4 st 5–11 23–64
Tambourissa spp. group 1
and group 2 uni mo di nr 0.5–7.5 green
brown
pink
orange
red purple
7–20 t c. 10 st c.
30–1800 c.
35–2000
LAURACEAE spp. bi uni mo di protogyn 0.2–2 whorl green
yellow
white red
1–2 t 6 st 9 sto 3 1
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 273
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Magnoliales
MYRISTICACEAE
Myristica spp. uni di mo nr 0.4–0.6 whorl white
yellow
pink red
green
1–3.5 t 2–5 st 2–40 1
DEGENERIACEAE
Degeneria spp. bi protogyn 6–7 whorl-spir cream
yellow
magenta
pink
1–2 s 3 p
12–25 st many
in sto many 1
HIMANTANDRACEAE
Galbulimima spp. bi protogyn? 2–4 spir cream 0 st 13–130
ou sto 3–23
in sto 13–20
7–28
MAGNOLIACEAE
Magnolia ovata and
Magnolia spp. Neotropics bi protogyn up to 16 whorl-spir yellow
cream-
white
2 s 3, p 6–9 st many many
Magnolia spp. Liriodendron
spp.
Temp. Zones
bi protogyn up to 20 whorl- spir white
cream
yellow
purple
2–4 t 6 or
more st many many
eschweizerbart_xxx
274 G. Gottsberger, Pollination in basal angiosperms
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
EUPOMATIACEAE
Eupomatia spp. bi protogyn 3–4 spir cream
yellow 1–2 0 st 20–100
in sto 40–80 13–70
ANNONACEAE
Anaxagorea spp. bi protogyn 2–2.5 whorl-spir cream
yellow 2 s 3 p 6 st many
in sto 15–20 8–22
Guatteria spp. and other
genera
(small owers)
bi protogyn 3–8 whorl-spir yellow
brown 2 s 3 p 6 st many many
Annona spp. and other
genera
(large owers)
bi protogyn up to 8 whorl-spir white
cream
yellow
brown
2 s 3 p 6 st many many
Bocageopsis spp. and other
genera bi protogyn up to 1.5 whorl-spir green
cream
white
2 s 3 p 6 st many many
Pseuduvaria spp. and other
genera uni nr c. 1.5 whorl-spir cream
purple 2 s 3 p 6 st many many
Uvaria elmeri bi protogyn 3–4 whorl-spir cream
white
brown
2 s 3 p 6 st many many
Unonopsis spp. bi protogyn up to 1.5 whorl-spir cream 2 s 3 p 6 st many many
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 275
Taxa Sex
expression Dicho/
Homogamy Size
(diam, cm) Phyllotaxis Color Duration
(days) Perianth
number No.
Stamens
Staminodes
No.
Carpels
Chloranthales
CHLORANTHACEAE
Chloranthus fortunei bi protogyn 1 white 5–6 0 st 3 1
C. serratus bi protogyn 0.3 white 8 0 st 3 1
C. spicatus bi protogyn small yellow c. 20 0 st 3 1
Sarcandra chloranthoides bi protogyn 0.7 yellow red c. 20 0 st 1 1
S. glabra bi protogyn 0.6 green c. 20 0 st 1 1
Ascarina rubricaulis uni di nr very small st red 0 st 1 1
Hedyosmum mexicanum uni di nr 0.3 green t 0–3 st 1 1
Ceratophyllales
CERATOPHYLLACEAE
Ceratophyllum spp. uni mo nr 0.1 whorl green 1–3 t 8–15 st 5–27 1
Sex expression: bi = bisexual, uni = unisexual, di = dioecious, mo = monoecious, andmo = andromonoecious, gynmo = gynomonoecious,
poly = polygamous; Dicho/Homogamy: protogyn = protogynous, protand = protandrous, homo = homogamous, nr = not relevant; Phyllotaxis:
spir-whorl (outer elements spiral, inner elements whorled), whorl-spir (outer elements whorled, inner elements spiral); Perianth number:
s = sepals, p = petals, t = tepals; No. Stamens/Staminodes: sta = stamens, sto = staminodes ( ou = outer, in = inner); empty elds = data not
known or not found.
eschweizerbart_xxx
276 G. Gottsberger, Pollination in basal angiosperms
Table 2. Floral biology and pollination of basal angiosperms
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
ANITA
Amborellales
AMBORELLACEAE
Amborella trichopoda diu noc up p po no no col dip hym
lep wind gen oblout
Nymphaeales
HYDATELLACEAE
Trithuria spp. no no no wind water ane hyd comp in bi
CABOMBACEAE
Cabomba caroliniana diu no po ne no no dip hym gen
Brasenia schreberi no po no no wind ane comp
NYMPHAEACEAE
Nuphar spp.diu p sweet
fruity po ne no no hym dip col gen comp
Euryale ferox diu po no no dip hym gen comp
Barclaya spp. diu fruity po ne no no dip myi
Nymphaea ondinea
(former Ondinea)diu no po no no hym col gen
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 277
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
Nymphaea subgen.
Nymphaea, Brachyceras,
Anecphya
diu no s
aromatic po stiex no no dip hym
col lep gen comp
N. subgen. Hydrocallis,
Lotos noc p pungent po tiss yes yes col canth comp
Victoria noc s fruity po foob yes yes col canth comp
Austrobaileyales
AUSTROBAILEYACEAE
Austrobaileya scandens diu s up po brood no no dip (col) sapmyi
(sapcanth) incomp
SCHISANDRACEAE
Schisandra glabra diu po brood yes no dip myi
S. henryi diu no po no no dip myi oblout
S. sphenanthera noc diu sweet po no no dip thr col
lep hym gen
Kadsura longipedunculata noc s fruity po yes no dip myi comp
Illicium oridanum diu noc s up ne po yes no dip col
hym lep gen
I. dunnianum noc no brood yes no dip myi incomp
I. tsangii noc no brood yes no dip myi
TRIMENIACEAE
Trimenia moorei diu s fruity po no no dip hym
col wind gen incomp
eschweizerbart_xxx
278 G. Gottsberger, Pollination in basal angiosperms
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
BASAL MONOCOTS
Acorales
ACORACEAE
Acorus spp.diu noc sweet po no no
Alismatales
ALISMATACEAE spp. diu sweet po ne no no dip hym lep
col gen comp incomp
ARACEAE spp. diu noc s p up po tiss
perfume ne no
yes no
yes dip col hym myi canth
mel comp incomp
MAGNOLIIDS
Canellales
CANELLACEAE spp.
WINTERACEAE
Takhtajania perrieri dip myi ? apomixis
Tasmannia piperita diu sweet po ne* stiex no no dip hym col gen oblout
Drimys brasiliensis diu aromatic po ne* stiex no no col dip thr gen comp
Pseudowintera colorata w p sweet po stiex no no col dip
(thr lep) gen incomp
Zygogynum crassifolium,
Z. pancheri, Z. pauciorum diu w sweet po stiex no yes thr thy comp
(pancheri)
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 279
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
Z. baillonii, Z. pomiferum,
Z. stipitatum diu s fruity po stiex tiss no yes col (lep) canth
Piperales
ARISTOLOCHIACEAE
Saruma henryi
Asarum europaeum diu noc s up p po no yes no self-poll comp
Asarum caudatum and
other spp. diu w no fungi po no yes dip myi comp
Aristolochia spp. diu s carrion up
fruity no po ne no yes dip myi sapmyi comp incomp
LACTORIDACEAE
Lactoris fernandeziana diu noc no po no no wind ane comp
HYDNORACEAE
Hydnora spp. noc diu s up putrid
carrion po yes yes col (dip) sapcan
sapmyi
Prosopanche americana
and spp. po yes yes col sapcan
PIPERACEAE
Piper spp., Pothomorphe
spp. and Peperomia spp. diu w
sweet-
lemmon
po (ne) no no hym col
dip wind gen comp incomp
eschweizerbart_xxx
280 G. Gottsberger, Pollination in basal angiosperms
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
SAURURACEAE
Saururus cernuus s sweet po no no hym dip
col wind gen incomp
Laurales
CALYCANTHACEAE
Idiospermum australe diu s fruity po tiss no yes col thr dip
lep hym gen
Chimonanthus praecox diu s sweet po ne no no hym dip gen
Calycanthus occidentalis
and C. oridus diu s fruity po foodb no yes col canth
Calycanthus chinensis no po tiss no yes col canth comp
SIPARUNACEAE
Siparuna spp. noc (diu) s lemmon po brood no no dip myi
GOMORTEGACEAE
Gormortega keule diu no po ne no no dip hym gen
ATHEROSPERMATACEAE
spp. no no dip hym gen
HERNANDIACEAE
Hernandia nymphaeifolia diu s sweet po ne no no hym and ? gen
Sparattanthelium
botocudorum diu s sharp po no no dip hym col gen incomp
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 281
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
MONIMIACEAE
Mollinedia spp. diu no po brood no yes thr thy oblout
Wilkiea huegeliana diu no po brood no yes thr thy oblout
Tambourissa spp. group 1
(6 spp.) diu s fruity po stiexs no yes dip myi
Tambourissa spp. group 2
(4 spp.) diu s fruity no col can
LAURACEAE spp. diu s p up
spermatic po ne no no hym dip
col (lep) gen often incomp
Magnoliales
MYRISTICACEAE
Myristica spp. noc diu p sweet up
musky po no yes hym dip
thr col gen can
DEGENERIACEAE
Degeneria spp. up p po no yes col can
HIMANTANDRACEAE
Galbulimima spp. p aromatic po no col can?
MAGNOLIACEAE
Magnolia ovata and
Magnolia spp. Neotropics noc s p fruity po tiss yes yes col can comp
Magnolia spp. Liriodendron
spp. Temp. Zones diu s p aromatic po ne tiss no yes col hym
dip thr gen comp
(incomp)
eschweizerbart_xxx
282 G. Gottsberger, Pollination in basal angiosperms
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
EUPOMATIACEAE
Eupomatia spp. diu noc s fruity
musky po tiss no yes col can comp
ANNONACEAE
Anaxagorea spp. diu s p fruity po stoex
stiex yes yes col (small) can comp
Guatteria spp. and other
genera (small owers) diu noc s p fruity po stiex yes no yes col (small) can comp
Annona spp. and other
genera (large owers) noc s p fruity,
sharp po tiss stiex yes yes col (large) can comp
Bocageopsis and other
genera diu w p sweet
up rancid po no yes thr thy
Pseuduvaria and other
genera diu s up po no no dip myi sapmyi
Uvaria elmeri noc s up
mushroom po stiex no no cockroaches cockroaches incomp
Unonopsis spp. diu p spearmint
lemmon po perfume no no hym mel
Chloranthales
CHLORANTHACEAE
Chloranthus fortunei diu w aromatic po no no thr thy
C. serratus diu w p po no no thr thy
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 283
Taxa Anthesis Scent Resources Thermo-
genesis Poll.
chamber Pollinators Pollination
mode Breeding
system
C. spicatus diu s lemmon po no no incomp
Sarcandra chloranthoides diu s up po no no agamosper-
mous
S. glabra diu w fruity po no no
Ascarina rubricaulis diu no po no no wind ane oblout
Hedyosmum mexicanum diu no po no no wind ane oblout
Ceratophyllales
CERATOPHYLLACEAE
Ceratophyllum spp. diu noc no no no no water hyd comp
Anthesis: diu = diurnal, noc = nocturnal; Scent: w = weak, s = strong, p = pleasant, up = unpleasant; Resources: po = pollen, ne = nectar, stiex =
stigmatic exudates, stoex = staminodes exudates, tiss = nutritious tissue, foob = food bodies, brood = brood site; Pollinators: col = coleopters
(beetles), dip = dipters (ies ), hym = hymenopters (bees), thr = thrips (thysanopters), lep = lepidopters (butteries, moths); Pollination mode:
gen = generalist, canth-cantharophilous, sapcan = saprocantharophilous, myi = myiophilous, sapmyi = sapromyophilous, mel = melittophilous,
thy = pollination by Thysanoptera, ane = anemophilous, hyd = hydrophilous; Breeding system: comp = self-compatible, incomp = self- incompatible,
oblout = obligate outcrossing; Empty elds: data not known or not found; * nectar glands on stamens.
eschweizerbart_xxx
284 G. Gottsberger, Pollination in basal angiosperms
Endress & Igersheim (2000) investigated the reproductive structures of Amborella
and found that the owers are unisexual but with an underlying bisexual organization,
since at least the pistillate owers regularly have one or two staminodes outside the
gynoecium. Moreover, the staminodes of the pistillate owers look like fertile stamens.
Evidence for ancestral bisexuality in Amborella to Poluszny & Tomlinson (2003) comes
from the similar ontogenetic synorganization of pistillate and staminate owers, while
the presence of outer staminodia in most pistillate owers also provides similar evidence,
as does the occasional presence of central carpels in staminate owers. The presence of
bisexual oral organization is a strong indication for a basal state of this condition in
angiosperms (Endress & Igersheim 2000). The relatively frequent occurrence of func-
tionally unisexual owers among basal angiosperms, to Endress & Igersheim (2000)
“. . . may be a method to support outbreeding in a group in which self-incompatibiliy
systems are lacking or unelaborated.”
Thien et al. (2003) found that owering of female and male plants of Amborella
within populations is synchronous and that A. trichopoda is both insect- and wind-
pollinated. Bud opening in staminate and pistillate owers is throughout the day and
night. Staminate owers last 4 to 5 days from bud opening to complete anther dehis-
cence. Pistillate owers last 3 to 4 days and stigma receptivity extends to 24–30 hours.
Floral odor, not always perceptible, was faint and smelled like licorice, scented hay, and
sometimes also like feces. A wide variety of mostly forest litter dwelling insects (1 mm
to 7 cm length) was observed visiting owers and leaves of A. trichopoda (Thien et al.
2003). Two species of Curculionidae (Cryptorhynchinae) were found to be common
pollinators along with a tenebrionid beetle (Neoadelium fauveli). Large cerambycid
beetles, as well as members of Homoptera, Hemiptera, Microlepidoptera, parasitic
Hymenoptera and cecidomyiid Diptera were additional pollen transporters and poten-
tial pollinators. Tests with jelly-covered microscope slides proved that clumps of pol-
len grains, apparently held together by pollenkitt, were transported by wind.
Amborella has a generalist pollination system, where several species of pollen- eating
and pollen-transporting insects belonging to different groups, as well as the wind can
be effective in pollination. The insects probably visit pistillate owers because of the
mimetic role of the staminodes, contributing to the overall similarity of both ower
types and presumably also because of the oral odor.
Nymphaeales
Hydatellaceae, are a group of small grass-like aquatic or subaquatic herbs, which for-
merly were placed among monocots. The phylogenetic placement of this family together
with Cabombaceae and Nymphaeaceae in the order Nymphaeales, however, is well
supported by both molecular and morphological data (e.g. Rudall et al. 2007, Saarela
et al. 2007, Sokoloff et al. 2013). Analyses supported placement of Hydatellaceae
as sister to Cabombaceae plus Nymphaeaceae (Saarela et al. 2007). The sole genus
Trithuria (Sokoloff et al. 2008) as currently recognized has 8 species endemic to main-
land Australia, while one species each occurs in Tasmania, New Zealand and India,
and one last species occurs in both Tasmania and mainland Australia (Sokoloff et al.
2011). The “reproductive units” in this seemingly highly reduced and modied group,
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 285
are interpreted as aggregations of reduced unisexual apetalous owers (Rudall et al.
2007, Endress & Doyle 2009, Taylor et al. 2010). Four of the twelve species have
bisexual reproductive units, four are dioecious, and four are monoecious. For exam-
ple, of two Western Australian species, T. austinensis is dioecious and thus obligately
outcrossing, while T. submersa is bisexual and selng (Taylor & Williams 2012). It is
not very clear whether Trithuria is pollinated in the air or in the water (Endress 2010).
Wind pollination has been hypothesized for several species and water pollination in
two permanently submerged species (Rudall et al. 2007). In T. submersa which has
bisexual reproductive units, buds opened and pollen matured under water, but anthers
were never dehiscent in submerged reproductive units. Submerged reproductive units
never received pollen. Only emergent reproductive units received pollen. The species
is characterized as mainly self-pollinated, self-compatible and primarily autogamous;
it occasionally also exhibits wind pollination. Stigmas are receptive before and dur-
ing anther dehiscence (Taylor et al. 2010). Thus, most Trithuria species have similar
reproductive features as T. submersa, which are associated with wind pollination; two
exceptional perennial species having permanently submerged reproductive units are
probably pollinated underwater (Taylor et al. 2010).
The monotypic Amborella and also Hydatellaceae, the latter consisting of very spe-
cialized, aquatic species, which are presumably highly modied related to the environ-
ment in which they grow, do not really provide many insights into early diversication
of angiosperms.
The aquatic family Cabombaceae consists of the genus Cabomba, having ve spe-
cies in tropical and temperate regions of the Americas, and the monotypic Brasenia
schreberi, distributed in tropical and temperate regions of the Old and New World.
The emergent owers of Cabomba caroliniana are trimerous and 2.5 cm in diameter
when fully open. The six white tepals are in two whorls and nectaries occur on the
adaxial side of the inner tepals (Vogel 1998a, Erbar 2014). Schneider & Jeter (1982)
observed that the protogynous owers have receptive stigmas on the rst day of ow-
ering. On the second day, the owers are in the staminate stage, the laments are
elongated and anthers dehisce above the nectaries, while the non-receptive stigmatas
are pressed together at the center of the ower. Autogamy does not occur because of
the strict dichogamous protogyny. The breeding system itself, self-compatibility or
- incompatibility, was not tested. Two ephydrid ies, Notiphila cressoni and Hydrellia
bilobifera, were observed in both rst-day and second-day owers consistently mov-
ing from ower to ower and were seen applying their mouth parts to the yellow nec-
taries. Flowers were interpreted to be myiophilous, since other ower visitors, such as
the halictid bee Lasioglossum sp., a curculionid beetle and brachonid wasps were occa-
sional visitors or did not contact the reproductive parts of the owers. The yellow ow-
ers of C. aquatica growing near Belem, Amazonia, were observed by Vogel (1998a) to
emerge in the morning of the rst day of anthesis and enter into the pistillate stage, to
close in the afternoon, and then to be redrawn into the water. The second day, owers
similarly emerged and unfolded but entered into the staminate stage; laments elon-
gated and anthers occupied supercially the former position of the stigmas. At the end
of the second day, owers closed and submerged denitely. Vogel (1998a) observed
nectar- and pollen-collecting stingless bees (Meliponidae) and concluded that instead
eschweizerbart_xxx
286 G. Gottsberger, Pollination in basal angiosperms
of classifying Cabomba as myiophilous he would rather classify them as allophilic,
exhibiting unspecialized entomophily.
The emergent owers of Brasenia schreberi have many more stamens (18–36) than
Cabomba species (3 or 6) and have long laments. Anthesis of the bisexual, protogy-
nous owers also lasts for two days, with the pistillate stage on the rst day and the
staminate stage on the second. Flowers of Brasenia are primarily wind-pollinated, but
were also visited by several insects mainly for pollen collection (Osborn & Schneider
1988). Seed set after pollination experiments in cages using pollen of the same plant
proved self-compatibility in this species (Osborn & Schneider 1988).
Nymphaeaceae have a global distribution and originally comprised the six genera
Nuphar, Barclaya, Euryale, Ondinea, Nymphaea and Victoria, together representing
about 70 extant species. Similar to the other two families in the Nymphaeales, they are
also all herbaceous aquatics.
The most basal genus of the family is thought to be Nuphar (Borsch et al. 2008).
