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Turkish Journal of Biodiversity
e-ISSN:2667-4386
Turk J Biod, March 2021, 4(1): 37-54
https://doi.org/10.38059/biodiversity.832706
Journal homepage: http://turkbiod.artvin.edu.tr/
http://dergipark.org.tr/biodiversity
37 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
REVIEW ARTICLE
Open Access
A review for the pollinators of Papilionaceous flowers
Kelebek şeklinde çiçek açan çiçeklerin tozlayıcıları için bir inceleme
Deniz AYGÖREN ULUER
Ahi Evran University, Çiçekdağı Vocational College, Department of Plant and Animal Production, 40700, Çiçekdağı, Kırşehir, Turkey
Article Info
©2021 Ali Nihat Gökyiğit Botanical
Garden Application and Research
Center of Artvin Coruh University.
Corresponding author
e-mail: d.aygoren@ahievran.edu.tr
ORCID: 0000-0002-2095-3816
Article history
Received: October 22, 2020
Received in revised form: March 29, 2021
Accepted: March 30, 2021
Available online: March 31, 2021
This is an Open Access
article under the CC BY NC ND license
(http://creativecommons.org/licenses
/by/4.0/).
Keywords:
Bee pollination, flower type, Fabaceae,
pollinator size, Polygalaceae
Anahtar Kelimeler:
Arı tozlaşması, çiçek tipi, Fabaceae,
tozlayıcı boyutu, Polygalaceae
To cite this article: Aygören Uluer D
(2021). A review for the pollinators of
Papilionaceous flowers. Turk J Biod
4(1): 37-54.
ABSTRACT
The evolution of keel flowers within Leguminosae, Polygalaceae and some other clades of
angiosperms is attributed to skilled and strong bees. However, whether this is true or not, is still an
open question. Therefore, the literature is surveyed for the Hymenopteran pollinators of keel
flowers, for 119 sources and for 112 species, six genera and two tribes for five characters which are
the size of the flowers, Hymenopteran flower visitors/pollinators, size of the Hymenopteran
pollinators, pollen and nectar robbers/thieves and size of the Hymenopteran thieves/robbers. The
results suggest that Fabales keel flowers are mainly pollinated by long-tongued bees, from Apidae
and Megachilidae families; and the most common pollinators of the keel flowers are small
Megachile and Osmia; medium-sized Apis, Anthophora and Eucera; and large Xylocopa, Bombus and
Centris. While the literature suggests that keel flowers are pollinated by skilled and strong bees, the
results of the current review have shown that this is not the whole case in terms of flower size and
bee size. There is no difference between pollinator diversity and flower size. While floral
robbers/thieves are mostly up to 2 cm, among them honey-bees (Apis mellifera) both pollinate and
rob the keel flowers. Keel flowers of Polygalaceae and other angiosperm lineages are somehow
similar to the keel flowers of Papilionoideae.
ÖZ
Baklagil çiçek tipinin Leguminosae, Polygalaceae ve diğer angiosperm gruplarındaki evriminin
becerikli ve güçlü arılar sayesinde olduğu fikri ortaya atılmıştır. Ancak, bunun doğruluğu tartışmalıdır.
Bu nedenle, bu derlemede toplam 119 kaynak (112 tür, altı cins ve iki tribe) beş karakter (çiçek
büyüklüğü, Hymenoptoran polinatörleri, Hymenoptoran polinatörlerinin büyüklüğü, polen ve nektar
hırsızları, Hymenoptoran polen ve nektar hırsızlarının büyüklüğü) açısından değerlendirilmiştir.
Derlemenin sonuçları göstermiştir ki, Fabales baklagil çiçekleri temelde Apidae and Megachilidae
familyalarından uzun dilli arılar ile döllenmekte, ve en yaygın polinatörler ise küçük Megachile ve
Osmia; orta boylu Apis, Anthophora ve Eucera; ve büyük Xylocopa, Bombus ve Centris’dir. Literatur,
baklagil çiçeklerinin becerikli ve büyük arılarla döllendiğini önerirken, bu derlemenin sonuçları çiçek
ve polinatör büyüklüğü açısından bunun tam anlamıyla doğru olmadığını göstermiştir. Ayrıca, çiçek
büyüklüğü ve polinatör çeşitliliği arasında da bir bağlantı görülmemiştir. Çiçek hırsızları genelde 2
cm’ye kadar olurken, bunların arasında bal arılarının (Apis mellifera) hem hırsız hem de polinatör
olarak işlev gördüğü anlaşılmıştır. Diğer taraftan, Polygalaceae ve diğer angiosperm baklagil benzeri
çiçeklerin gerçek baklagil çiçeklerine polinatör açısından benzer olduğu görülmüştür.
1. INTRODUCTION
Keel flowers (Westerkamp, 1997) or papilionateous
flowers are bilaterally symmetrical (in most cases),
pentamerous flowers with the reproductive organs
enclosed by keel petals (Polhill & Raven, 1981; Endress,
1994; Westerkamp, 1997; Pennington et al., 2000;
Persson, 2001; Tucker, 2002; Tucker, 2003; McMahon &
Hufford, 2005; Westerkamp & Claßen-Bockhoff, 2007;
Bello et al., 2010). Keel flowers are dominant in two
species-rich lineages within Fabales Bromhead, tribe
Polygaleae Chodat of Polygalaceae family and subfamily
Papilionoideae of Leguminosae family (Bello et al., 2007;
Bello et al., 2010). While subfamily Papilionoideae with
Citation:
A review for the pollinators of Papilionaceous flowers
38 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
ca. 14,000 species in 504 genera constitutes almost 72%
of species richness of family Leguminosae (Tucker, 2003;
Lewis, 2005; LPWG, 2017), similarly tribe Polygaleae with
ca. 800 spp. holds 80% of the species richness of the
Polygalaceae family (Persson, 2001; Bello et al., 2010;
Bello et al., 2012).
Keel flowers are also found outside of Papilionoideae, in
Cercidoideae, Dialioideae and Caesalpinioideae: Cercis
L., Poeppigia procera C.Presl and Peltophorum (Vogel)
Benth. (Arroyo, 1981; Polhill et al., 1981); and in many
unrelated families, such as Ranunculaceae (e.g.,
Aconitum L.), Hippocastanaceae (now a polyphyletic
group), Geraniaceae (e.g., Pelargonium rapaceum (L.)
L’Hér.), Solanaceae (e.g., Schizanthus Ruiz& Pav.),
Campanulaceae (e.g., Monopsis lutea (L.) Urb.),
Fumariaceae (now subfamily Fumarioideae) (e.g.,
Corydalis cava (L.) Schweigg & Körte), Plantaginaceae
(e.g., Collinsia Nutt.), Calceolariaceae (e.g., Calceolaria
L.), Strelitziaceae (e.g., Strelitzia reginae Banks),
Onagraceae, Trigoniaceae, Tropaeolaceae, Acanthaceae
and Commelinaceae (Westerkamp, 1997). Indeed, it was
suggested that keel flowers evolved at least 16 times
within 10 different angiosperms orders, both in
monocots and eudicots (Westerkamp, 1997). However,
excepting Trigoniaceae and Fumarioideae, existence of
keel flowers in other angiosperm families is not as
extensive (i.e., as number of species) as in Fabales
(Westerkamp, 1997; Westerkamp & Weber, 1997).
Particularly, Cercis is well known by its "pseudo-
papilionoid" flowers with a bilaterally symmetrical
corolla, and three different petal types: standard, wings
and keels (Polhill et al., 1981). However, Cercis lacks
some floral characteristics, such as connected stamens,
and the tripping mechanism seen in most Papilionoideae
flowers (Tucker, 2002).
Until now, many possible causes have been reported for
the evolution of keel flowers such as a bigger display
area (mainly the standard) and protection of ovarium
and stamens from environmental factors such as rain,
strong wind, high temperatures and evaporation
(Breteler & Smissaert-Houwing, 1977; Polhill & Raven,
1981; Westerkamp & Claßen-Bockhoff, 2007; Shi et al.,
2010; Etcheverry & Vogel, 2018). However, the most
widely accepted view for the evolution of complex
flowers such as keel and bilabiate flowers is an
“adaptive response” to bees; keel flowers may have
evolved to attract bees and/or to protect the flower
from pollen robbery (i.e., nectar/pollen stealers, pollen
eaters and occasional visitors) (Leppik, 1966; Faegri &
van der Pijl, 1979; Arroyo, 1981; Polhill et al., 1981;
Brantjes, 1982; Schrire, 1989; Westerkamp, 1989;
Howell et al., 1993; Proctor et al., 1996; Westerkamp,
1996; Westerkamp, 1997; Westerkamp & Weber, 1999;
Fenster et al., 2004; Westerkamp & Claßen-Bockhoff,
2007; Etcheverry & Vogel, 2018). Pollen is hidden in the
deepest part of the flower by the keel petals to secure
pollination and promote cross-pollination, where pollen
cannot be easily removed during grooming (Brantjes,
1982; Lloyd & Schoen, 1992; Westerkamp, 1996;
Westerkamp, 1997; Zhang et al., 2011). Therefore, this
particular adaptation has driven the evolution of keel
flowers across several angiosperm groups, and keel
flowers are not unique to Fabales, similar to other
melittophilous (i.e., bee pollinated) complex flowers;
they are widely distributed in many more angiosperm
orders (Faegri & van der Pijl 1979; Westerkamp, 1997;
Hingston & McQuillan, 2000; Etcheverry & Vogel, 2018).
While there are many pollination biology studies on the
keel flowers (mainly Papilionoideae), an explicit study on
the pollinators of keel flowers has never been performed
until now. Such a study would be useful in clarifying the
main bee pollinators of the keel flowers. The literature
suggests that keel flowers are pollinated by skilled and
strong bees, but which skilled/strong bees? Is large
Bombus pollination more common than large Centris or
Xylocopa Latreille pollination? Is there a difference
among Papilionoideae keel flowers, Polygalaceae keel
flowers, and Scrophulariaceae (i.e., Collinsia) keel
flowers in terms of their pollinators? Therefore, the first
aim of the current study is to synthesize information on
the pollinators of keel flowers.
