Bat pollination in Bromeliaceae

Abstract

Background: Chiropterophily encompasses the floral traits by which bats are attracted as the main pollinators. Among the chiropterophilous flowering plants of the New World, Bromeliaceae is one of the most ecologically important families; however, information about the chiropterophilous interaction in this family is still scarce. Aims: We present a comprehensive review of bat pollination in bromeliads, covering floral traits, rewards offered to pollinators, floral attractants and the identity of visiting bat species. Methods: We discuss traits shared among chiropterophilous bromeliads and present general trends in an evolutionary context. We constructed a phylogenetic tree to elucidate the ancestral pollination syndromes of the 42 extant bromeliad species (ca. 1% of total) known to be bat-pollinated. Results: Most of the species within the ten genera reported belong to the Tillandsioideae subfamily, with three genera appearing to be exclusively bat-pollinated. Floral visitors include 19 bat species of 11 genera from the Phyllostomidae. Conclusions: Our analysis indicated that chiropterophilous floral features originated multiple times in bromeliad evolution, most probably from ornithophilous. The evidence for floral traits associated with bat pollination and the chiropterophilous syndrome presented by certain Bromeliaceae indicate the important role played by bats in the evolution of this plant family.

Full text

ARTICLE
Bat pollination in Bromeliaceae
Pedro A. Aguilar-Rodríguez
a
, Thorsten Krömer
a
, Marco Tschapka
b,c
, José G. García-Franco
d
,
Jeanett Escobedo-Sarti
e
and M.Cristina MacSwiney G.
a
a
Centro de Investigaciones Tropicales, Universidad Veracruzana, Xalapa, Veracruz, Mexico;
b
Institute of Evolutionary Ecology and
Conservation Genomics, University of Ulm, Ulm, Germany;
c
Smithsonian Tropical Research Institute, Balboa Ancón, Panamá, República
de Panamá;
d
Red de Ecología Funcional, Instituto de Ecología, Xalapa, Veracruz, México;
e
Facultad de Ciencias Biológicas y
Agropecuarias, Universidad de Colima, Crucero de Tecomán, Tecomán, Colima, México
ABSTRACT
Background: Chiropterophily encompasses the floral traits by which bats are attracted as the
main pollinators. Among the chiropterophilous flowering plants of the New World,
Bromeliaceae is one of the most ecologically important families; however, information
about the chiropterophilous interaction in this family is still scarce.
Aims: We present a comprehensive review of bat pollination in bromeliads, covering floral
traits, rewards offered to pollinators, floral attractants and the identity of visiting bat species.
Methods: We discuss traits shared among chiropterophilous bromeliads and present general
trends in an evolutionary context. We constructed a phylogenetic tree to elucidate the
ancestral pollination syndromes of the 42 extant bromeliad species (ca. 1% of total) known
to be bat-pollinated.
Results: Most of the species within the ten genera reported belong to the Tillandsioideae
subfamily, with three genera appearing to be exclusively bat-pollinated. Floral visitors include
19 bat species of 11 genera from the Phyllostomidae.
Conclusions: Our analysis indicated that chiropterophilous floral features originated multiple
times in bromeliad evolution, most probably from ornithophilous. The evidence for floral
traits associated with bat pollination and the chiropterophilous syndrome presented by
certain Bromeliaceae indicate the important role played by bats in the evolution of this
plant family.
ARTICLE HISTORY
Received 2 May 2017
Accepted 3 January 2019
KEYWORDS
Anoura; bromeliads;
chiropterophily; floral scent;
nectar; pollination; Werauhia
Introduction
The floral syndrome concept has been criticised
for failing to consider the complete diversity of
floral traits, as well as the entire spectrum of floral
visitors (Ollerton et al. 2009). Nevertheless, it
remains a useful tool for predicting the main pol-
linators of plants, especially in tropical regions
(Rosas-Guerrero et al. 2014;Ashworthetal.2015
and references therein). This seems to be the case
for bat-pollinated plant species, which tend to
possess flowers that are morphologically distinct
from those of other pollination guilds (von
Helversen 1993; Fleming and Muchhala 2008).
Chiropterophily, or the syndrome of pollination via
interaction with bats, encompasses the floral traits (e.g.
size, shape, colour, nectar characteristics and scent)
shared by many angiosperms in order to attract bats
(Mammalia: Chiroptera) as their main pollinators
(Tschapka and Dressler 2002;vonHelversenand
Winter 2003;Flemingetal.2009). Bat pollination
occurs in the tropical and subtropical regions of both
the Old and New World and is found in more than
500 plant species (Dobat and Peikert-Holle 1985;
Fleming et al. 2009). The chiropterophily syndrome
may encompass the following characteristics (van der
Pijl 1961;vonHelversen1993;vonHelversenetal.
2000;TschapkaandDressler2002;vonHelversenand
Winter 2003;Krömeretal.2008;Rosas-Guerreroetal.
2014): (1) nocturnal or crepuscular anthesis; (2) pale
or dullish colours in the perianth (predominantly
white, pale green, yellow) without nectar lines; (3)
flagelliflory (flowers suspended on long stalks, situated
at a distance from the branches and leaves) and/or
cauliflory (flowers emerging directly from the tree
trunk or from larger branches); (4) tubular, zygo-
morphic or radially symmetrical flowers that fitthe
snout of the bat like a ‘mask’,andalso‘brush-type’
flowers/inflorescences with protruding stamens; (5)
large and sturdy flowers; (6) musty or unpleasant
odour, described as garlic- or onion-like; (7) relatively
large amounts of dilute nectar with an average sugar
concentration of ca.17%,andapredominantlyhex-
ose-rich composition (e.g. low sucrose content, high
levels of glucose and fructose); (8) large quantities of
CONTACT M. Cristina MacSwiney G. cmacswiney@uv.mx
Supplemental data for this article can be accessed here.
PLANT ECOLOGY & DIVERSITY
https://doi.org/10.1080/17550874.2019.1566409
© 2019 Botanical Society of Scotland and Taylor & Francis

