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Received: 9 June 2021 Revised: 18 October 2021 Accepted: 12 November 2021
DOI: 10.1111/1442-1984.12364

ORIGINAL ARTICLE

First report on generalized pollination systems

in Melastomataceae for the Andean pa
ramos

Naisla Manrique Valderrama1,2 | Isabela Galarda Varassin3,4 |

3,4 2
Luan Salles Passos | María Eugenia Morales Puentes

1
Estudiante Maestría en Ciencias
Biol

ogicas, Escuela de Posgrados en Abstract
Ciencias, Universidad Pedag
ogica y Melastomataceae is a megadiverse family with records of transitions from special-
Tecnol
ogica de Colombia, Tunja,
ized to generalized pollination systems for several species. These transitions are
Colombia
2 associated with the colonization of new, unpredictable and/or impoverished polli-
Grupo Sistem
atica Biol

ogica, Herbario
UPTC, Universidad Pedag
ogica y nator habitats or habitats where specialized pollinators are scarce (e.g., in high-
Tecnol

ogica de Colombia, Tunja, land environments). The bee species diversity is low in highlands. Therefore,
Colombia
3
autonomous breeding systems such as apomixis and self-pollination emerge in
Programa de P
os-Graduaç~ao em
Botânica, Universidade Federal do these environments. In this paper, we studied the floral traits associated with the
Paran
a, Centro Politécnico, Curitiba, generalization of pollination systems and registered the floral visitors of two spe-
Brazil
cies in the Colombian Andes: Miconia cataractae and M. elaeoides. We investi-
4
Laborat
orio de Interações e Biologia
gated the breeding system of M. elaeoides. Both species presented small flowers,
Reprodutiva, Universidade Federal do
Paran
a, Centro Politécnico, Curitiba, short anthers of medium pore size, and nectar-producing stomata on the base of
Brazil the anthers. Miconia cataractae produced an average of 1.62 μl nectar/flower, a
Correspondence
sugar concentration of 6.78%, whereas M. elaeoides produced 0.09 μl nectar/
Naisla Manrique Valderrama, Universidad flower, a sugar concentration of 6.13%. We recorded a wide diversity of pollinators
Pedag
ogica y Tecnol
ogica de Colombia, for both species, mainly insects from the orders Hymenoptera and Diptera.
Herbario UPTC, Avenida Central del
Norte, 39-115, Edificio Centro de
Miconia elaeoides presented a mixed breeding system and was also capable of set-
Laboratorios LS-109, Herbario UPTC, ting fruits by apomixis. We conclude that flower and anther morphology, com-
Tunja, Boyac
a, Colombia. bined with nectar production, thus represent convergent traits resulting in a
Email: naislamanrique@gmail.com
generalist pollination system shared by M. cataractae and M. elaeoides. Here, we
Funding information presented the first generalist pollination system recorded for Miconia (and the
Brazilian Coordination for the
Melastomataceae) in the Andes, the first report for a species from the small-pored
Improvement of Higher Education
Personnel, Grant/Award Number: section Amblyarrhena, and the first report for a species from the large-pored
88882.382585/2019-01; National Council section Cremanium in Colombia.
for Scientific and Technological
Development, Grant/Award Number: KEYWORDS
313801/2017-7
anther, buzz pollination, Colombia, Miconieae, pollen

1 | INTRODUCTION adaptations to less efficient pollinators can evolve if there

Specialized pollination systems are, in general, a conse-
quence of the evolution of floral traits in response to cer-
tain functional groups of most effective pollinators
(Fenster et al., 2004; Stebbins, 1971). Nonetheless, floral
is a gain in fitness (Aigner, 2001) and if the trade-offs
generated by these pollinators are minimal (Castellanos
et al., 2004; Muchhala, 2003), providing the emergence
of generalist pollination systems. Moreover, although
there is a greater prevalence of generalist systems in

160 © 2022 The Society for the Study of Species Biology wileyonlinelibrary.com/journal/psbi Plant Species Biol. 2022;37:160–172.