Formerly, the genus was considered monotypic comprising a single variable species,
N. lutea, distributed throughout the temperate northern hemisphere. After molecular
studies, 13 distinct lineages were recognized, ve species in Europe and Asia, and
eight species in North America (summarized in Lippok et al. 2000). The literature on
the oral biology of Nuphar is vast and goes back to Sprengel (1793). Schneider &
Moore (1977) reviewed the observations of other authors and provided new data from
studies of N. lutea subsp. macrophylla (=N. advena), in Texas. The yellow owers are
protogynous and anthesis occurs over a period of several days. First-day owers emit
an intense sweetish scent, somewhat like brandy or papaya fruits. During this rst-day
pistillate stage, the stigmatic disc is covered with a sticky, mucilaginous secretion. The
authors observed numerous insects visiting rst-day owers, especially Coleoptera,
Hemiptera, Homoptera and Hymenoptera. The most numerous visitors of the owers
were the beetle Donacia piscatrix (Chrysomelidae) and bees of the genera Halictus
and Apis hypothesized to be attracted by the yellow perianth and strong scent. The
dorsal side of the inner tepals produce nectar and have been called “honey leaves”
(Müller 1893). In Erbar’s recent detailed comparative study of nectaries, she remarks
that Nuphar is the only genus of Nymphaeaceae in which nectar is presented in dis-
tinct drops (Erbar 2014). Schneider and Moore (1977) found that during the night,
rst-day owers closed their tepals over the stigmatic disc and enclosed many of the
beetles. The stamens reexed and pollen was shed. In the second morning of anthesis,
the tepals re-opened, the stigmatic disc began to dry, and the pollen-covered beetles
could be observed to emerge from the owers and to y to rst-day and older owers.
Although the Donacia beetles and the Halictus and Apis bees appeared to be ef-
cient pollinators, Schneider & Moore (1977) thought that the overall oral structure,
scent emissions, tepal closing during the night, in addition to other characteristics,
represent primary adaptations for beetle pollination. Subsequent studies have shown,
however, that Nuphar pollination is somewhat more complex. Michels (1993) studied
the oral biology of N. lutea from the river Lahn close to Giessen, Central Germany,
where owers were visited by 30 different insect species, including chrysomelid
(Donacia clavipes) and nitidulid (Meligethes aeneus) beetles, and ies of the families
Calliphoridae, Ceratopogonidae, Empididae, Ephydridae, Muscidae, Sarcophagidae,
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 287
Scatophagidae, Sepsidae, Syrphidae and Tachinidae, Heteroptera, Homoptera and
Hymenoptera (Apis mellifera and Bombus spp.). Insects collected pollen as well as
imbibed nectar and stigmatic exudates. The most frequent visitors were ies (70%),
especially syrphid ies. In the summer months, during the owering period the visi-
tor spectrum of insects varied strongly. Flies preferred to visit second-day and older
owers in the staminate stage and were 3.6 times more common than on rst-day
owers in the pistillate stage. In contrast, bees visited pistillate stage owers as often
as staminate stage owers. Beetles were only rarely found in the receptive rst-day
owers. Thus, the most efcient pollinators of N. lutea at Giessen were bumblebees
(Bombus terrestris/lucorum complex), followed by honeybees and ies, especially syr-
phid ies, as well as the Cabomba/Nuphar/Nymphaea specialists Hydrellia (one spe-
cies), Notiphila (two spp., Ephydridae), and Hydromyza livens (Scatophagidae) (see
also van der Velde & Brock 1980). Ervik et al. (1995) investigated N. lutea in Norway,
and found that besides Apis mellifera and Bombus spp., syrphid ies were efcient
pollinators. The chrysomelid beetle Donacia crassipes played a minor role in polli-
nation. The authors concluded that in Norway, N. lutea appears to have shifted from
a typical beetle pollination system, as suggested by Schneider & Moore (1977) for
N. advena, to a non-specic pollination syndrome. In a later study, Lippok & Renner
(1997) compared N. lutea and N. pumila at sites in Norway and southwest Germany.
Flies were the main pollinators in both species, while the beetle Donacia crassipes
played an insignicant role for both Nuphar species in Norway and was absent at
the German site. In the study of N. pumila by Zhou & Fu (2007) in China, no beetle
visits occurred and halictid bees and ies were the most frequent visitors to owers.
Lippok & Renner (1997) had already hypothesized that the open bowl-shaped ow-
ers of Nuphar having accessible nectar and pollen “. . . might simply sample locally
available insects”, and thus, there seems to be no specialization to any particular insect
group. At that time, however, it was not yet clear whether New World Nuphar species
have a tendency to be principally beetle-pollinated. To resolve this question, Lippok
et al. (2000) re-studied N. advena in Texas and also studied N. ozarkana in Missouri,
and concluded that. . .”The comparison of pollination spectra in the two Old World
and the three New World Nuphar species studied so far suggests that the relative con-
tribution of ies, bees, and beetles to pollen transfer in any one population depends
more on these insects’ relative abundances (and in the case of Donacia, presence) and
alternative food sources than on stamen length differences between Old World and
New World pond-lilies.”
Lippok & Renner (1997) and Lippok et al. (2000) conrmed self-compatibility for
N. lutea, N. pumila (see also Zhou & Fu 2007) and N. advena and strong protogyny of
their owers, preventing automatic selng; hence, insect pollination is necessary for
seed production. Also Michels (1993) found N. lutea to be self-compatible and polli-
nation experiments with pollen of the same plant, including 16 rst- and second-day
owers, resulted in a 100% fruiting success and 95% seed-set.
The two Asian genera Euryale and Barclaya were reported to have cleistogamous
and chasmogamous owers; sometimes both types occur within a single individual
(Schneider and Williamson 1993). The sole Euryale species, E. ferox has cleistoga-
mous, self-pollinating submerged owers that appeared more than one month earlier
eschweizerbart_xxx
288 G. Gottsberger, Pollination in basal angiosperms
than chasmogamous ones; chasmogamous owers were fewer than chleistogamous
ones and were already self-pollinated at opening, some occasional small ies (Notiphila
spp.) and solitary bees did not enter the oral tube or touch the stigmatic surface and,
thus, were not responsible for seed set (Kadono & Schneider 1987). The four spe-
cies of the genus Barclaya have been studied by Williamson & Schneider (1994).
Both, Barclaya longifolia and B. kunstleri were observed to have only cleistoga-
mous, self-pollinated owers. On the other hand, B. motleyi produces chasmogamous,
self-pollinated owers; no ower visitors were seen during a three-week observation
period. In B. rotundifolia which has aerial, chasmogamous owers, the outer tepals are
greenish to white and inner tepals and stamens are purplish. For three days, individual
owers open in the morning and close at dusk; they emit a pungent, fermented odor.
Unidentied small- to medium-sized ies were collected around the owers, which
occasionally suffocated in the mucilage that covers the surface of the stigmatic cup.
The occurrence of ies in the owers, the oral construction, color and odor suggest
myiophily for this species. The cleistogamous and chasmogamous owers are self-
pollinated, the latter type facilitated partly by ies in emergent owers. Three of the
four species were tested and found to be self-compatible.
After careful study, it was discovered that the former Australian monotypic genus
Ondinea was nested in Nymphaea and so was recently transferred under the new name
N. ondinea (Löhne et al. 2009). It is unusual because it is atepalous, the original dis-
tinction between Ondinea and Nymphaea, however a second subspecies having violet
tepals was discovered later. Study of the oral biology of the tepal-bearing subspe-
cies (Schneider 1983, Schneider et al. 1984) indicated that anthesis lasts for 3 days.
First-day owers are in the pistillate stage and characterized by reexion of the purple
perianth and stamens. The stigmas secrete a uid that lls the stigmatic cup. Second-
and third-day owers are in the staminate stage and present pollen. The most common
visitors in both stages were bees (Trigona spp.) besides some minor pollinators, cur-
culionid and chrysomelid (Donacia) beetles. In rst-day owers, bees approached the
stigmatic area where pollen carried by the insects was washed off by the uid. On the
second and third day of anthesis, the stamens assume a vertical erect position forming
a cone and again trigonid bees were observed to land on the stamens to collect pollen.
Nymphaea, the largest and most diverse genus of the family, consists of about
50 species, has a world wide distribution, and species have more or less large (up
to 20 cm diam.), showy, white, yellow, red or blue owers, which may or may not
be scented. Anthesis of water lilies can occur over a 2–5 day period, depending on
the species. There are diurnally owering species (subgen. Nymphaea, Brachyceras,
Anecphya) with tropical and temperate zone representatives, which are jointly vis-
ited and pollinated by a wide array of Diptera, Hymenoptera and Coleoptera (e.g.
Robertson 1889, Knuth 1898/1899, Schmucker 1932, Meeuse & Schneider 1979/80,
Schneider 1982a, 1982b, Capperino & Schneider 1985). For example, N. odorata,
examined in Texas by Schneider & Chaney (1981) opens its owers each morning
and closes them about noon for three successive days. The owers are protogynous
and rst-day owers are receptive having secreting stigmas; the uid, which contains
a surfactant responsible for washing pollen off the bodies of visiting insects, lls the
stigmatic cup (Wiersema 1988). Pollen quickly germinates in the stigmatic secretions
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 289
and pollination is achieved (Williams et al. 2010). During the following two days,
the stigmas of N. odorata become non-receptive, anther dehiscence occurs and pol-
len is offered to insect visitors. After the third day of anthesis, the owers submerge.
Beetles belonging to the families Chrysomelidae (among others Donacia piscatrix),
Curculionidae and Scarabaeidae, as well as syrphid ies and Hymenoptera were
observed visiting the owers. The bee Lasioglossum versatum (Halictidae) appeared
to be the most efcient pollinator. Another well-studied species is N. alba. Michels
(1993) studied this species for a whole owering season at several lakes and ponds
around Giessen, Central Germany. In total, 24 insect species belonging to four orders
visited the owers. Bees, beetles and butteries were negligible as pollinators. The
most important pollinators of N. alba at that site were ephydrid ies, namely three
species of Hydrellia and two species of Notiphila. These insects collected pollen and
were also seen absorbing the sweet, 2.8–3.8% sugar-containing stigmatic exudates
(see also Baker et al. 1973).
The derived groups of Nymphaea, species of the subgenera Hydrocallis
(Neotropics) and Lotos (Paleotropics) (Borsch et al. 2008), also have protogynous
owers with nocturnal anthesis over two nights (at least in Neotropical species) and
emit a strong scent. Exclusive pollinators are nocturnally active, large dynastid scarab
beetles (Scarabaeidae: Dynastinae) of the genus Cyclocephala. Cramer et al. (1975)
found C. castanea as pollinator in owers of Nymphaea blanda var. fenzliana and
N. rudgeana in Surinam. A third species, also in Surinam, N. amazonum, was found
by the above authors to be pollinated by C. verticalis (see also Prance & Anderson
1976). In a later paper, Prance (1980) found N. amazonum in the Pantanal of Mato
Grosso to be pollinated by C. mollis. Although not measured, it can be deduced from
similar phenomena in Magnolia, Annonaceae, Araceae and other groups, that the ow-
ers of all these nocturnal, dynastid scarab beetle-pollinated Neotropical Nymphaea
species are probably thermogenic, warming-up during the night hours. One of the two
known Paleotropical representatives of the tribe Cyclocephalini (Ratcliffe et al. 2013),
Ruteloryctes morio, visits and pollinates (besides certain bees) the African N. lotus in
Ivory Coast (Hirthe & Porembski 2003; Krell et al. 2003); the protogynous owers are
nocturnal, with anthesis lasting 4 to 5 days. Flower temperature increased in the rst
half of the night, with recorded values of 5°C on the rst, and 7°C on the second, night
above ambient air; the temperate difference was less on subsequent nights. In Senegal,
Ervik & Knudsen (2003) found the same species, N. lotus, to be exclusively pollinated
by R. morio. At their site, Apis mellifera was observed to collect only pollen but did
not touch the stigma. Thus, N. lotus, at least in Senegal, appears to be exclusively
beetle-pollinated.
Nymphaea lotus was tested and found to be self-compatible (Hirthe & Porembski
2003), as were N. rudgeana and N. ampla in the vicinity of Manaus (Prance &
Anderson 1976), in addition to eight other Nymphaea species mentioned by Wiersema
(1988), among them the temperate species N. alba (see also Michels 1993).
The two Amazonian species of Victoria, V. amazonica (Fig. 1) and V. cruziana,
exhibit exclusive cantharophily. In both species the very large (up to 25–30 cm diam.)
protogynous owers have a two-night rhythm, warming up strongly during the rst
night of owering (5–11 °C above ambient air temperature in V. amazonica) followed
eschweizerbart_xxx
290 G. Gottsberger, Pollination in basal angiosperms
by a lower temperature increase in the second evening when the beetles leave. Heat
was generated mainly in the oral chamber on the rst evening and by the stamen com-
plex on the second (Seymour & Matthews 2006). The strong temperature elevation
of the rst night is accompanied by a potent, fruity, pineapple-like fragrance. During
the second day, the originally white inner tepals become purplish-red and lose their
fruity scent. By the afternoon, the anthers shed pollen and nally, in the evening, the
pollinators emerge from the owers, squeezing through the pollen-shedding stamens.
The most common beetle species is Cyclocephala hardyi, along with three other more
occasionally visiting Cyclocephala species (Prance & Arias 1975, Kite et al. 1991).
The starch-containing carpellary appendages are eaten by the beetles while they are
inside the oral cavity. Self-pollination in the self-compatible V. amazonica resulted in
fruit- and seed-set (Prance & Arias 1975). The owers of Victoria cruziana, apparently
also self-compatible, behave in a similar manner to V. amazonica, and were found to
be pollinated in Argentina by a species of Chalepides, a beetle also belonging to the
group of Cyclocephalini dynastid scarabs (Valla & Cirino 1972, Skubatz et al. 1990,
Lamprecht et al. 2002).
Fig. 1. Victoria amazonica. A. Second-day ower (diam. of expanded petals ca. 25–30 cm.)
with internal petals starting to change color from white to red. B. First-evening ower with
closed white petals, in pistillate stage, being approached by its pollinating beetle, Cyclo-
cephala hardyi. C. Cut ower showing the pollination chamber and one beetle. D. Reddish,
second-evening ower with expanded petals, in staminate stage. The beetles, covered with
pollen grains, are coming out of the pollination chamber; some beetles are mating before
ying off.
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G. Gottsberger, Pollination in basal angiosperms 291
Austrobaileyales
Austrobaileyaceae is a monotypic family represented by the relict Austrobaileya
scandens, a liana endemic to North Queensland, Australia. Its bisexual, large (5–6 cm
diam.), showy, solitary owers are pendent and phyllotaxy is spiral throughout. The
perianth exhibits a series of appendages transitional from small green bracts to large
yellowish petal-like organs. Inner staminodes and stamens are yellowish. The pro-
togynous owers emit a strong scent of decaying sh and were visited by ies, some
of which oviposited there (Endress 1993a); beetles were also observed (Thien et al.
2009). The combination of an unpleasant odor, coloration of the stamens and stami-
nodes, dark brown spots on a yellow background pattern of the perianth, and observed
visitors, strongly suggest that Austrobaileya is mimicing rotten organic matter. The
carpels are covered by the connivent parts of the staminodes and are not visible from
outside. It is thought that the visiting ies may reach the stigmatic region by slipping
through the gaps between the stamens and staminodes, which form a labyrinth-like
structure (Endress 1980c). Apparently, the bisexual owers of A. scandens are self-in-
compatible (Prakash & Alexander 1984).
The Schisandraceae now consist not only of the two genera Schisandra (25 spp.)
and Kadsura (22 spp.), having mostly Southeast Asian species, but also of Illicium
(formerly Illiciaceae with 30–40 species; Morris et al. 2007; APG III 2009), which
has a distribution in Southeast Asia and southeastern North America. Ueda (1988)
reported on labile sex expression and sex change in the woody vine Schisandra chin-
ensis, which can produce staminate owers one year, and pistillate and rarely even
bisexual owers in another year. The study of Zhao et al. (2013) showed that this
species is mainly monoecious and that gender expression and reproductive output
is age-dependent, with young and old plants having lower female ratios. Labile sex
expression is mentioned also for Kadsura japonica and might occur in other species of
Schisandraceae (Ueda 1988).
The only species of Schisandra occurring outside Asia is S. glabra, which grows
in southeastern United States and Mexico. It was shown that this monoecious plant
has thermogenic pistillate and staminate owers, which function as a host site pri-
marily for Diptera and also small Coleoptera that inadvertently pollinate while ovi-
positing (Liu et al. 2006). The woody vine S. henryi, studied in South-Central China
by Yuan et al. (2007), was found to be strictly dioecious, having small (several mm
diam.) pendulous owers with green or yellow tepals. It is not thermogenic and did
not emit any detectable scent. The small diameter of the oral orice and the small
space inside the ower interior only permit small insects to enter. Of several insects
observed, only adult females of Megommata sp. (Cecidomyiidae, Diptera), that eat
pollen grains, are effective pollinators. As pollen is the only food resource for the
insects, the pistillate owers of S. henryi attract pollinators by deceit. Wind pollination
was not ruled out, but the authors conclude that the drum-shaped, pendulous owers
have such small orice that wind pollination would likely be prohibited. Another, dio-
ecious species, S. sphenanthera, from Central China has an extragynoecial compitum
and it was observed that pollen tubes can easily cross via this compitum from one car-
pel to another (Du & Wang 2012). The observed populations of this species were male
eschweizerbart_xxx
292 G. Gottsberger, Pollination in basal angiosperms
biased, and, principally, diurnally-active gall midges (Reseliella sp., Cecidomyiidae)
and thrips (Thrips avidulus) were the most common visitors to owers (oral diam.
1.6–1.8 mm, tepal color red or yellow, fragrance sweet); additional visitors included
a few hoveries, beetles and butteries. The gall midges, which fed on pollen, were
more common in staminate owers and thrips were more common in pistillate owers.
Du et al. (2012a) thought that the pistillate owers attracted pollinators by deceit.
The monoecious Kadsura longipedunculata was studied by Yuan et al. (2008) in
the same area as S. henryi. It has larger owers (1.5–2.6 cm diam.) than the afore-
mentioned Schisandra species. Its tepals are yellow and stamens may be yellow or
red. Tepals of the staminate owers are reexed when open, while pistillate owers
form a drum-shaped chamber. Both pistillate and staminate owers are thermogenic
during the night and emit a strong fragrance. This species, like S. henryi, is polli-
nated by female, pollen-eating cecidomyiid ies (Megommata spp.); pistillate owers,
which do not offer any nutritive tissues are visited by deceit. This species combines an
extragynoecial compitum, which distributes the pollen tubes to the individual free car-
pels, with a dry-type stigmatic tissue (Lyew et al. 2007). Tests showed that this species
can form some fruits after selng and therefore shows a degree of self-compatibility
(Yuan et al. 2008). Kadsura japonica, as opposed to K. longipedunculata has a nectary
tissue located on the adaxial surface of the inner tepals (Saunders 1998).