pollen and, in some cases, (9) edible plant tissues as
rewards (see Cox 1984;Cunningham1995). However,
these characteristics are highly variable among plant
families and some of the allegedly chiropterophilous
traits (such as nocturnal anthesis) are not exclusive to
plants pollinated by bats. A possible explanation for
this is that bats present relatively low floral constancy,
so a bat can visit flowers of many species in a single
night and will thus frequently deliver mixed pollen
loads to receptive stigmas (Fleming et al. 2005;
Muchhala et al. 2008;butseeevidencefordifferential
pollen placement by bats in Muchhala and Thomson
2012;StewartandDudash2016). In this sense, most
bat-pollinated plants have evolved as a pollination-
guild, comprising non-related species that share a
pollinator with similar behaviour and morphology
(Muchhala and Jarrín-V 2002)ratherthanbeingspe-
cialised to one bat species pollinating only one plant
species (but see Centropogon nigricans and the bat
Anoura fistulata;Muchhalaetal.2005;Muchhala
and Thomson 2009).
The study of bat-pollination has developed
considerably since the early observations of
Moseley (1870)andBurck(1892). The beginning
of formal studies dates back to the 1930s and 1960s
(e.g. Porsch 1932 or Vogel 1958,1969;seealsovan
del Pijil 1961). Classic studies by Faegri and van
der Pijl (1979) and Dobat and Peikert-Holle
(1985) then provided detailed information about
the chiropterophilous syndrome and confirmed a
number of bat-pollinated plants, to which other
examples have since been added (e.g. Fleming et
al. 2009; Geiselman and Defex 2015).
The Bromeliaceae is one of the most frequently
reported bat-pollinated plant families (von Helversen
1993;Flemingetal.2009). It includes more than 3500
herbaceous species from 70 genera (Barfuss et al. 2016;
Gouda et al. 2017). The specialised nectarivorous bats
responsible for most reports of bat-pollination in the
Neotropics are found within the subfamilies
Glossophaginae and Lonchophyllinae, among the
highly diverse leaf-nosed bats (Phyllostomidae).
These bats comprise 20 genera and more than 50
species (Simmons 2005;Mantilla-MelukandBaker
2010;Bolzanetal.2015;MoratelliandDias2015;
Cirranello et al. 2016).
Pollination by vertebrates occurs within the
Bromeliaceae more frequently than insect pollination
(Benzing 2000;KesslerandKrömer2000;Canela
and Sazima 2005;Krömeretal.2006)andsome
species, especially among the Tillandsioideae and
Bromelioideae subfamilies, present a mixed pollina-
tion system (Benzing 2000;Givnishetal.2014). Bats
are the second most common vertebrate pollinators of
the Bromeliaceae, more frequently reported than pas-
serine birds or opossums, and surpassed only by hum-
mingbirds (Trochilidae) (Martinelli 1994,1997;
Kessler and Krömer 2000;Araujoetal.2004;Canela
and Sazima 2005;Hornung-LeoniandSosa2006;
Krömer et al. 2006;Queirozetal.2016). Most of our
current knowledge of bat-pollinated bromeliads,
defined as species in which bats perform most of the
legitimate visits to the flowers, comes from opportu-
nistic observations. Comprehensive and quantitative
information remains scarce, and a detailed under-
standing of the reproductive biology exists for only a
few species (e.g. Pitcairnia albiflos, Pseudalcantarea
macropetala, Werauhia gladioliflora;Aguilar-
Rodríguez et al. 2014;Wendtetal.2001;Cascante-
Marín et al. 2005;TschapkaandvonHelversen2007).
Variation in floral adaptations exhibited by
Bromeliaceae probably accounts for their adaptability
in terms of changing traits associated with different
pollinators and reproductive systems, even between
closely related species (Gardner 1986;Varadarajan
and Brown 1988;Benzing2000;Givnishetal.2014).
To consolidate the rather scattered information
currently available, we present a comprehensive
review based on all available reports of bat polli-
nation in the Bromeliaceae, including the identity
of bat species involved where available. We
obtained information about chiropterophilous
bromeliads from an extensive review of the avail-
able literature, as well as common scientificdata-
bases including ISI Web of Science, SciELO and
Redalyc and internet search engines such as
Google Scholar, using operators such as ‘chirop-
terophily’and ‘bromeliads’or ‘Bromeliaceae’;
‘bat-pollination’and ‘Anoura’,‘Glossophaga’
and ‘Lonchophylla’;‘Alcantarea’,‘Encholirium’,
‘Pitcairnia’,‘Puya’,‘Vriesea’and ‘Werauhia’’,
either in the title, keywords or abstract. In addi-
tion, we searched the grey literature (e.g. theses)
and cross-checked references between studies,
including those provided in Fleming et al. (2009)
and Geiselman and Defex (2015), as well as asking
certain authors to suggest publications related to
the topic (see Acknowledgements). Furthermore,
in order to improve our understanding of the
evolution of chiropterophily in the Bromeliaceae,
we constructed a phylogenetic tree for the family,
based on chloroplast (cp) DNA sequence varia-
tion, and used this tree as a means to examine
the origin of chiropterophily in different clades
of the family and to determine which pollination
systems might be ancestral across these clades.
2P. A. AGUILAR-RODRÍGUEZ ET AL.