MANRIQUE VALDERRAMA ET AL.
plant–pollinator interactions (Waser et al., 1996), meth-
odological biases combined with the complex nature of
generalist pollination systems and their variability in time
and space have created constraints on the construction of
an empirical structure from an evolutionary perspective
(G
omez & Zamora, 2006; King et al., 2013; Waser
et al., 1996). This transition is associated with the coloniza-
tion of new, unpredictable and/or depauperate pollinator
habitats (Armbruster & Baldwin, 1998; Martén-Rodríguez
et al., 2010) or habitats where specialized pollinators are
scarce (e.g., diversity of bees in highland environments,
Arroyo et al., 1982; Kriebel & Zumbado, 2014). Besides that,
when pollinators are scarce or absent, autonomous breed-
ing systems may emerge (Barrett, 1996), such as apomixis
or self-pollination (Kriebel et al., 2015).
Melastomataceae is a megadiverse family of angio-
sperms with about 5750 species in 177 genera (Michelangeli
et al., 2019). Most species have flowers with heteromorphic
stamens and poricidal anthers (Renner, 1989). These floral
traits, especially the tubular anthers with minute pores, pos-
sibly evolved as a response to avoid excessive pollen loss to
pollinators (Buchmann, 1983; De Luca & Vallejo-
Marín, 2013), considering that pollen is the main or only
resource offered by these flowers to floral visitors
(i.e., “pollen flowers,” sensu Vogel, 1978). These flowers are
pollinated legitimately by some bee species capable of
buzzing the anthers to extract and collect pollen, an interac-
tion called buzz pollination (Buchmann, 1983). Moreover,
this kind of pollination is common among Melastomataceae
species, such that up to 98% of Neotropical species are polli-
nated in this way (Renner, 1989), indicating that this spe-
cialized pollination system is conserved.
However, several shifts in these traits have been
described for the family, such as changes from pollen
flowers to nectar flowers in different and unrelated genera,
resulting in pollination by other insects than bees, mainly
in the tribe Miconieae (Brito et al., 2017; Kriebel &
Zumbado, 2014; Maia et al., 2016), as well as by verte-
brates (Dellinger et al., 2018, 2019; Varassin et al., 2008).
Furthermore, many studies suggested transitions from a
specialized to a generalized insect pollination system in
the Miconieae tribe (Brito et al., 2016; Brito et al., 2017;
Gavrutenko et al., 2020; Kriebel & Zumbado, 2014; Maia
et al., 2016; Michelangeli et al., 2019; Santos et al., 2010).
This transition can be associated with changes in stamen
morphology and floral symmetry that are likely evolution-
ary responses, related to pollination shifts and changes in
mating systems in the tribe (Brito et al., 2016, 2017;
Gavrutenko et al., 2020; Goldenberg et al., 2008;
Goldenberg & Shepherd, 1998). For instance, for species of
the Cremanium section, stamens are short and the anthers
are large pored (Goldenberg et al., 2008), contrasting with
the Amblyarrhena section, where the flowers present
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161
short, small-pored anthers (Goldenberg et al., 2008).
These changes from small to large pores have allowed
these species to explore new pollinator guilds beyond
buzzing bees (i.e., flies and wasps) and thus more gener-
alized plant–pollinator interactions (Brito et al., 2016;
Goldenberg et al., 2008; Kriebel & Zumbado, 2014).
Moreover, in Miconia (Miconieae), herkogamy is less
common (Goldenberg et al., 2008), and self-incompati-
ble, self-compatible, and apomictic species have been
reported (Goldenberg & Shepherd, 1998; Goldenberg &
Varassin, 2001; Maia et al., 2016; Renner, 1989; Santos
et al., 2010). Curiously, self-compatible species of
Miconia present a generalized pollination system (Maia
et al., 2016; Santos et al., 2010).
In Colombia, there are 987 species of Melastomataceae,
and the genus Miconia is represented by 382 species (Bernal
et al., 2015). Studies involving reproductive biology and pol-
lination ecology of Melastomataceae from Colombia are
scarce. There are only two studies on the topic: one on bee
dependency of Melastomataceae species (Henao, 2019) and
the other one on the reproductive system of M. serrulata
(DC.) Naudin in the Colombian Amazon (Cadavid, 2004).
However, there is no information on the reproductive sys-
tem and plant–pollinator interaction considering the eleva-
tion in the Andes. With the increase in altitude, we
expected not only a reduction of species of the main pollina-
tors in Melastomataceae (i.e., buzzing bees) (Arroyo
et al., 1985) but also a transition from specialized interac-
tions between buzzing bees to interactions with other func-
tional groups of pollinators (e.g., Dellinger et al., 2021;
Gavrutenko et al., 2020; Kriebel & Zumbado, 2014).
In this study, we investigated whether floral traits of
Melastomataceae species from highland environments
can indeed be associated with a generalized pollination
system, as well as reflect a generalist pollination system,
and are also reflected in a generalization of reproductive
strategies, such as mixed reproductive systems and nectar
production. For this purpose, we selected Miconia
cataractae Triana and M. elaeoides Naudin as models due
to their traits: their small and isomorphic flowers and
shorter anthers but from clades with contrasting pore
size. Our study represents the first generalist pollination
system recorded for Miconia (and the Melastomataceae)
in the Andes and the first report for a species from the
small-pored section Amblyarrhena.
2 | MATERIALS AND METHODS
2.1 | Study site and model species
We carried out our field work from December 2019 to
March 2020 in the municipality of Ventaquemada in the