Illicium oridanum, studied in Louisiana (Thien et al. 1983) has showy (ca. 7 cm
diam.), deep red or purple, thermogenic (Thien et al. 2009) owers which, in a func-
tional stage, last for 12–14 days and emit an intense, unpleasant odor, smelling like
freshly caught sh. A wide spectrum of insects emerging from the surrounding leaf
litter and stream in the riverine community visited the owers. Principally Diptera
were pollinators. Hymenoptera and Hemiptera visited the owers only occasionally
and Coleoptera rarely, the last usually approaching only partially opened owers. The
insects fed on nectar that was produced in very small quantities at the base of the
inner tepals and stamens. Flowers exhibited complete dichogamy. The original report
of pre-zygotic self-incompatibility of this species (Thien et al. 1983) is now thought
to be due to inbreeding depression, although late-acting post-zygotic ovarian self-
incompatibility cannot be ruled out (Koehl et al. 2004). Williams et al. (1993) reported
on intercarpellary growth of pollen tubes in the apocarpous I. oridanum. An apical
residuum with its associated unfused carpel margins acts as an extragynoecial compi-
tum for pollen tube transfer between carpels. A compitum is thought to be a mecha-
nism by which more ovules can be fertilized and thus may increase the efciency of
seed set. The small-owered (oral diam. ca. 0.8 cm), protogynous I. parviorum of
eastern Florida produces o faint sweet scent. Flowers last 2–3 days and open during
the day and night; the pistillate stage lasts for the rst 24 hours. Mainly gall midges
(Cecidomyiidae), along with some psychodid and ceratopogonid ies were the princi-
pal pollinators; these insects, among others probed on stamen nectaries (White & Thien
1985). As compared, in particular to I. oridanum, the Malayan species I. peninsulare,
I. tenuifolium and I. ridleyanum have relatively small, inconspicuous owers, which
are pale yellow or white and only faintly scented; although not observed, Keng (1993a)
hypothesizes that they are insect pollinated. Illicium dunnianum (self- incompatible)
and I. tsangii from China, both having bisexual owers (oral diam. 1–1.5 cm) with no
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G. Gottsberger, Pollination in basal angiosperms 293
perceptible oral scent, are exclusively pollinated by gall midges that use the owers
as brood sites and not for pollen feeding. First-night owers were in the pistillate stage
and second- or third-night owers in the staminate stage. There was a slight oral
heating of ca. 1.6°C above-ambient temperature, mainly during the pistillate stage
and the later larval nursing phase following the staminate stage of owers; experi-
ments showed that this post-anthetic warming beneted larval development of the gall
midges, not fruit development (Luo et al. 2010).
Trimeniaceae consists of a single genus having 5–8 species distributed from
Celebes to eastern Australia and the Southwest Pacic (Philipson 1993b, Bernhardt
et al. 2003). Trimenia papuana and T. neocaledonica were both found to be andromo-
noecious, with small, inconspicuous owers. Most owers were bisexual, but a few
were staminate and had the gynoecium reduced or lacking. No nectar is produced.
The pollen was found to be dry and easily dispersed by wind (Endress & Sampson
1983). Trimenia moorei is also andromonoecious and both male and bisexual (pro-
togynous) owers (ca. 1 cm diam.) were found to be strongly scented. Hover ies
(Syrphidae), sawies (Pergidae) and several bees (Apidae, Colletidae and Halictidae)
carried pollen of T. moorei and acted as pollinators. Pollen is also shed directly into
the air, permitting wind pollination. This species was found to be self-incompatible
(Bernhardt et al. 2003).
Pollination in basal monocots
Acorales
There is strong support that Acorus (Acoraceae) is sister to all other monocots (e.g.
APG III). The inorescences and owers of the two to four species bear supercial sim-
ilarities to those of Araceae, and for a long time, Acorus was considered to be a member
of that family. The distribution of this northern hemisphere genus is temperate to tropi-
cal. The bisexual owers are protogynous. Ever since Knuth (1899), the entomophilous
characters, e.g. sticky pollen, sweet scent of Acorus inorescences have been stressed,
but apparently there are no observations of insect visits to owers. One hundred years
after reports by Knuth, the situation has not much improved: “The pollinators or pol-
linating agency of Acorus are unknown; both entomophily and anemophily have been
suggested, but entomophily appears more likely.” (Bogner & Mayo 1998). Azuma &
Toyota (2012) found a rare scent compound (for angiosperms) in A. gramineus and
they, as have several other authors, suggested that the species was entomophilous.
Alismatales
Both Acorales and Alismatales are early-divergent monocot groups and most phy-
logenetic studies resolve Alismatales as the sister group to all other monocots except
Acorus (Acorales). Alismatales is a cosmopolitan and diverse clade of monocots, com-
prising about 4500 species in 13 families (e.g. Iles et al. 2013).
Alismataceae consist of 12 genera and about 80 species of subcosmopolitan dis-
tribution. Flowers are bisexual or unisexual by abortion of either stamens or carpels.
Sex expression of plants with unisexual owers is commonly either monoecious
(Sagittaria), polygamous (Limnophyton, Sagittaria), or dioecious (Burnatia). The pet-
als are delicate and white, pink, or purple in color (Haynes et al. 1998).
eschweizerbart_xxx
294 G. Gottsberger, Pollination in basal angiosperms
Observed ower visitors and pollinators of Alisma plantago-aquatica are several
species of syrphid and muscid ies and occasionally also a bee or a buttery, which
feed on nectar, and in case of Syrphidae also eat pollen. Nectar is produced by the
carpels and accumulates at the base of the laments. The homogamous owers open
between 9 and 11 a.m. and fade between 5 and 7 p.m. of the same day. Pollenkitt is not
well developed in A. plantago-aquatica, such that the pollen is not only transported by
insects, but also by strong air currents (Knuth 1899, Daumann 1965). Nectar produc-
tion is reported not only for Alisma, but also for Sagittaria, Damasonium, Baldellia,
Caldesia and some species of Echinodorus, such as E. grandiorus (Pansarin 2008).
Robertson (1929) observed 66 species of insects in four orders visiting both staminate
and pistillate owers of Sagittaria latifolia in Illinois. Flowers of S. brevirostra in
Nebraska were found to be full of small insects, at least some of which are surely pol-
linators (Kaul 1979). Flowers of S. guyanensis in Bolivia were principally visited by
bees, some beetles and an occasional buttery (Gumbert & Kunze 1999), and in China
occasionally by certain syrphid ies (Huang 2003). In contrast, at a site in China,
S. potamogetifolia, S. trifolia and S. pygmaea were frequently visited by bees, ies
and butteries (Huang 2003). The two species, S. australis and S. latifolia, were both
found to be visited in Ohio by a similar spectrum of generalist bees, and addition-
ally by some ies, wasps, other bees, and a few butteries (Muenchow & Delesalle
1994), and Echinodorus grandiorus owers in Bolivia by bees and additionally by
Coleoptera, Lepidoptera and an occasional y (Gumbert & Kunze 1999). Comparative
studies on two Echinodorus species in São Paulo State revealed that E. longipetalus is
gynodioecous (the rst report for this sex distribution in the genus), offers only pollen
as a reward, and is pollinated principally by several bees. The pistillate owers, which
do not offer any reward, attract by deceit. Other visiting beetles and hoveries were
not seen to contact the pistils, and thus have to be considered at least poor pollinators
if pollinators at all (Pansarin 2008). In contrast, E. grandiorus has bisexual owers
that offer pollen and nectar. Also this species was found to be pollinated nearly exclu-
sively by social and solitary bees, which collected only pollen. The additional ower
visitors were beetles, which fed on petals, stamens and pistils, and damaged them,
and bombyliid ies which collected nectar without touching the stamens (Pansarin &
Pansarin 2011). Since the authors report for the latter species that pollen-collecting
bees appeared immediately when owers opened, it can be deduced that the ow-
ers of E. grandiorus must be either homogamous or protandrous. Flower visitors
of Caldesia grandis and C. parnassifolia in China were ies and bees, with the lat-
ter being more effective pollinators. C. grandis was found to be protandrous. Anther
dehiscence occurs soon after ower opening at about 10:00 a.m., when the rst ower
visitors approach, and stigmas were found to be receptive between 12:30 and 1:00 p.m.
(Gituru et al. 2002).
Kugler (1955) and Daumann (1965) tested Alisma plantago-aquatica and found
it to be self-compatible. Self-compatibility was also found in Sagittaria guyanensis
(Huang 2003) and in the ve species of the genus Damasonium; four of the ve spe-
cies are homogamous and D. californicum is protandrous (Vuille 1987). Baldellia
ranunculoides subsp. repens is self-incompatible, whereas B. ranunculoides subsp.
ranunculoides and B. alpestris are self-compatible. The genus Baldellia is noted to
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G. Gottsberger, Pollination in basal angiosperms 295
be primarily insect-pollinated with a trend toward self-pollination (Vuille 1988).
Caldesia grandis and C. parnassifolia are also self-compatible (Gituru et al. 2002). In
the gynodioecous Echinodorus longipetalus, individuals having bisexual owers were
found to be self-compatible (Pansarin 2008), whereas E. grandiorus, wherein only
bisexual owers are known is self-incompatible (Pansarin & Pansarin 2011).
Another family of the Alismatales, the Araceae, comprise 120–130 genera and
over 3300 species having a cosmopolitan distribution; Araceae are most abundant and
diverse in tropical latitudes. Flowers and inorescences of Araceae are very different
in construction from other families in the order. The inorescence is composed of an
unbranched spike made of densely grouped owers known as the spadix; this is sub-
tended by a bract called the spathe. Flowers can have a perigon or be without it. The
spadix itself can bear bisexual owers only or can be specialized, having proximally
pistillate owers and distally staminate owers, and there can be one or several zones
of sterile owers or entirely naked axial zones, and smooth or staminodial terminal
appendices. The development of the spathe into a lower tube and an upper expanded
blade is another differentiation. Araceae are all protogynous (Mayo et al. 1997). With
regard to pollination, Araceae are principally pollinated, more or less exclusively, by
ies, bees and beetles (Grayum 1984, 1990, Mayo et al. 1997). Since the literature
on Araceae is extensive, I provide only a few examples each of myiophilous, melit-
tophilous and cantharophilous species from observations of our group as well as other
authors, and in the general discussion section there is reference to the hypothesized
evolution of pollination in the family.
Pollination has been well-studied in several Arum species; they attract ies or bee-
tles, searching for breeding sites in decaying organic matter, and are kept inside the
inorescence “kettle” during the pistillate stage, and later released covered with pollen,
after the staminate stage. Several species are known to warm-up (e.g. Bermadinger-
Stabentheiner & Stabentheiner 1995, Seymour et al 2009a, Linz et al. 2010). Not all
Arum species attract their pollinators by deception, some provide resources to the
insects (e.g. Lack & Diaz 1991, Albre et al. 2003, Diaz & Kite 2006). Species of
Arisaema attract fungus gnats (Mycetophilidae and Sciaridae), which are released in
the few monoecious species, but die inside the female inorescences of the dioecious
ones, after pollen deposition on stigmas (Vogel & Martens 2000, Barriault et al. 2010).
Anthurium and Spathiphyllum species are known to have several different pollination
systems, among which are some pollinated by euglossine bees (Williams & Dressler
1976, Croat 1980). For example, Anthurium sagittatum, A. thrinax, A. rubrinervum,
and Spathiphyllum humboldtii, observed in French Guiana, are pollinated by scent-
collecting male euglossine bees (Hentrich et al. 2007, 2010). Different bee species
visited the inorescences of the sympatric, simultaneously owering Araceae in the
pistillate and staminate stages. Analysis of the scent samples showed that each plant
species emitted a specic oral bouquet that clearly differed from the bouquets of the
other studied sympatric species. It was hypothesized that the different oral scents lead
to clear separation of the main pollinating euglossine species, providing a directed and
efcient intraspecic pollen ow that results in high reproductive success.
The large genus Philodendron with 500–700 species has a complex inorescence
morphology, with pistillate owers proximally on the spadix, followed by a sterile
eschweizerbart_xxx
296 G. Gottsberger, Pollination in basal angiosperms
staminate zone and a distal fertile staminate zone. The large spathe forms a pollina-
tion chamber, known as a kettle at the spathes’ base and which opens in the upper
part. The rst correct description of pollination in Philodendron, probably of P. lun-
dii, growing at Lagoa Santa, Minas Gerais, was by Warming (1883). One hundred
years later, the two species, P. selloum and P. bipinnatidum (both species, together
with P. lundii, belonging to the P. bipinnatidum complex of subgen. Mecanostigma)
were compared. It was recognized that the inorescences warm-up strongly in the rst
night of owering in the pistillate stage (P. selloum), or can warm-up also in subse-
quent nights in the pistillate and staminate stages (P. bipinnatidum), and depending
on the spectrum of potent scent compounds emitted during heating (thermogene-
sis), attract species specic dynastid scarab beetles, namely Erioscelis emarginata in
P. selloum (Fig. 2) and Cyclocephala variolosa in P. bipinnatidum (Gottsberger &
Amaral 1984). Studies on these species were extended and the olfactory and visual
attraction of the beetles to the inorescences was tested (Gottsberger & Silberbauer-
Gottsberger 1991). Subsequently, we studied other Philodendron species in the
Amazon region (Silberbauer-Gottsberger et al. 2001). The scent compounds of two
species of the P. bipinnatidum complex were analyzed and their attractivity to the
respective pollinating beetles was tested. The comparative data were rened and
placed in context of the population structure of the investigated species, their geo-
graphical distribution, the pollination processes, including anthesis and thermogene-
sis, and the behavior of the beetles (Dötterl et al. 2012, Gottsberger et al. 2013). The
results showed convincingly that pollination in Philodendron is very sophisticated
and highly specialized. Each species of Philodendron attracts usually only one spe-
cies of dynastid scarab beetle. The oral scent emissions that accompany the intense
heating (thermogenesis) of the inorescences, which in P. selloum reaches a world
record for plant tissues, of greater than 45°C, and a relative heating of more than
30°C, are essential for attraction of the specic beetle species, as well as for their
behavior, maintenance and welfare inside the kettle. Studies on other Philodendron
species have revealed many further interesting details about this fascinating system
(see Gibernau & Barabé 1999, Gibernau et al. 1999, 2000, Seymour & Gibernau
2008, Maia et al. 2010, Pereira et al. 2014).
With regard to the breeding system of Araceae, self-compatibility was found in
many cases, although some authors remarked that there was a lower fruit set in selfed
inorescences as compared to out-crossed ones: Pinellia tripartita (Uhlarz 1985),
Dieffenbachia longispatha (Young 1986), Spathiphyllum friedrichsthalii (Montalvo &
Ackerman 1986), Peltandra virginica (Patt et al. 1995), Montrichardia arborescens
(self-compatible or apomictic, Gibernau et al. 2003), Xanthosoma daguense (García-
Robledo et al. 2004), Arum maculatum and A. italicum (Diaz et al. 2006), Anthurium
acaule, A. cristalinum, A. fendleri, A. salviniae, A. spectabile, A. trinerve, A. upa-
lahense (Chouteau et al. 2006), Alocasia portei, Anthurium longistamineum and
A. schlechtendalii, Dieffenbachia oerstedii, D. seguine (Chouteau et al. 2008) and
Taccarum ulei (Maia et al. 2013b). On the other hand, Arisarum vulgare was found to
be self-incompatible (Koach & Galil 1986). For Arum maculatum there are conicting
results, because Dieterle (1999) found the species to be self-incompatible, while cer-
tain authors of the aforementioned found it to be self-compatible.
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G. Gottsberger, Pollination in basal angiosperms 297
Fig. 2. Philodendron selloum (length of inorescence ca. 25 cm). A. One individual of pol-
linating beetles (Erioscelis emarginata) is approaching a rst-evening, pistillate stage ino-
rescence. After collision with the spathe the beetle will fall into the kettle where the pistillate
owers are in the receptive stage. B. During the second day, the accumulated beetles try
to protect themselves against daylight at the base of the kettle. C. On the second eve-
ning, the distal staminate owers of the spadix press out pollen grain chains. The spathe
is closing and the beetles are obliged to move upwards and to pass the pollen-producing
region. D. Pollen-covered beetles arriving at the top of the spadix, shortly before ying off.
eschweizerbart_xxx
298 G. Gottsberger, Pollination in basal angiosperms
Pollination in Magnoliids
The magnoliids comprise four orders, the clade Canellales and Piperales, which appar-
ently are sister taxa to the clade Laurales and Magnoliales (APG III 2009).
Canellales
To the best of our knowledge, there are few reports on the oral biology of Canellaceae.
The family comprises ve or six genera and about 20 species in Madagascar, Africa,
South and Central America and the Caribbean (Kubitzki 1993b). Flowers are bisexual
having a basic trimerous or pentamerous organisation. Protogyny was observed in the
Caribbean species, Canella winterana, and all owers of a tree were strictly synchro-
nized: they were either all in the pistillate or the staminate stage (Wilson 1982). The
epidermal cells of the lament tube produce nectar (Erbar 2014), and, in addition to
small insects, the owers attract paper wasps, butteries, leaf-cutting bees and hum-
mingbirds (Wilson 1986). Kubitzki (1993b) remarked that in herbarium material of
Cinnamodendron dinisii he found that the androecial tube was elongated and enclosed
the stigma in a later stage.
Phylogenetic studies of Winteraceae (e.g. Ehrendorfer et al. 1979, Suh et al.
1993, Endress et al. 2000, Ehrendorfer & Lambrou 2000, Karol et al. 2000, Doust &
Drinnan 2004) assign a basal position to the endemic Madagascan monotypic genus
Takhtajania, which is sister to the remainder of the Winteraceae; the next branches
are Tasmannia (7 spp., Philippines to Tasmania), Drimys (7 spp., distributed from
southern Mexico to the south of South America), and Pseudowintera (3 spp., New
Zealand). The former genera Bubbia, Belliolum, Exospermum and Zygogynum were
combined into a single genus Zygogynum s.l (Vink 1993). The generic relationships
in Winteraceae were re-studied by Marquinéz et al. (2009a), and their analyses based
on nuclear and plastid sequence data corroborated monophyly of Drimys, Tasmannia,
Pseudowintera, Zygogynum s.l. and they also corroborated the same phylogenetic rela-
tionships obtained by Karol et al. (2000) and Doust & Drinnan (2004). Flowers are
usually bisexual (unisexual in Tasmannia) and are either small or relatively large, and
petal color is white, yellow, yellow-purple or red.
Flowers of the apparently earliest-divergent Winteraceae, Takhtajania perrieri, were
found to be visited by ies (pers. comm. in Thien et al. 2000). In the dioecious genus
Tasmannia, staminate owers having sterile carpels can occur and bisexual owers are
also sometimes been observed (Vink 1970, 1993, Frame 2003b). Tasmannia insipida
has a ventral stigmatic crest running the length of the carpel. The sepals fuse laterally
and form a protective cover, called calyptra. The carpel grows up as a completely open
structure in the early stages of its development. Later the carpels close and cells of the
stigmatic surface excrete a sticky uid. First, there appeared calyptra-formed drop-
lets on both pistillate and staminate owers, which probably function as a “reward”
to potential pollinators in advance of ower opening. Pollen tubes were observed to
grow along epidermal cells of the stigmatic crest but did not germinate in the calyptra-
formed droplets (Frame-Purguy 1996, Frame 2003b). In Papua New Guinea, individual
plants of T. piperita had pistillate, staminate and bisexual owers. The white-petaled
owers were functional for 10–12 days and did not close at night. Upon opening, the
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G. Gottsberger, Pollination in basal angiosperms 299
stigmatic crests of the carpels of pistillate or bisexual owers secreted large drops of
sugar-containing uid. Stamen connectives also secreted nectar. In addition to carpel-
lary and staminal secretions, the base of the petals in some infraspecic taxa of this
species also exuded a liquid upon which visitors fed. The only published account of
insect pollination is that of Thien (1980), who found ies visiting the sweet-scented
owers of T. piperita, at very high altitudes (3200–3500 m). Coleoptera, Hymenoptera
and Hemiptera were occasional visitors. At high elevation, where it is cold, ies usu-
ally replace other pollinators, which might be present at lower elevations. There are
other species of Tasmannia, growing at lower altitudes, that may likely be insect pol-
linated. Tasmannia has open owers, and there is nothing to prevent other insects
visiting the owers, such that it does not appear to have owers specialized on ies,
as it is denitely not a trap ower, nor is the ower foul smelling (pers. comm. Dawn
Frame, 2015). It is possible too, that some species may be wind-pollinated, in view
of the large fraction of Tasmannia pollen recorded in regional pollen rain in Australia
(Sampson 1987).
Drimys brasiliensis, studied in southeastern Brazil, was found to open its owers
for the whole day, without any synchronization. As the bisexual white owers (2 cm
diam.) open, they are already in the pistillate stage; stigmas are covered in exudates,
but anthers are still closed (protogyny). From about the second or third day of ower-
ing, stamens start to shed pollen, and this pistillate-staminate stage can last for a few
days until the owers pass into the nal, purely staminate stage (Gottsberger et al.