We summarise and discuss some of the traits
that characterise chiropterophily within brome-
liads, presenting an overview of documented
bat-pollinated species and their geographic distri-
butions. Finally, we highlight some additional
bromeliad species that appear to exhibit the chir-
opterophilous syndrome and which may also
therefore be pollinated by bats.
Studies of bat-pollinated bromeliads
Following early comments about chiropterophi-
lous floral traits in the bromeliad family by Müller
(1897)andPorsch(1932,1934)), initial field
observations were reported by Vogel (1969), with
more detailed studies conducted in the 1990s (e.g.
Martinelli 1994,1997;Sazimaetal.1999).
Bromeliads with apparently chiropterophilous
flowers are most commonly found in wet lowland
forests (Kessler and Krömer 2000;Flemingetal.
2005,2009), where the diversity of flower-visiting
bats is also highest. However, this contrasts with
the diversity of confirmed bat-pollinated brome-
liads, which peaks at high elevations such as in the
humid montane forests of the Andean region
(Benzing 2000;Givnishetal.2011). This apparent
contradiction might be due to sampling bias, with
researchers focusing on few and frequently (or
recurrently) studied regions. Only a handful of
studies cover large study areas or a broad altitudi-
nal range (e.g. Martinelli 1994,1997;Sazimaetal.
1999; Kessler and Krömer 2000;Krömeretal.
2006). Lowland records come from Brazilian
Vriesea (5–500 m asl; Martinelli 1994;1997;
Sazima et al. 1995,1999)andCostaRican
Werauhia (40 m; Tschapka and von Helversen
2007), while records from high altitude have
been obtained from the Bolivian Andes (over
2000 m asl; Kessler and Krömer 2000)andCosta
Rica (3000 m a.s.l.; Salas 1973). Most studies, how-
ever, have been conducted at elevations between
1000 and 1600 m a.s.l. (e.g. Sazima et al. 1989;
Vogel 1969; Martinelli 1997; Kaehler et al. 2005;
Fabián et al. 2008; Aguilar-Rodríguez et al. 2014;
Aguilar-Rodríguez et al. 2016; see Tables S2, S3).
Most reports regarding bromeliads with chir-
opterophilous traits are from species of the sub-
family Tillandsioideae in humid montane forests
(i.e. Aguilar-Rodríguez et al. 2014;Salas 1973;
Ramírez and Seres 1994;Sazimaetal.1995;Seres
and Ramírez 1995; Martinelli 1997;Muchhalaand
Jarrín-V 2002;Krömer2003;Cascante-Marínet
al. 2005; Kaehler et al. 2005;Krömeretal.2005,
2007). Other studies have been conducted in tro-
pical rainforest habitats (e.g.vonHelversen1993;
Martinelli 1994,1997;Sazimaetal.1995,1999;
Tschapka and von Helversen 2007), while some
have taken place on granitic/rocky outcrops, espe-
cially for species of the subfamily Pitcairnioideae
(Fischer 1994; Martinelli 1994;Wendtetal.2001;
Christianini et al. 2013), in deserts (Kessler and
Krömer 2000), the Brazilian ‘cerrado’(Sazima et
al. 1989) and in tropical coastal ‘restinga’and
‘caatinga’(e.g. Fischer 1994;Queirozetal.2016)
habitats.
According to our literature review, bats have
been confirmed as floral visitors for 42 bromeliad
species belonging to four of the eight
Bromeliaceae subfamilies (Table 1). Most reports
suggest that bats are the only probable pollinator
of these bromeliads (Table S2). Bat pollination is
also suggested for a number of additional species
(based on their floral characteristics) and, thus, a
total of more than 100 species of bromeliads from
13 genera and five subfamilies (Tables S2, S3) are
thought to be bat-pollinated. Most of these bro-
meliads belong to the genera Vriesea and
Werauhia of the subfamily Tillandsioideae (see
Table 1. The number of bromelia species confirmedorsuggestedtobebat-pollinated(i.e.withchiropterophilousfloral traits) in the
literature.
Subfamily Genus Confirmed Putative Total
Bromelioideae Billbergia 112
Brocchinioideae Brocchinia 011
Pitcairnioidea Encholirium 505
Pitcairnia 61016
Puyoideae Puya 224
Tillandsioideae Alcantarea 279
Guzmania 01313
Lutheria 101
Pseudalcantarea 303
Stigmatodon 011
Tillandsia 202
Vriesea 13 18 31
Werauhia 72835
Total 42 81 123
PLANT ECOLOGY & DIVERSITY 3

Figure 1), and most (Table S2) are reported to
possess a ‘typical’chiropterophilous flower
(short, wide and large flowers with pale petals;
Figure 1) and are visited mainly by bats of the
genus Anoura, especially at elevations of 1000 m
a.s.l. or higher in tropical montane forests.
However, Alcantarea and Encholirium species
possess less restrictive floral morphologies that
may also allow visits by non-specialised nectari-
vorous bats. The dry and hot environment and the
reduced presence of bats in habitats where these
Alcantarea and Encholirium species occur might
act to promote these more generalist floral fea-
tures. In addition, these species are frequently
locally abundant and may thus serve as an impor-
tant resource for many different flower-visiting
animals, a role analogous to that of the columnar
cacti and Agave in North America (Fleming 2004),
and may therefore receive many secondary polli-
nators or opportunistic floral visitors.
Even if many bromeliad species have the potential
for self-pollination (Matallana et al. 2010:butsee
Encholirium spp.; Christianini et al. 2013;Hmeljevski
et al. 2017), pollinators such as far-ranging bats are
valuable in terms of promoting gene flow among plant
populations (see Vriesea gigantea in Palma-Silva et al.
2009). Such occasional cross-pollination by animal
pollen vectors, including bats, could be important
in terms of mitigating the potential disadvantages
of a reproductive system that is based mainly on
self-pollination (Shivanna and Tandon 2014), as well
as maintaining the boundaries between species
(see Pitcairnia spp. in Palma-Silva et al. 2011).
Nevertheless, Barbará et al. (2007)suggestedthat
Figure 1. Examples of some bat-pollinated bromeliads: (a) Alcantarea imperialis, (b) Billbergia horrida, (c) Encholirium spectabile,
(d) Pitcairnia albiflos, (e) Pitcairnia recurvata, (f) Tillandsia heterophylla, (g) Puya ferruginea, (h) Vriesea longiscapa, (i), Werauhia cf.
sanguinolenta visited by Lonchophylla robusta. Note the pale-colored corolla in all species, and the predominance of the cup-like
floral morphology in the members of the Tillandsioideae subfamily (e, f, h, i). Photos: A, C, D, H: Elton M. C. Leme. B: Ana Paula
G. Faria. E, F, I, J: Pedro A. Aguilar-Rodríguez. G: Thorsten Krömer. I: Marco Tschapka.
4P. A. AGUILAR-RODRÍGUEZ ET AL.