On the other hand, flower size is frequently reported to
be an important part of floral constancy related to
searching time and pollinator attraction (Conner & Rush,
1996; Chittka et al., 1999; Goulson, 1999; Stout, 2000;
Spaethe et al., 2001; Gegear, 2005; Gegear & Laverty,
2005; Skorupski et al., 2006; Benitez-Vieyra et al., 2007;
Galloni et al., 2008; Lihoreau et al., 2016). Pollinator size
also reported to be correlated to flower size
(Gottsberger & Gottsberger, 1988; Galloni et al., 2008),
pollen placement (Elle & Carney, 2003) and pollination
success (Cristofolini et al., 2012). The literature on the
effect of pollinator/flower size is case-dependent: while
one study reports that large flowers are worked by only
large bees and small flowers are pollinated by all sizes of
bees (e.g., Herrera, 2001), another study suggests that
A review for the pollinators of Papilionaceous flowers
39 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
flower size and pollinator size are mostly correlated in
which large flowers are pollinated by large bees, and
small flowers are pollinated by small bees (e.g.,
Gottsberger & Gottsberger, 1988). Thus, whether floral
size and pollinator size are important criteria for the
pollinators of keel flowers has never been explicitly
addressed until now. While, employing field
observations on this issue is possible, an easier way to
gather this information would be through reviewing
existing literature, published articles which is particularly
prevalent for Papilionoideae (Leguminosae). Therefore,
the second aim of the current review is to investigate
pollinators of keel flowers within angiosperms in detail,
to answer the questions below represent a subset of the
questions were introduced above: Is there an overall size
difference among pollinators of small and large keel
flowers? Are small keel flowers pollinated by large bees
too? Are medium-sized honeybees really
robbers/thieves of keel flowers? To answer these
questions and provide an overview of the pollinators of
angiosperm keel flowers, a comprehensive literature
review is performed.
2. MATERIALS AND METHODS
Between 2018 and 2019, the literature for information
on the Hymenopteran pollinators of keel flowers was
surveyed, for 119 sources and for 112 species, six genera
(Chamaecrista (L.) Moench, Cassia L., Senna Mill.
Leguminosae; Monnina Ruiz&Pav., Polygalaceae;
Collinsia, Penstemon Schmidel, Plantaginaceae) and two
tribes: Crotalarieae (Benth. Hutch) and Genisteae
(Bronn) Dumort, Leguminosae; for five characters which
are the size of the flowers, Hymenopteran flower
visitors/pollinators, size of the Hymenopteran
pollinators, pollen and nectar robbers/thieves and size
of the Hymenopteran thieves/robbers (please see
detailed information below on how characters were
defined and included in the analysis). Other type of
animal pollination studies (e.g., bird pollination, wasp
pollination) are excluded.
Most of the studies reviewed here do not report the size
of the bee visitors and studied flowers. Therefore, in
these cases the flower and bee size data were obtained
from alternative sources, such as, other published
studies or suitable internet sources. In some cases,
instead of the flower size, petal (corolla), standard
(banner, flag) or keel size is given, and in these cases
these sizes were accepted as the minimum flower size
for simplicity. If the body size of a bee
species/subspecies/variations could not be found, the
body size of the species or genus was accepted to make
approximate estimations. Non-bee visitors were not
included in the visitor/pollinator column, because in
some cases, instead of giving the species name of the
wasps (Vespidae Latreille), hoverflies (Syrphidae
Latreille), butterflies (Lepidoptera Linnaeus), flies
(Diptera Linnaeus), beetles (Coleoptera Linnaeus), ants
(Formicidae Latreille) among others, only the common
name (e.g., flies) or the name of the order (e.g., Diptera)
or the family name (e.g., Vespidae) is given. For brevity,
where multiple sources present the same information,
this information was not repeated while all appropriate
citations are made.
Data is compiled in Supplementary Table 1. This table
includes 106 entries from 119 studies which reported
floral visitors, in some cases possible pollinators and
nectar/pollen thieves of the keel flowers of
Papilionoideae and Polygalaceae in Fabales, keel flowers
outside of Polygalaceae and Papilionoideae, but still in
Fabales (i.e., Cercidoideae), keel-flowers outside of
Fabales (Ranunculales Juss. ex Bercht. & J.Pres and
Lamiales), and some taxa which have non-keeled flowers
from Papilionoideae (Fabales), Caesalpinioideae
(Fabales) and Detarioideae (Fabales). These non-keeled
flowered taxa and their pollinators/ robbers were
included to the study just for comparison (to detect
whether these flowers are pollinated with similar suits of
pollinators of the keel flowers). Rows were numbered
and listed according to flower type (1 to 95 keel flowers
and 95 to 106 non-keeled flowers) and phylogeny (1 to
89 keel flowers of Fabales and 89 to 95 keel flowers
outside of Fabales). The Hymenopteran pollinators were
approached at the genus level.
In many studies, the most common visitors are accepted
as the most effective pollinators; however, visitation
frequency can be misleading and least common visitors
can be more effective pollinators (Fenster et al., 2004).
For instance, large flowers of Collaea cipoensis Fortunato
visited by nectar-robbers (83%), nectar-thieves (9%),
florivores (flower-eaters) (1%) and possible pollinators
(only 3%) (Gelvez-Zuniga et al., 2018). Similarly, among
24 different species of visitors, only four of them were
reported to be the effective pollinators of Polygala
vayredae Costa (Castro et al., 2013). Therefore, a second
table (Table 1) was constructed which includes only the
studies in which possible nectar/pollen stealers as well
A review for the pollinators of Papilionaceous flowers
40 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
as flower visitors and pollinators were distinguished.
Flower visitors include all the categories: nectar/pollen
stealers, nectar/pollen thieves, and pollinators.
In Table 1, 40 entries from 50 studies which reported
floral visitors, possible pollinators and nectar/pollen
stealers of the keel flowers of Polygalaceae (Fabales),
Papilionoideae (Fabales), keel-flowers out of Fabales
(Ranunculales and Lamiales), and some of exemplar taxa
which have non-keeled flowers (Papilionoideae and
Caesalpinioideae) were included. In contrast to
Supplementary Table 1, the species was numbered in
this table to make following the results and discussion
parts easier. However, similar to Supplementary Table 1,
studies were listed according to their flower type (1 to
37 keel flowers and 37 to 40 non-keeled flowers),
phylogeny (keel flowers of Fabales from 1 to 33 and keel
flowers out of Fabales from 33 to 37) and flower size (1
to 7 flower sizes up to 1.2 cm, 7 to 37 flower sizes larger
than 1.2 cm. From now on, both the results and the
discussion will be based on this table which includes only
the studies that reported not only all Hymenopteran
visitors but also the legitimate pollinators and
pollen/nectar stealers of the studied species.
Table 1. Fifty studies which reported floral visitors, possible pollinators and nectar/pollen robbers/thieves of the keel flowers of
angiosperms. Name of the plant, size of the flowers, bee visitors and range of their sizes, nectar/pollen stealers (if given), size range
of the Hymenopteran thieves, and the source(s) were indicated in separate columns. The sizes of both flowers and bees were given
as centimetres (cm), and this information was found from proper sources, if it was not stated in the original study. The bee size
range includes females, queens, males and workers in some cases. For the Hymenopteran visitors, if the percentage of visits or
number of visits were given in the source, they were indicated within brackets. If the flower size could not be found, petal (corolla),
standard (banner, flag) or keel size is given, and in these cases these sizes were accepted as the minimum flower size. Study areas
were not indicated. Keeled flowers from Lamiales and Ranunculales families, and representative flowers of non-keeled Fabales are
indicated. Same information from various sources is not repeated."/" and ";" represent different sources or information about
different species. Question marks (?) indicate the information is not certain. Decimals are rounded to the nearest whole number to
avoid fractional points. Empty cells represent unavailable information.
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
1-Apios
americana
0.1 cm
Flies are possible pollinators
(but not confirmed), Megachile
spp.
0.7-1.2 cm
Apis mellifera,
Lasioglossum sp.,
Halictidae (?)
0.3-1.2
cm
Bruneau &
Anderson,
1988;
Westerkamp
& Paul, 1993;
Bruneau &
Anderson,
1994
2-
Aeschynomene
amorphoides
0.43 cm
Tetraloniella jaliscoensis
About 1 cm
Apis mellifera, Trigona
fulviventris, wasps,
ants, some
Lepidoptera and
Coleoptera
0.5-1.2
cm
Carleial et al.,
2015
3-Polygala
monticola (Syn.
Polygala
violacea)
(Polygalaceae)
About
0.5 cm
Apis africana hybrid (the most
frequent visitor), Megachile
sp., Coelioxys sp., Exomalopsis
sp. (all activated the pollination
mechanism)
0.7-1.2 cm
Ceratina sp.
Up to
0.8 cm
Brantjes,
1982
4-Pultenaea
villosa
Corolla
0.6 cm
Apis mellifera (54%),
Lipotriches spp., Lasioglossum
convexum, Trigona carbonaria,
unknown solitary bees,
Hyleoides sp.
0.3-1.7 cm
Vespidae, Formicidae,
Buprestidae,
Chrysomelidae,
Bombyliidae,
Muscidae, Syrphidae,
Heteroptera
Ogilvie et al.,
2009
A review for the pollinators of Papilionaceous flowers
41 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
5-Polygala
vauthieri
(Polygalaceae)
About
0.7 cm
Apis africana hybrid (the most
frequent visitor), Megachile
sp., Hypanthidium sp. (all
activated the pollination
mechanism)
0.7-1.2 cm or
larger
Ceratina sp.,
Melissodes sp.
0.8-1.8
cm
Brantjes,
1982
6-Anthyllis
vulneraria
subsp. vulgaris
(Syn. Anthyllis
vulneraria
subsp.
carpatica)
0.7-1.2
cm
Anthophora acervorum (=A.
plumipes) (45%), A. robusta
(2%), Andrena fulva (3%),
Eucera longicornis (2.4%),
Melecta luctuosa (1%),
Megachile sp. (1%),
0.7-1.7 cm
Bombus terrestris and
B. jonellus (45%)
(nectar robbers)
1.1-2.2
cm?
Navarro, 2000
7/8-Vigna
longifolia, V.
luteola
Standar
d 1.4-2.2
cm and
1.3-2.5
cm,
respecti
vely
Bombus morio, Megachile
susurrans, M. tenuitarsis,
Xylocopa brasilianorum (these
four are the most important
pollinators), Apis mellifera,
Centris decolorata, C. tarsata,
Coelioxys sp., Eufriesea
mussitans, Pseudaugochlora
sp., Xylocopa frontalis,
Exomalopsis analis
0.7-3 cm
Lepidoptera, Diptera,
Coleoptera
de Souza et
al., 2017
9-Crotalaria
juncea
Keel 1.5
cm
Large Megachilid bees,
Megachile sculpturalis,
Xylocopa, Xylocopa virginica
and X. micans
1.2-2.7 cm
Apis mellifera
About
1.2 cm
Hall & Avila,
2016
10-Lupinus
perennis
About
1.5 cm
Bombus spp., solitary bees
(mostly Osmia, Andrena vieina,
Megachile melanophaea
melanophaea), A. mellifera,
Xylocopa virginica
0.5-2.3 cm
Small bees, wasps,
butterflies and
hummingbirds
Bernhardt et
al., 2008
11-Pongamia
pinnata
1.5-1.8
cm
Apis dorsata, A. cerana indica,
A. florea (in total ~70%)
Amegilla sp. (~10%), Megachile
sp. (~5%), Xylocopa latipes and
X. pubescens (~10%)
0.7-3.5 cm
Trigona iridipennis,
Ceratina simillima,
Pithitis binghami
(pollen thieves)
0.4-1.8
cm
Raju & Rao,
2016
12-Polygala
vayredae
(Polygalaceae)
About
1.6 cm
Bombus pascuorum (17%),
Anthophora sp (5%) (both main
pollinators), Eucera longicornis,
Halictus sp.