1980). The open owers emitted a slight, pleasant odor, principally from the petals,
recalling the scent of vanilla or violets, and which was especially strong during the
day hours. During the rst and second night, as long as the owers are in the purely
pistillate stage, the petals bend over the ower center, until the ower is closed, and
unfold again the following morning. A broad spectrum of insects visited the owers.
The most common visitors were small Coleoptera (Curculionidae, Nitidulidae,
Mordellidae, Anobiidae, Tenebrionidae, Chrysomelidae, Dermestidae), and Diptera
(Bibionidae, Scatopsidae, Sciaridae, Syrphidae, Chloropidae) and Thysanoptera, and
occasionally also Lepidoptera, Hemiptera and Collembola. On very hot days, ies
outnumbered beetles. With regard to the beetles, curculionids searched regularly for
pollen and stigmatic exudates often in one and the same ower. Further effective
pollen eaters and transporters were nitidulid, mordellid and tenebrionid beetles; ies
and thrips visited the top of the stamens, probably to feed from small anther glands
found there, as well as on the sticky stigmas. The endemic species D. confertifo-
lia, on Juan Fernández Island was found to have nectarless, anemophilous owers
and to be self-compatible (Anderson et al. 2001). Drimys granadensis, studied close
to Bogotá, Colombia was visited by 29 morpho-species representing 21 families of
Coleoptera, Diptera, Hymenoptera, Psocoptera, Neuroptera and Thysanoptera; con-
sidering the pollen loads carried by the insects, four species of beetles (Curculionidae
and Chrysomelidae) and two species of ies (Bibionidae and Empididae) probably
were the most efcient pollinators (Marquinéz et al. 2009b). Several of the ower vis-
itors were preyed upon by spiders (12 morpho-species belonging to seven families),
which have camouage colors and were observed also to forage on stigmatic exudates
(Marquinéz et al. 2010).
eschweizerbart_xxx
300 G. Gottsberger, Pollination in basal angiosperms
The greenish-white, protogynous owers of Pseudowintera colorata, studied in
New Zealand (Lloyd & Wells 1992), have a pistillate stage lasting on average 6 days.
Afterwards pollen is shed. Pollination occurred during the day, with ower visitors
spanning a rather broad taxonomic range. Holodid beetles and chironomid ies of the
genus Smittia were by far the most abundant visitors. The ies visited staminate phase
owers infrequently and probed the stigmatic exudates rather than fed on pollen. Flies
were more common than beetles, but beetles carried more pollen and they visited both
ower stages more consistently.
Zygogynum s.l. seems to be late-divergent among the Winteraceae (e.g. Karol
et al. 2000, Doust & Drinnen 2004, Marquinéz et al. 2009a), and its approximately
40 species are distributed in Australia, New Guinea, Moluccas, New Caledonia and
the Solomon Islands. Three New Caledonian species of Zygogynum s.s., Z. pancheri,
Z. pauciorum and Z. crassifolium were studied by Thien (1980). The relatively large,
scented, yellow owers, are protogynous and function all in a similar manner; they
were all found to be pollinated by a single species of thrips, Taeniothrips novocaledon-
ensis. The insects chewed on the stigmas and ate pollen.
Zygogynum baillonii and Z. pomiferum were also studied in New Caledonia (Thien
1980). The remarkable characteristics of the owers of these two species are the thick
and leathery petals, which make movements during anthesis. Zygogynum baillonii has
yellow-orange, protogynous owers with a strong burnt-orange scent. The upright
owers open over several hours in the morning. The outer petals extend, but the inner
ones only open slightly, forming a kind of pollination chamber. The owers close
again in the late afternoon of the rst day of anthesis. Early on the second day all
petals open, the stigmas are no longer receptive and the anthers dehisce and release
pollen. Zygogynum pomiferum has thick pale green petals and a strong banana-like
scent; petal movement and duration of anthesis, with the pistillate stage during the
rst day and the short staminate stage during the morning of the subsequent day, are
similar to the former species. Chrysomelid beetles in Z. baillonii and curculionids in
Z. pomiferum were found to enter the oral chamber during the rst day and to leave
the owers during the second day in the staminate stage when all petals expand. An
additional ower visitor was a species of Sabatinca, a representative of the basal moth
group Micropterigidae. In subsequent studies (Thien et al. 1985, Pellmyr et al. 1990)
the importance of beetles and the micropterigid moth Sabatinca was shown. Adult
Sabatinca moths have grinding mandibles and usually feed on spores of ferns and
pollen. The moths use the owers of Zygogynum as mating sites and eat the pollen
which is immersed in a dense pollenkitt. Since fossil records of both the moth and
the Winteraceae extend to the Early Cretaceous, it was assumed that this association
is an ancient one. Visitors to several Zygogynum s.l. species were found to be two
species of Sabatinca and three species of weevils (Palontus spp., Curculionidae). The
Palontus beetles often carried pollen on their body, while the moth Sabatinca carried
only light loads on their heads. Thien and co-workers concluded that the beetles are
regular pollinators while Sabatinca is a more occasional pollinator. Thien et al. (1990)
found densely packed polysaccharide granules at the inner surface of petals of several
species of Zygogynum and interpreted them as “food-bodies”, which function as polli-
nator rewards for beetles.
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 301
We found (Gottsberger et al. 1980) that cross-pollinated owers of Drimys brasilien-
sis had a 24% higher fruit set than bagged self-pollinated owers. Still, self- pollinated
owers formed normal ripe fruits and seeds, an indication that self-compatibility is
a possible mode of reproduction in this species. Also Thien (1980) mentioned that
bagged buds of Zygogynum pancheri set fruit after owering. Adam & Williams
(2001) reported of high levels of selng in monoecious individuals of the otherwise
dioecious Tasmannia insipida. On the other hand, Pseudowintera colorata did not form
fruits after self-pollination (Godley & Smith 1981), and self-incompatibility in this
species was later conrmed by Lloyd & Wells (1992; see also Sage & Sampson 2003
for P. axillaris). Sage et al. (1998) mention several authors which, recording to them,
have reported on self-sterility in the genera Belliolum, Bubbia, Drimys, Exospermum,
Pseudowintera, Tasmannia and Zygogynum, essentially deduced from the failure to
produce fruit following self-pollination. Sage et al. (1998) studied Pseudowintera axil-
laris and Drimys winteri and found that “. . . self-sterility mechanisms in both species
appear to result in failure of embryo sac development after double fertilisation has
been effected by self-pollen tubes.”
Piperales
According to the APG III (2009) classication, the order Piperales comprises fam-
ilies having a perianth, i.e. Aristolochiaceae and Lactoridaceae, and those lacking a
perianth, i.e. Piperaceae and Saururaceae (e.g. Jaramillo et al. 2004). The relation-
ships of the holoparasitic Hydnoraceae is unclear within Piperales, but molecular
and morphological data indicate that the two genera of Hydnoraceae, Hydnora and
Prosopanche, comprise a clade together with Aristolochiaceae sensu lato (including
Lactoridaceae). This clade is sister to the other clade composed of Piperaceae and
Saururaceae (Nickrent et al. 2002, Neinhuis et al. 2005). Recently, Christenhusz et al.
(2015) reported that there is support for Lactoridaceae and Hydnoraceae being nested
in Aristolochiaceae s.l.
Accepting two subfamilies in Aristolochiaceae s.s. has gained support especially
in light of the study of Neinhuis et al. (2005). Subfamily Asaroideae has about 85 spe-
cies occurring mainly in northern temperate regions, with a center in Asia; subfamily
Aristolochioideae has about 420 species having a predominantly pantropical distri-
bution. Results by the aforementioned authors also provides evidence that within
Asaroideae, Saruma is sister to Asarum. The monotypic Saruma henryi from China
is outstanding in Aristolochiaceae by possessing apocarpy, a free green outer, and
yellow, inner perianth, free anthers and carpels, and sulcate pollen. This species also
has small, trimerous polysymmetric owers, and supercially similar to Annonaceae
owers (Dickison 1992, Leins & Erbar 1995). A cladistic analysis and examination
of the pollination mechanisms of the protogynous owers in the genus Asarum seems
to support the conclusion that herkogamy (short laments and spatial isolation of
dehisced anthers and stigmas), and thus obligate insect pollination, is derived from a
plesiomorphic condition of autonomous self-pollination (stamen movements with dep-
osition of copious amounts of pollen directly on the stigmatic surface) (Kelly 1997).
Such a plesiomorphic condition, for example, occurs in A. europaeum, which despite
an intense unpleasant or pleasant scent (various authors have either perceived the scent
eschweizerbart_xxx
302 G. Gottsberger, Pollination in basal angiosperms
differently or there exist mutants having different scents) was never found to be visited
by insects and is self-pollinating (e.g. Kugler 1934, Daumann 1972). On the other
hand, Asarum caudatum and other Asarum species are regularly pollinated by fungus
gnats (e.g. Fungivora fungorum, Mycetophilidae) (Vogel 1978, but see criticism by
Lu, 1982). The fungus gnat owers of Asarum species are fungi mimics and attract
midges, which mate on the ower and even oviposit; the subsequent larvae, incapable
of eating ower tissue, die before anthesis ends. Pollination by brood-site deception
appears to be common in Asarum and also occurs in Aristolochia (Vogel 1978, Burgess
et al. 2004).
Flowers of the Aristolochioideae are also basically trimerous, functionally protogy-
nous and the perianth is mostly gamophyllous. Most species depend on insects for
pollination and they are all myiophilous or sapromyiophilous. The basic oral mech-
anism of Aristolochia has been known since Sprengel (1793). Huber (1993) summa-
rized characters typically associated with y pollination, such as ower gigantism,
something not intuitively obvious given the small size of the pollinators (e.g. Hipolito
et al. 2012); caudate perianth lobes often bearing osmophores (Vogel 1962); ower
parts imitating fruiting bodies of mushrooms (including their lamellae), and the ow-
ers indeed being pollinated by fungus gnats (Vogel 1978); in some species there are
limb-born oral nectaries or nectarioles, which play a role in attraction of certain ies
(Daumann 1959, Vogel 1998b, Murugan et al. 2006), and in some cases the nectar
functions as food to guarantee survival of the imprisoned pollinators, in which case
the nectaries are of the trichomatous type located inside the utricle (e.g. Vogel 1998c,
Erbar 2014); dark purple, brown to black coloration, often set against yellow or green
background; a musky, fruit-, fungus-, urine- or carrion-like odor in several species;
and the perianth tube converted into a trap, which commonly retains the visitors by
a smooth, oily inner surface or by stiff “trap hairs”. These hairs allow the visitors to
enter the basal part of the perianth tube, the utricle, harboring the stigmas and anthers,
but inhibits their exit until hairs wilt after pollination. For new data on the contri-
bution of trapping trichomes to the capture, retention and release of pollinators see
Oelschlägel et al. (2009). Oelschlägel et al. (2015) described an extraordinary klepto-
myiophilous strategy for A. rotunda. The main pollinators are female chloropid ies.
The ies are food thieves that feed on secretions of true bugs (Miridae) while these
are eaten by arthropod predators. Freshly killed mirids and A. rotunda owers release
the same scent compounds that chloropids use to nd their food sources. Most species
of Aristolochia have a oral longevity of 2–3 days, however, A. chilensis and other
species occurring in arid and low productive environments, produce owers lasting up
to 8 days. This might be correlated with the low abundance of pollinators in dry and
unfertile habitats (Stotz & Gianoli 2013). Data presented in Endress (1994), Murugan
et al. (2006), Nakonechnaya et al. (2008), Berjano et al. (2009) and Stotz & Gianoli
(2013) indicate that ies of the following families visit and eventually pollinate
Aristolochia species: Agromyzidae, Anthomyiidae, Asillidae, Bibionidae, Borboridae,
Calliphoridae, Cecidomyiidae, Ceratopogonidae, Chironomidae, Chloropidae,
Dolichopodidae, Drosophilidae, Empididae, Ephrydidae, Fanniidae, Heleomycidae,
Heteromyzidae, Lauxanidae, Lonchaeidae, Millichiidae, Muscidae, Mycetophilidae,
Neriidae, Ortalidae, Otitidae, Phoridae, Piophilidae, Pipunculidae, Platystomatidae,
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 303
Psychodidae, Richardiidae, Sarcophagidae, Scatopsidae, Sciaridae, Sepsidae,
Spaeroceridae, Syrphidae, Tachinidae, Tephrididae, Trypetidae and Ulididae.
With regard to the breeding systems of Aristolochiaceae, as mentioned pre-
viously, studies of Asarum indicate that self-compatibility (Kugler 1934, Daumann
1972, Lu 1982), partly with autonomous self-pollination is basal in the genus, while
herkogamy with obligate cross-pollination by insects, seems to be derived; it is not
clear whether the herkogamous species have a self-compatible or self- incompatible
breeding system (Kelly 1997). The genus Aristolochia has both self-compatible
(e.g. A. argentina, Trujillo & Sérsic 2006) and self-incompatible species. For example,
Nakonechnaya et al. (2008) attribute (partly based on the literature) self-pollination
and self- compatibility for A. manshuriensis, A. littoralis, A. barbata, A. brasiliensis,
A. bracteolata. Aristolochia arborea (Cammerloher 1922) and A. paucinervis (Berjano
et al. 2006) have autonomous self-pollination leading to fruit set. Cleistogamy occurs
in A. serpentaria (Pfeifer 1966). Murugan et al. (2006) found self-compatibility in
A. tagala and note that few Aristolochia species are self-incompatible, as for example
A. maxima, A. gigantea and A. grandiora.
The monotypic Lactoris fernandeziana (Lactoridaceae), endemic to the Juan
Fernández Islands, has small, green, trimerous, solitary owers (or few-owered
inorescences); the unisexual owers have vestiges of staminodia or pistils (Kubitzki
1993e). The study by Bernardello et al. (1999) and Anderson et al. (2001) has shown
that this species is gynomonoecious and wind-pollinated. Bisexual owers are her-
kogamous and protogynous. Based on experimental hand self-pollinations, the plant
is self-compatible (geitonogamous) and capable of outcrossing. The coupling of wind
pollination and self-compatibility in Lactoris might by a consequence of the scarcity
of pollinators on Juan Fernández Islands (Anderson et al. 2001).
Members of the holoparasitic family Hydnoraceae have a rhizome-like under-
ground organ on which ower buds develop and emerge from the soil at anthesis. The
actinomorph protogynous ower is a more or less large (5.5–11 cm diam.), cylindrical,
eshy tube having eshy lobes, which bear the reproductive organs on the inner tube
wall and on its base. Hydnoraceae comprises two genera, Hydnora and Prosopanche.
Hydnora has seven species and is distributed in Africa, Réunion, Madagascar and
Saudi Arabia. Three species of Prosopanche are known and occur in South and Central
America (The Plant List 2013). In Hydnora only the perianth lobes and sometimes
part of the oral tube emerge above the soil. In H. africana, osmophores on the thick,
orange-red tepal lobes emit a putrid, carrion-like odor that attracts beetles, which drop
into the deep oral tube of the protogynous ower. The smooth inner surface and the
vertical inclination of the tube prevents most visitors from escaping. After about 3 days
of strong odor production in the pistillate stage, anthers open and shed pollen. At about
this time, too, the surface of the oral chamber begins to change, creating a surface
that facilitates release of the pollen-impregnated insects. Among the 10 beetle species
that visit owers, the most common one (77% of all visits) was Dermestes maculatus
(Dermestidae), which is known to oviposit exclusively on carrion (Bolin et al. 2009).
Recently, a new Hydnora species, H. visseri was recognized upon segregation from
H. africana (Bolin et al. 2011). The primary pollinator of H. visseri was found to be
Dermestes maculatus (no y visitors), while H. africana was found to attract numerous
eschweizerbart_xxx
304 G. Gottsberger, Pollination in basal angiosperms
esh ies (Sarcophagidae) in addition to beetles. It appears that different oral scent
compounds of these two Hydnora species attract a different insect spectrum. Hydnora
triceps also attracts dermestid beetles and blow or carrion ies (Calliphoridae), and
H. johannis is pollinated by scarab beetles (Musselman & Visser 1989, Bolin et al.
2009). Hence, Hydnora owers can be classied as exhibiting brood-site mimicry
with imprisonment. Low thermogenesis (in H. abyssinica 2.8 °C and in H. esculenta
3.8 °C above ambient temperature in the pistillate stage) appears to be associated with
scent production. On the other hand, in H. africana no temperature elevation could
be measured (Seymour et al. 2009b). The pollinating carrion beetles and carrion and
esh ies of Hydnora apparently do not oviposit while inside the owers (Bolin et al.
2009). Among American members of the Hydnoraceae, owers of the South American
Prosopanche americana, which exhibit thermogenesis (Cocucci & Cocucci 1996), also
emit an unpleasant smell and were found to be pollinated by nitidulid (Neopocadius
nitiduloides) and curculionid (Oxycorynus hydnorae) beetles. Both beetle species,
besides being considered effective pollinators of Prosopanche, have been observed
to oviposit in the oral tube; their larvae fed on tube tissue and they completed their
development underground on the plant (Bruch 1923). The second Argentinian spe-
cies, P. bonacinae, is associated with two weevil species, Hydnorobius hydnorae and
H. parvulus (Ferrer & Marvaldi 2010). Thus, several members of Hydnoraceae are
strictly cantharophilous (saprocantharophilous), while others (e.g. H. africana, H. tri-
ceps) eventually have a mixed saprocantharophilous/sapromyiophilous pollination
system. The role of y-mediated pollination, however, was not yet been fully worked
out (Bolin et al. 2009). At present, nothing is known about the breeding system of
Hydnoraceae (see Bolin et al. 2009).
Piperaceae are pantropical, but the great centers of diversication are in the
Neotropics and Southeast Asia. They are poorly represented in Africa wherin there
are only two native species of e.g. Piper (Smith et al. 2008). Piperaceae are notable
for their spicate or racemose inorescences having minute perianthless owers, each
subtended by a single bract. Flowers are bisexual or unisexual; in the latter case spe-
cies are monoecious or dioecious (Tebbs 1993). Early on, largely due to their incon-
spicuous owers and inorescences, many researchers thought that Piperaceae had
abiotic pollination, by wind and/or rain water (e.g. Martin & Gregory 1962). This
despite even earlier workers e.g. F. Müller (1922) and Wettstein (1935), having men-
tioned ies, bees and beetles as visitors of the inorescences and from this deducing
entomophily for Piperaceae. Semple (1974), Vogel (1998a) and Figueiredo & Sazima
(2000) have shown that insects regularly visit and pollinate Piperaceae owers. In
the study by Semple (1974) in Costa Rica, Piper aduncum, P. auritum, P. friedrichs-
thalii, P. villiramulum and Pothomorphe peltata were investigated. The owers of all
studied species are bisexual and protogynous, the stigmas being exserted several days
before anther dehiscence. Several species of Trigona (Apidae) besides Augochloropsis
and Lasioglossum bees (Halictidae) and several small unidentied beetles visited the
inorescences of these species. Trigona bees were the most common, and small bee-
tles were the next most numerous, visitors. Trigona seemed to be the most efcient
pollinater, because these bees collected large amounts of pollen by working up and
down the spikes, and they were observed to y from spike to spike. Up to six bees
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 305
were observed on a spike at a time. Individual bees were seen ying from one Piper
species to another, indicating weak species constancy on single foraging trips. Wind
pollination was found to be unlikely because of the sticky nature of the pollen grains.