pollinators of Alcantarea imperialis (which probably
include Anoura caudifer and Artibeus lituratus;
Martinelli 1994)arelikelytobeinsufficient in number
to maintain connectivity among populations of this
species in the Brazilian ‘inselbergs’,havingfound
that such populations were highly differentiated
genetically. However, further studies are required to
confirm this hypothesis. In species that produce many
flowers per day, for example Alcantarea spp., foraging
bats might promote geitonogamy over allogamy. This,
in addition to short pollen movement distances
between individuals within populations (see discussion
in Hmeljevski et al. 2017)couldleadtoacertainlevelof
inbreeding.
Evolution of bat-pollinated bromeliads
The Bromeliaceae originated in South America in
the Guiana shield region over 70–100 million years
ago (mya) (Givnish et al. 2007,2011), but extant
lineages did not appear until 15–19 mya. This
coincides with the origin of epiphytism in the
family and the rise of the Andean mountain
chain (Barfuss et al. 2005; Givnish et al. 2007)in
the so-called ‘bromeliad revolution’(ca. 15 mya),
when the family spread to other parts of tropical
and subtropical America, such as the Northern
Andes and Central America (Givnish et al. 2014).
Our understanding of the phylogeny of the
Bromeliaceae has changed repeatedly over the last
two decades, revealing that some groups formerly
defined by floral morphology and habit are in fact
paraphyletic (e.g. Terry et al. 1997; ; Barfuss et al.
2005; Givnish et al. 2007,2011,2014; Escobedo-
Sarti et al. 2013; see the revision in Palma-Silva et
al. 2016). However, the monophyly of
Bromeliaceae has been commonly accepted on the
basis of morphological, anatomical and molecular
characters (Gilmartin and Brown 1987; Crayn et al.
2004; Givnish et al. 2004,2007).
The ancestral pollination mode of bromeliads
seems to be entomophily, but ornithophilous flow-
ers evolved independently on two occasions: first in
the ancestral Tillandsioideae (ca. 15.4 mya)
and secondly, in the common ancestor of
Bromelioideae/Pitcairnioideae/Puyoideae (ca. 14.4
mya; Givnish et al. 2007,2014).
Within the family, there are more bromeliads with
ornithophilous than with chiropterophilous charac-
ters (60–80% vs.10–20%; see Martinelli 1994,1997;
Sazima et al. 1999; Kessler and Krömer 2000; Araujo
et al. 2004). The characters of bird pollination include
red floral bracts, showy but small flowers and anthers,
a tube-like purple or yellow corolla and diurnal
anthesis. Ornithophily seems to be the main pollina-
tion mode within all genera, including the allegedly
chiropterophilous bromeliads (Givnish et al. 2014;
Figure 2), except for the genera Encholirium
(Givnish et al. 2007;butseeEncholirium heloisae;
Christianini et al. 2013)andWerauhia (Grant
1995). The clades comprising the hummingbird-pol-
linated species are three to five times richer in species.
Ornithophilous bromeliad lineages have higher
rates of diversification than species that possess floral
traits associated with other syndromes, as demon-
strated by Givnish et al. (2014). This might be a result
of the synergy between 1) the occurrence in humid
montane habitats, which 2) favours epiphytism, and
3) having a water-holding ‘tank-like’body (phyto-
telma), all three of which promoted the development
of avian pollination (Givnish et al. 2014).
It is noteworthy that the putative pollination
syndromes of bromeliad species included in phy-
logenetic analyses are not always mentioned (see
Givnish et al. 2014 as an exception), and where
they are, most species are reported as bird-polli-
nated, leading to a deficit of species with other
pollination syndromes.
To examine the evolution of chiropterophylous
bromeliad species in more detail, we generated a
phylogenetic tree of bromeliads and mapped the
pollination syndromes of these species on to the
tree. For this purpose, we modified the cpDNA
sequence super-matrix used in Escobedo-Sarti et
al. (2013) with additional sequences downloaded
from GenBank and selected a wide spectrum of
bromeliad species with different pollination syn-
dromes, including more chiropterophilous species
(totalling 41) than in previous phylogenetic studies
of the family. All eight subfamilies of Bromeliaceae
(Tillandsioideae, Bromelioideae, Brocchinioideae,
Lindmanioideae, Hechtioideae, Puyoideae,
Navioideae and Pitcairnioidea s.str.) proposed by
Givnish et al. (2007), and which are mainly char-
acterised by molecular data and the morphology of
flowers, fruits and seeds (Givnish et al. 2007,2011),
were represented in the analysis. The final matrix
included 136 taxa and 9049 characters (ca. 6.13%
of gaps, with most taxa having complete sequences
for all cpDNA regions), based on the regions: atpB-
rbcL, ndhF, psbA-trnH, rpl32-trnL, rps16, trnK-
matK and trnL-F (see Table S1 for vouchers of all
sequences). In this matrix, 135 species belong to
the Bromeliaceae, while Rapatea paludosa
(Rapateaceae) was selected as an outgroup (see
Givnish et al. 2007,2011,2014).
PLANT ECOLOGY & DIVERSITY 5

We aligned sequences of the regions using Muscle
(Edgar 2004)andanalysedthedatawithJModelTest
2.7.1 in order to estimate the evolutionary model
(Darriba et al. 2012). The best-fitting model for the
regions was GTR+I + G. We concatenated the data in
a supermatrix that was analysed in GARLI (Zwickl
2006) on the CIPRES Science Gateway platform
(Miller et al. 2010). We used independent models
among regions, and additionally used the phyloge-
netic tree of Escobedo-Sarti et al. (2013)todefine
topological constraints, assuming an accurate topol-
ogy that would reflect the phylogeny of bromeliads.
Pollination syndromes of bromeliad species
according to the literature, and our field observations,
were coded as follows: 0, entomophily; 1, ornithoph-
ily; 2, chiropterophily; 3, autogamous; 4, generalist
Figure 2. Phylogenetic tree of bromeliads and their pollination syndromes. Different colours on the nodes indicate different
pollination syndromes (green: entomophily, red: ornithophily, blue: chiropterophily, pink autogamous, yellow: generalist
pollination). Notes: Alcantarea duarteana is not mentioned in the literature as bat-pollinated, but we consider that it possible
is; however, since Siqueira Filho (2003) suggested also moth-pollination within the genus, we provisionally refer to it as bimodal.
Tillandsia malzinei is referred as a species with chiropterophilous flowers; it was considered a member of the former Vriesea
subg. Xiphion (currently, the accepted name would be sect. Synandra; see Barfuss et al. 2016). We describe Tillandsia
heterophylla with a bimodal pollination syndrome since diurnal floral visitors could serve as pollinators, even if most of the
visits are by bats (Aguilar-Rodríguez et al. 2016). The form of Pitcairnia flammea represented in this figure with chiropter-
ophilous floral traits refers only to P. flammea var. pallida.
6P. A. AGUILAR-RODRÍGUEZ ET AL.