0.8-1.7 cm
Bombus terrestris
(64%), B. pratorum
(both are nectar
robbers); Apis
mellifera (nectar
thieves)
1.1-1.7
cm
Castro et al.,
2008a, Castro
et al., 2008b;
Castro et al.,
2013
13-Bowdichia
virgilioides
1.75 cm
Centris aenea (main visitor), C.
fuscata (main visitor) Xylocopa
sp., Apis mellifera, Trigona
spp., Partamona sp.,
Geotrigona sp. (all occasional
visitors)
0.3-3 cm
Vespidae, Braconidae,
Lepidoptera,
Hesperidae,
Gomes da
Silva et al.,
2011
A review for the pollinators of Papilionaceous flowers
42 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
14-Lathyrus
japonicus
Standar
d 1.8-2.3
cm
Bombus pascuorum, B.
lapidarus, B. hortorum, B.
terrestris, Osmia sp.
0.6-2.2 cm
B. terrestris workers
(nectar robber/thief),
Apis mellifera,
Coelioxys (nectar
thief)
0.7-1.7
cm
Asmussen,
1993
15-Coronilla
emerus (Syn.
Hippocrepis
emerus)
About 2
cm
Eucera is the most important
pollinator, other than
Habropoda Osmia, Xylocopa,
Bombus, Antophora sp.,
Megachile sp.
0.6-2.6 cm
Apis mellifera,
Bombus sp., Halictae
0.4-2.3
cm
Galloni et al.,
2008; Aronne
et al., 2012
16-Crotalaria
retusa
Flag 2
cm
Xylocopa frontalis (49%) X.
grisescens (44%), Centris
leprieuri
2.9-3 cm
Trigona spinipes
(nectar robber)
0.5-0.7
cm
Jacobi et al.,
2005
17-Crotalaria
micans
2-2.5 cm
Pseudocentron (Megachile) sp.
(the most effective pollinator),
Xylocopa macrops, X.
ordinaria, X. eximia
0.7-2.6 cm
Apis mellifera and
Bombus morio (nectar
thieves)
1.2-2.5
cm
Etcheverry et
al., 2003
18-Lupinus
pilosus
2-2.5 cm
Apis mellifera, Antophora sp.
(both activated the tripping
mechanism)
0.8-1.6 cm
Small solitary bees
0.5-1.7
cm
Ne’eman &
Nesher, 1995
19/20-Cratylia
hypargyrea, C.
mollis
About
2.5 cm
Five Xylocopa and four Centris
species
1.2-3 cm
Some bees are too
small to pollinate the
flowers
Queiroz, 1996
21-Robinia
pseudoacacia
About
2.5 cm
Apis mellifera (63%)
About 1.2 cm
Apis mellifera
About
1.2 cm
Giovanetti &
Aronne, 2012
22-Cytisus
scoparius
2-3 cm
Apis mellifera, Andrena,
Anthophora, Bombus, one
solitary bee, Osmia, Tetralonia
nipponensis, Xylocopa
appendiculata circumvolans,
Campsomeriella annulata
annualata, Lasioglossum spp.,
Halictus acerarius, Bombus
melanopygus (10),
Lasioglossum pacificum (4),
and Lasioglossum olympiae (4),
Bombus mixtus, Andrena
salicifloris, B. flavifrons, B.
vosnesenskii, Evylaeus sp.
0.3-2.3 cm
Small bees, A.
mellifera
About
1.2 cm
Parker, 1997;
Suzuki, 2000;
Malo &
Baonza, 2002;
Parker et al.,
2002; Galloni
et al., 2008;
Muir, 2013
23-Collaea
cipoensis
Corolla
2-3 cm
Apis mellifera, Xylocopa
muscaria
1.2-2.6 cm
Trigona spinipes,
Toxomerus musicus
(nectar robber bees),
Apis mellifera,
Exomalopsis sp.,
Megachile sp.
Melipona marginata,
Augochloropsis sp.,
Ceratina sp.
0.3-1.3
cm
Gélvez-Zúniga
et al., 2018
A review for the pollinators of Papilionaceous flowers
43 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
24-Periandra
mediterranea
Petals
about
2.3
cm/stan
dard 3.3
cm
Xylocopa frontalis, Acanthopus
excellens and Epicharis sp.
(both occasional visitors)
1.5-3 cm
Apis mellifera,
Acanthopus excellens,
Epicharis sp., Polybia
spp (wasp),
butterflies,
hummingbirds
1.2-2.5
cm
Meireles et
al., 2015
25-Canavalia
virosa (Syn.
Canavalia
cathartica)
Standar
d 2.7-3
cm
Xylocopa flavorufa, Megachile
combusta, Apis mellifera
(occasional visitor)
1.2-2 cm
Bees smaller than
Megachile combusta,
Apis mellifera / Small
ants as nectar robbers
Less than
1.2 cm
Stirton, 1977;
Sahai, 2009
26-Canavalia
gladiata
Standar
d 3.5 cm
Apis mellifera (occasional
visitor)
About 1.2 cm
Small ants as nectar
robbers
Sahai, 2009
27-Lathyrus
latifolius
Flag 3.3
cm
Megachile ericetorum,
Xylocopa violacea and other
megachilids as the main
visitors
0.7-2.8 cm
Apis mellifera
About
1.2 cm
Westerkamp,
1993
28-Centrosema
virginianum
2.5-4 cm
(petals
2.1-3.5
cm)
Mostly large bees. Bombus
pennsylvanicus, Xylocopa
micans, Melissodes communis,
Megachile campanulae
wilmingtoni, Megachile
policaris, Colletes distinctus
0.8-2.7 cm
Coleoptera, Diptera,
Lepidoptera,
Othoptera are
florivores or folivores
Cardel, 2004
29/30-
Centrosema
pubescens, C.
brasilianum
Banner
3.4 and
3.6 cm,
respecti
vely
Euglossa, Eufriesea, Eulaema,
Bombus brevivillus, Centris,
Epischaris, Xylocopa,
Acanthopus, however Euglossa
cordota, three Eulaema
species, Bombus brevivillus,
Epicharis flava, Xylocopa
frontalis were the most
common pollinators
up to 2 cm
Oxaea, Ceratina,
Augochloropsis,
Ceratina,
Pseudaugochlora,
Exomalopsis, Centis,
Epicharis
up to
1.5 cm
Ramalho et
al., 2014
31-Vicia faba
3-4 cm
Eucera pulveracea (50%), Apis
mellifera (42%)
1.2-1.6 cm
Apis mellifera (42%)
(both pollinator and
nectar robber),
Xylocopa violacea
(1.6%) (nectar robber)
1.2-3 cm
Aouar-Sadli et
al., 2008
32-Vigna
caracalla (Syn.
Cochliasanthus
caracalla)
4.8 cm
and 4-7
cm,
respecti
vely
Bombus morio, Xylocopa
eximia, Centris bicolor,
Eufriesea mariana
1.3-2.5 cm
Apis mellifera,
Meliponini sp. (both
small pollen robbers)
0.3-1.2
cm
Etcheverry et
al., 2008;
Etcheverry &
Vogel, 2018
RANUNCULA
LES
33-Aconitum
napellus ssp.
lusitanicum
(Ranunculales)
About 2
cm
Pollinated by long-tongued
bumblebees, Bombus
pascuorum, B. terrestris
About 1.7 cm
Honeybees (nectar
robbers)
About
1.2 cm
Mayer et al.,
2014
A review for the pollinators of Papilionaceous flowers
44 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
34-Corydalis
cava
(Ranunculales)
2.35 cm
Bombus terrestris queens (the
most important pollinator),
Anthophora acervorum, B.
pratorum and B. hortorum
(both are rare)/Queens of
Bombus lucorum and B.
cryptarum (34%), B. terrestris
(38%), B. hortorum (24%), B.
pratorum (0.2%), B. lapidarius
(0.5%), Apis mellifera (2%)
(1.4%), Anthophora plumipes
(1.4%)
1-2.2 cm
All Bombus species
are also nectar
robbers/ Apis
mellifera, Andrena,
Nomada, Sphecodes
0.4-2.3
cm
Olesen, 1996;
Myczko et al.,
2015
LAMIALES
35-Collinsia
sparsiflora
(Lamiales)
0.9-1.6
cm
Apis mellifera, Bombus
edwardsii, B. vosnesenskii, B.
caliginosus, B. californicus,
Synhalonia hurdi, S. lunata, S.
edwardsii, Osmia lignaria, O.
glauca, O. bruneri, O. bakeri, O.
nemoris, Chelostomopsis
ribifloris, Hoplitis fulgida,
Lasioglossum sp.
0.3-2.3 cm
Flies, moths,
butterflies
Rust &
Clement,
1977
36-Collinsia
spp. (Lamiales)
0.4-1.7
cm
Bombus, Osmia, Anthophora,
Emphoropsis, Synhalonia, long-
tongued bees/ Apis mellifera,
short-tongued bees
0.9-1.9 cm
Flies moths,
butterflies, short-
tongued bees
Armbruster,
1980;
Kampny,
1995;
Armbruster et
al., 2002
NON-KEELED FLOWERS OF FABALES
37-Amorpha
canescens
(non-keeled,
Papilionoideae)
Banner
0.5-0.6
cm
Solitary bees, Lasioglossum
(Dialictus and Evylaeus),
Honeybees, Andrena quintilis,
Calliopsis andreniformis,
Colletes robertsonii
0.3-1.7 cm
Syrphid flies
1-1.2 cm
Slagle &
Hendrix, 2009
38-Caesalpinia
echinata (non-
keeled,
Caesalpinioide
ae)
About
2.5 cm
The most effective pollinators
are medium-sized to large bees
(larger than 1.2 cm). Apis
mellifera, Centris aenea, C.
analis, Xylocopa frontalis, X.
grisescens, and X. suspecta
1.2-3 cm
Trigona spinipes,
Trigona sp.,
Augochlora sp.,
Pseudaugochlora sp.
0.3-1.3
cm
Borges et al.,
2009
39-
Chamaecrista
chamaecristoid
es (non-keeled,
Caesalpinioide
ae)
3 cm?
Only large insects such as
Xylocopa, Eufriesea, Eulaema,
Euglossa and Ptiloglossa
contact and vibrate sexual
organs
1.1-2.7 cm
Apis mellifera,
Florilegus sp.,
Protoxaea sp.,
Exomalopsis sp.