162
Rabanal P
aramo (5
250 06.900 N, 73
320 46.900 W, 3131–
3355 m. a. s. l), vereda Montoya, sector Mata Negra.
There, the minimum and maximum monthly tempera-
ture is 12 and 16.5
C, respectively, with a multi-year
average value of 14.4
C. The mean precipitation varies
between 650 and 950 mm (Corporaci
on Aut
onoma
Regional Cundinamarca [CAR] et al., 2014). The climate
is classified as a very humid montane forest according to
the Holdridge system (Morales et al., 2007) and presents
a bimodal distribution of rains in periods from March to
July and from October to November. The dry periods are
from February to August (21 mm) (Morales et al., 2007).
Miconia cataractae Triana (sect. Amblyarrhena) is a
native tree from the Colombian and Venezuelan Andes
(Bernal et al., 2015; Goldenberg et al., 2013). Currently,
information about the characteristics of the species is scarce
and restricted to insights provided in the original work of
description of the species (see Triana, 1871). In the studied
area, individuals of M. cataractae were found in short
parches of Andean cloud forests (3131–3350 m. a. s. l.).
Miconia elaeoides Naudin (sect. Cremanium) occurs
in Colombia and Venezuela (Goldenberg et al., 2013) and
is part of the clade Miconia III, which assembles Miconia
species from the Andes (Goldenberg et al., 2008). Miconia
elaeoides is a shrub, 2.5–5 m high, present in open areas
of p
aramo and high mountain forests (Jardín Bot
anico de
Bogot
a [JBB], 2020). Its small flowers are arranged in a
thyrsoid panicle, nonherkogamous flowers with a cam-
panulate hypanthium, 10 isomorphic stamens, and two-
pored anthers (Naudin, 1850a, 1850b). Individuals of
M. elaeoides can be found at altitudes above 3350 m. a. s.
l., under the influence of wind, mist, and low tempera-
tures (12
–16.5
C). The surrounding vegetation consists
of dwarf trees, shrubs, and grassland, besides the threat-
ened Andean species of the genus Espeletia Bonpl.
(Asteraceae; Mav
arez, 2021).
2.2 | Flower biology and morphology
We studied aspects of floral biology, such as flowering
time, stigma receptivity, and morphometry of the floral
whorls. We described the floral morphology based on
30 flowers selected randomly (in three individuals per
species). We determined stigma receptivity by surface cat-
alytic activity (Dafni et al., 2005; Fleet, 1952) in flower
buds and newly open flowers, bagged before anthesis. We
collected nectar from flowers (12 flower/species; Varassin
et al., 2008) in the morning session. We recorded the vol-
ume/flower with a graduate capillary, as well as the total
sugar content, weight by weight, using a handheld refrac-
tometer (concentration range 0%–32% Brix). For flower
morphometry, we measured the flowers preserved in 70%
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MANRIQUE VALDERRAMA ET AL.
alcohol with a stereomicroscope Leica EZ4 W/E with a
built-in camera and the Leica LAS EZ software. We
recorded the following measures: total length of the
flower (FLF), taken from the base of the peduncle to the
apex of the anthers; width and length of the petal (PW,
PL); total length of the anther (AL; four to six anthers/
flower); length of the gynoecium (GL); width and length
of the anther pore (WP, LP; four to six anthers/flower);
and the pore area (PA), with the ellipse formula. We cal-
culated the relationship between the pore area and the
anther length (PA/AL ratio; Brito et al., 2016) because
the pollen release can be different between anthers with
the same pore area, depending on the anther length
(Goldenberg et al., 2008). In addition, we counted the
number of seeds (SN) from a single fruit from five differ-
ent individuals (n = 5 fruits/species). We compared the
PA/AL ratio and the SN with Brito et al. (2016).
Additionally, we checked for the occurrence of nectary
stomata as in Varassin et al. (2008) through scanning elec-
tron microscopy (SEM, Carl Zeiss RA-ZEI-001 EVO MA
10 serial 994 448). For SEM, we dehydrated the samples in
an ethanol–acetone series and coated them for 4.5 min with
gold–palladium in a Quorum Q150R ES Turbo Metallizer/
evaporator supported by a turbomolecular pump.
2.3 | Floral visitors
We performed focal observations (sensu Dafni, 1992) to
record the flower visitors in three individuals per species
from October to December in M. cataractae and January to
March in M. elaeoides. The observations were during 8-h
sessions, in 4 days, totaling 32 h of observation per species.
We recorded the species, and the number of flowers visited
in a given plant. According to the visitor behavior (contact
with the stigma, perching, consumption of nectar, con-
sumption of pollen, consumption of nectar and pollen) and
adjustment in the flowers, we characterized the visitors as
pollinators, when they access the resource and touch the
stigma; thieves, when they access the resources without
touching the stigma; and robbers, when they accessed the
resource illegitimately (Inouye, 1980). We photographed
the insects and collected individuals to further identify
them at the entomology laboratory at the Universidad
Pedag
ogica y Tecnol
ogica de Colombia (UPTC). We depos-
ited the insects at the Museo de Historia Natural Luis
Gonzalo Andrade, UPTC.
2.4 | Breeding systems of M. elaeoides
We described the breeding system of M. elaeoides through
controlled pollination treatments. We applied five
 14421984, 2022, 2, Downloaded from https://esj-journals.onlinelibrary.wiley.com/doi/10.1111/1442-1984.12364 by UFPR - Universidade Federal do Parana, Wiley Online Library on [30/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MANRIQUE VALDERRAMA ET AL. 163