pollination (species with two or more complementary
pollinators from different functional groups; see
Schmid et al. 2011; Aguilar-Rodríguez et al. 2016).
We used this information to assemble a character
matrix and selected the most appropriate evolution-
ary model for pollination syndrome, based on this
matrix and the ML tree obtained with GARLI, as well
as the Geiger package and APE (Paradis et al. 2004;
Harmon et al. 2008), implemented in R (R Core Team
2016). The test consisted of calculating the plausibility
of all of the evolutionary models available in Geiger.
Based on the Akaike Information Criterion (AIC),
we then identified the Automatic Relevance
Determination regression (ARD) model to present
the best fit, before reconstructing ancestral characters
with more plausibility and the ARD model.
Our phylogenetic tree (Figure 2) strongly suggests
that chiropterophilous floral features have appeared
multiple times from ornithophilous ancestors in the
Bromeliaceae, especially within Tillandsioideae.
Thus, all clades of the bromeliads with chiroptero-
philous traits are embedded within groups of
ornithophilous species, and in general, chiroptero-
philous floral traits appear derived from ornithophi-
lous or sphingophilous floral traits (Tschapka and
Dressler 2002; von Helversen and Winter 2003;
Fleming et al. 2009).The transition within plant
families from ornithophilous to chiropterophilous
traits seems to be more common than in the opposite
direction, and also more common than transitions
from other syndromes (e.g.melittophilyorsphin-
gophily) to chiropterophily (van der Niet and
Figure 3. Examples of some bromeliads with diurnal anthesis: A) Alcantarea geniculata, bird-pollinated, B) Aechmea tilland-
sioides, bimodal pollination by birds and insects, probably bees, C) Billbergia issingiana, bird-pollinated, D) Catopsis sessiliflora,
probably entomophilic, E) Pitcairnia ringens, bird-pollinated, F) Puya riparia, probably bird-pollinated, G) Tillandsia multicaulis,
bird-pollinated, H) Tillandsia violacea, bird-pollinated, I) Vriesea platynema, probably bird-pollinated. Note the bright-coloration,
principally red, of the bird-pollinated species, and the tubular shape of the corolla. Photos: A, I: Elton M. C. Leme. B, C, D, F, G, H:
Thorsten Krömer. E: Pedro A. Aguilar-Rodríguez. This image was elaborated by J. Escobedo Sarti, one of the coauthors.
PLANT ECOLOGY & DIVERSITY 7

Johnson 2012;Rosas-Guerreroetal.2014), suggest-
ing that it may constitute an evolutionary ‘dead-end’
(Tripp and Manos 2008). Within the Bromeliaceae,
this transition seems to have occurred independently
in different genera, particularly within the
Tillandsioideae subfamily (Versieux et al. 2012;
Givnish et al. 2014). As a whole, chiropterophilous
flowers have appeared independently many times in
clades with different evolutionary histories; in differ-
ent genera among the ‘core’members of the
Tillandsioideae subfamily, once in the Encholirium
clade, independently in Pitcairnia within the
Pitcairnioideae, and separately in Puya and
Billbergia, each within its own subfamily. However,
it is important to acknowledge that the taxonomy of
this family has proved difficult to resolve (Givnish et
al. 2007;Barfussetal.2016).
Some bat-pollinated bromeliads may use
diurnal visitors as secondary pollinators (see
examples in Billbergia, Encholirium, Guzmania,
Pitcairnia and Tillandsia;Krömer2003;
Christianini et al. 2013; Marques et al. 2015;
Aguilar-Rodríguez et al. 2016;Queirozetal.
2016;SilvaJorgeetal.2018), with humming-
birds being the most frequently reported floral
visitors/secondary pollinators (Table S1). In
many angiosperms, secondary pollinators fre-
quently coincide with the probable ancestral
pollinator group (Rosas-Guerrero et al. 2014),
and this is reflected in our inference that chir-
opterophilous features in bat-pollinated brome-
liads are derived from ornithophilous traits
present in hummingbird-pollinated species.
Changes in the corolla, as well as the time of
anthesis/flower duration, might be important
modifications to restrict hummingbird visits.
However, there is evidence of ‘intermediate’
floral traits in some species, suggesting either
that this transition is ongoing or that this is a
steady state in which different functional groups
of pollinators complement each other in contri-
buting to the reproductive success of the bro-
meliad (e.g. Billbergia horrida, Tillandsia
heterophylla;Marques et al. 2015;Aguilar-
Rodríguez et al. 2016).
The chiropterophilous syndrome within
Bromeliaceae
The comparably recent origin of both Neotropical
nectarivorous bats and bromeliads (Givnish et al.
2007,2011;Bakeretal.2012)indicatesthattherehas
been only a relatively short time span in which to
develop similar, highly specificadaptationstobat-pol-
lination as in other, much older plant families such as
the Asparagaceae (Agave)andCactaceae(Fleminget
al. 2009;Rosas-Guerreroetal.2014). In this section,
we examine the chiropterophilous floral traits present
in bromeliads.
Phenology related to bat visitation
Anthesis in the bat-pollinated bromeliads mainly starts
at dusk, although some species open their flowers
during mid-afternoon (i.e. Encholirium spectabile, E.
vogelii, Tillandsia heterophylla, Vriesea bituminosa
var. bituminosa, V. hydrophora, V. longicaulis, V. long-
iscapa and Werauhia ororiensis;Salas1973;Martinelli
1994,1997;SeresandRamírez1995;Christianinietal.
2013;Aguilar-Rodríguezetal.2016). Duration of
anthesis varies considerably between species; from
the shortest in Pitcairnia (5 to 10 h in P. albiflos and
P. flammea;Martinelli1994;Wendtetal.2001)tothe
longest in Billbergia horrida Regel (24 h; Marques et al.
2015)andEncholirium subsecundum (3 d; Sazima et al.
1989).
The crepuscular anthesis of these species might be
a remnant of ornithophilous ancestors with diurnal
anthesis (except in Pitcairnia recurvata, which opens
flowers late at night, P. A. Aguilar-Rodríguez et al.,
unpublished data). In addition, an extended anthesis
could increase the probability of pollination by other
animals, such as hummingbirds, although these
might not be as effective pollinators as bats
(Christianini et al. 2013; Marques et al. 2015;
Aguilar-Rodríguez et al. 2016;Queirozetal.2016;
Silva Jorge et al. 2018; but see Tschapka and von
Helversen 2007). Hummingbirds, moths and, to a
lesser extent, various species of bees, are often fre-
quent alternative visitors of bat-pollinated brome-
liads (Table S1); however, the timing of visits in
relation to stigma receptivity, and floral morphology
may preclude pollination by bees (Aguilar-Rodríguez
et al. 2014;Christianinietal.2013; Marques et al.
2015; Aguilar-Rodríguez et al. 2016).
Nearly all bat-pollinated bromeliad species studied
present a ‘steady-state’flowering pattern (i.e. each
individual in the population produces one or two
flowers per night, over many days or weeks; sensu
Gentry 1974), with an annual or biannual flowering
period (Martinelli 1997). Two exceptions are
Alcantarea imperialis and Vriesea gigantea with large
inflorescences that open up to 18 and 10 flowers per
day, respectively (Martinelli 1994;Araujoetal.2004).
Another exception, Pitcairnia flammea,exhibitsa
8P. A. AGUILAR-RODRÍGUEZ ET AL.