0.8-1.2
cm
Arceo-Gómez
et al., 2012
A review for the pollinators of Papilionaceous flowers
45 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Name of the
plant
Size of
the
flowers
Hymenopteran flower visitors
/pollinators
Size range of
Hymenopteran
pollinators
(cm)
Hymenopteran pollen
and nectar robbers
/thieves
Size
range of
robber
/thieves
(cm)
Source
40-Cassia,
Chamaecrista,
Senna (non-
keeled
Cassia/Senna
and with a keel
like petal
Chamaecrista;
Caesalpinioide
ae)
Chamae
crista
petals to
1-2 cm
or
more/Ca
ssia up
to 6 cm,
Senna
up to 5
cm
Mainly large bees, Xylocopa,
Centris, Epicharis, Exomolopsis,
Bombus, Euglossa,
Augochloropsis,
Pseudaugochloropsis,
Ptiloglossa, Florilegus,
dependent on the flower size
some small bees; large Oxaea,
0.8-3 cm
Oxaea flavescens,
Pseudaugochloropsis,
Trigona
up to 1.5
cm
Gottsberger
&
Gottsberger,
1988;
Dulberger et
al., 1994
3. RESULTS
Both Table 1 and Supplementary Table 1 show that
Fabales keel flowers are mostly pollinated by long-
tongued bees, Apidae L. and Megachilidae families, but
rarely by Andrenidae (Andrena Fabricius), Halictidae
Thomson (Lasioglossum Curtis, Halictus Latreille,
Pseudaugochlora Michener, Lipotriches Gerstaecker),
Colletidae Lepeletier (Colletes Latreille), flies, wasps,
birds and other animals, such as rodents. These last
animals (not Hymenopteran) are not included in any of
the two tables.
The most common pollinators of the keel flowers at the
genus level are Xylocopa (19 spp. of keel flowers), Apis
Linnaeus (16 spp.), Megachile Latreille (14 spp.), Bombus
(13 spp.), Centris (8 spp.), Osmia Panzer (5 spp.),
Anthophora Latreille (4 spp.), Eucera Scopoli (4 spp.).
Other pollinators were recorded for less than three plant
species. In terms of bee body sizes, large bees such as
Bombus, Centris, Eufriesea and Xylocopa visit almost
always only large flowers measuring at least 1.3 cm
length (however, note Bombus visits of smaller Collinsia
flowers), the remaining bees (e.g., Apis, Megachile,
Anthophora) visit all sizes of flowers (Table 1). Here, it is
possible to interpret these results as the relative
abundancy of large bee visits (up to 3 cm, Xylocopa,
Centris and Bombus). The small (up to 1.2 cm, Osmia and
Megachile) and medium-sized (up to 2 cm, Apis,
Antophora and Eucera) bee visits are also not rare (Apis
and Megachile visits for 16 species and 14 species of
keel flowers, respectively).
In terms of flower sizes, seven studies (studies 1 to 6
and, 37, including two Polygalacae and one non-keeled-
Papilionoideae studies) suggested that flowers with a
size up to 1.2 cm are pollinated by bees with a size of
0.3-1.7 cm, but not larger than 1.7 cm. On the other
hand, if the flower size is larger than 1.3 cm (including
one Polygalacae study, four keel flowers out of Fabales
and three non-keeled flower studies), the pollinator size
varies (0.3-3.5 cm). However, it should be noted that the
pollinator size of large flowers (0.3-3.5 cm) includes the
pollinator size of small flowers (0.3-1.7 cm). There was
no correlation between pollinator species diversity and
flower size, other than these size differences.
Nectar/pollen thieves and robbers are from different
insect groups such as (mostly) Hymenoptera,
Lepidoptera and Heteroptera. The Hymenopteran
robbers/thieves are generally up to 2 cm. Bombus and
Xylocopa are reported to be robber/thief by only a few
studies. Among the studies in which the thief/robber
size are known (excepting taxa 4, 7, 8, 10, 13, 19, 20, 26,
28, 35, 36), for nine taxa (including one keel flowers out
of Fabales and two non-keeled flower studies) the
robber size is clearly smaller than the pollinator size
(taxa 9, 16, 23, 24, 25, 32, 33, 38, 39). In the other
studies, robber/thief size is within the pollinator size
range. In six studies, the robber size is larger than the
pollinator size, or almost equal (taxa 5, 6, 12, 17, 21, 31),
while in the remaining 13 studies the robber size is
somehow smaller than the pollinator size, but still within
the range of pollinator size.
Out of 36 keel-flowered taxa (Table 1), for six taxa Apis
mellifera Linnaeus is suggested as both pollinator and
nectar-pollen thief/robber, for eight taxa honeybees are
suggested as only pollinators, and for 11 taxa honeybees
are reported to be only nectar/pollen thieves or robbers.
According to these results, it is possible to conclude that
if the flower size is larger than 2 cm, A. mellifera tends to
A review for the pollinators of Papilionaceous flowers
46 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
be both pollinator and robber/thief (taxa 21, 22, 23, 25,
31 and 34), rarely only a pollinator (taxa 18 and 26).
However, there were no keel flowers smaller than 2 cm
to show this pattern. On the other hand, if the flower
size is smaller than 2 cm, honeybees are able to pollinate
the keel flowers (taxa 4, 7, 8, 10, 13, 35, 36).
Except Hypanthidium (Megachilinae), the Polygalaceae
pollinators are not different from Papilonoideae
pollinators. The pollinators/visitors of non-keeled
flowers of Fabales and other keel flowered lineages are
somehow different (Table 1). Other than some common
pollinators such as Apis, Anthophora, Bombus, Xylocopa,
Centris, Eufriesia Cockerell, Eulaema Lepeletier and
Euglossa Latreille; these different pollinators/visitors are
Calliopsis Smith (Amorpha canescens Pursh), Ptiloglossa
Smith (Chamaecrista), Augochloropsis Cockerell (Senna,
Chamaecrista), Pseudaugochloropsis Cockerell (Senna),
Chelostomopsis Cockerell (Collinsia sparsiflora Fisch. & C.
A. Mey.), Emphoropsis Ashmead (Collinsia), Synhalonia
Patton (Collinsia, Cercis canadensis L.). However, in
terms of size, the pollinators of non-Fabales keel flowers
and non-keeled flowers compared to floral size, were
not different from Papilonoideae pollinators.
4. DISCUSSION
4.1. Pollinators of keel flowers
Convergent floral traits among unrelated taxa driven by
shared pollinators are referred as pollination syndromes
sensu Faegri & van der Pijl (1979) (Armbruster, 1993;
Ollerton & Watts, 2000; Johnson et al., 2003; Fenster et
al., 2004; Johnson & Jürgens, 2010; Schiestl & Johnson,
2013). Many studies have attributed the evolution of
keel flowers within Leguminosae, Polygalaceae and
other clades of angiosperms to bees (Leppik, 1966;
Westerkamp, 1989; Endress, 1994; Westerkamp, 1997;
Westerkamp & Weber, 1999), but particularly to skilled
and strong bees (Leppik, 1966; Faegri & van der Pijl,
1979; Westerkamp, 1997). Similar to the results of
Hingston & McQuillan (2000), the current review
supports that keel flowers are bee flowers (i.e., bee
pollination syndrome), but particularly long-tongued bee
(Apidae and Megachilidae) flowers. The dominance of
long-tongued bee visitors was also significant in
Robertson’s (1928) classification. The most common
genera of pollinators among these long-tongued bees
are large Xylocopa, Bombus, Centris; small to medium
Apis, Megachile, Osmia, Anthophora and Eucera, in
which Xylocopa, Bombus, Centris, Apis and Megachile
are by far the most common ones (Table 1).
While van der Pijl (1961) grouped large flowers as
“Xylocopa pollinated large flowers”, similarly Arroyo
(1981) suggested that some papilionoid flowers are
specialized to large bees such as Centris and Xylocopa. At
first, it may seem appropriate that large bees are strong
enough to trip the keel flowers and their hairy bodies
match perfectly to the large-keel flowers’ pollination
(Heering, 1995; Shambhu, 2013), in addition to the
occurrence of morphological obstacles such as thick
petals, floral connections, wing sculptures on the large
flowers to exclude small visitors to reach the pollen
(Queiroz, 1996; Etcheverry et al., 2008; Etcheverry &
Vogel, 2018). However, the current study suggests that
while large bees prefer large flowers, small and medium-
sized bees also visit and pollinate these large flowers, as
well as they visit medium and small flowers. It should be
noted that, these results contradict to Herrera (2001),
who indicates that large flowers are worked by only
large bees and small flowers are pollinated by all sizes of
bees. Yet, in the currect review, in terms of bee body
sizes, there was also evidence that large bees such as
Bombus, Centris, Xylocopa and Eufriesea visit only large
flowers which are larger than 1.3 cm, small-medium
bees such as Apis, Anthophora, Osmia, Eucera and
Megachile do not have a preference, they visit and
pollinate both small, medium and large flowers.
Moreover, in terms of flower sizes, this study has shown
that while flowers up to 1.2 cm are pollinated by bees
with a size of 0.3-1.7 cm, larger flowers are pollinated by
all sizes of bees (0.3-3.5). Indeed, these results
correspond to general trends which are large flowered
species (>15 mm length) are pollinated by large bees),
but also medium-sized Osmia (Megachilidae); medium-
sized flowers (8-15 mm) are pollinated mostly by small-
medium sized Osmia and small flowered species (<8mm)
are pollinated by small Osmia and other very small bees
(Scott Armbruster, personal observation). Therefore, in
contrast to common belief, this review partly supports
that keel flowers are pollinated particularly by skilled
and strong bees (Leppik, 1966; Faegri & van der Pijl,
1979; Westerkamp, 1997); because, the results have
clearly showed that keel flowers are not pollinated by
only large and strong bees, only that large bees prefer
large flowers.
The current literature review on the pollination biology
of keel flowers showed that many bee species move
A review for the pollinators of Papilionaceous flowers
47 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
freely between small and large flowers. In this case, it is
possible that rather than only the bee size, other
characteristics of the pollinators such as optimum size of
the bees (Stout, 2000; Stanley et al., 2016; de Souza et
al. 2017), strength (Córdoba & Cocucci, 2011), handling
type (Stanley et al., 2016), constancy (Gumbert & Kunze,
1999; Gegear & Laverty, 2005), flower colour (Raine &
Chittka, 2007; Peter & Johnson, 2008), bee fauna (Gross,
2001; Bernhardt et al., 2008), environmental conditions
such as temperature (Parker et al., 2002) and pollination
mechanisms of Papilionoideae (valve, pump, explosive
and brush, e.g., Westerkamp, 1997) may be also
important or bee preferences. For example, it was
observed that the legume-loving megachilids commonly
move between both small and large Collinsia flowers at
least if the flowers have somewhat similar colour and
plants themselves can support their weight (Scott
Armbruster, personal observation). Megachilids have a
behaviour that allows them to depress the keel even
when they are too small for their weight to do it. They
brace their head/mandibles against the base of the flag
and push with their legs. They pop the keel down very
effectively despite their light weight. This allows a much
broader range of bee sizes for any given flower size and
vice versa (Scott Armbruster, personal observation).
Similarly, Megachilide visit three sympatric coflorecent
species of the Crotalaria genus, with a yellow corolla.