treatments (Radford et al., 1974): (1) autonomous pollina-
tion, where we bagged the buds; (2) self-pollination,
where we manually removed the pollen from the anthers
to a slide and deposit it on the stigma of the same flower
with a brush, and the flowers were bagged; (3) cross-pol-
lination, where the pollen was manually transferred from
the anthers of one individual to the stigma of another
individual, bagging the flowers; (4) open pollination (con-
trol), where the flower was only marked; and (5) apo-
mixis, where the stigmas in buds were covered with glue
and then bagged. We performed the treatments in three
individuals and 10 flowers per treatment in each individ-
ual, resulting in 30 flowers per treatment. The fruit develop-
ment was followed until ripening, for about a month.
Reproductive success was estimated by the number of fruits
formed per treatment. We did not perform the statistical
analysis of our data because our samples did not meet some
assumptions, such as sufficient sample size. We calculated
the index of self-incompatibility (ISI, sensu Bullock, 1985)
as the fruit set ratio between self- and cross-pollination.
We interpreted values higher than 0.25 as an indication
of self-compatibility (Oliveira & Gibbs, 2000; Zapata &
Arroyo, 1978). We also calculated the reproductive efficacy
index (RE, Oliveira & Gibbs, 2000; Zapata & Arroyo, 1978),
which is the ratio between fruit set by open pollination and
cross-pollination.
3 | RESULTS
3.1 | Flower biology and morphology
The flowering phenophase of both species lasted approxi-
mately 6 to 8 weeks in the dry season, between October
and December for M. cataractae, and January and
February for M. elaeoides. The flowers of M. cataractae

F I G U R E 1 Flowers of Miconia cataractae (a–e) and M. elaeoides (f–j). Some measurements: FLF, total length of the flower; PW width of
the petal; PL, length of the petal; AW, anther width. Flower of M. cataractae (a). Stamen of M. cataractae (b). Detail of anther (c). Petal (d).
Capitate to peltate stigma in M. cataractae (e). Flower of M. elaeoides (f). Stamen of M. elaeoides (g). Detail of anther (h). Petal (i) and
punctiform stigma in M. elaeoides (j). The lines represent a scale of 0.8 mm

TABLE 1 Size of flower whorls of Miconia cataractae Triana

Flower whorl Min Max Mean SD CV

Full flower length (mm) 7.90 12 9.61 1.10 11.53
Petal width (mm) 1.84 2.97 2.32 0.28 12.19
Petal length (mm) 2.53 3.26 2.94 0.20 6.84
Anther width (μm) 117.2 287.5 217 52.39 24.14
Anther length (μm) 1983 3653 2760 375.63 13.60
2
Anther pore area (μm ) 27368.62 50965.10 39135.67 7691.48 19.65
PA/AL 14.24 3.45
SN 57.71 9.8

Note: Sample size = 30 flowers.

Abbreviations: AL, anther length; CV, coefficient of variation; PA, pore area; SD, standard deviation; SN, seed number.
 14421984, 2022, 2, Downloaded from https://esj-journals.onlinelibrary.wiley.com/doi/10.1111/1442-1984.12364 by UFPR - Universidade Federal do Parana, Wiley Online Library on [30/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
164 MANRIQUE VALDERRAMA ET AL.

TABLE 2 Size of flower whorls in Miconia elaeoides Naudin

Flower whorl Min Max Mean SD CV

Full flower length (mm) 9.46 12.40 10.97 0.83 7.58
Petal width (mm) 2.13 3.09 2.59 0.21 8.15
Petal length (mm) 2.53 3.26 2.94 0.20 6.84
Anther width (um) 341 629.6 419.26 83.63 19.94
Anther length (um) 1698 2930 2568 286.27 11.14
Anther pore area (μm2) PA 36,135.91 165,131.16 80,872.23 39,080.19 48.32
PA/AL 31.49 17.99
SN 42.23 9.8

Note: Sample size = 30 flowers.

Abbreviations: AL, anther length; CV, coefficient of variation; PA, pore area; SD, standard deviation; SN, seed number.