The author found that even after rain storms pollen still was present on the spikes. The
study of Figueiredo & Sazima (2000) in southeastern Brazil included eleven species
of Piper, two species of Ottonia and Pothomorphe umbellata. The majority of the
species studied exhibited incomplete protogyny, Piper mikanianum showed complete
protogyny, P. xylosteoides incomplete protandry, and P. regnelli homogamy. All but
one species had bisexual owers; the exception was Piper arboreum, which had some
inorescences having only staminate owers and others only bisexual ones. Prior to
this, andromonoecy had not been recorded in Piperaceae. In Peperomia fraseri another
unique sex distribution was found by Remizowa et al. (2005), here, the lower owers
of each spike are bisexual and the distal region of the same inorescence bears pistil-
late owers (gynomonoecy). The inorescences of the species studied by Figueiredo &
Sazima (2000) were creamy, yellowish or whitish in color, and most of them (except
Piper aduncum) produced a sweet, lemon-like odor. Nectar was not discernible in the
owers, although heretofore observed by other authors. Pollen of all species was found
to be dry. Insects visited inorescences of all species for pollen, moving up and down
the inorescences. The most important were syrphid ies and apid bees, while some
Coleoptera and Hemiptera behaved as herbivores and appeared not very important
for pollination. Wind pollination was found to occur additionally to entomophily in at
least seven species, leading to the conclusion that the investigated Piperaceae showed
attributes commonly associated with entomophily and anemophily and have therefore
to be considered ambophilous. These authors studied eight further Peperomia spe-
cies (Figueiredo & Sazima 2007). Pollination by wind and Syrphidae was conrmed
for two self-incompatible species. The remaining six species are self-compatible and
their high fruit set was accounted by autonomous self-pollination or agamospermy.
In Peperomia magnoliifolia (protandrous with a distinct fruity smell reminiscent of
Alocasia odorata) and some related taxa, Vogel (1998a) described nectarioles on the
oral bracts, which are extraoral but nuptial in function; these produced a sugar-
containing liquid that attracted sciarid and muscid ies. On the basis of his observa-
tions, Vogel hypothesized a sapromyiophilous syndrome for the study species. Piper
marginatum, studied north of Recife, Northeast Brazil, was revealed to have bisexual,
also protandrous owers (Ulbricht 2006). The cream-colored, sweet-aromatic-scented
inorescences were visited by a broad spectrum of insects between 7:30 a.m. and
4 p.m., which consisted principally of bees (Tetragonisca angustula, Exomalopsis sp.,
Augochloropsis sp., Apis mellifera), ies (5 spp. of Syrphidae), lacewings (one species
of Chrysopidae, Neuroptera) and beetles (among others Chrysomelidae).
The breeding systems in Piperaceae are known for only few species. The Paleotropic
Piper nigrum and the Neotropical P. arieianum are reported to be self-compat-
ible (Martin & Gregory 1962, Marquis 1988, Sasikumar et al. 1992), while the
Paleotropical P. methysticum is self-incompatible (Prakash et al. 1994). Five of the
eleven species investigated by Figueiredo & Sazima (2000) show a substantial degree
of self- compatibility (of these ve species, Piper aduncum and Pothomorphe umbel-
lata, may be agamospermous, since all inorescences developed fruits), while the
eschweizerbart_xxx
306 G. Gottsberger, Pollination in basal angiosperms
other species evinced a low degree of self-compatibility or were self-incompatible.
Piper marginatum was revealed to be self-incompatible (Ulbricht 2006).
Saururaceae (6 species) have a disjunct distribution in North America and East and
Southeast Asia. The inorescences are dense spikes, which in Houttuynia, Anemopsis
and Gymnotheca have showy bracts at the base of the spike, giving the inorescence
a pseudanthial appearance. The owers are bisexual and without perianth (Cheng-
Yih & Kubitzki 1993). The nectarless owers of Saururus chinensis have a faint scent
and were found to be visited by many insects, especially syrphid ies (Tanaka 1979).
Saururus cernuus, investigated in southern United States near New Orleans (Thien
et al. 1994), has sweet smelling, protogynous owers, pollinated by wind, bees, ies
and beetles. When large insects land on the spike, small clouds of pollen are released
into the air (insect-mediated wind pollination). Thien and collaborators concluded that
wind, insect-mediated anemophily and insects alone or in combination contribute to
fruit set in this self-incompatible species.
Laurales
Based on evidence from both molecular and morphological data, the order Laurales
consists of seven families (Renner 1999, see also APG III 2009). The Calycanthaceae
(including Idiospermum) are sister to the remaining six families, which form two groups,
the Siparunaceae-Gomortegaceae-Atherospermataceae clade and the Hernandiaceae-
Monimiaceae-Lauraceae clade (Renner 1999, Renner & Chanderbali 2000).
The deepest split within Calycanthaceae is between the monotypic tropical
Idiospermum australiense (Idiospermoideae) and the temperate shrubs of the two
other genera (Calycanthoideae) (Li et al. 2004, Zhou et al. 2006). Flowers of nearly
all ten species of the family are bisexual and protogynous, and have a cup-shaped or
urceolate receptacle (Kubitzki 1993).
Flowers of Idiospermum australiense, a canopy tree in tropical rainforests of North
Queensland, are relatively large (ca. 3.5 cm in diam.), with some populations of the
species being andromonoecious while others having only bisexual owers (Worboys &
Jackes 2005). Just as in other Calycanthaceae, tepals of I. australiense become pro-
gressively smaller distally, grading into persistent, rigid inner tepals, which cover the
androecium. The stamens and their extended connective appendages exhibit a tran-
sitional series into staminodes. Food bodies on tepals, staminodes and stamens such
as found in Calycanthus, or nectar production on tepals as in Chimonanthus, are not
present in Idiospermum. The anthesis of an individual ower of Idiospermum lasts
three to four days, although the wilting owers remain attached up to 10–16 days.
Tepals are creamy white during the initial pistillate stage, and strongly fragrant
throughout the day. Moreover, during the staminate stage, which starts on the third
day after tepal opening, fragrance is still strong, and tepals have meanwhile turned to a
dull purple color. From the fourth day on the fragrance fades and owers start to wilt.
In the center of the ower, the inner tepals, together with the staminal appendages and
staminodia form a crater, providing access to the stigmas for insects. A wide diversity
of arthropods, including Diptera and 13 species of beetles, and most commonly thrips
visited the owers. Particularly thrips were most abundant in pistillate and staminate
stage owers. The authors conclude that Idiospermum has a generalist pollination
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 307
system, and that thrips and beetles are the main pollinators, rewarded by pollen and/
or oral tissue.
Vogel (1998a) found the strong-smelling owers of the Chinese Chimonanthus
praecox to have melittophilous characters. The outer tepals are cream or light yellow
and the inner ones are smaller and dull purple with yellow spots. In the pistillate stage,
the stamens are bent toward the tepals and thereby expose the pistils. After two days,
the stamens commence to bend toward the oral center (which may take from one to
four days) until they enclose the pistil, thereafter the anthers shed their pollen (Azuma
et al. 2005). Flowers of cultivated plants in Europe attracted bees (Osmia cornuta and
honeybees), as well as syrphid, anthomyiid and drosophilid ies (Vogel 1998a). All
insects imbibed the freely exposed nectar produced by nectarioles (Erbar 2014), an
assemblage of glandular cells arranged around a single stomatal sap-hole on the inner
petaloid tepals. Studies in China have conrmed that this species is pollinated by Apis
bees as well as syrphid and muscid ies (Azuma et al. 2005).
The large, dark red owers of Calycanthus occidentalis emit a wine-like, fermented
fragrance at anthesis and were found to last 12–36 hours. After opening of the outer
tepals and the beginning of the pistillate stage, the inner tepals maintain their semi-
closed position and form a kind of pollination chamber. The innermost tepals, stamens
and inner staminodes have pearl-white food bodies on their tips. In California, the
nitidulid Colopterus truncatus (about 3 mm long) was found to be the main pollinator
of this species (Grant 1950); the beetles eat the food bodies, which contain high levels
of protein and low quantities of lipid and starch (Rickson 1979). At other places in the
U.S., other nitidulid species of the genera Colopterus and Carpophilus were found
to be effective pollinators of C. occidentalis and C. oridus (Nicely 1965, Williams
et al. 2008).
The Chinese Calycanthus chinensis has owers of 4–7 cm in diameter. The outer
tepals are whitish with a tinge of pink, while the inner tepals are pale yellow to white
with maroon markings; they are eshy and form a kind of pollination chamber. The
owers are scentless and do not produce nectar. The distal margins of the petals and
the connective appendages were found to bear a warty cover. Several subjacent cell
layers were rich in cytoplasm and quite similar in consistence to the food bodies of the
North American Calycanthus species. They represent food tissue rather than distinct
food bodies as occur in the other two Calycanthus species. Vogel (1998a) suggested
that the owers of this species might reveal to be cantharophilous. Li & Del Tredici
(2005) conrmed that this species is indeed pollinated by small beetles.
Information regarding breeding systems in Calycanthaceae is quite scarce.
Calycanthus chinensis was found to be self-compatible and not apomictic (Zhang &
Jin 2009) and Chimonanthus praecox to be self-compatible (Zhou et al. 2006, Du
et al. 2012b).
Siparunaceae comprises two genera, the West African Glossocalyx and the New
World tropics Siparuna. Flowers of Siparuna are strictly unisexual, small (a few
mm in diameter), and sex distribution is monoecious (15 species) or dioecious (the
remaining 38 spp. of Siparuna, as well as also Glossocalyx). The monoecious spe-
cies are proposed to be evolutionarily basal to dioecious species (Renner & Hausner
2005). Reproductive organs in Siparuna are completely enclosed in massive cup-like
eschweizerbart_xxx
308 G. Gottsberger, Pollination in basal angiosperms
receptacles. A membrane, called oral roof or velum covers the reproductive organs
except for a small pore in the center. At anthesis, the styles and anthers emerge through
this pore. The styles may fuse postgenitally at the height where they emerge from the
massive receptacle, resulting in a joint transmission track for pollen tubes that origi-
nally landed on different stigmas (Renner et al. 1997). Pollination has been studied in
13 dioecious species in Ecuador and Colombia (Feil & Renner 1991, Feil 1992, Peña
Paz 2000), and six monoecious species in Central Amazonia (Schulz-Burck 1997).
Data for these 19 species in addition to data from herbarium material suggest that
pollination mode is identical throughout the genus (Renner & Hausner 2005). Flowers
of dioecious species in Ecuador were found to be pollinated by gall-midges (Asynapta
sp., Clinodiplosis sp., Dasineura sp., Cecidomyiidae, Diptera). Female cecidomyiids
are attracted at night by the lemon-scented owers and try to insert their abdomen into
the pore of the oral roof of pistillate and staminate owers in an effort to deposit an
egg into the owers’ interior. Egg laying was chiey in staminate owers because they
are more readily accessible than pistillate ones; pistillate owers are almost entirely
closed, with only the stigmas protruding, and thus unsuited for the ovipositing gall-
midges. Pistillate owers also aborted if eggs were laid in them. As insects moved
during oviposition in the staminate owers, their abdomens become covered in pol-
len. Mature larvae of cecidomyiids, drop from their host plants and construct silk
cocoons in the soil. Holes have been observed in the receptacles of a few staminate
owers of Siparuna species that may have been created by exiting midges (Renner &
Hausner 2005).
Gomortega keule, of monotypic Gomortegaceae, from Central Chile, produces
small (4–5 mm diam.), white, protogynous owers. Based on the size and shape of its
owers and the presence of large nectary glands at the bases of the laments of outer
staminodes (Kubitzki 1993c), Renner et al. (1997) postulated that it is pollinated by
small ies and bees. Lander et al. (2009) collected 34 insects of six families at the
owers, 26 syrphids and 8 non-Syrphidae (among others one species each of lauxanid
ies, sphecid and vespid wasps, a colletid bee and a Psocidae). Syrphid ies were the
most common ower-visiting insects, carried the largest proportion of G. keule pollen
and appeared to be effective pollinators of the species.
The Atherospermataceae may have unisexual or bisexual owers (protogyny in
bisexual owers of Daphnandra conrmed by Endress 1992). Staminal appendages in
Laurelia, Daphnandra and Atherosperma moschatum secrete nectar (Sampson 1969,
Endress 1992, Erbar 2014). Sampson (1969) observed a considerable number of bees
and blowies (Calliphoridae) visiting the owers for nectar; Schodde (1969) found
them to be pollinated by ies and bees.
Flowers of the pantropical Hernandiaceae are bisexual or unisexual, in the latter
case the plants are polygamous or monoecious, rarely dioecious. The laments are usu-
ally provided with a pair of nectariferous glands and in pistillate owers nectariferous
staminodes are present; the anthers dehisce by valves (Kubitzki 1993d). For the strongly
scented monoecious Hernandia nymphaeifolia, Endress & Lorence (2004) described
a novel type of heterodichogamy of unisexual owers not yet known for angiosperms.
Within a population, two kinds of individuals occurred: individuals having pistillate
owers that open in the morning and staminate owers that open in the afternoon,
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 309
while other individuals exhibited the reverse behavior. Heterodichogamy is considered
a strategy to promote outbreeding; nonetheless, in H. nymphaeifolia geitonogamy is
possible because anthesis of the morning and afternoon owers overlap during midday.
Pollination by small ies and bees was postulated for the family (Renner et al. 1997).
The nectar-producing owers of Illigera and Hernandia are mentioned as pollinated
by bees or ies, and the small-owered species of Sparattanthelium and Gyrocarpus
said to be wind-pollinated (Michalak et al. 2010). Studies of Sparattanthelium botocu-
dorum, in Atlantic forests in Northeast Brazil (Ulbricht 2006), found that the bisexual
owers (which initially emitted a sharp smell) opened between 4:00 and 5:00 a.m.
and exhibited four or ve, whitish, extended tepals (ca. 2 mm length), and presented
an apparently receptive stigma as well as laments and anthers; it was not observed if
the owers are slightly protogynous or not. From 8:00–9:30 a.m., tepals and stamens
changed color becoming beige and nally brown. At the end of this stage, owers
scent was more sweetish and fruity. This stage lasted until about 10:30 a.m., as owers
became progressively browner, the scent faded and the owers (from about 3:30 p.m.
on) nally wilted. Pollination experiments indicated self-incompatibility for this spe-
cies. Flower visitation, observed over two days, occurred during a relatively short
period in the early morning hours when the owers were still whitish and emitted their
sharp scent, viz. between 5:45–7:45 a.m. in September and 4:45–8:00 a.m. in October.
Observed ower visitors were ve different unidentied y species, two beetle spe-
cies and two bee species (Exomalopsis sp., Apidae; and an Anthidiini, Megachilidae).
Flies and bees were the most abundant visitors and appeared to be the most effective
pollinators.
Among the pantropical Monimiaceae, most species have unisexual owers
(monoecious or dioecious), but several basal genera, e.g. Hortonia (Hortonioideae),
Dryadodaphne, Nemuaron, Doryphora and Daphnandra (Atherospermatoideae)
(Perkins & Gilg 1901) have regular bisexual owers; protogyny has been conrmed
in Hortonia and Daphnandra (Endress 1992). In Hortonia angustifolia and Peumus
boldus, laments bear two basal appendages, which are probably nectariferous (Erbar
2014). Under its present circumscription (Renner 1998), Monimiaceae are distin-
guished by having a massive cup-like receptacle that shows a trend towards enclosure
of the reproductive organs (Endress 1979, 1980a, 1980b, 1994).
The genus Mollinedia is always dioecious. Mollinedia oribunda and M. widgrenii,
investigated in Brazilian upland Atlantic rainforests in São Paulo and Botucatu, both
in São Paulo State (Gottsberger 1977), were found to bear small roundish owers of
ca. 4–5 mm diam. Four tepals close the small opening of the receptacle during the
bud stage. Buds and open owers are greenish and had no perceptible smell. Female
thrips (Thysanoptera) punctured the still closed pistillate and staminate buds in the
region of the closed tepals with their ovipositor and deposited their eggs in the inte-
rior of the receptacle. When the owers opened, their interior contained thrips eggs,
larvae and adults. Adults not only stay inside owers but can y off; movements from
staminate to pistillate owers lead to pollination. Emerged female thrips also ovipos-
ited in new buds. Thrips visiting M. oribunda were identied as Liothrips seticol-
lis (Phlaeothripidae) and Heterothrips sp. (Heterothripidae). Similarly, Mound and
Marullo (1996) identied the heterothripid Lenkothrips sensitivus in large numbers in
eschweizerbart_xxx
310 G. Gottsberger, Pollination in basal angiosperms
the owers of Mollinedia latifolia in Ecuador, and David H. Lorence (pers. comm. in
letter, December 16, 1988) wrote that he had collected thrips from owers of M. viridi-
ora in Veracruz, Mexico, indicating that thrips-pollination may be the standard mode
of pollination within the genus. Also Wilkiea huegeliana in Australian subtropical rain-
forests is exclusively pollinated by thrips (Williams et al. 2001, Frame 2013), by the
sole species Thrips setipennis. Similarly, in this species, both pistillate and staminate
owers serve as brood sites, with the difference that the entry of the thrips is always
via the small apical ostiole of open owers.
Endress (1979) discovered a most interesting structure, a “hyperstigma”, unique to
angiosperms, in Tambourissa purpurea. It is a secretary zone in the narrow entrance of
the oral cup. At anthesis, the pistillate owers of T. purpurea produce a mucilaginous
plug in the apical oral entrance, and inside the oral cup there is a continuous muci-
laginous lm from the oral entrance to the carpels. Pollen grains deposited on the
outer surface of the mucilaginous plug germinate and the pollen tubes grow through
the mucilage to the carpels. Hyperstigmas not only occur in Tambourissa but also in
Wilkiea, Kibara and Hennecartia (Endress 1980b). Anthesis of owers of different
Tambourissa species lasts 10–15 days. Flower color can be purple, pale white, cream,
pink or pale orange, and oral scent of observed species has been recorded as more or
less strong, fruity, sweet, sour, fermented, rancid or musky. All eleven species investi-
gated produced mucilage on the free surface of the carpels, and Tambourissa purpurea,
as described above, additionally produced mucilage at the hyperstigma. Staminate
owers do not produce any mucilaginous secretion. Flies (Drosophilidae, Lauxaniidae
and Syrphidae) were visitors in six of the seven Tambourissa species studied, whereas
beetles (Hydrophilidae, Nitidulidae, Rhizophagidae and Staphylinidae) were the main
visitors of the four species T. cus, T. quadrida, T. sieberi and T. tau (Endress &
Lorence 1983).
Experiments provide evidence of self-incompatibility for Tambourissa quadrida,
T. tau and T. purpurea, while T. sieberi was partly self-compatible (Endress & Lorence
1983). Pollinator exclusion experiments with the usually monoecious (sometimes dio-
ecious) Wilkiea huegeliana were inconclusive but indicated possible facultative aga-
mospermy (Williams et al. 2001).
Lauraceae have relatively small (1-)2–8(-20) mm diam. owers, organized in com-
pact or loose inorescences. Flowers are open and easy accessible for most insects
and their color usually is greenish, yellowish or white. Flowers are mostly trimerous,
bisexual and protogynous, or unisexual. Plants with unisexual owers are monoecious
or dioecious. Tepals are in two whorls and stamens usually in four whorls, of which the
innermost is sterile or lacking; sometimes other stamen whorls are sterile or lacking.
Anthers open by valves. Stamens of the third androecial whorl of many Lauraceae have
a pair of nectar glands (staminal glands) at their base (Rohwer 1993). Most Lauraceae
having bisexual owers possess an additional fourth androecial whorl that is sterile
but provided with a glandular tissue (staminoidal glands). In the initial pistillate stage
of these bisexual owers, the staminoidal glands (whorl IV) produce nectar, whereas
in the later staminate stage, the staminal glands (whorl III) produce nectar. These two
different, short-use nectaries occur in heterodichogamous Lauraceae having bisexual
owers (Kurz 1982, Rohwer 2009). In such heterodichogamous species there exist
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 311
two cohorts of individuals in a population. Some individuals open their bisexual ow-
ers in the morning in the pistillate stage and become staminate in the afternoon. The
reciprocal individuals open their owers in the afternoon (pistillate stage) and enter the
staminate stage the next morning. The stamens do not open until the stigma of the same
ower wilts. It was described in some species that the owers close after the pistillate
stage and open again at the onset of the staminate stage. Nectaries in both sexual stages
are certainly useful to attract insects to visit both pistillate and staminate stage owers.