Bombus attratus and B. morio visit Cologania
broussoneti, Desmodium uncinatum, two legumes with
magenta flowers, while visiting Hyptis mutabilis
(Lamiaceae) and Mimosa sp. (Mimosoideae) in a
Northwestern community of Argentina (Trinidad
Figueroa & Angela Etcheverry, unpublished results).
On the other hand, while some studies reported that
small-keel flowers are generally pollinated by different
bee species and large flowers show the highest
pollinator specificity with few large bee groups such as
Bombus and Xylocopa (e.g., Brantjes, 1982; Queiroz,
1996; Herrera, 2001; Galloni & Cristofolini, 2003; Jacobi
et al., 2005; Cane, 2006; Hargreaves et al., 2009), there
was no correlation between pollinator diversity and
flower size, other than size differences of the bees.
Aronne et al. (2012) reported similar results that bee
species diversity and flower sizes were not related;
however, they showed that an increase in flower sizes
were certainly correlated to an increase in the
pollination by large Bombus. It was not encountered that
Bombus have pollinatated flowers which are less than
1.3 cm (Table 1). However, this also does not seem like a
universal pattern (e.g., Spaethe et al., 2001).
4.2. The situation of Apis mellifera
The efficiency of honey bees (Apis meliifera) is an
interesting issue for the keel flowers. As nectar or pollen
thieves/robbers, A. mellifera do not show a preference
between different floral sizes. These results suggest that
due to their medium size (about 1.2 cm), honeybees can
pollinate small flowers (whatever their purpose is);
however, they probably accidently pollinate larger
flowers during stealing (i.e., beneficial effect of a robber,
Maloof & Inouye, 2000). In this case, it is possible to
relate this issue to the size of pollinators compared to
the flower size which is very important for the fitness of
a plant species in terms of the place of pollen deposition,
tripping the mechanism and foraging behaviours (i.e.,
handling time, flying distances, visitation frequency)
(Herrera, 2001; Vivarelli et al., 2011), because a
mismatch between the flower and the pollinator may be
result in nectar/pollen robbing or thieving (Hargreaves
et al., 2009). Thus, I agree with Westerkamp (1991 and
1993), in which A. mellifera referred as “clumsy-poor
pollinators; they learn by trial, they are active in all
seasons including when there is little choice, and in
these periods, they learn how to avoid from the blows
that accompany explosive pollination, by collecting
nectar without pollinating the flowers”. Actually, many
studies have presented similar results which indicate
honeybees as poor pollinators compared to their size
(e.g., Henning et al., 1992; Eynard & Galetto, 2002;
Córdoba & Cocucci, 2011; Aronne et al., 2012), however,
they still are able to work on flowers of many different
plant species (Córdoba & Cocucci, 2011).
4.3. The situation of Polygalaceae, other keel flowered
lineages, and non-keeled Fabales flowers
The pollinators of Polygalaceae keel flowers are also
similar to pollinators of the Papilionoideae keel flowers.
On the other hand, some of exemplar non-keeled
flowers of Leguminosae which are included to this
review are visited by different Hymenopteran genera, in
which some of them have never been reported for the
keel flowers before. However, other factors such as the
bee fauna of the area and the limited number of studies
available may be the key factors on this issue. Therefore,
further studies are needed to confirm whether all keel
flowers are pollinated by similar suites of pollinators or
not.
A review for the pollinators of Papilionaceous flowers
48 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Gottsberger & Gottsberger (1988) stated that, in
contrast to small-flowered and non-keeled Chamaecrista
which is pollinated by mostly small bees; non-keeled but
large Cassia, Chamaecrista and Senna are pollinated by
large bees such as Xylocopa, Centris, Epicharis Klug and
Bombus; small bees are too small to pollinate these
flowers (i.e., occasional pollinators or robbers).
Interestingly, some small flowers of Chamaecrista which
show corolla modifications are mostly visited by large
bees. Similarly, Borges et al. (2009) stated that the non-
keeled flowers of Caesalpinia echinata Lam. are
pollinated by medium to large bees such as Xylocopa,
Centris and Apis mellifera. Therefore, in general, while
keel and non-keeled flowers of Leguminosae share some
similar suit of floral visitors, still there are differences.
Indeed, both Senna, Chamaecrista and Cassia show
some characteristics of keel flowers (i.e., a bilateral
symmetry, partly enclosed reproductive organs by a
tubular petal, petal differentiation), and this may explain
these similar pollinators with the keel flowers. However,
in this case, again, the bee fauna of the study area, floral
size, odour, inflorescence size, colour among others may
be the principal factors which effects pollinators’ choice.
Still, compared to generalist Gentiana lutea L. with more
than 30 insect visitors (Rossi et al., 2014), not only keel
flowers but also keel-like flowers of Leguminosae are
clearly far from being generalist. Therefore, in contrast
to Arroyo (1981), the pollinator specialization does not
have to be with only one type of pollinator, having more
than one pollinator with similar characteristics can also
be an indicator of specialization (Fenster et al., 2004;
Galloni et al. 2008; Cristofolini et al. 2012).
Similar to the Fabales keel flowers, Collinsia heterophylla
Buist ex Graham (Lamiales), Aconitum napellus ssp.
lusitanicum Rouy (Ranunculales) and Corydalis cava
(Ranunculales) keel flowers were also reported to be
specialized onto long-tongued bees (Rust & Clement,
1977; Armbruster, 1980; Kampny, 1995; Olesen, 1996;
Armbruster et al., 2002; Fenster et al., 2004; Mayer et
al., 2014; Myczko et al., 2015). Among them, similar to
the Papilionoideae keel flowers, Collinsia heterophylla
seems generalist at first; however, a close look revealed
that this species is pollinated by only long-tongued bees
of 14 different species (Armbruster, 1980; Fenster et al.,
2004). For Collinsia, except a few long-tongued bees
(Chelostomopsis, Emphoropsis and Synhalonia), most of
the pollinators were common in Fabales keel flowers
(i.e., Apis, Anthophora, Bombus, Xylocopa, Centris,
Eufriesia, Eulaema and Euglossa). Similarly, other than
Synhalonia (which is a long-tongued bee and a common
visitor of Collinsia), the visitors of Cercis were not
different from the Papilionoideae keel flowers. Thus, in
the light of these findings, it may be more appropriate to
refer the keel flowers of not only Papilionoideae, but
also all angiosperm keel flowers as “long-tongued bee
specialized”. Since Harder (1983) concluded that long-
tongued bees are more efficient pollinators compared to
the short-tongued bees with a similar size, keel flowers
might be evolved to host these efficient pollinators, not
only large and strong bees to take guarantied the
pollination success (Galloni et al., 2008; Cristofolini et al.,
2012).
4.4. Limitatons of the current study and literature
There are some important caveats to this review. This
study does not include all studies on the pollination
biology of the keel flowers, instead a subset selection of
studies aproach was maintained. Similarly, since non-
Hymenopteran pollination is not very common among
keel flowers (Hingston & McQuillan, 2000), these studies
(e.g., bird pollination, wasp pollination) are excluded.
Second, flowering phenology (Hingston, 1999),
population density (Bernhardt et al., 2008; Hattori et al.,
2015), floral size of the populations (Elle & Carney,
2003), inflorescence size (Parker et al., 2002; Bauer et
al., 2017), pollination mechanisms (Galloni et al., 2008;
Cristofolini et al., 2012), reward (nectar or pollen)
(Galloni et al., 2008; Cristofolini et al., 2012), floral
colour (Streinzer et al., 2009), floral height (Waddington,
1979; Dafni et al., 1997; Gumbert & Kunze, 1999;
Spaethe et al., 2001; Valido et al., 2002; Rafferty & Ives,
2013), floral chamber (Amaral-Neto et al., 2015) among
others are not included here, even though these
characters are reported to be very important for
pollinator attraction. Third, the Hymenopteran fauna
where the studies were done and pollinator
abundance/absence/behaviour are other important
factors (Gross, 2001; Stout et al., 2002; Elle & Carney,
2003; Bernhardt et al., 2008; Pando et al., 2011; Rossi et
al., 2014; Myczko et al., 2015) for any pollination study,
and these were not included in the current review. For
example, Kožuharova & Firmage (2009) and Castro et al.
(2013) showed that number of visits of different
pollinators, robbers and thieves changes from year to
year and population to population, even between close
plant populations. Similarly, Apis mellifera was the most
important pollinator of Collinsia sparsiflora in one
region, while the numbers were very low in other
A review for the pollinators of Papilionaceous flowers
49 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
regions (Rust & Clement, 1977). Indeed, these
differences could be related to plant community
differences and co-occurring plant species,
microclimates, geographic region, season, weather
conditions, humidity, altitude, low temperatures, wind
and habitat degradation (Armbruster, 1980; Asmussen,
1993; Primack & Inouye, 1993; Hingston & McQuillan,
2000; Malo & Baonza, 2002; Parker et al., 2002; Galloni
& Cristofolini, 2003; Rodríguez-Riaño et al., 2004;
Vivarelli et al., 2011; Castro et al., 2013). Fourth,
pollinator efficiency and successful seed set may be a
more reliable signifier of the pollination biology of
species than visitation. For example, while it was
observed that bees with similar sizes Anthophora,
Megachile, Eucera and Bombus visit Coronilla emerus L.
flowers, no pollen grains were found on Bombus and
Anthophora, which indicates Megachile and Eucera were
more efficient pollinators of C. emerus (Aronne et al.,
2012). Similarly, Vivarelli et al. (2011) showed that even
though Ononis masquillierii Bertol. flowers are mostly
visited by small bees (83%), flowers visited by large bees
yielded increased seed sets compared to the flowers
which were visited by smaller bees, because probably
small bees increase selfing by activating the pollination
mechanism many times and larger bees can carry the
pollen grains for longer distances. Even for the small
flowers of Desmodium incanum DC., the pollen release
was lower if the small bees activated the explosive
pollination mechanism, compared to larger bees
(Alemán et al., 2014). However, this information (i.e.,
pollinator efficiency and successful seed set) was found
rarely in the literature review. Fifth, strength
(Westerkamp, 1993; Córdoba & Cocucci, 2011), tongue
size (Ramalho et al., 2014) and pollinator fidelity
(Cristofolini et al., 2012) are as important as the bee size
in terms of keel flower pollination. For instance,
Megachile ericetorum Lepeletier males were able to
trigger the pollination mechanism of Lathyrus latifolius L.
flowers, while similar sized A. mellifera cannot
(Westerkamp, 1993). Lower fidelity of small–medium
bees (Megachilidae) compared to the other sizes of bees
were also reported (Cristofolini et al., 2012).
In most of the studies reviewed here only the visitors of
the keel flowers are indicated; however, these visitors
may easily include occasional visitors, nectar/pollen
stealers, pollen/flower eaters among others (Shivanna,
2014). Similarly, it seems necessary to include both
pollinator and floral sizes in any pollination study,
because both flower and pollinators sizes may show
differences from one area to another. This information
(especially the size of the visitors) was not indicated in
most of the studies.