F I G U R E 2 Scanning electron microscopy images under electron high tension (EHT) = 20 kV (a–f) of anthers of Miconia cataractae
(a–c) and M. elaeoides (d–f). Anthers with a single pore in M. cataractae, work distance (WD) = 33.5 mm, magnitude of increase
(mag) = 100 X (a). The basal part of anthers with projections (indicated with an arrow) and the possible presence of stomata of
M. cataractae, WD = 34.0 mm, mag = 70 X (b). Anther pore in M. cataractae, WD = 34.0 mm, mag = 500 X (c). Stomata positioned at the
basal part of the anther and in the distal part of the anther filament in the projections of the anthers (indicated with an arrow),
WD = 9.0 mm, mag = 90 X (d). Detail of two-pored anther of M. elaeoides, WD = 9.5 mm, mag = 275 X (e). The nectary stoma with the
shape of a patelliform gland in the anthers in M. elaeoides, WD = 10.5 mm, mag = 5.00 K X (f)
 14421984, 2022, 2, Downloaded from https://esj-journals.onlinelibrary.wiley.com/doi/10.1111/1442-1984.12364 by UFPR - Universidade Federal do Parana, Wiley Online Library on [30/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MANRIQUE VALDERRAMA ET AL. 165

TABLE 3 Floral visitors of (1) Miconia cataractae and (2) M. elaeoides: species, plant visited, number of records, resource collected, and
behavior

Species Plant visited N
of records Behavior Resource

APODIFORMES
Metallura tyrianthina 2 1 Nectarivore, pollinator N
COLEOPTERA
Chrysomelidae sp. 1, 2 10 Nectarivore, pollinator N/P
Phaenolis sp. 2 1 Perched on leaves and flowers, potential pollinator N.O.
Magdalis sp. 1, 2 12 Nectarivore, pollinator N/P
DIPTERA
Sylvicola fasciatus 1 2 Nectarivore, pollinator N
Bibionomorpha sp. 1, 2 28 Nectarivore, pollinator N
Brachypremna sp. 1, 2 4 Nectarivore, pollinator N
Callicera sp. 1 1 Nectarivore, pollinator N/P
Calliphora nigribasis 1, 2 38 Nectarivore, pollinator N
Lucilia sericata 1, 2 8 Nectarivore, pollinator N
Elachiptera sp. 1, 2 2 Nectarivore, pollinator N/P
Eristalis arbustorum 1, 2 4 Nectarivore, pollinator N/P
Ocyptamus sp. 1 1 Nectarivore, pollinator N/P
Platycheirus sp. 1, 2 19 Nectarivore, pollinator N/P
Syrphus sp. 1, 2 2 Nectarivore, pollinator N/P
Toxomerus sp. 2 1 Nectarivore, perched on leaves and flowers, pollinator N/P
Bradysia sp. 1, 2 2 Nectarivore, pollinator N
Adejeania sp. 1, 2 2 Nectarivore, pollinator N
Parepalpus sp. 2 2 Nectarivore, pollinator N
HEMIPTERA
Nezera viridula 1 1 Perched on leaves and flowers, potential pollinator N.O.
HYMENOPTERA
Agelaia sp. 1 1 Nectarivore, pollinator N
Vespidae sp. 1 1 Nectarivore, pollinator N
Apis mellifera 1, 2 40 Nectarivore, pollinator N/P
Bombus robustus 1, 2 2 Nectarivore, pollinator N/P
Bombus atratus 2 3 Nectarivore, pollinator N/P
Bombus hortulanus 2 3 Nectarivore, pollinator N/P
Bombus rubicundus 1, 2 52 Nectarivore, pollinator N/P
Camponotus polymorphicus 2 7 Nectarivore, pollinator N
Braconidae sp. 1, 2 2 Nectarivore, pollinator N
LEPIDOPTERA
Pedaliodes sp. 2 2 Nectarivore, pollinator N
MESOSTIGMATA
Gnatosoma sp. 2 1 Perched on flowers N.O.
ORTHOPTERA
Gryllidae sp. 2 1 Perched on leaves and flowers, pollinator N

Abbreviations: N, nectar; P, pollen; N.O., not observed.


166
and M. elaeoides were arranged in paniculate inflores-
cences of terminal dichasium. Miconia cataractae pro-
duced an average of 344 flowers per inflorescence,
and M. elaeoides produced an average of 42 flowers. Her-
kogamy was absent in the flowers of both species
(Figure 1a,f). They stayed open for 2–3 days, and then
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MANRIQUE VALDERRAMA ET AL.
F I G U R E 3 Habitats and flower
visitors of Miconia cataractae (a–h) and
M. elaeoides (i-o). Image of M. cataractae
(a). Patches of Andean cloud forest and
habitat of M. cataractae (photo by
W. Medina) (b). Braconidae contacting
the flowers’ anthers and gynoecium (c).
Bibinomorpha sp. walking between
flowers (d). Bombus rubicundus
pollinating flowers (e). Calliphora
nigribasis contacting the anthers and
stigma (f). Toxomerus sp. walking into
flowers and looking for nectar (g).
Syrphus sp. walking on the flowers (h).
Image of M. elaeoides (i). Habitat of
M. elaeoides with p
aramo vegetation
with dwarf trees, shrubs, and grassland,
beside the threatened Andean species of
the genus Espeletia Bonpl. (Asteraceae)
(j). Calliphora nigribasis contacting the
anthers and stigma (k). Bombus
rubicundus pollinating flowers (l). Fly
(Syrphidae) walking between flowers
(m). Apis mellifera pollinating flowers
(n). Eristalis arbustorum eating nectar
(o). The line represents a scale of one cm
anthers and petals started to fall. The flowers of both spe-
cies are small with creamy-white petals (M. cataractae in
Table 1, Figure 1a–e; M. elaeoides in Table 2, Figure 1f–j).
Both their flowers had pleasant smells and their stigmas
were receptive still in the bud stage. We observed an exu-
date on the flowers of both species, specifically at the