In Lauraceae, heterodichogamy with ower closing after the pistillate stage was early
described for Persea species by Stout (1927) and Skutch (1932, 1945).
Amazonian heterodichogamous species of Aniba, Clinostemon and Licaria were
visited by several small species of Trigona (Meliponinae), while dioecious unpleasant
smelling species of Ocotea were visited by unidentied bees, ies, wasps and moths
(Kurz 1982, Kubitzki & Kurz 1984). Six dioecious species of Lindera in Kyoto, Japan,
were visited by a large number of mainly Coleoptera, Diptera and Hymenoptera, typi-
cal visitors of the generalist-pollinated Lauraceae owers (Dupont & Kato 1999). The
Brazilian cerrado species Cinnamomum hausknechtii has bisexual greenish-yellow
owers that emit a distinct sperm-like odor during the initial pistillate and the later
staminate stage. Probably because of the spermatic odor, the spectrum of visitors was
dominated by ies (eight families), and to a lesser degree visited by bees and wasps;
beetles were rather rare pollinators (Gottsberger & Silberbauer-Gottsberger 2006). The
dioecious Laurus azorica studied in the Canary Islands (Forfang & Olesen 1998) has
a male-biased sex ratio. The population consisted of 2.5 times more male than female
trees. Additionally, males produced more owers and their inorescences lasted longer.
Flowers were visited by ten different species of Hymenoptera, Diptera, Lepidoptera,
Coleoptera and Hemiptera, however, the bees Halictus sp. and Lasioglossum spp.
(Halictidae) and the y Tachina canariensis (Tachinidae) accounted for 97% of the
total number of insect visits. The bees collected pollen and nectar and the y collected
nectar from owers of both sexes. Laurus nobilis in Italy was mainly visited by Apis
mellifera, Bombus, other bees, as well as ies and wasps (D’Albore & D’Ambrosio
1982). Another cultivated species, avocado, Persea americana, studied in its region
of origin, Mexico, was visited by about 100 different insect species (Hymenoptera,
Diptera, Coleoptera and Heteroptera) at undisturbed sites and backyards. The most
efcient pollinators were 8–10 relatively small species of stingless bees, as well as
Apis mellifera and the wasp Brachygastra mellica. In commercial orchards sprayed
with insecticides, only a small number of visitors were observed, and those were pre-
dominantly honeybees (Ish-Am et al. 1999). In the Neotropics, Apis mellifera is an
introduced bee species and it is unlikely to be the most efcient pollinator of this
small-owered Persea species (Westerkamp & Gottsberger 2000). Avocado is culti-
vated in many regions having a Mediterranean climate where honeybees commonly
dominate. Apis, however, is an inadequate pollinator because of its preference for
owers of other species, which limits fruit set of P. americana in e.g. Israel (Ish-Am &
Eisikowitch 1993, 1998, Ak et al. 2006).
Thus far, all studies have shown that Lauraceae species have generalist pollination
by pollinators consisting of a mixture of small to medium-sized beetles, ies, bees and
wasps. In the tropical canopy tree Nectandra umbrosa the number of beetles attracted
eschweizerbart_xxx
312 G. Gottsberger, Pollination in basal angiosperms
to inorescences was considerable (723 individuals representing 121 species, collected
during two owering periods for a total of sampling hours) and came mostly from the
following subfamilies: Cerambycinae, Cryptocephalinae, Eumolpinae, Galerucinae,
Baridinae and Curculioninae, however, only a subset of these are likely pollinators,
nor were other insect visitors recorded in this study (Ødegaard & Frame 2007).
Articial geitonogamous pollination in Aniba panurensis, A. roseaodora, Licaria
guianensis and Clinostemon maguireanum, led to no fruits being formed, indicating
self-incompatibility; agamospermy or apomixis apparently did not occur (Kurz 1982,
Kubitzki & Kurz 1984). Self-incompatibility, although not tested, appears likely for
Ocotea tenera, too (Gibson 1995, Gibson & Diggle 1998). Persea americana was
found to set fruits due to spontaneous self-pollination in Florida, however, this does
not occur in the cooler Mediterranean climate in Israel (Ish-Am & Eisikowitch 1998).
Magnoliales
As presently circumscribed, Magnoliales includes six families. Myristicaceae appar-
ently is sister to two clades: one in which Degeneriaceae and Himantandraceae are
sister to Magnoliaceae, and another comprising Eupomatiaceae and Annonaceae (e.g.
Qiu et al. 1999, 2006, Doyle & Endress 2000, Sauquet et al. 2003, Endress & Doyle
2009, APG III 2009). All extant Magnoliales are trees, shrubs or rarely lianas, and
owers are typically large (with the exception of Myristicaceae), bisexual (here again
with the exception of Myristicaceae) and have an apocarpous gynoecium (excepting
Myristicaceae and Degeneriaceae, which are monocarpellate).
Pantropical Myristicaceae are mostly dioecious, with monoecy occurring in a few
genera. Flowers are in inorescences and quite small (4 to 6 mm diam.), actinomorphic,
funnel-shaped, campanulate, or urceolate, and ower color may be yellowish-white,
yellow, pink or red (Kühn & Kubitzki 1993). The dioecious Iryanthera macrophylla
and Virola calophylla in Central Amazonian forests (Ackerly et al. 1990), as well as
Myristica fragrans in plantations in India and M. insipida in rainforests of northern
Queensland (Armstrong & Drummond III 1986, Armstrong & Irvine 1989a) showed
male-biased sex ratios. Male plants of Myristica fragrans produced over 50 times
as many owers as female plants, and its P/O ratio of 801,000:1 was found to be
extremely high for an insect-pollinated plant. Both pistillate and staminate owers of
this species are light cream to yellow, and owers have a sweet, musky scent during
the night. Three species of beetles were observed to visit the owers of M. fragrans
for pollen foraging, but only Formicomus braminus (Anthicidae, an ant-mimicking
beetle) was collected from inside the staminate owers. This beetle is too large to
enter the interior of the pistillate owers, but probing attempts by the beetles would,
nonetheless, deposit pollen on the stigma. It was concluded that the pistillate owers,
which provide no reward, are probably mimics of the staminate owers (Armstrong &
Drummond III 1986). Myristica insipida, investigated in northern Queensland, has a
oral biology similar to M. fragrans. Female and male trees owered synchronously,
producing display maxima between 6 p.m. and 6 a.m., and male trees produced three
times the number of owers of female trees. Although this species inititates anthesis at
night, arrival of ower visitors was observed to begin only the next morning. The most
frequent visitors and most efcient pollinators were small beetle species of the families
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 313
Curculionidae, Mordellidae, Nitidulidae, Scolytidae and Staphylinidae. Thrips were
less effective visitors. The perianth of the pistillate owers excludes beetles from the
oral interior, but during brief visits to pistillate owers they may touch the stigmas; as
beetles do not receive any reward, the pistillate owers seem to function here again by
automimicry (Armstrong & Irvine 1989b, Armstrong 1997). The dioecious Myristica
dactyloides in India showed a generalist pollination system (Sharma & Shivanna 2011)
wherein Thysanoptera (one species of Phlaeothripidae and one species of Thripidae),
which used owers and buds as brood sites (a situation similar to Mollinedia in the
Monimiaceae), and beetles (mainly Staphylinidae and Curculionidae), bees (mainly
Halictidae) and ies (Syrphidae and Phoridae) carried pollen from staminate to pis-
tillate owers. The authors cited earlier research (Givnish 1980, Bawa et al. 1985a,
1985b) which suggests that other species of Myristica conform to a generalized, small
insect pollinator type, too, and not only to a cantharophilous one. Increased research
and sampling intensity in Myristica and other genera of the family will probably reveal
a more diverse pollinator assemblage than presently known. To our knowledge nothing
is known about the breeding system of monoecious Myristicaceae species.
Degeneriaceae historically have been regarded as monotypic, with the single spe-
cies Degeneria vitiensis endemic to the Fiji Islands. Miller (1988, 1989) described a
second species, D. roseiora, which occurs on the islands of Vanua Levu and Taveuni,
while the former species D. vitiensis occurs about 60 km distant on the island Viti
Levu. Either species may reach tree heights of 35 m. Degeneria roseiora has different
(smaller) owers, coloration (pinkish white to rose or magenta), oral smell (a musty
rose smell) and several other differences in ower characteristics as compared to
D. vitiensis. Both species have pendulous owers and are protogynous. The perianth
is differentiated into a calyx having 3 sepals and 12–25 petals. The stamens are fol-
lowed by inner staminodes and a monocarpellate gynoecium. Anthesis of owers
lasts 9–11 h. Fragrance is already emitted before the imbricate buds open in the early
evening. By 9 p.m. the owers are completely open. Upon opening, the yellow petals
and staminodes of D. vitiensis spread, revealing the single carpel. The staminodes
secrete a thick, slimy yellow substance and emit a foul odor (for other authors it resem-
bles the pleasant smell of Cananga; Miller 1989). After the rst night of owering, the
petals and staminodes close over the ower center and on the second evening the petals
and dehisced stamens reex again, the staminodes, however, remain curved over the
carpel. Many male and female individuals of the nitidulid Haptoncus takhtajani were
found in both pistillate and staminate stage owers of this species and are its likely
pollinators (Thien 1980, Miller 1989). As far as we know, there are no data on the
breeding system of Degeneria.
Himantandraceae, comprising two species of Galbulimima, occurs in New Guinea,
the Moluccas, Celebes and Queensland. Their owers are 2–4 cm in diam., bisexual,
probably protogynous and cream-colored. There are no sepals or petals, but there is a
oral envelope consisting of two caps formed by bracts. Stamens are between outer
and inner staminodes. Secretory regions occur on the inner stamens and inner stami-
nodes. Apparently, there are no observations about pollination or the breeding system;
however, a number of oral features seem to point to cantharophily (Endress 1984a,
1993c, 2010).
eschweizerbart_xxx
314 G. Gottsberger, Pollination in basal angiosperms
In former times, Magnoliaceae was one of the families thought to be evolutionarily
basal of extant angiosperms. Their large, solitary owers having an elongated receptacle,
on which numerous stamens and free carpels are spirally arranged, were long held to be
prototypical of ”primitive” owering plants (see Frame & Gottsberger 2007). However,
as previously noted, new phylogenetic data do not support this concept. Modern inter-
pretations treat Magnoliaceae as having two subfamilies, Liriodendroideae with two
species of Liriodendron, and Magnolioideae with 220–240 species, of a single genus,
Magnolia, itself further subdivided into three subgenera and 12 sections (Figlar &
Nooteboom 2004, Figlar 2006). The extant members of the family exhibit disjunct trop-
ical/subtropical/temperate distributions in the Americas and in East and Southeast Asia.
One of the earlier studies on oral biology and pollination of temperate species
was that of Heiser (1962), who studied Magnolia tripetala, M. grandiora, M. macro-
phylla and M. virginiana, all North American natives to the U.S.A., and worked mainly
with cultivated individuals in Bloomington, Indiana. He discovered that the large,
white-petaled owers were protogynous, strong smelling and attracted principally bee-
tles, which were the main pollinators of these Magnolia species; ies and bees were
less important. Eight Magnolia species native to the southeastern United States were
investigated by Thien (1974), here, too, they are pollinated by several species of bee-
tles that entered buds as well as closed and open owers, and fed on stigmatic exudates
and on pollen and petal secretions. Individual owers last from two to four days and
undergo a series of petal, stigma and stamen movements that assure beetle pollination,
and even exclude other insects, such as bees. Thien (1974) mentioned visitation of
bees to owers, but attributed to them a very low if any importance for pollination,
and classied the owers of Magnolia as highly specialized for exclusive pollination
by beetles. In a later paper, Thien et al. (1995) admitted that at least in M. macro-
phylla, M. ashei and M. dealbata (the petals of the last mentioned species have uo-
rescence patterns in ultraviolet light), beetles and bees were pollinators. Allain et al.
(1999), after observations of cultivated individuals of Magnolia grandiora in South
Louisiana (which also exhibits oral UV reectance patterns) concluded that although
beetles were occasional oral visitors and carried pollen, . . . “bees (non-native Apis
mellifera and indigenous Lasioglossum bruneri) were frequent oral visitors and were
the only oral visitors whose behavior showed any correlation with the array of oral
changes that occurred over the 3–4 day owering period.” In their study, Hymenoptera
and Thysanoptera accounted for 87% of the insect visits, while the remaining 13% of
insect visits were by Coleoptera, Diptera, Hemiptera, Homoptera and Plecoptera. The
Japanese M. stellata is said to be pollinated principally by rove beetles (Staphylinidae)
and Thysanoptera, but rarely also by bumblebees, honeybees, and ies (Hirayama
et al. 2005, Setsuko et al. 2008). Likewise, M. praecocissima in Japan is principally
pollinated be beetles. About 78% of its visitors crawling on stigmas and stamens were
Coleoptera (Chrysomelidae, Curculionidae, Nitidulidae, Oedemeridae, Scraptiidae
and Staphylinidae), and the remaining 22% were Diptera and Hymenoptera (Ishida
1996). Studying eight Magnolia taxa native to Japan, Yasukawa et al. (1992) found
that a very large spectrum of insects visited the owers, including not only Coleoptera,
but also a number of Diptera and Hymenoptera, which nearly all played at least some
role as pollinating agents. The picture is not much different for species in China. In
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G. Gottsberger, Pollination in basal angiosperms 315
Liriodendron chinense, bees, ies and beetles behaved as generalist foragers, and none
of them seemed to be especially adapted to the owers (Huang et al. 1999). Again, in
Magnolia coriacea, insects of the three orders Coleoptera, Diptera and Hymenoptera
were ower visitors. The most effective pollinators appeared to be chrysomelid bee-
tles, ies (Fanniidae) and Bombus (Apidae) (Zhao & Sun 2009). Strong indications that
not only the mainly pollen- and tissue-eating beetles but also nectar-sucking insects
are pollinators of the above mentioned Magnolia species, are provided by Daumann
(1930) and especially Erbar & Leins (2013), who investigated M. stellata in detail and
found an epithelial nectary involving the epidermis of the entire carpels. Nectar pro-
duction is limited mainly to the pistillate phase of anthesis. This way, the attractiveness
of the owers is also assured in the initial non-pollen presentation stage of anthesis.
In conclusion, one gets the impression that in nearly all northern hemisphere temper-
ate Magnolia species studied so far, beetles are important for pollination, and in some
sites may even be the predominant pollinators, but that also other insect groups, espe-
cially bees, ies and thrips are more or less important and effective co-pollinators, too.
Studies of Neotropical species of Magnolia, however, have revealed strict canth-
arophily. Gibbs et al. (1977) found the large thick-petaled owers of the Brazilian
species M. ovata to be nocturnal; anthesis is protogynous, the owers open and close
in a two-night rhythm and are pollinated by large dynastid scarab beetles. Later it was
found that the owers of this species are thermogenic in both the pistillate and stami-
nate stages, attaining 6.0 and 10.6 °C above ambient air, in the pistillate and staminate
stages, respectively (Seymour et al. 2010). Female and male individuals of only one
beetle species, Cyclocephala literata (Dynastinae: Scarabaeidae), are attracted to the
scented, warm owers in both pistillate and staminate stages (Fig. 3). Once inside
the owers they feed on petal tissue (in pistillate stage owers) and on pollen (in the
staminate stage) and also mate inside the owers (Gottsberger et al. 2012). The two
Mexican species, M. schiedeana and M. tamaulipana apparently also have nocturnal
anthesis and are visited and pollinated by Cyclocephala species (Dieringer & Espinosa
1994, Dieringer et al. 1999). The owers of the Paleotropical species M. persuave-
olens, observed for a short time at Mt. Kinabalu, Sabah, Borneo (Gottsberger, pers.
obs.), were found full of small ies but contained no beetles at all.
With regard to the breeding system, Magnolia ovata, a member of the most early
divergent section Talauma was found to be self-compatible (Gibbs et al. 1977). Two
other tropical American species, the Mexican M. schiedeana and M. tamaulipana are
also self-compatible (Dieringer & Espinosa 1994, Dieringer et al. 1999). The North
American species M. tripetala, M. virginiana, M. grandiora, M. macrophylla and
M. ashei likewise revealed self-compatibility (Heiser 1962, Thien 1974, Allain et al.
1999), and this breeding system was also found in the Japanese species M. praecocis-
sima var. borealis, M. obovata, and M. stellata (Ishida 1996, 2008, Ishida et al. 2003,
Isagi et al. 2004, 2007, Hirayama et al. 2005, Setsuko et al. 2008, Matsuki et al. 2008,
Tamaki et al. 2009, Setsuko & Tomaru 2011) and in the Chinese species Liriodendron
chinense, Magnolia coriacea and M. denudata (Huang & Guo 2002, Zhao & Sun
2009, Wang et al. 2010); notwithstanding, some of these species showed breeding
depression. The two North American species M. fraseri and M. pyramidata are men-
tioned as being self-incompatible (Thien 1974).
eschweizerbart_xxx
316 G. Gottsberger, Pollination in basal angiosperms
The three species Eupomatia laurina, E. bennettii and E. barbata (Eupomatiaceae)
occur in eastern Australia and New Guinea and have relatively large (3–4 cm diam.),
bisexual, protogynous owers, which are interpreted as lacking a perianth, having
petal-like stamens and staminodes instead. Protection of the bud is by a calyptra, an
amplexicaul bract. The petal-like inner staminodes produce sticky, oily exudates and
emit a strong, fruity-musky smell (Endress 2003, Kim et al. 2005). Anthesis lasts one
day in E. laurina, which has cream-colored owers, and two days in E. bennettii,
which has yellow owers and innermost staminodes that are purple. In the initial
Fig. 3. Magnolia ovata. A. Half-open rst-evening ower in the pistillate stage ( expanded
petals ca. 13 cm diam.). B. Pollinating beetles (Cyclocephala literata) after arriving in a pistil-
late stage ower. Some beetles are gnawing at the inner side of the inner petals and others
are initiating to mate. C. Flower in staminate stage, in the second-evening. A beetle is feed-
ing on pollen. D. Open ower in the late-staminate stage with expanded petals, showing one
beetle covered with pollen. Feeding marks caused by beetles are visible mainly at the inner
side of the inner petals.
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 317
pistillate stage, the staminodes expand and function as organs of visual and olfac-
torial attraction. In a later stage, the staminodes bend over the center of the ower
and hide the gynoecium, while the stamens shed their pollen (Endress 1984b, 1993b).
Several species of Elleschodes (Curculionidae) visit and pollinate Eupomatia ow-
ers. As many as 80 beetle individuals would congregate in a single ower, feeding
on staminodes, contacting the stigmas, and in a later stage, impregnated with pollen,
leave the owers. They also oviposited in the owers; later, when the androecium
abscised as a synandrous unit, it served as a place of feeding for the beetles’ larvae
until they pupated in the soil (Hamilton 1897, Diels 1916, Hotchkiss 1959, Endress
1983, Armstrong & Irvine 1990). For E. laurina and E. bennettii self-compatibility
was conrmed (Endress 1984b).
Flowers of the large, pantropical family Annonaceae are mostly bisexual and pro-
togynous, commonly having a trimerous perianth consisting of one whorl of sepals
and two whorls of thick, eshy, strongly scented petals. The numerous stamens, com-
monly having broad connective shields, and the apocarpous carpels have a helical
arrangement. Stigmatic exudates function as a compitum, distributing the growing
pollen tubes to the carpels. The family is predominantly pollinated by beetles, but
in some genera and species, thrips (Thysanoptera), ies, cockroaches and even bees
are the exclusive pollinators of owers (Gottsberger 2012). There are two major sorts
of beetles pollinating owers of Annonaceae. The large majority of cantharophilous
species of Annonaceae are pollinated by small beetles (Nitidulidae, Curculionidae,
Staphylinidae, Chrysomelidae), having a body length up to 7 mm, and a smaller group
of species attract Scarabaeidae (Dynastinae, Rutelinae, Cetoniinae, Trichiinae), which
are large beetles having a body length of 14–20 mm.