Although they are not as extensive as in Fabales
(Westerkamp, 1997; Westerkamp & Weber, 1997), the
information on the keel flowers of non-Fabales
angiosperm orders is very limited. For instance, while
tripping mechanisms are reported for the keel flowers of
Papilionoideae and Polygalaceae (Westerkamp & Weber,
1997), for other keel-flowered lineages among
angiosperms the situation is unknown. Therefore, a
broader study which covers all these lineages would
provide a clearer answer for the evolution of keel
flowers within angiosperms. Pollination studies on other
angiosperm families with keel flowers may shed light on
the results of the current survey. Similarly, choice tests
of keel flower pollinators may reveal whether these
pollinators actually move freely between different
angiosperm keel flowers or not.
As a general conclusion, in contrast to literature which
suggests that keel flowers are pollinated particularly by
skilled and strong bees, this review shows that keel
flowers are mainly pollinated by small to large long-
tongued bees, from Apidae and Megachilidae families. In
terms of size, keel flowers of Polygalaceae and other
angiosperm lineages, and exemplar non-keeled Fabales
flowers were not very different from Papilonoideae
pollinators. However, the current study also highlights
the lack of information in many pollination studies such
as most effective pollinators and pollinator/floral sizes.
Acknowledgments
I am grateful to Professor Julie A. Hawkins and Professor
Scott Armbruster for their constructive suggestions.
REFERENCES
Alemán M, Figueroa-Fleming T, Etcheverry Á, Sühring S, Ortega-Baes
P (2014). The explosive pollination mechanism in Papilionoideae
(Leguminosae): An analysis with three Desmodium species. Plant
Systematics and Evolution, 300(1): 177–186.
https://doi.org/10.1007/s00606-013-0869-8
Amaral-Neto LP, Westerkamp C, Melo GA (2015). From keel to
inverted keel flowers: functional morphology of “upside down”
papilionoid flowers and the behavior of their bee visitors. Plant
Systematics and Evolution, 301(9): 2161-2178.
Aouar-Sadli M, Louadi K, Doum SE (2008). Pollination of the broad
bean (Vicia faba L. var. major) (Fabaceae) by wild bees and honey
bees (Hymenoptera: Apoidea) and its impact on the seed
production in the Tizi-Ouzou area (Algeria). African Journal of
Agricultural Research, 3(4): 266-272.
A review for the pollinators of Papilionaceous flowers
50 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Arceo-Gómez G, Martínez ML, Parra-Tabla V, García-Franco JG
(2012). Floral and reproductive biology of the Mexican endemic
Chamaecrista chamaecvistoides (Fabaceae). The Journal of the
Torrey Botanical Society, 260-269.
Armbruster WS (1980). Pollination relationships between four
sympatric species of Collinsia (Scrophulariaceae). Botanical
Society of America Miscellaneous Series, 158(8).
Armbruster WS (1993). Evolution of plant pollination systems:
hypotheses and tests with the neotropical vine Dalechampia.
Evolution, 47(5): 1480-1505.
Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H
(2002). Comparative analysis of late floral development and
mating‐system evolution in tribe Collinsieae (Scrophulariaceae
s.l.). American Journal of Botany, 89(1): 37–49.
Aronne G, Giovanetti M, De Micco V (2012). Morphofunctional traits
and pollination mechanisms of Coronilla emerus L. flowers
(Fabaceae) . The Scientific World Journal, 1–8.
https://doi.org/10.1100/2012/381575
Arroyo K (1981). Breeding systems and pollination biology in
Leguminosae. In: Polhill RM and Raven PH, eds. Advances in
Legume Systematics. Part 2, Royal Botanic Gardens, Kew, 723-
769.
Asmussen CB (1993). Pollination biology of the sea pea, Lathyrus
japonicus: floral characters and activity and flight patterns of
bumblebees. Flora (Jena), 188(2): 227–237.
https://doi.org/10.1016/S0367-2530(17)32270-3
Bauer AA, Clayton MK, Brunet J (2017). Floral traits influencing plant
attractiveness to three bee species: Consequences for plant
reproductive success. American Journal of Botany, 104(5): 772–
781. https://doi.org/10.3732/ajb.1600405
Bello MA, Hawkins JA, Rudall PJ (2007). Floral morphology and
development in Quillajaceae and Surianaceae (Fabales), the
species-poor relatives of Leguminosae and Polygalaceae. Annals
of Botany, 100(7): 1491–1505.
https://doi.org/10.1093/aob/mcm228
Bello MA, Hawkins JA, Rudall PJ (2010). Floral ontogeny in
Polygalaceae and its bearing on the homologies of keeled flowers
in Fabales. International Journal of Plant Sciences, 171(5): 482–
498. https://doi.org/10.1086/651945
Bello MA, Rudall PJ, Hawkins JA (2012). Combined phylogenetic
analyses reveal interfamilial relationships and patterns of floral
evolution in the eudicot order Fabales. Cladistics, 28(4): 393-421.
Benitez-Vieyra S, De Ibarra NH, Wertlen AM, Cocucci AA (2007). How
to look like a mallow: Evidence of floral mimicry between
Turneraceae and Malvaceae. Proceedings of the Royal Society B:
Biological Sciences, 274(1623): 2239–2248.
https://doi.org/10.1098/rspb.2007.0588
Bernhardt CE, Mitchell RJ, Michaels HJ (2008). Effects of population
size and density on pollinator visitation, pollinator behavior, and
pollen tube abundance in Lupinus perennis. International Journal
of Plant Sciences, 169(7): 944–953.
https://doi.org/10.1086/589698
Breteler FJ, Smissaert Houwing AAS (1977). Revision of Atroxima
Stapf and Carpolobia G. Don (Polygalaceae). Meded.
Landbouwhogesch. Wageningen, 77: 1-45.
Borges LA, Sobrinho MS, Lopes AV (2009). Phenology, pollination,
and breeding system of the threatened tree Caesalpinia echinata
Lam. (Fabaceae), and a review of studies on the reproductive
biology in the genus. Flora: Morphology, Distribution, Functional
Ecology of Plants, 204(2): 111–130.
https://doi.org/10.1016/j.flora.2008.01.003
Brantjes NBM (1982). Pollen placement and reproductive isolation
between two brazilian Polygala species (Polygalaceae). Plant
Systematics and Evolution, 141(1): 41–52.
https://doi.org/10.1007/BF01006478
Bruneau A, Anderson GJ (1988). Reproductive biology of diploid and
triploid Apios americana (Leguminosae). American Journal of
Botany, 75(12): 1876-1883.
Bruneau A, Anderson GJ (1994). To bee or not to bee?: The
pollination biology of Apios americana (Leguminosae). Plant
Systematics and Evolution, 192(1–2): 147–149.
https://doi.org/10.1007/BF00985913
Cane JH (2006). An Evaluation of Pollination Mechanisms for Purple
Prairie-clover, Dalea purpurea (Fabaceae: Amorpheae). The
American Midland Naturalist, 156(1): 193–197.
https://doi.org/10.1674/0003-
0031(2006)156[193:aeopmf]2.0.co;2
Cardel Y (2004). Linking herbivory and pollination: costs and selection
implications in Centrosema virginianum Bentham (Fabaceae:
Papilionoideae). https://doi.org/10.25148/etd.FI14052571
Carleial S, Delgado-Salinas A, Domínguez CA, Terrazas T (2015).
Reflexed flowers in Aeschynomene amorphoides (Fabaceae:
Faboideae): A mechanism promoting pollination specialization?
Botanical Journal of the Linnean Society, 177(4): 657–666.
https://doi.org/10.1111/boj.12264
Castro S, Loureiro J, Ferrero V, Silveira P, Navarro L (2013). So many
visitors and so few pollinators: Variation in insect frequency and
effectiveness governs the reproductive success of an endemic
milkwort. Plant Ecology, 214(10): 1233–1245.
https://doi.org/10.1007/s11258-013-0247-1
Castro S, Silveira P, Navarro L (2008a). Effect of pollination on floral
longevity and costs of delaying fertilization in the out-crossing
Polygala vayredae Costa (Polygalaceae). Annals of Botany,
102(6): 1043–1048. https://doi.org/10.1093/aob/mcn184
Castro S, Silveira P, Navarro L (2008b). How flower biology and
breeding system affect the reproductive success of the narrow
endemic Polygala vayredae Costa (Polygalaceae). Botanical
Journal of the Linnean Society, 157(1): 67-81.
Cercis orbiculata. Retrieved April, 2016 from
https://www.fs.fed.us/database/feis/plants/shrub/cerorb/all.ht
ml.
Chittka L, Thomson JD, Waser NM (1999). Flower constancy, insect
psychology, and plant evolution. Naturwissenschaften, 86: 361-
377.
Conner JK, Rush S (1996). Effects of flower size and number on
pollinator visitation to wild radish, Raphanus raphanistrum.
Oecologia, 105(4): 509–516.
https://doi.org/10.1007/BF00330014
Córdoba SA, Cocucci AA (2011). Flower power: Its association with
bee power and floral functional morphology in papilionate
legumes. Annals of Botany, 108(5): 919–931.
https://doi.org/10.1093/aob/mcr196
Cristofolini G, Galloni M, Podda L, Vivarelli D (2012). Pollination
ecology provides some new insight into evolution and
systematics of Mediterranean Legumes. Bocconea, 24: 22–26.
Dafni A, Lehrer M, Keyan PG (1997). Spatial flower parameters and
insect spatial vision. Biological Reviews, 72(2): 239–282.
https://doi.org/10.1111/j.1469-185X.1997.tb00014.x
A review for the pollinators of Papilionaceous flowers
51 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
de Souza JMT, Snak C, Varassin IG (2017). Floral divergence and
temporal pollinator partitioning in two synchronopatric species of
Vigna (Leguminosae-Papilionoideae). Arthropod-Plant
Interactions, 11(3): 285–297. https://doi.org/10.1007/s11829-
017-9498-4
Dulberger R, Smith MB, Bawa KS (1994). The stigmatic orifice in
Cassia, Senna, and Chamaecrista (Caesalpiniaceae):
morphological variation, function during pollination, and possible
adaptive significance. American Journal of Botany, 81(11): 1390-
1396.
Elle E, Carney R (2003). Reproductive assurance varies with flower
size in Collinsia parviflora (Scrophulariaceae). American Journal of
Botany, 90(6): 888-896.
Endress PK (1994). Floral structure and evolution of primitive
angiosperms: Recent advances. Plant Systematics and Evolution,
192(1–2): 79–97. https://doi.org/10.1007/BF00985910
Etcheverry AV, Protomastro JJ, Westerkamp C (2003). Delayed
autonomous self-pollination in the colonizer Crotalaria micans
(Fabaceae: Papilionoideae): Structural and functional aspects.