MANRIQUE VALDERRAMA ET AL.
F I G U R E 4 Mean of visits per hour
for different orders of flower visitors
along the day in Miconia cataractae
(a) and M. elaeoides from Colombia (b)
base of the anthers and in the apical part of the connec-
tive. We concluded that this exudate was nectar because
we registered nectary stomata at the base of the anthers
and on the anther connective (Figure 2). The flowers of
M. cataractae produced an average nectar volume of
1.62 μl ± 0.4 with a sugar concentration of 6.78%, and
M. elaeoides produced an average nectar volume of
0.09 μl ± 0.01 with a sugar concentration of 6.13%. The
anthers are white to light yellow, cuneate, and genicu-
late, with a single medium-sized pore in M. cataractae
(Table 1, Figure 1a–e). Miconia elaeoides has obovate
anthers with a large pore and a well-defined septum
between both thecas (Table 2, Figure 1f–j). The stigma is
capitate to peltate in M. cataractae and punctiform in
M. elaeoides (Figure 1e,j). The PA/AL ratio was 14.24
± 3.45 in M. cataractae with 57.71 ± 18.59 seeds/fruit
and 31.49 ± 17.99 in M. elaeoides with 42.23 ± 9.89
seeds/fruit.
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167
3.2 | Flower visitors
We recorded 20 species of insects visiting flowers in
M. cataractae and 28 species of visitors in M. elaeoides
including one arachnid and one vertebrate. The visitors
were mostly insects, with a predominance of the orders
Hymenoptera and Diptera (15 and 8 species, respectively;
Table 3). Bees and flies visited M. cataractae and
M. elaeoides flowers more frequently. We observed both
groups accessing nectar and/or collecting pollen in the
flowers of two species (Figures 3 and S1).
Nectar was the main resource searched by visitors in
both species, allowing the visit of several groups other
than buzzing bees, including the hummingbird Tyrian
metaltail, Metallura tyrianthina (Apodiformes). However,
bees of the genus Bombus were the most abundant visi-
tors, especially the species Bombus rubicundus (Table 3).
These bees visited several flowers and inflorescences of