The earliest-divergent genus in Annonaceae is Anaxagorea (Scharaschkin & Doyle
2006). Where studied, owers have been found to have a diurnal, 2-day owering
rhythm, with the pistillate stage occurring during the rst day and the staminate stage
during the second. In Anaxagorea brevipes, A. manausensis, and A. phaeocarpa,
investigated in the Central Amazon of Brazil (Webber 1996), and in A. dolichocarpa,
studied in the northeastern Atlantic forests (also Brazil) (Braun & Gottsberger 2011),
ower temperature rises approximately 1.5–6 °C above ambient air temperature in the
pistillate and staminate stages, a phenomenon that accelerates the emission of fruit-like
odors, which attract the pollinators, species of Colopterus (Nitidulidae). Anaxagorea
prinoides, studied in French Guiana, was found to be heterodichogamous; its owers
did not warm up and were also pollinated by Colopterus species (Teichert et al. 2011).
Anaxagorea owers have inner staminodes, which make movements during anthesis.
In the pistillate stage they spread outwards, making space around the stigmas for the
incoming beetles, and in the staminate stage they incline towards the carpels thereby
facilitating beetle access to the pollen-providing stamens.
Many Annonaceae in the Neotropics and Paleotropics have diurnal or nocturnal ow-
ers, with or without thermogenesis which are pollinated by small beetles, such as in the
genera Annona, Cathostemma, Deeringothamnus, Duguetia, Enciosanthum, Fissistigma,
Friesodielsia, Goniothalamus, Guatteria, Haplostichanthus, Isolona, Meiogyne,
Melodorum, Monocarpia, Piptostigma, Polyalthia, Sapranthus, Tetrameranthus, Uvaria
and Xylopia (e.g. Gottsberger 1970, 1999, Webber 1981a, 1981b, 1996, Deroin 1989,
eschweizerbart_xxx
318 G. Gottsberger, Pollination in basal angiosperms
Nagel et al. 1989, Olesen 1992, Andrade et al. 1996, Küchmeister et al. 1998, Momose
et al. 1998a, Bernhardt 2000, Silberbauer-Gottsberger et al. 2001, 2003, Norman 2003,
Ratnayake et al. 2006, 2007, Weerasooriya & Saunders 2010, Gottsberger et al. 2011,
Teichert et al. 2012, Paulino-Neto 2014).
In the Neotropics, pollination by large dynastid scarab beetles, mostly of the genus
Cyclocephala, occurs in nocturnal, large-owered species of the genera Annona,
Cymbopetalum, Duguetia, Fusaea, Malmea, Porcelia and others (e.g. Webber 1981a,
Gottsberger 1989a, 1989b, Schatz 1990, Webber 1996, Momose et al. 1998a, Braun
et al. 2011). Their petals are very eshy with nutritious tissue principally at the base
of the inner petals (Gottsberger et al. 1989a). Thermogenesis can be remarkable high,
reaching temperatures up to 12 °C above ambient air, and co-incident scent emissions
are very strong and either sharp or fruity. The beetles, which often stay inside the pol-
lination chamber for as long as 24 hours, are rewarded by nutritious tissue and pollen,
they are protected against predators and, as beetles of both sexes are attracted, they can
mate. Elevated temperatures inside the oral chamber permit beetles to expend less
energy to keep warm and in this way promotes their activities (Seymour et al. 2003).
Asimina species in Florida are pollinated by scarabs, but by members of the subfami-
lies Trichiinae and Cetoniinae (Norman & Clayton 1986), and large-owered African
species of Uvariodendron are pollinated by scarabs of the subfamilies Trichiinae and
Rutelinae (Gottsberger et al. 2011).
Thrips are the exclusive or additional pollinators in species of Bocageopsis,
Xylopia, Popowia, Oxandra and Cananga (e.g. Kessler 1993, Webber & Gottsberger
1995, Webber 1996, Momose et al. 1998b), y-pollination occurs in unpleasant scent-
ing owers of Pseuduvaria and Uvariopsis (Morawetz 1988, Silberbauer-Gottsberger
et al. 2003, Gottsberger et al. 2011), and Uvaria elmeri was veried in Malaysia to be
pollinated by cockroaches (Nagamitsu & Inoue 1997). A highly sophisticated case of
bee pollination was described for species of the genus Unonopsis. Males of Euglossa
and Eulaema, so called “orchid bees” (Euglossinae) collect perfume at osmophores
produced on the inner side of the inner petals of Unonopsis owers and pollinate them
(Carvalho & Webber 2000, Silberbauer-Gottsberger et al. 2003, Teichert et al. 2009).
Inner ower petals of some Annonaceae species can provide nectar. In Pseuduvaria
both staminate and pistillate owers secrete nectar through small slits from a multi-
layered mesophyllary nectary, which is a resource for the pollinating ies (Silberbauer-
Gottsberger et al. 2003). Nectaries are indicated also in species of Orophea (Kessler
1988), and nectaries of the epithelial type were described by Erbar (2014) for Asimina
species; this nectar might be consumed by visiting and pollinating beetles, ies and
thrips (e.g. Kral 1960).
Annonaceae have developed a number of sophisticated and highly specialized pol-
lination syndromes. The large majority of species are beetle-pollinated, but different
lines of cantharophily have evolved: pollination by small beetles versus pollination by
large beetles, diurnally versus nocturnally active owers, and owers with thermogen-
esis (especially notable in nocturnal species). Other lines of specialization are evident
in the few species pollinated by thrips (e.g. very narrow pollination chambers linked
to small ower size), cockroaches, ies (often unpleasant scent or nectaries) and bees.
A more or less closed pollination chamber as found in cantharophilous owers, would
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 319
be an obstacle for ies, cockroaches and bees trying to reach to the ower reproductive
organs. As an adaptation to these “free working” pollinators, the myiophilous, melit-
tophilous or cockroach-pollinated Annonaceae have open owers with reexed petals
which gives pollinators free access to the ower center. Small and elongate thrips do
not need an open ower to penetrate into its center, and thrips adapted owers are
either closed or semiclosed.
As in cantharophilous owers, non-cantharophilous owers have characteristics
related to the behavior and senses of their respective pollinating insects. Still, non-
cantharophilous species often retain one or more cantharophilous associated charac-
ters, e.g. thick, eshy petals, attened and scleried connective shields, or protogynous
dichogamy (Gottsberger 2012).
Studies on breeding systems in Annonaceae have shown that self-compatibility is
prevalent in most studied species. In Anaxagorea, self-compatibility was found to occur
in A. phaeocarpa, A. crassipetala and A. dolichocarpa (Webber 1996, Armstrong &
Marsh 1997, Braun & Gottsberger 2011); in the species A. manausensis, A. brevipes
and A. prinoides, self-compatibility is likely (for example, as indicated by p/o-ratio) but
has not been conrmed by other studies (Webber 1996, Teichert et al. 2011). In Annona,
the majority of studied species were found to be self-compatible: A. cacans, A. cheri-
mola, A. exsucca, A. glabra, A. montana, A. mucosa, A. muricata, A. nitida, A. reticu-
lata, A. sericea, A. squamosa (e.g., Wester 1910, Webber 1981a, 1982, 1992, Murray &
Johnson 1987, Nagel et al. 1989, Gottsberger 1989b, Gazit et al. 1982, Richardson &
Anderson 1996, Paulino Neto & Oliveira 1998, Tsukada et al. 2008, Gonzáles & Cuevas
2011). Only the African Annona senegalensis was found to be self-incompatible (Deroin
1989). Self-compatibility was further found in Asimina parviora, A. obovata and
A. triloba (Norman & Clayton 1986, Norman et al. 1992, Menges & Matthias 2002),
Deeringothamnus pulchellus and D. rugelii (Norman 2003), Cardiopetalum calophyl-
lum, Duguetia lanceolata and D. pycnastera (Paulino Neto & Oliveira 1998, Webber
1996), Guatteria megalophylla and two other unidentied Guatteria species occur-
ring close to Manaus (Webber 1996), Cymbopetalum torulosum and Cymbopetalum
sp. (Schatz 1984, Bawa et al. 1985a), Mitrephora heyneana (Weerasooriya & Saunders
2010), Polyalthia cf. cauliora, P. littoralis, P. coffeoides and P. korinti (Okada 1990,
Ratnayake et al. 2006), Pseudoxandra coriacea (Webber 1996), Uvaria concava
(Silberbauer-Gottsberger et al. 2003), Xylopia amazonica, X. aromatica, X. benth-
ami and X. brasiliensis (Andrade et al. 1996, Paulino Neto & Oliveira 1998, Webber
1996,). Conversely, Cymbopetalum costaricense (Schatz 1987), Polyalthia glauca and
P. hypoleuca (Rogstad 1994), as well as Popowia pisocarpa (Momose et al. 1998b),
Sapranthus palanga (Bawa 1974) and Uvaria elmeri (Nagamitsu & Inoue 1997), were
found to be self-incompatible. Xylopia championii appears to be intermediate between
being self-incompatible and self-compatible (Ratnayake et al. 2007). Cymbopetalum
brasiliense apparently is apomictic (Braun et al. 2011).
Pollination in Chloranthales and Ceratophyllales
Chloranthaceae diverged at some point above the ANITA grade, but below the
divergence of magnoliids (e.g. Doyle et al. 2003), and there seems to be still some
eschweizerbart_xxx
320 G. Gottsberger, Pollination in basal angiosperms
evidence that Chloranthaceae may be sister to magnoliids (e.g. Bell et al. 2010).
The Ceratophyllaceae (Ceratophyllales) have shifted back and forth in different phy-
logenies, but in more recent publications they are considered sister to Chloranthaceae,
and most recently, both families combined are suggested to be the older sister clade to
eudicots (Zeng et al. 2014).
Chloranthaceae, the sole family of Chloranthales, consists of ca. 75 pantropically
distributed species. Their habit varies from herbs and subshrubs (Chloranthus and
Sarcandra) to shrubs and large trees (Ascarina and Hedyosum). Flowers are bisexual
(Chloranthus and Sarcandra) or unisexual (Ascarina, dioecious, rarely monoecious;
Hedyosmum, monoecious or dioecious) (Todzia 1993). All species of Chloranthus and
Sarcandra have protogynous, long-lasting owers with a dry stigma (Hristova et al.
2005). The pistillate phase begins ve to seven days before the staminate phase and
continues during the staminate phase (Balthazar & Endress 1999). Usually the owers
lack a perianth and consist of an extremely low number of organs, often only of one
stamen and one carpel. Endress (1987) afrms that Chloranthus and Sarcandra have
entomophilous characteristics, such as bright colors and a penetrating scent from the
androecium in, e.g. S. chloranthoides, and a fruity scent in S. glabra, while Ascarina
and Hedyosmum show tendencies to wind pollination, which, however is quite pro-
nounced in Hedyosmum. Endress (1987) found Chloranthaceae to be an instructive
example “. . . that oral biological differentiation into certain entomophilous and
anemophilous groups took place already in the initial stages or at least very early in
angiosperm evolution.”
Two Chloranthus species, C. serratus and C. fortunei were studied by Luo & Li
(1999) in China. Anthesis of a single ower of C. serratus lasted 5–6 days and owers
are slightly protogynous. Flowers started to emit a scent when the androecium became
white. Both species are entomophilous with thrips as exclusive pollinators (see also
Ma et al. 1997 for C. holostagius). Some chrysomelid beetles visited the owers as
well, but were too large to enter the oral-axial chamber. The beetles were blocked by
the androecial appendages and, thus, can be dismissed as pollen vectors.
Sarcandra glabra was investigated in its natural habitat in Japan (Tosaki et al.
2001). The small (ca. 0.3 cm diam.), protogynous owers having a weak fragrance
bear one stamen having a creamish white connective and thecae, which turn orange
or reddish-brown upon dehiscence (several days after the beginning of stigma recep-
tivity). Stigma receptivity dropped off signicantly following anther dehiscence. The
authors found that pistillate-stage and bisexual-stage owers were visited by several
beetles, bees, hemiptera, ies and rarely ants that foraged for pollen and/or small drop-
lets of liquid that occasionally were secreted by the carpels and inorescence axes.
Pollination experiments showed that fruit set of S. glabra after experimental crossing
and selng was not signicantly different, and automatic selng sometimes occurred
when pollen fell from upper owers onto the stigmas of lower owers.
After different pollination treatments (Luo & Li 1999) it was concluded that
Chloranthus serratus and C. fortunei form fruits after cross-pollination, self-
pollination and by agamospermy, but with a substantially higher fruit set after cross-
pollination. Similar treatments by Balthazar & Endress (1999) indicated Sarcandra
glabra to be self-compatible, S. chloranthoides agamospermous and Chloranthus
eschweizerbart_xxx
G. Gottsberger, Pollination in basal angiosperms 321
spicatus self- incompatible. However, the results on breeding systems, especially on self-
compatibility of Sarcandra glabra were contested by Hristova et al. (2005), afrming
that self-fruit/seed set can occur in the presence of a leaky self-incompatibility system.
Their opinion is that “. . . all conclusions regarding the presence of agamospermy, SI
or SC in any species of Chloranthaceae are inconclusive.”, and demand that “. . . more
rigorous studies are required to provide denite evidence of the presence or absence of
the phenomenon in any of the species with bisexual owers in the Chloranthaceae.”
The small aquatic family Ceratophyllaceae (Ceratophyllales) consists of a mono-
typic cosmopolitan genus having six submergent species. This family has proven dif-
cult to place in phylogenetic schemes and has changed its position several times.
Probably on the basis of a shared aquatic habit, Ceratophyllum was usually aligned
with Nymphaeales, and it has also been placed near other early diverging groups
prior to the divergence of monocots and dicots (Les 1993). The family has been even
proposed to represent the most basal clade of extant angiosperms, which was con-
tested by e.g. Endress (1984c). At present, Ceratophyllaceae are considered sister to
Chloranthaceae (e.g. Zeng et al. 2014).
All species of Ceratophyllum are hydrophilous, i.e. pollination occurs below the
water surface. They are monoecious and sex ratio is commonly male-biased. The pis-
tillate owers occur near the shoot apex while the staminate owers develop more
basally. Pistillate owers seem to be receptive somewhat prior to pollen release from
the staminate owers. The stamens, with a remarkable behavior of successive matu-
ration, are lighter than water and detach from the ower and become buoyant with a
tendency to rise. Stamen dehiscence and pollen release occurs while stamens are still
attached to the ower or during their rise to the water surface. After their release, the
water is full of pollen grains and some of them may reach the stigmatic opening and
leading to pollination (Knuth 1899, Endress 1984, Les 1993). Studies have indicated
self-compatibility of several species, which permits sexual reproduction in clonal pop-
ulations. Related to this, it was found that outcrossing rates and genetic diversity of
populations is quite low (Les 1993).
General discussion
Floral characteristics and sex expression
A few representatives of the ANITA group have very small owers or reproductive units
(viz. Hydatellaceae), usually less than 1 cm diam., such as Amborella and Trithuria.
Flowers somewhat larger, up to 2 cm diam. occur in Brasenia schreberi, Schisandra
glabra, S. henryi and Trimenia moorei. Medium-sized owers up to 4 cm diam. are
characteristic for Cabomba caroliniana, Nuphar spp., Euryale ferox, Nymphaea ond-
inea and Illicium oridanum. Austrobaileya scandens (up to 6 cm ower diam.) and
core Nymphaea species and Victoria have large to very large owers: Nymphaea
subgenera Nymphaea, Brachyceras and Anecphya have owers up to 14 cm diam.,
Nymphaea subgenera Hydrocallis and Lotos up to 20 cm diam., and Victoria exhibits
the largest owers of the whole order having owers up to 25–30 cm diam. Moreover,
in the basal monocots, magnoliids and the clade Chloranthales plus Ceratophyllales,
there also is a large variation in ower size, from very small to small, often reduced
eschweizerbart_xxx
322 G. Gottsberger, Pollination in basal angiosperms
owers, such as in Acorus, Araceae, Chloranthaceae, Ceratophyllaceae, Lactoridaceae,
Piperaceae, Siparuna, some Monimiaceae, Lauraceae and Myristicaceae, to large
and very large owers in other groups, where ower diameter or length of petals can
reach 5–6 cm in species of Zygogynum (Winteraceae), 8–12 cm in Asarum and even
occasionally 100 cm in Aristolochia (Aristolochiaceae), 5–11 cm in Hydnoraceae,
4–8 cm in Calycanthus (Calycanthaceae), 6–7 cm in Degeneriaceae, 16–20 cm in
Magnoliaceae, and 3–8 cm in Annonaceae. Nearly all of the large to very large owers
belong to groups either specialized for beetles or ies. The possible reasons for the
evolution of oral gigantism especially in beetle- and carrion-y-pollinated species are
discussed in Davis et al. (2008).
Flower color ranges from cream in Amborella trichopoda and Trimenia moorei and
greenish in Trithuria spp., to green, yellow and brown in Austrobaileya scandens,
and further to green, yellow, orange, crimson, red and purple in several species of
Schisandraceae. Probably the broadest color range in the ANITA group is found among
owers of Cabombaceae/Nymphaeaceae, which possess white, yellow, pink, purple,
red and blue (Table 1). True blue ower color is chemically complex and quite rare
in basal angiosperms, only occurring in Nymphaea, which belongs to the rst herba-
ceous clade of the angiosperms. Blue owers occur in those taxa of the angiosperms
characterized by an evolutionary trend towards the herbaceous habit, and are increas-
ingly more abundant in the more advanced monocots and herbaceous higher dicots
(Gottsberger & Gottlieb 1980, 1981).
Unisexual owers exhibiting dioecious or monoecious sex expression (see also
e.g. andromonoecy in Trimenia moorei, gynomonoecy in Lactoris fernandeziana
or gynodioecy in Echinodorus longipetalus) occur in Amborella, Schisandra and
Kadsura species (ANITA), partly in Alismataceae and Araceae (monocots), partly in
Winteraceae (Tasmannia), partly or totally in Piperaceae, Siparunaceae, Hernandiaceae,
Monimiaceae, Lauraceae, Myristicaceae and Annonaceae (e.g. in Pseuduvaria),
all belonging to the magnoliids, in Ascarina and Hedyosmum (Chloranthaceae)
and Ceratophyllaceae. Bisexual owers are typical for some Trithuria species,
Cabombaceae, Nymphaeaceae, Austrobaileya and Illicium (ANITA), Acorus, several
Araceae and Alismataceae, the majority of the magnoliid families and for Sarcandra
and Chloranthus (Chloranthaceae).
Dichogamy was broadly discussed by Lloyd & Webb (1986) and Bertin & Newman
(1993), and many factors for the prevalence of either protogyny or protandry were men-
tioned. For basal angiosperms having bisexual owers, it is remarkable that nearly all
have protogynous dichogamy. Only in some Piperaceae and Alismataceae, homogamy
or even protandry have been observed. It appears that protogyny is an archaic character-
istic in angiosperms. It may nd an explanation in the principal visitors to their owers,
mainly beetles, ies and thrips which, contrary to bees, butteries, birds and mammals
move slowly or little during their ower visits and often remain on and in an individual
ower or inorescence for a long time; in some cases, beetles and thrips, or trapped
ies, may remain 24 hours or more in a ower. In this situation, receptive stigmas at
the insects’ arrival and pollen shedding stamens at their departure provides the best and
most efcient mechanism to promote outcrossing. Even in abiotically pollinated plants,
e.g. by wind, protogyny is more appropriate and more efcient than protandry, because
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G. Gottsberger, Pollination in basal angiosperms 323
only then it is guaranteed that the available pollen during the initially pistillate stage of
a ower is exclusively from another ower. Although the incoming pollen can be from
other owers of the same individual, still the probability that it is coming from other
individuals is higher than it would be in protandrous owers. In a bisexual protandrous
anemophilous ower the rst pollen available would be from its own ower, a situation
which might even “clog” the stigmas and thus, make difcult or even inhibit cross-
pollination. Other reasons for this kind of dichogamy may be found in ower construc-
tion of basal angiosperms, which often have many densely crowed reproductive organs
and stamens lacking long laments, or anthers and laments without clear delimitation,
so that pollen presentation is close to potentially receptive stigmas.