Plant Systematics and Evolution, 239(1–2): 15–28.
https://doi.org/10.1007/s00606-002-0244-7
Etcheverry AV, Alemán MM, Fleming TF (2008). Flower morphology,
pollination biology and mating system of the complex flower of
Vigna caracalla (Fabaceae: Papilionoideae). Annals of Botany,
102(3): 305–316. https://doi.org/10.1093/aob/mcn106
Etcheverry AV, Vogel S (2018). Interactions between the
asymmetrical flower of Cochliasanthus caracalla (Fabaceae:
Papilionoideae) with its visitors. Flora: Morphology, Distribution,
Functional Ecology of Plants, 239: 141–150.
https://doi.org/10.1016/j.flora.2017.10.006
Eynard C, Galetto L (2002). Pollination ecology of Geoffroea
decorticans (Fabaceae) in central Argentine dry forest. Journal of
Arid Environments, 51(1): 79–88.
https://doi.org/10.1006/jare.2001.0923
Faegri K, van Der Pijl L (1979). The Principles of Pollination Ecology.
Pergamon Press, Oxford.
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD
(2004) Pollination syndromes and floral specialization. Annual
Review of Ecology, Evolution, and Systematics, 35: 375-403.
Galloni M, Cristofolini G (2003). Floral rewards and pollination in
Cytiseae (Fabaceae). Plant Systematics and Evolution, 238(1–4):
127–137. https://doi.org/10.1007/s00606-002-0270-5
Galloni M, Podda L, Vivarelli D, Quaranta M, Cristofolini G (2008).
Visitor diversity and pollinator specialization in Mediterranean
legumes. Flora: Morphology, Distribution, Functional Ecology of
Plants, 203(1): 94–102.
https://doi.org/10.1016/j.flora.2006.12.006
Gegear RJ (2005). Multicomponent floral signals elicit selective
foraging in bumblebees. Naturwissenschaften, 92(6): 269-271.
Gegear RJ, Laverty TM (2005). Flower constancy in bumblebees: A
test of the trait variability hypothesis. Animal Behaviour, 69(4):
939–949. https://doi.org/10.1016/j.anbehav.2004.06.029
Gélvez-Zúñiga I, Neves AC, Teixido AL, Fernandes GW (2018).
Reproductive biology and floral visitors of Collaea cipoensis
(Fabaceae), an endemic shrub of the rupestrian grasslands. Flora:
Morphology, Distribution, Functional Ecology of Plants, 238: 129–
137. https://doi.org/10.1016/j.flora.2017.03.012
Giovanetti M, Aronne G( 2012). Honey bee handling behaviour on the
papilionate flower of Robinia pseudoacacia L. Arthropod-Plant
Interactions, 7(1): 119–124. https://doi.org/10.1007/s11829-012-
9227-y
Gomes da Silva AL, Chaves SR, Brito JM (2011). Reproductive biology
of Bowdichia virgilioides Kunth (Fabaceae). Acta Scientiarum.
Biological Sciences, 33(4): 463-470.
https://doi.org/10.4025/actascibiolsci.v33i4.9003
Gottsberger G, Silberbauer-Gottsberger I (1988). Evolution of flower
structures and pollination in neotropical Cassiinae
(Caesalpiniaceae) species. Phyton, 28:293–320.
Goulson D (1999). Foraging strategies of insects for gathering nectar
and pollen, and implications for plant ecology and evolution.
Perspectives in Plant Ecology, Evolution and Systematics, 2(2):
185-209.
Gross CL (2001). The effect of introduced honeybees on native bee
visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a
fragmented ecosystem. Biological Conservation, 102(1): 89–95.
https://doi.org/10.1016/S0006-3207(01)00088-X
Gumbert A, Kunze J (1999). Inflorescence height affects visitation
behavior of bees - A case study of an aquatic plant community in
Bolivia. Biotropica, 31(3): 466–477.
https://doi.org/10.1111/j.1744-7429.1999.tb00389.x
Hall HG, Avila L (2016). Megachile sculpturalis, the giant resin bee,
overcomes the blossom structure of sunn hemp (Crotalaria
juncea) that impedes pollination. Journal of Melittology, (65): 1-
11.
Harder LD (1983). Functional differences of the proboscides of short-
and long-tongued bees (Hymenoptera, Apoidea). Canadian
Journal of Zoology, 61(7): 1580-1586.
Hargreaves AL, Harder LD, Johnson SD (2009). Consumptive
emasculation: The ecological and evolutionary consequences of
pollen theft. Biological Reviews, 84(2): 259–276.
https://doi.org/10.1111/j.1469-185X.2008.00074.x
Hattori M, Nagano Y, Itino T (2015). Geographic variation in flower
size and flower-visitor composition of two bumblebee-pollinated,
spring-flowering herbs, Lamium album L. var. barbatum
(Lamiaceae) and Meehania urticifolia (Lamiaceae). American
Journal of Plant Sciences, 6(05): 737.
Heering JH (1995). Botanical and Agronomic Evaluation of a
Collection of Sesbania sesban and Related Perennial Species.
Landbouw Universiteit Wageningen, Netherlands.
Henning JA, Peng YS, Montague MA, Teuber LR (1992). Honey bee
(Hymenoptera: Apidae) behavioral response to primary alfalfa
(Rosales: Fabaceae) floral volatiles. Journal of Economic
Entomology, 85(1): 233-239.
Herrera J (2001). The variability of organs differentially involved in
pollination, and correlations of traits in Genisteae (Leguminosae:
Papilionoideae). Annals of Botany, 88(6): 1027–1037.
https://doi.org/10.1006/anbo.2001.1541
Hingston AB (1999). Affinities between southern Tasmanian plants in
native bee visitor profiles. Australian Journal of Zoology, 47(4):
361-384.
Hingston AB, McQuillan PB (2000). Are pollination syndromes useful
predictors of floral visitors in Tasmania? Austral Ecology, 25(6):
600-609.
Howell GJ, Slater AT, Knox RB (1993). Secondary pollen presentation
in angiosperms and its biological significance. Australian Journal
of Botany, 41(5): 417-438.
Jacobi CM, Ramalho M, Silva M (2005). Pollination biology of the
exotic rattleweed Crotalaria retusa L. (Fabaceae) in NE Brazil.
A review for the pollinators of Papilionaceous flowers
52 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
Biotropica, 37(3): 357–363. https://doi.org/10.1111/j.1744-
7429.2005.00047.x
Johnson SD, Alexandersson R, Linder HP (2003). Experimental and
phylogenetic evidence for floral mimicry in a guild of fly-
pollinated plants. Biological Journal of the Linnean Society, 80(2):
289–304. https://doi.org/10.1046/j.1095-8312.2003.00236.x
Johnson SD, Jürgens A (2010). Convergent evolution of carrion and
faecal scent mimicry in fly-pollinated angiosperm flowers and a
stinkhorn fungus. South African Journal of Botany, 76(4): 796–
807. https://doi.org/10.1016/j.sajb.2010.07.012
Kampny CM (1995). Pollination and flower diversity in
Scrophulariaceae. The Botanical Review, 61(4): 350-366.
Kožuharova E, Firmage D (2009). Notes on the reproductive biology
of Astragalus dasyanthus Pall. (Fabaceae) a rare plant for
Bulgaria. Comptes rendus de l’Académie bulgare des Sciences,
62(9): 1079-1088.
Leppik EE (1966). Floral evolution and pollination in the Leguminosae.
Annales Botanici Fennici 3: 299 -308.
Lewis G (2005). Caesalpinieae. In Legumes of the world, G Lewis, B
Schrire, B Mackinder and M Lock (eds.). Royal Botanic Gardens,
Kew, Richmond, U.K. p. 127-161
Lihoreau M, Ings TC, Chittka L, Reynolds AM (2016). Signatures of a
globally optimal searching strategy in the three-dimensional
foraging flights of bumblebees. Scientific Reports, 6(1):1-13.
Lloyd DG, Schoen DJ (1992). Self-and cross-fertilization in plants. I.
Functional Dimensions. International Journal of Plant Sciences,
153(3, Part 1), 358-369.
LPWG (2017). A new subfamily classification of the Leguminosae
based on a taxonomically comprehensive phylogeny. Taxon, 66
(1): 44-77.
Malo JE, Baonza J (2002). Are there predictable clines in plant–
pollinator interactions along altitudinal gradients? The example
of Cytisus scoparius (L.) Link in the Sierra de Guadarrama (Central
Spain). Diversity and Distributions, 8(6): 365-371.
Maloof JE, Inouye DW (2000). Are nectar robbers cheaters or
mutualists? Ecology, 81(10): 2651-2661.
Mayer C, Dehon C, Gauthier AL, Naveau O, Rigo C, Jacquemart AL
(2014). Nectar robbing improves male reproductive success of
the endangered Aconitum napellus ssp. lusitanicum. Evolutionary
Ecology, 28(4): 669–685. https://doi.org/10.1007/s10682-014-
9696-9
McMahon M, Hufford L (2005). Evolution and development in the
amorphoid clade (Amorpheae: Papilionoideae: Leguminosae):
petal loss and dedifferentiation. International Journal of Plant
Sciences, 166: 383-396.
Meireles AC, Queiroz JA, Quirino ZGM (2015). Mecanismo explosivo
de polinização em Periandra mediterranea (Vell.) Taub.
(Fabaceae) na Reserva Biológica Guaribas, Paraíba, Brasil.
Biotemas, 28(4): 71-81.
Muir J (2013). Scotch Broom (Cytisus scoparius, Fabaceae) and the
Pollination and Reproductive Success of Three Garry Oak-
Associated Plant Species. University of Calgary, Canada.
Myczko Ł, Banaszak-Cibicka W, Sparks TH, Tryjanowski P (2015). Do
queens of bumblebee species differ in their choice of flower
colour morphs of Corydalis cava (Fumariaceae)? Apidologie,
46(3): 337–345. https://doi.org/10.1007/s13592-014-0326-x
Navarro L (2000). Pollination ecology of Anthyllis vulneraria subsp.
vulgaris (Fabaceae): nectar robbers as pollinators. American
Journal of Botany, 87(7): 980-985.
Ne'eman G, Nesher R (1995). Pollination ecology and the significance
of floral color change in Lupinus pilosos L. (Fabaceae). Israel
Journal of Plant Sciences, 43(2): 135-145.
Ogilvie JE, Zalucki JM, Boulter SL (2009). Pollination biology of the
sclerophyllous shrub Pultenaea villosa willd. (Fabaceae) in
southeast Queensland, Australia. Plant Species Biology, 24(1):
11–19. https://doi.org/10.1111/j.1442-1984.2009.00235.x
Olesen JM (1996). From naivete to experience: bumblebee queens
(Bombus terrestris) foraging on Corydalis cava (Fumariaceae).
Journal of the Kansas Entomological Society, 274-286.
Ollerton J, Watts S (2000). Phenotype space and floral typology:
towards an objective assessment of pollination syndromes. Det
Norske Videnskaps-Akademi. I. Matematisk-Naturvidenskapelige
Klasse, Skrifter, Ny Serie, 39: 149-159.