‘cornucopia’pattern (i.e. various individuals in the
population present many flowers simultaneously,
over a short period of time; Martinelli 1994), while
individuals of E. spectabile may flower over 30 days
with an entire population of E. subsecundum some-
times flowering for three to four months (Sazima et al.
1989).
Sympatric bromeliad species that share polli-
nators may present staggered flowering seasons
to avoid competition for pollinators (Fischer
1994;Araujoetal.2004), while simultaneously
preventing hybridisation. However, this stag-
gered flowering pattern is not present in all bro-
meliad communities (see Martinelli 1997;
García-Franco et al. 2001;Versieuxetal.2012).
Floral morphology
While the flower buds of many Tillandsioideae are
initiated in two opposite rows along the inflorescence,
they undergo reorientation during ontogeny to face
the same direction at anthesis (e.g. Werauhia spp.),
thus allowing a bat to visit the inflorescence over
several days always from the same direction. Most
bat-pollinated bromeliads have pale yellow, green,
creamy or white petals, occasionally with a reddish
tint on the calyx, for example some species of
Alcantarea and Vriesea (Martinelli 1994,1997;
Sazima et al. 1999;MouraandCosta2014;Versieux
and Wanderley 2015). At least four distinct flower
shapes can be distinguished among such bromeliads:
i) the zygomorphic tube-type of some Billbergia,
Vriesea, Pitcairnia and Puya species (Sazima et al.
1999;KesslerandKrömer2000;SchmidH2000;
Kowalski and Tardivo 2015;Macías-Rodríguezetal.
2007;ScultoriDaSilva2009;Figure 1(b,c,g)); ii) the
zygomorphic bell-shape type present in Vriesea and
Werauhia and even Tillandsia (Utley 1983;Grant
1995;Leme1995;TschapkaandvonHelversen2007;
Figure 1(f,h,i)); iii) the heliciform actinomorphic
flower with strap-like petals and protruding stamens
in Alcantarea and Pseudalcantarea (Martinelli 1994;
Krömer et al. 2012;Versieuxetal.2012;Aguilar-
Rodríguez et al. 2014;Figure 1(a)); and iv) the brush-
type flower of Encholirium (Sazima et al. 1989;
Christianini et al. 2013;Queirozetal.2016;Gomes
et al. 2018;Figure 1(c);butseeEncholirium horridum
in Hmeljevski et al. 2017).
These distinct flower shapes could be related to
intrinsic differences in the floral morphology
between subfamilies and genera (but see the simi-
larities between flowers in Alcantarea,
Pseudalcantarea, Tillandsia baliophylla and T.
paniculata; Beaman and Judd 1996; Barfuss et al.
2016). Ornithophilous bromeliads share several
floral features with chiropterophilous species, and
the latter pollination syndrome may have evolved
quite easily from the former, as indicated by several
evolutionary shifts observed among other species
(van der Niet and Johnson 2012) (see also exam-
ples among the genus Alcantarea; Versieux et al.
2012).
Floral morphology plays an important role in pol-
len placement on the body of the bat,and in reducing
the amount of pollen wasted on heterospecificstig-
mas (Stewart and Dudash 2017). In most species of
Vriesea and Werauhia, the anthers are positioned on
the dorsal or ventral side of the corolla, but in some
species, such as Vriesea gigantea and V. limae,orin
Stigmatodon spp., the anthers are radially or laterally
oriented (von Helversen 1993;Sazimaetal.1995;
Siqueira Filho 2003). One important difference
between diurnal and chiropterophilous bromeliad
species is that the former present tubular corollas
with stamens arranged in a bundle around the centre
of the flower such that pollen is deposited on the beak
of perching and hovering birds; in contrast, chirop-
terophilous species have larger, broader, cup-like and
generally quite open flowers with stamens spreading
from the centre. Stamen position during anthesis is
an important floral trait that separates chiropterophi-
lous from ornithophilous Alcantarea species (spread-
ing vs. bundle forming; Versieux et al. 2012). The
model of Muchhala (2007)suggeststhatwidercor-
ollas would be selected in flowering species where
bats conduct more than 44% of all visits, in order to
match the bat morphology and reduce pollen waste
by hummingbirds. This might apply to flowers of
Werauhia (Tschapka and von Helversen 2007)and
even to the spirally twisted petals of P. macropetala.
In the latter species, the petals form an open corolla,
in which only a bat can contact both the exerted
anthers and the stigma simultaneously during a visit
to the flower, while hummingbirds fail to do this due
to their visitation behaviour and because of changes
to floral parts following anthesis, for example the
stigma pointing downwards due to turgor loss in
the style, so the hummingbird does not come into
direct contact with it (Aguilar-Rodríguez et al. 2014).
Pollen of bell-shaped chiropterophilous bromeliad
flowers, for example in Werauhia and Vriesea,is
placed on the head of the bat (Figure 1(k)), while in
actinomorphic helicoiform flowers, such as in
Pseudalcantarea macropetala, it is deposited on the
ventral side of the wings (Aguilar-Rodríguez et al.
2014).
PLANT ECOLOGY & DIVERSITY 9