168
T A B L E 4 Fruit set in different controlled pollination
treatments in Miconia elaeoides in P
aramo de Rabanal,
municipality of Ventaquemada, Boyac
a
Treatment
Open pollination
Autonomous self-pollination
Self-pollination
Cross-pollination
Apomixis
Index
ISI
RE
Note: Sample size = 30 flowers.
Abbreviations: ISI, index of self-incompatibility (selfing/crossing fruit set);
RE, reproductive efficacy (open pollination/crossing fruit set).
both species, collecting nectar and pollen by buzz polli-
nation (Figure 3e,l). The species Apis mellifera also
showed a high number of visits for both species, as
well as other Hymenoptera species (i.e., wasps and
ants; Table 3). These bees walked on several flowers
foraging for nectar and touched anthers and stigma
(Figure 3c,n). Among the Diptera, we observed many spe-
cies of Bibionidae, Calliphoridae, and Syrphidae walking on
the flowers and contacting the anthers and stigma
(Figure 3d,f–h,k,m,o).
Diptera and Hymenoptera species visited the flowers
with higher frequency. Species of Diptera proved most
active in the morning between 8:00 and 9:00 a.m., when
they displayed a higher visit frequency to M. cataractae
(Figure 4a) and between 9:00 at 10:00 a.m. to M. elaeoides
(Figure 4b). We observed two tall peaks in Hymenoptera
visits in M. cataractae at different times; one peak was at
8:00 a.m. (Figure 4a), with a reduction in visits to follow
and another peak at 10:00 am to M. elaeoides (Figure 4b).
After 1:00 p.m., M. cataractae was predominantly visited by
Diptera, while M. elaeoides by Hymenoptera. Although
there was some temporal separation in their visits among
both Miconia species, the visits of Hymenoptera and Dip-
tera were recorded more frequently between 9:00 and
11:00 a.m. in M. cataractae (Figure 4a) and 9:00 and
12:00 a.m. in M. elaeoides (Figure 4b). We suggest that the
species are producing rewards (nectar and pollen) during
all anthesis (Figure 4a,b).
3.3 | Breeding systems of M. elaeoides
We recorded fruit set in all pollination treatments including
open pollination treatment but in different proportions. The
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MANRIQUE VALDERRAMA ET AL.
treatments with a higher fruit set were open pollination,
autonomous self-pollination, and cross-pollination. Miconia
elaeoides was considered self-compatible because the fruit
% Fruit set did not differ significantly between selfed and outcrossed
set (# fruits) treatments with a high ISI (0.6). It was also capable of set-
97 (29)
ting fruit by apomixis and showed high efficacy of natural
pollination (RE = 1.45; Table 4).
80 (24)
40 (12)
67 (20) 4 | DISCUSSION
57 (17)
Values Our results support the initial hypothesis that the shared
floral traits (i.e., small flowers, lack of floral herkogamy,
0.6
isomorphic stamens, and nectar production) are associ-
1.45
ated with generalized pollinators in M. cataractae and
M. elaeoides. Besides that, we also found support for a
generalized mating system, such as mixed mating system
and apomixis, at least for M. elaeoides.
According to the time that the flowers stay open (2–
3 days) and because most species of Melastomataceae
present an anthesis period shorter than 24 h
(Renner, 1989), as well as due to the adverse climatic
conditions of the p
aramos highlands, we may suppose
that the anthesis (of up to 3 days) in the studied species
may lead to an adaptive advantage, assuming that it
could result in greater chances of pollinator visits
(Kriebel & Zumbado, 2014; Renner, 1989). Floral traits
such as white petals and light-yellow anthers with
minute pores are characteristic of the probable ancestral
flower of Miconieae, a phenotype associated with buzz
pollination (Gavrutenko et al., 2020). Therefore, both
M. cataractae (sect. Amblyarrhena) and M. elaeoides (sect.
Cremanium) have a floral morphology related to a paral-
lel evolutionary trend resulting in convergent floral phe-
notypes, which made possible the transition from a
specialized (i.e., buzz pollination) to a generalist system
of pollination (Brito et al., 2016; Gavrutenko et al., 2020;
Goldenberg et al., 2008). Both species' transition to a gen-
eralist floral phenotype might be associated with the col-
onization of high-Andean environments (Gavrutenko
et al., 2020), considering that the presence of buzzing
bees is inconstant in highlands (Arroyo et al., 1982; Brito
et al., 2016; Kriebel & Zumbado, 2014).
Both species have pores that can be considered
medium sized (M. cataractae 39,135.67 μm2; M. elaeoides
80,872.23 μm2), as well as medium-sized anthers
(M. cataractae, 2760 μm; M. elaeoides 2568 μm) compared
with other Miconieae species (pore areas range from 5320
to 227,326 μm2; anther length ranges from 972 to
8067 μm in Brito et al., 2016). Also, the PA/AL ratio and
the number of seeds per fruit recorded for both species
can be associated with visits by different groups of polli-
nators (i.e., generalist pollinators; Brito et al., 2016),