Pando JB, Fohouo FNT, Tamesse JL (2011). Foraging and pollination
behaviour of Xylocopa calens Lepeletier (Hymenoptera: Apidae)
on Phaseolus coccineus L. (Fabaceae) flowers at Yaounde
(Cameroon). Entomological Research, 41(5): 185–193.
https://doi.org/10.1111/j.1748-5967.2011.00334.x
Parker IM (1997). Pollinator limitation of Cytisus scoparius (Scotch
broom), an invasive exotic shrub. Ecology, 78(5): 1457-1470.
Parker IM, Engel A, Haubensak KA, Goodell K (2002). Pollination of
Cytisus scoparius (Fabaceae) and Genista monspessulana
(Fabaceae), two invasive shrubs in California. Madroño, 25-32.
Pennington RT, Klitgaard BB, Ireland H, Lavin M (2000). New insights
into floral evolution and basal Papilionoideae from molecular
phylogenies. In: Herendeen PS and Bruneau A. eds. Advances in
Legume Systematics: Part, 9, Royal Botanic Gardens, Kew, 233-
248.
Persson C (2001). Phylogenetic relationships in Polygalaceae based
on plastid DNA sequences from the trnL-F region. Taxon, 763-
779.
Peter CI, Johnson SD (2008). Mimics and magnets: The importance of
color and ecological facilitation in floral deception. Ecology, 89(6):
1583–1595. https://doi.org/10.1890/07-1098.1
Polhill RM, Raven PH (1981). Advances in Legume Systematics. Parts 1
and 2, Royal Botanic Gardens, Kew.
Polhill RM, Raven PH, Stirton C (1981). Evolution and systematics of
the Leguminosae. In: Polhill RM and Raven PH. eds. Advances in
Legume Systematics, Part 1, Royal Botanical Gardens, Kew, 1-26.
Primack RB, Inouye DW (1993). Factors affecting pollinator visitation
rates: a biogeographic comparison. Current Science, (65): 257-
262.
Proctor M, Yeo P, Lack A (1996). The Natural History of Pollination.
Harper Collins Publishers, London, UK.
Queiroz LDE (1996). Pollination ecology studies in Cratylia Mart. ex
Benth.(Leguminosae: Papilionoideae) and its taxonomic and
evolutionary implications. Sitientibus (UEFS), (15): 119–131.
Rafferty NE, Ives AR (2013). Phylogenetic trait-based analyses of
ecological networks. Ecology, 94(10): 2321–2333.
https://doi.org/10.1890/12-1948.1
Raine NE, Chittka L (2007). The adaptive significance of sensory bias
in a foraging context: floral colour preferences in the bumblebee
Bombus terrestris. PLoS ONE, 2(6): 1–8.
https://doi.org/10.1371/journal.pone.0000556
Raju AJS, Rao CP (2016). Pollination mechanism and pollinators of the
endemic plant Rhynchosia beddomei Baker. International Journal
of Botany Studies, 1(7): 1–3.
Ramalho M, Silva M, Carvalho G (2014). Pollinator sharing in
specialized bee pollination systems: A test with the
A review for the pollinators of Papilionaceous flowers
53 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
synchronopatric lip flowers of Centrosema Benth. (Fabaceae).
Sociobiology, 61(2): 189–197.
https://doi.org/10.13102/sociobiology.v61i2.189-197
Redbud (Cercis canadensis). Retrieved April, 2016 from
http://www.illinoiswildflowers.info/trees/plants/redbud.htm.
Robertson C (1928). Flowers and insects. Lists of visitors of 453
flowers. The Science Press Printing Company, Lancaster, PA.
Rodríguez-Riaño T (2004). Reproductive biology in Cytisus multiflorus
(Fabaceae). Annales Botanici Fennici, 41: 179–188.
Rossi M, Fisogni A, Nepi M, Quaranta M, Galloni M (2014). Bouncy
versus idles: On the different role of pollinators in the generalist
Gentiana lutea L. Flora: Morphology, Distribution, Functional
Ecology of Plants, 209(3–4): 164–171.
https://doi.org/10.1016/j.flora.2014.02.002
Rust RW, Clement SL (1977). Entomophilous pollination of the self-
compatible species Collinsia sparsiflora Fisher and Meyer. Journal
of the Kansas Entomological Society, 37-48.
Sahai K (2009). Reproductive biology of two species of Canavalia DC.
(Fabaceae)-A non-conventional wild legume. Flora: Morphology,
Distribution, Functional Ecology of Plants, 204(10): 762–768.
https://doi.org/10.1016/j.flora.2008.11.005
Schiestl FP, Johnson SD (2013). Pollinator-mediated evolution of
floral signals. Trends in Ecology and Evolution, 28(5): 307–315.
https://doi.org/10.1016/j.tree.2013.01.019
Schrire BD (1989). A multidisciplinary approach to pollination biology
in the Leguminosae. Advances in Legume Biology. Monographs in
Systematic Botany from the Missouri Botanical Garden, 29, 183-
242.
Shambhu B (2013). Studies on flower visitors of field bean Lablab
purpureus (L.) Sweet and their role in pollination and pod set.
University of Agricultural Sciences, GKVK, India.
Shi X, Wang JC, Zhang DY, Gaskin JF, Pan BR (2010). Pollination
ecology of the rare desert species Eremosparton songoricum
(Fabaceae). Australian Journal of Botany, 58(1): 35–41.
https://doi.org/10.1071/BT09172
Shivanna KR (2014). Biotic pollination: how plants achieve conflicting
demands of attraction and restriction of potential pollinators.
Reproductive Biology of Plants, 218-267.
Skorupski P, Spaethe J, Chittka L (2006). Visual search and decision
making in bees: time, speed, and accuracy. International Journal
of Comparative Psychology, 19: 342-347.
Slagle MW, Hendrix SD (2009). Reproduction of Amorpha canescens
(Fabaceae) and diversity of its bee community in a fragmented
landscape. Oecologia, 161(4): 813–823.
https://doi.org/10.1007/s00442-009-1429-3
Spaethe J, Tautz J, Chittka L (2001). Visual constraints in foraging
bumblebees: flower size and color affect search time and flight
behavior. Proceedings of the National Academy of Sciences, 98(7):
3898-3903.
Stanley D, Otieno M, Syeijven K, Berlin ES, Piironen T, Willmer P,
Nuttman C (2016). Pollination ecology of Desmodium setigerum
(Fabaceae) in Uganda; do big bees do it better? Journal of
Pollination Ecology, 19 (7): 43-49.
Stirton CH (1977). The pollination of Canavalia virosa by Xylocopid
and Magachilid bees. Bothalia, 12(2): 225-227.
Stout JC (2000). Does size matter? Bumblebee behaviour and the
pollination of Cytisus scoparius L. (Fabaceae). Apidologie, 31(1):
129-139.
Stout JC, Kells AR, Goulson D (2002). Pollination of the invasive exotic
shrub Lupinus arboreus (Fabaceae) by introduced bees in
Tasmania. Biological Conservation, 106(3): 425–434.
https://doi.org/10.1016/S0006-3207(02)00046-0
Streinzer M, Paulus HF, Spaethe (2009). Floral colour signal increases
short-range detectability of a sexually deceptive orchid to its bee
pollinator. Journal of Experimental Biology, 212(9): 1365–1370.
https://doi.org/10.1242/jeb.027482
Suzuki N (2000). Pollinator limitation and resource limitation of seed
production in the Scotch broom Cytisus scoparius (Leguminosae).
Plant Species Biology, 187–193.
Tucker SC (2002). Floral ontogeny of Cercis (Leguminosae:
Caesalpinioideae: Cercideae): does it show convergence with
papilionoids? International Journal of Plant Sciences, 163(1): 75-
87.
Tucker SC (2003). Update on floral development floral development
in legumes. Plant Physiology, 131: 911–926.
https://doi.org/10.1104/102.017459.center
Valido A, Dupont YL, Hansen DM (2002). Native birds and insects, and
introduced honey bees visiting Echium wildpretii (Boraginaceae)
in the Canary Islands. Acta Oecologica, 23(6): 413–419.
https://doi.org/10.1016/S1146-609X(02)01167-0
van der Pijl L (1961). Ecological aspects of flower evolution. II.
Zoophilous flower classes. Evolution, 15(1): 44-59.
Vivarelli D, Petanidou T, Nielsen A, Cristofolini G (2011). Small-size
bees reduce male fitness of the flowers of Ononis masquillierii
(Fabaceae), a rare endemic plant in the northern Apennines.
Botanical Journal of the Linnean Society, 165(3): 267–277.
https://doi.org/10.1111/j.1095-8339.2010.01105.x
Waddington KD (1979). Divergence in inflorescence height: an
evolutionary response to pollinator fidelity. Oecologia, 40(1): 43-
50.
Westerkamp C (1989). Von Pollenhaufen, Nudelspritzen und Pseudo-
staubblättern. Blütenstaub aus zweiter Hand. Palmengarten, (53)
146-149.
Westerkamp C (1991). Honeybees are poor pollinators—why? Plant
Systematics and Evolution, 177(1): 71-75.
Westerkamp C (1993). The co-operation between the asymmetric
flower of Lathyrus latifolius (Fabaceae-Vicieae) and its flowers.
Phyton, 33(1): 121–137.
Westerkamp C, Paul H (1993). Apios americana, a fly-pollinated
papilionaceous flower? Plant Systematics and Evolution, 187(1-4):
135-144.
Westerkamp C (1996). Pollen in bee-flower relations some
considerations on melittophily. Botanica Acta, 109: 325-332.
Westerkamp C (1997). Keel blossoms: bee flowers with adaptations
against bees. Flora: Morphologie, Geobotanik, Oekophysiologie,
192:125-32.
Westerkamp C, Weber A (1997). Secondary and tertiary pollen
presentation in Polygala myrtifolia and allies (Polygalaceae, South
Africa). South African Journal of Botany, 63(5): 254–258.
https://doi.org/10.1016/S0254-6299(15)30762-6
Westerkamp C, Weber A (1999). Keel flowers of the Polygalaceae and
Fabaceae: a functional comparison. Botanical Journal of the
Linnean Society, 129: 207-221.
Westerkamp C, Claßen-Bockhoff R (2007). Bilabiate flowers: The
ultimate response to bees? Annals of Botany, 100(2): 361–374.
https://doi.org/10.1093/aob/mcm123.
Zhang D, Xiang SHI, JianCheng Wang, Gaskin HLJF (2011). Breeding
system and its consequence on fruit set of a rare sand dune shrub
Eremosparton songoricum (Fabaceae: Papilionoideae).
Implications for Conservation. 干旱区科学, 3(4): 231-239.
A review for the pollinators of Papilionaceous flowers
54 | Aygören Uluer D (2021). Turkish Journal of Biodiversity 4(1): 37-54