The position of the stigma below the anthers and
facing downwards in some Vriesea and Werauhia
species might allow the stigma to make contact with
the bat fur before it reaches the anthers, thus favour-
ing outcrossing when the flower is fully opened, in
spite of self-compatibility (Salas 1973).
Nectar characteristics
Nectar is one of the main rewards offered to
flower-visiting bats in the Neotropics, with the
nectar of bat-pollinated species possessing charac-
teristics that distinguish it from that provided by
plant species to other floral visitors ((von
Helversen and Winter 2003), see also Mosti et al.
2013 for information about nectar secretion in
bromeliads). In fact, some of the most robust evi-
dence for bat-pollination in bromeliads is based on
the particular characteristics of nectar. The
sucrose/hexose ratio of various bromeliad species
studied by Krömer et al. (2008) indicated that the
nectar of chiropterophilous species is hexose-rich,
leading them to suggest that some Bolivian
Guzmania species which produce hexose-rich nec-
tar are bat-pollinated, even though they present
brightly-coloured floral bracts more often asso-
ciated with bird-pollinated species. Many brome-
liads with chiropterophilous floral traits within
Tillandsioideae show tank-forming rosettes, in
which water and detritus are collected. Givnish et
al. (2014) suggested that the tank-habit might ori-
ginally have favoured ornithophily, since the
water-filled tanks may facilitate the production of
relatively large amounts of nectar. However, the
same reasoning holds true for chiropterophilous
species since nectarivorous bats require an even
higher amount of nectar than hummingbirds
(Tschapka and Dressler 2002). Nectar volume var-
ies widely among chiropterophilous bromeliads
species (Table S1, Table S2), ranging from 4 µl in
Encholirium vogelli (Christianini et al. 2013)to
1129 µl in W. gladioliflora (Tschapka and von
Helversen 2007). Moreover, sugar concentration
ranges from 4% in Encholirium subsecundum
(Sazima et al. 1989) to 21% in Vriesea atra var.
atra (Fischer 1994). This high variability in nectar
volume and constituency could, at least partly, be
attributed to the different methodologies used in
different studies. For example, measurement of
accumulated nectar over the entire life of the
flower vs. standing crop measurements (Corbet
2003). Furthermore, there is interplant variation
of nectar traits (e.g. Hodges 1993) and
environmental factors may also affect nectar mea-
surements (Jakobsen and Kritjánsson 1994;
Willmer 2011). Another explanation could be that
the rather short evolutionary time span of the
mutualism between bats and bromeliads may not
yet have allowed the development of a clear nectar
production pattern (Rodríguez-Peña et al. 2016).
In general, bat-pollinated bromeliads present lower
nectar volumes and sugar concentrations than other
bat-pollinated plants (Tschapka and Dressler 2002;
Fleming et al. 2009). The study of Krömer et al.
(2008)showedthatchiropterophilousspecieshadthe
lowest sugar concentration of all bromeliads studied
(11.5 ± 4.0%; but see W. gladioliflora;T
schapka and
von Helversen 2007). The low nectar sugar concentra-
tion in bat-pollinated bromeliads (Table S1) might
require visitors to consume rather high quantities of
nectar to meet their energetic needs (von Helversen
and Reyer 1984), thus necessitating an increased num-
ber of flower visits. More dilute nectar may evolve
when competition for food among bats is higher
(Nachev et al. 2017), but we still lack sufficient infor-
mation to confirm this hypothesis.
Floral scent
Floral scent probably serves as a long-distance
attractant for bats, but will also aid close-range
location of flowers (von Helversen et al. 2000;
Gonzalez-Terrazas et al. 2016). Many authors
report that chiropterophilous bromeliads present
a characteristic floral scent described as ‘musky’
or garlic-like (Table S1, Table S2). However, to
date, the scent volatiles of only two species of
bat-pollinated bromeliads have been identified: in
Werauhia gladioliflora (Bestmann et al. 1997) and
Pseudalcantarea macropetala (Aguilar-Rodríguez
et al. 2014). In the former, dimethyl disulphide
was present, a volatile that is innately attractive to
New World nectarivorous bats (von Helversen et
al. 2000). Sulphur-containing compounds are com-
mon in the scent of chiropterophilous plants, but
not omnipresent (Knudsen and Tollsten 1995).
Thus, in the case of P. macropetala, no sulphur-
containing volatiles were found. It is possible that
this specific attractant has evolved in Werauhia,a
genus highly specialised in bat-pollination, but not
yet in P. macropetala. The volatiles identified from
13 species of different Bromeliaceae genera of all
pollination syndromes are highly variable, even
within the same genus (Hilo de Souza et al.
2016), and some of the volatile compounds
detected in these diurnally flowering species are
10 P. A. AGUILAR-RODRÍGUEZ ET AL.