The few cases of homogamy and protandry observed in some Alismataceae and
Piperaceae, two generalist pollination families, may be the rst signs of a reversal and
an adaptation to more rapidly-acting pollen- and/or nectar-searching visitors, bees.
Indeed, in a few species of both families, bees become dominant or even exclusive
ower visitors and pollinators. However, such a reversal is not a general trend in basal
angiosperms, especially not in families with specialist pollination. For example, both
Araceae and Annonaceae have specialist pollination, Araceae apparently starting with
beetles and/or ies, and Annonaceae with beetles as basic pollinators. Some Anthurium
and Spathiphyllum species (Araceae) and Unonopsis (Annonaceae) are specialized for
perfume-collecting male euglossine bees, but even so their owers exhibit protogyny.
It may be that specialist families of basal angiosperms are too xed or canalized in
their original function such that their members have not been able to adapt and switch
to the seemingly more appropriate condition of protandry.
Breeding systems
As the pistillate and staminate stages in bisexual owers of basal angiosperms are
in most cases completely separated, insect-mediated self-pollination can be avoided.
This is important in cases where species are self-compatible. On the other hand, the
breeding systems of basal angiosperms might have become self-compatible because
their owers are strongly dichogamous without overlapping of pistillate and stam-
inate stages in an individual ower. However, as was remarked by Endress (1994),
dichogamy can only be an efcient outcrossing factor, when there are other temporal
mechanisms at the level of inorescences, the individuals or the populations (see also
Lloyd & Webb 1986, Bertin & Newman 1993).
In the present paper, a special effort was made to document data on the breeding sys-
tems in basal angiosperms. Several authors apparently are convinced that angiosperms
have started as a group with obligatory oucrossing, viz. having a self- incompatible
breeding system. The main argument for the prevalence of outcrossing of early angio-
sperms was the explosive development of angiosperm groups, evident from Cretaceous
fossil records (e.g. Friis et al. 2011). It is believed that such a rapid speciation and
diversication could only have been possible in groups having principally outcrossing
breeding systems.
Some authors, myself included, are puzzled 1) by the high number of species, gen-
era and even families of basal angiosperms bearing unisexual owers, and 2) princi-
pally also by the high number of self-compatible species found in these groups.
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324 G. Gottsberger, Pollination in basal angiosperms
A good documentation of the breeding system of a plant is a difcult job and it is
not sure that all data about breeding systems in the literature are good data. On the
other hand, we cannot neglect the abundant reports about self-compatibility in basal
angiosperms and certainly not all data are wrong.
As cited above, also Endress & Igersheim (2000), after the study of Amborella
trichopoda, referred to the frequent occurrence of functionally unisexual owers
among basal angiosperms, mentioning that this might be one method to support out-
breeding in a group in which self-incompatibility systems are lacking or unelaborated.
In the rst clade of ANITA with bisexual owers, the Nymphaeales, all tested species
of Trithuria, Brasenia, Nuphar, Euryale, Barclaya, Nymphaea and Victoria revealed
to be self-compatible. The situation is somewhat different in the Austrobaileyales.
Austrobaileya scandens, Trimenia moorei and Illicium dunnianum are self- incompatible,
Kadsura longipedunculata appears to be self-compatible, and for Illicium oridanum
it is not yet clear whether it is self-incompatible or self-compatible.
In the basal monocot family Alismataceae, ve tested taxa of Alismataceae were
self-compatible and one was self-incompatible. In the literature I found 20 accounts
for self-compatibility in Araceae species and one account for self-incompatibility.
In the magnoliids, Drimys brasiliensis, D. confertifolia, Tasmannia insipida, and per-
haps Zygogynum pancheri are self-compatible, while Pseudowintera colorata, P. axil-
laris, and Drimys winteri are self-incompatible. In the Aristolochiaceae, the larger
number of species was found to be self-compatible, and also the monotypic Lactoris
fernandeziana is self-compatible. In the Piperaceae about the same number of self-
compatible and self-incompatible species are reported. Saururus cernuus (Saururaceae)
is self- incompatible, and Calycanthus chinensis (Calycanthaceae) was found to be
self-compatible. Sparattanthelium botocudorum (Hernandiaceae) is self-incompatible.
In different species of the genus Tambourissa (Monimiaceae) both types of breeding sys-
tems were found. In the few species of Lauraceae tested, self-incompatibility prevailed.
In the Magnoliaceae self-compatibility is much more common than self- incompatibility.
Two tested species of Eupomatia are also self- compatible. In the Annonaceae self-
compatibility is numerically dominating by far over self-incompatibility.
For the Chloranthaceae there are several data for species being either self- compatible
or self-incompatible, but all results about breeding systems in this family were con-
tested by Hristova et al. (2005), who afrm that self-fruit/seed set can also occur in the
presence of a leaky self-incompatibility system. Self-compatibility was conrmed in
several species of Ceratophyllum (Ceratophyllaceae).
The data above indicate that self-compatibility in basal angiosperms is a common
phenomenon and that this phenomenon also exists in the Nymphaeales, the earliest-
divergent bisexual clade.
Thus, one might ask whether unisexuality and protogyny in bisexual owers, both
well established in basal angiosperms, are perhaps indeed characteristics to avoid self-
ing in plants that predominantly have a self-compatible breeding system? Might it be
possible that the basal angiosperms have started as self-compatible lines, which at their
beginning evolved and developed relatively slowly, and which only much later and
after the acquirement of self-incompatible breeding systems had their broad and rapid
diversication mainly along the Cretaceous?
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G. Gottsberger, Pollination in basal angiosperms 325
Resources for pollinators: pollen, nectar, nutritious tissues and oral
heating
Pollen is likely the rst and oldest resource provided for angiosperm ower visiting
insects and pollinators (e.g. Amborella). Pollen continues to be a main resource for
most ower visitors, but in the Cabombaceae and Nymphaeaceae, nectar, an energet-
ically much richer food than pollen, as well as abundant stigmatic secretions or less
abundant stigmatic exudates are additional important resources (for a review of the
occurrence of nectar and nectaries see Erbar 2014). Both pollen and/or liquid secre-
tions, the latter containing sugars, amino acids and many other substances, are the
main resources provided by the majority of angiosperm owers. Several groups of
plants, especially cantharophilous basal angiosperms, provide another resource for
their visiting beetles, namely more or less specialized nutritious tissues, provided on
tepals, petals and staminodes and even food bodies on several oral organs. Small bee-
tles often eat pollen and also feed on tepals, petals or staminodes during their extended
stay in the interior of their owers, in the so-called pollination chamber. The canth-
arophilous owers of certain Zygogynum species seem to have food bodies on the
petals. A very sophisticated case of food-providing to small beetles occurs in the genus
Calycanthus. In the Chinese C. chinensis, the distal margins of the tepals and the con-
nective appendages bear a warty cover which, together with the subjacent cell layers,
seem to represent a kind of food tissue for the visiting beetles. In the North American
species C. occidentalis and C. oridus, the innermost tepals, the stamens and inner
staminodes have whitish food bodies on their tips, which contain high levels of protein
and are eaten by Colopterus and Carpophilus (Nitidulidae) species during their visits
to the owers.
In owers that are pollinated by the large-sized beetles of the Dynastinae, Rutelinae,
Cetoniinae and Trichiinae (all Scarabaeidae), either the whole tepals or petals, espe-
cially the inner sides, are eaten by the beetles, or the owers provide specic nutritious
regions on tepals or petals. Victoria (Nymphaeaceae) species have starch-containing
carpellary appendages that are eaten by the large beetles. In Philodendron species,
beetles not only nourish themselves on stigmatic exudates and large amounts of pol-
len but also on sterile and fertile staminate owers. In Magnolia ovata, beetles start
eating at the nutritious tissue at the base of the inner petals and after consumption of
these regions extend their gnawing to the whole petals. In Annonaceae, pollinated by
dynastid scarab beetles, we found that after their arrival, beetles preferentially fed on
special areas of the inner side of the three inner petals. These food areas apparently
are a preferred resource for beetles during the initial pistillate ower phase; during the
staminate phase the beetles feed also on pollen. In species of the annonaceous genera
Annona, Malmea, Cymbopetalum and Duguetia, histochemical studies revealed the
presence, in a more or less concentrated form, of starch, lipids, tannins (including
polyphenols in a compact polymerized form) and mucilage cells (Gottsberger et al.
1998) in the nutritious tissues. Starch and lipids, besides being eaten by the large bee-
tles, also provide fuel for ower thermogenesis.
Another resource or reward, especially for beetles, is provided by the ability of
some plants to raise ower temperature above ambient temperature through meta-
bolic heat production, resulting in a warm oral chamber. Besides being an aid in
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326 G. Gottsberger, Pollination in basal angiosperms
strongly volatilizing the oral scent compounds for attracting the pollinators, warming
of owers helps beetles, which are facultative endotherms and need a great deal of
energy for reducing thermoregulatory costs, to increase their activity levels in mating,
locomotion, digestion and growth (Seymour & Schultze-Motel 1997, Seymour et al.
2003, 2009a, Seymour 2010, McCallum et al. 2013).
Thermogenesis occurs earliest in the ANITA grade, in the clade Nymphaeales,
however, in the derived subgenera of Nymphaea and in Victoria, and it is associ-
ated with pollination by large dynastid scarab beetles. Also, in species of Schisandra
and Illicium (Austrobaileyales) thermogenesis occurs, and for Illicium dunnianum it
was found that the slight oral heating during the pistillate stage and the later nurs-
ing phase (after the staminate stage) benets larval development of the pollinating
gall midges. Flower heating is found in the cantharophilous genera Hydnora and
Prosopanche (Hydnoraceae), too. The slight heating in Hydnora species was associ-
ated with scent production only. In Magnoliaceae, thermogensis was found in tropical
American species being pollinated by dynastid scarab beetles. Several small-owered
and large-owered cantharophilous Annonaceae, which are pollinated either by small
or large beetles, are also thermogenic. Annonaceae species pollinated by large beetles,
exhibit stronger heating, probably because larger, thicker petals have more accumu-
lated starch and lipids than species with smaller and less eshy owers associated with
small beetles.
Flowers as mating, oviposition and breeding places
Mating on owers by pollinating beetles is a common phenomenon. We observed it
in owers and inorescences of Victoria amazonica, Philodendron spp., Magnolia
ovata and many Annonaceae spp. As observed in Philodendron selloum, scent stimu-
lated mating of its pollinating dynastid scarab, Erioscelis emarginata (Gottsberger &
Silberbauer-Gottsberger 1991). The thick, eshy tepals or petals of cantharophilous
species are not only important for the pollination process itself and for the polli-
nating beetles, but are also used by many insects other than pollinators as oviposi-
tion and breeding places. For example, in Anaxagorea crassipetala (Annonaceae),
Armstrong & Marsh (1997) found besides the pollinating nitidulid beetles also a wee-
vil species (Cyriomyx sp., Baridinae, Curculionidae), which oviposited into young
ower buds and afterwards its larvae were ovule predators. Another ower preda-
tor of this species was Diathoneura tesselate (Drosophilidae, Diptera), which ovi-
posited into the thick and eshy outer petals of immature ower buds on the tree,
and even in postanthetic fallen owers. Each of the outer petals might contain sev-
eral larvae of this drosophilid y (Collier & Armstrong 2009). The petals of Annona
coriacea were found to be oviposited and used as breeding places by a moth of the
family Stenomidae, whose larvae nourished themselves on petal tissue (Moreira de
Barros et al. 2014). In Sapranthus palanga owers, Olesen (1992) detected larvae of
a mining moth (Pyralidae, Lepidoptera), and Braun et al. (2011) found in a popula-
tion of Cymbopetalum brasiliense (also Annonaceae) the buttery larvae Oenomaus
ortygynus (Lycenidae) destroying ripe buds and open owers by eating petals, sta-
mens and the entire gynoeceum. Additionally, Gottsberger & Silberbauer-Gottsberger
(2006) show for Annonaceae occurring in cerrado vegetation, that many species of
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G. Gottsberger, Pollination in basal angiosperms 327
non-pollinating beetles belonging to Curculionidae, Nitidulidae, Staphylinidae,
Chrysomelidae, Elateridae, Dermestidae, Meloidae, Elateridae and Scarabaeidae vis-
ited the owers without entering the pollination chamber, and several of those beetles
besides feeding on petal tissue, mated on and oviposited the petals. If time is too short
for larvae to nish development in owers on the tree, they can continue their devel-
opment in the fallen ower and pupate in the soil. Likewise, predation of owers of
Amazonian Annonaceae was shown by Webber (1996).
There are few documented cases wherein pollinating beetles use their owers as
breeding places where they mate and oviposit. The examples belong to Prosopanche
(Hydnoraceae) and Eupomatia (Eupomatiaceae), but these phenomena are probably
more common than the few described cases would suggest.
Flies were found mating, ovipositing and/or breeding on owers, as for instance
in Austrobaileya, as well as in Cabomba, Nuphar and Nymphaea (ies of the gen-
era Hydrellia, Notiphila, Ephydridae; and Hydromyza, Scatophagidae) (van der Velde
et al. 1978, van der Velde & Brock 1980). In Schisandraceae (Schisandra and Illicium),
and in Siparunaceae (Siparuna), cecidomyiid ies were found to oviposit and breed
in owers that they pollinate. Similar phenomena, albeit involving other y groups or
a much broader y spectrum, occur in several Araceae and in most Aristolochiaceae.
In Monimiaceae, the cup-like receptacle of Mollinedia and Wilkiea is a oviposit-
ing and breeding place for their exclusive thrips (Thysanoptera) pollinators. Also in
Myristica dactyloides, owers are used by thrips species as brood sites; the additional
pollinators, beetles, bees and ies only exploit the pollen.
Floral scent
Scent emitted by owers is usually regarded as a pollinator attracting cue, indicating
food, oviposition places or even sexual partners, but certain compounds of an odor
bouquet can also have antagonistic or defensive function and repel undesired or harm-
ful ower visitors (Junker & Blüthgen 2010).
In Nymphaeales, basal monocots, magnoliids and Chloranthales, nearly all major
classes of oral scent compounds can occur, such as C5-branched chain compounds,
aliphatics, benzenoids and phenyl propanoids, monoterpenes, sesquiterpenes, diter-
penes and irregular terpenes (Knudsen et al. 2006). Of the numerous studies on oral
scent chemistry, just a very few will be mentioned here, in beetle-pollinated groups.
For example, the large magnoliid family Annonaceae is basically a beetle-pollinated
group (see above) and species of the most early-divergent genus Anaxagorea are polli-
nated by beetles of the genus Colopterus (Nitidulidae). The owers of Anaxagorea spe-
cies have a fruit-like scent. Members of other genera of Annonaceae, such as Duguetia,
Annona, Guatteria or Xylopia, also have banana-like, ananas-like, fruity-acetonic
and fermenting scents, and are also pollinated by nitidulids, Staphylinidae, and in
Xylopia aromatica, additionally by Thysanoptera. The analyzed scent compounds in
Anaxagorea species consist mainly of esters and occasionally also of alcohols. The
scents of Duguetia asterotricha consist of monoterpenes, those of Annona insignis
of benzenoids and ketones, and Xylopia aromatica and X. benthamii have high
amounts of benzenoids including alcohols (Jürgens et al. 2000, Teichert et al. 2011).
The most abundant oral scent compound identied in Anaxagorea prinoides and in
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328 G. Gottsberger, Pollination in basal angiosperms
A. dolichocarpa is ethyl isovalerate (greater than 50%), and isobutyl isovalerate is also
plentiful. Ethyl isovalerate is known to be produced by beetle-attracting species of
Araceae, Cycadaceae and Magnoliaceae, whereas isobutyl isovalerate is known only
from the oral scent of Annonaceae species (Knudsen et al. 2006). Both esters, which
also occur in fruits, seem to be effective beetle attractants (Teichert et al. 2011). It was
reported some time ago that several Annonaceae owers are associated with nitidulid
and other beetles that normally live, nourish themselves and breed on rotten bark and
fruits. Fruit scents produced and given off in the closed, dark pollination chambers of
several Annonaceae attract these same fruit-inhabiting beetles, which in response enter
the interior of Annonaceae owers and pollinate them (Gottsberger 1970, 1974).
Another Annonaceae species, Duguetia cadaverica has foul-smelling owers,
and among the 18 identied scent compounds were characteristic earthy odors of
fungi, suldes, and 4-methylpentanoic acid, molecules associated with carcass and
cheese odors, respectively. The pollinator of D. cadaverica is likely a nitidulid bee-
tle (Pycnocnemus sp.), which belongs to the Oxycnemus genus complex, known to
have fungal hosts of the order Phallales. Thus, the ower of the saprocantharophil-
ous D. cadaverica appears to be a stinkhorn (Phallales) mimic (Teichert et al. 2012).
With respect to their odor, species of the Annonaceae genus Unonopsis, are quite the
opposite to D. cadaverica, because they emit a pleasant, aromatic smell. Many mono-
terpenes were detected in the scent samples, among them trans-carvone oxide. This
component and others occur in U. stipitata, but also in several orchids, Euphorbiaceae
and Araceae, and attract male bees of Euglossa and Eulaema (Euglossini, Apidae) to
visit owers of these four families, in what is thought to be an example of conver-
gence. The bees collect liquid scent, or “perfume”, produced by the inner petals and
doing so, become pollinators of the Unonopsis owers, as well as of the owers of the
families mentioned above (Carvalho & Webber 2000, Silberbauer-Gottsberger et al.
2003, Teichert et al. 2009). A review of chemical composition, and summary of the
diversity of scents, in Annonaceae is given by Goodrich (2012).
A very special situation occurs in dynastid scarab beetle-pollinated Annonaceae.
For example, Annona coriacea, A. crassiora and A. dioica were observed to grow
sympatrically in the Brazilian cerrado vegetation. They exhibited staggered ower-
ing peaks and all three species attract the beetle Cyclocephala atricapilla with the
same single scent compound 4-methyl-5-vinylthiazole. Also Annona montana and
Caladium bicolor in Northeast Brazil attract their pollinators (Cyclocephala vestita
in the former and C. celata in the later species) with the identical thiazole compound.
This highly specic attraction linked to the presence of a single compound is an exam-
ple of rarely documented, scent-driven, “private communication channels” (Maia et al.
2012). Such private communication channels involving basal angiosperms and dynas-
tid scarab beetles were documented also for Magnolia ovata (Gottsberger et al. 2012),
Philodendron acutatum (Maia et al. 2010), P. selloum (Dötterl et al. 2012, Gottsberger
et al. 2013), P. adamantinum (Pereira et al. 2014), Taccarum ulei (Araceae) (Maia
et al. 2013a), and occur probably also in species of Nymphaea subgen. Hydrocallis
(Maia et al. 2014) and Victoria (Kaiser 2006). One further example shows the simplic-
ity and at the same time complexity of these chemical and behavioral interrelationships
of owers, their scents and the beetles attracted. The C5-branched chain ester Methyl
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G. Gottsberger, Pollination in basal angiosperms 329
2-methylbutanoate is the principal oral scent compound of Magnolia ovata and
attracts the pollinating Cyclocephalini beetle Cyclocephala literata (Gottsberger et al.
2012). This compound occurs also in Magnolia mexicana and M. hypoleuca (Azuma
et al. 2004). The same compound occurs in high proportion in