MANRIQUE VALDERRAMA ET AL.
considering that these traits are phylogenetically related,
indicating an independent evolution with pollinator spe-
cies (Brito et al., 2016). Therefore, our findings support
this evolutionary trend, with a relationship between mor-
phological traits and the generalist pollinators system in
species of Miconieae, considering the different ecological
scenarios addressed in both papers: Atlantic tropical for-
est (Brito et al., 2016) and the Andean highlands (this
paper).
As predicted, we recorded a wide range of visitors for
both species of Miconia, including nonbuzzing bees and
Diptera species. Due to the floral traits of both species
(i.e., nonherkogamous, small, and abundant flowers;
medium-pore anthers; and nectar production), most of
the visitors can be considered pollinators, as they walked
on the flowers foraging for nectar or pollen and touched
the anthers and stigma. This inclusion of other pollina-
tors besides buzzing bees in highland ecosystems where
climatic conditions change drastically can ensure the
reproductive success of these Miconia species, consider-
ing the lower diversity of bees that perform buzz pollina-
tion in these environments (Arroyo et al., 1985; Brito &
Sazima, 2012; Brito et al., 2017). Moreover, Diptera spe-
cies have been recognized for playing an important role
in plant pollination, as they record high pollen loads in
plants from high-Andean forests (Marquínez et al., 2009;
Thien, 1980).
The presence of foraging hummingbirds on inconspicu-
ous, nectar-producing, small-flowered species of Miconia
was reported only once in the Atlantic tropical forest
(Varassin et al., 2021). Therefore, this second report of
Metallura tyrianthina (species confirmed consulting Medina
et al., 2015) visiting flowers of M. elaeoides may indicate that
nectar production might be the main trait to predict hum-
mingbird visits in Miconieae species found on other
melastome clades (Varassin et al., 2008). Butterflies and
wasps were also probably related to nectar production, even
if in low amounts (1.62 and 0.09 μl) and with a low concen-
tration of sugar (6.78% and 6.13%) in M. cataractae and
M. elaeoides, compared with other species from the same
family (14%–20%, Stein & Tobe, 1989). Therefore, flower
morphology is not the only clue to understand changes in
pollination systems in Melastomataceae. The presence of
nectar also plays an important role in the evolution of new
pollination systems (Dellinger et al., 2018; Ollerton
et al., 2007; Renner, 1989; Varassin et al., 2008). This gener-
alization of pollination systems associated with nectar pro-
duction was also observed for M. hyemalis A.St. – Hil &
Naudin (Varassin et al., 2008) and M. theaezans Cogn.
(Brito et al., 2017), species from the section Cremanium.
Likewise, production of nectar and high diversity of pollina-
tors have been found in M. angelana R. Romero &
R. Goldenb (Santos et al., 2010). We also found the presence
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169
of nectary stomata in anthers and the anther connective,
already described for Miconia (Kriebel & Zumbado, 2014)
and for other clades (Varassin et al., 2008), supporting
the hypothesis that the presence of nectaries in Melasto-
mataceae is a derived trait (Gavrutenko et al., 2020;
Varassin et al., 2008).
The experimental approach to detect the mating sys-
tems in M. elaeoides indicated the potential occurrence of
mixed mating systems and apomixis. On the other hand,
our approach cannot set which mating mechanism is more
relevant. In Melastomataceae, specifically in the Miconieae
tribe, is common the apomixis (Goldenberg & Shep-
herd, 1998; Goldenberg & Varassin, 2001; Hokche &
Ramírez, 2008; Melo et al., 1999), with a high phylogenetic
signal for apomixis in Melastomataceae (Goldenberg &
Shepherd, 1998). Miconia elaeoides is a shrub that occurs in
low densities in open environments with secondary vegeta-
tion (two individuals in a studied area of 1000 m2,
Manrique-V.N., personal observation), both traits (habit
and habitat) highly associated with apomixis (Bawa, 1974;
Goldenberg & Shepherd, 1998; Jaimes & Ramírez, 1999;
Ramírez & Brito, 1990; Ramírez & Seres, 1994). Moreover,
apomixis seems to be a reproductive strategy for plant spe-
cies in disturbed habitats (Bawa, 1974), as well as in early
successional plants (Cruden, 1977). The treatment with the
highest fruit set was spontaneous self-pollination; however,
it is possible that the handling of flowers during pollination
treatments might have led to abortive events in other treat-
ments. The values of the ISI index indicate the relative self-
compatibility of this species, which is common among other
species of the family (Franco et al., 2011; Goldenberg &
Shepherd, 1998; Maia et al., 2016; Pereira et al., 2011). In
addition, the high values for reproductive efficacy suggest a
high efficacy of natural pollination in the presence of effi-
cient pollinators or without them. The values reported are
even higher than in other species of Melastomataceae
(Malucelli et al., 2018). Taken together, our findings de-
monstrate a reproductive versatility that might be asso-
ciated with the ability of this species to colonize new areas
(Gavrutenko et al., 2020; Holsinger, 2000; Toräng
et al., 2017) and/or to be a successful species in the early
stages of succession in restoration processes (Cantillo
et al., 2009) on the Andes Mountain range.
Our results showed that both M. cataractae and
M. elaeoides present convergent morphological traits that
possibly evolved in response to ecological pressures and
enabled the transition to a generalist pollination system
(Brito et al., 2016; Gavrutenko et al., 2020; Goldenberg
et al., 2008). These floral traits combined with nectar pro-
duction allow several functional groups to visit and polli-
nate these flowers, not exclusively buzzing bees. Besides
that, reproductive mechanisms such as self-fertilization
and apomixis may favor colonization and establishment

170
of M. elaeoides in restrictive environments, such as the
highlands of the Andean p
aramos.
A C K N O WL E D G M E N T S
The postgraduate in Biological Science of UPTC,
Vicerrectoría de Investigaci
on y Extensi
on, Direcci
on de
Investigaciones and Centro de Investigacio
n y Extensio
n
CIEC for grant VIE No 8-2019. The Brazilian National
Council for Scientific and Technological Development
(CNPq) grant 313801/2017-7 to IGV. The Brazilian Coordi-
nation for the Improvement of Higher Education Person-
nel (CAPES), scholarship to LSP (88882.382585/2019-01).
Instituto para la Investigaci
on e Innovaci
on en Ciencia y
Tecnología de Materiales (INCITEMA) at Universidad
Pedag
ogica y Tecnol
ogica de Colombia (UPTC) to scan-
ning electron microscopy and specialists in the identifica-
tion of visitants insects (Laboratorio de Entomología de la
UPTC). The research group Sistem
atica Biol
ogica SisBio of
Universidad Pedag
ogica y Tecnol
ogica de Colombia, and
the Laboratorio de Interações e Biologia Reprodutiva of
the Universidade Federal do Paran
a.
ORCID
Naisla Manrique Valderrama https://orcid.org/0000-
0002-8925-8395
Isabela Galarda Varassin https://orcid.org/0000-0001-
9189-8765
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SU PP O R TI N G I N F O RMA TI O N
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How to cite this article: Manrique Valderrama,
N., Varassin, I. G., Passos, L. S., & Morales
Puentes, M. E. (2022). First report on generalized
pollination systems in Melastomataceae for the
Andean p
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160–172. https://doi.org/10.1111/1442-1984.12364