shared with those identified for W. gladioliflora by
Bestmann et al. (1997) and P. macropetala in
Aguilar-Rodríguez et al. (2014).
Acoustic signals
A study by von Helversen et al. (2003) has sug-
gested that W. gladioliflora might have flowers with
special echo-reflecting properties. Unlike other
bromeliads, W. gladioliflora presents flowers that
are largely embedded within the stalk of the inflor-
escence, covered by bracts, and only exposed when
fully opened. The only section protruding from the
stalk is the distal portion of the corolla, as well as
the stamens and stigma. The cup-like corolla of
Werauhia could produce a distinctive echo that
might help a bat investigate the inflorescence and
locate the flower entrance (von Helversen et al.
2003).
Characteristics of bats visiting bromeliads
The bat family Phyllostomidae of New World Leaf-
nosed bats originated about 30.3 mya (Rojas et al.
2016). Nectarivorous feeding habits evolved twice
within the family (Baker et al. 2012;Tschapkaetal.
2015); firstly, around 21.55 mya (23.4–19.7; subfamily
Glossophaginae) and secondly around 11.13 mya
(11.4–10.9; subfamily Lonchophyllinae) in South
America, with the exception of some genera
(Brachyphylla, Erophylla, Phyllonycteris, Monophyllus,
Leptonycteris and Glossophaga;Rojasetal.2016)that
originated in the Antilles. The oldest fossil of a
Neotropical nectarivorous bat is from Palynephyllum
antimaster (about 12–13 mya; Morgan and Czaplewki
2012)andthemajorityofextantnectarivorousbat
genera originated around 10–5mya(Rojasetal.
2016). There is evidence of the presence of Anoura
in the Peruvian Andes dating from the Pleistocene
(at least 2.5 mya; Shockey et al. 2009). Thus, specialised
nectarivorous bats occurred at the same time and
location as the ‘bromeliad revolution’,withmostof
the extant nectarivorous genera already present by the
time of the origin of some bromeliad genera such as
Encholirium, Pseudalcantarea and Werauhia (Givnish
et al. 2014).
The Andean region is particularly important for
species diversity of genera comprising bat-pollinated
bromeliads, as well as for the bat genus Anoura
(Patterson et al. 1996;Muchhalaetal.2008;
Mantilla-Meluk et al. 2009;Shockeyetal.2009;
Mantilla-Meluk and Baker 2010). This bat genus
diversified over the last 10 mya or less (Rojas et al.
2011)andcomprisesthe‘core’species of the nectar-
ivorous bat guild at higher elevations (Fleming et al.
2005;Morasetal.2013), as well as being the bat genus
most frequently reported to visit bromeliads (Table
S1). In addition to other characteristics (i.e. long
dense fur, reduced uropatagium, hairy feet and toes,
small ears and a higher body mass than the lowland
nectarivorous bats; Soriano et al. 2002), the basal
metabolic rate of most Anoura species (Figure 4(a,b))
reflects their tolerance to lower environmental tem-
peratures (Ortega-García et al. 2017;butseeAnoura
caudifer in the lowland of the Amazonian region) and
allows them to remain active during cold nights at
high elevations. This might be the reason for the
frequent reports of members of this bat genus as floral
visitors of bromeliads at high elevations. In contrast, at
low elevations in Mexico and Central America, the
‘core’nectarivorous bat-fauna is formed by the genus
Glossophaga (Fleming et al. 2005,2009), as shown by
studies carried out in Costa Rica on W. gladioliflora
(Tschapka 2004;TschapkaandvonHelversen2007).
To date, a total of 19 species from ten phyllostomid
genera have been recorded visiting bromeliad flowers
(Table S1), 15 of which belong to the specialised
nectarivorous subfamilies Glossophaginae and
Lonchophyllinae: Anoura (4 spp.), Glossophaga (2
spp.), Hylonycteris (1 sp.), Lichonycteris (1 sp.),
Lonchophylla (5 spp.), Platalina (1 sp.) and
Xeronycteris (1 sp.) (Figure 4). Furthermore, three
frugivorous species from the subfamily
Stenodermatinae are reported: Artibeus lituratus and
Pygoderma bilabiatum,visitingbromeliadswithopen
or brush-like corollas (Alcantarea imperialis, A. regina,
Vriesea bituminosa var. bituminosa and V. hoehneana;
Martinelli 1994;Kaehleretal.2005); and Carollia
perspicillata visiting the ‘tube-like’flower of
Pitcairnia paniculata (Maguiña et al. 2012). In addi-
tion, Phyllostomus discolor from the Phyllostominae
subfamily visits and pollinates flowers of Encholirium
spectabile (Queiroz et al. 2016).
It has been proposed that bats re-visit flowers over
the course of the night in a behaviour known as ‘trap-
lining’(sensu Janzen 1971;vonHelversen1993;
Fleming et al. 2009). Almost all authors who observed
bat visits to bromeliads have suggested the occurrence
of such a foraging mode; however, no study to date has
experimentally confirmed this behaviour. The dura-
tion of the actual flower visit is extremely short (less
than one second; Aguilar-Rodríguez et al. 2014;
Sazima et al. 1995;Wendtetal.2001;Tschapkaand
von Helversen 2007)andthebatsusuallyinserttheir
head into the corolla or lap the nectar directly from the
inflorescence (as in Encholirium;Sazimaetal.1989).
PLANT ECOLOGY & DIVERSITY 11

Some non-glossophagine bats, such as P. discolor
(Queiroz et al. 2016;andseealsoreportsoffrugivor-
ous bats in; Martinelli 1994,1997), cannot forage for
nectar during hovering-flight, and instead perch
upside down from the inflorescence to gain access.
High plant abundance and high nectar produc-
tion make bromeliads an important resource for
bats, birds and insects (Howell and Burch 1974;
Siqueira Filho 2003; Maguiña Conde 2016;
Maguiña and Amanzo 2016; Morales 2016;
Cordero-Schmidt et al. 2017). In the Maquiné
river valley in Brazil, Anoura caudifer were found
to feed on an unidentified Vriesea species for six
months, accounting for over 50% of their total diet
during the austral summer and almost 18% of their
diet over the course of the year (Barros et al. 2013).
Due to the local high abundance of Werauhia
gladioliflora and its high nectar volume, the energy
density offered by this plant in Costa Rica reaches
up to 349.3 kJ/ha/day during the peak flowering
season, thus constituting one of the most efficient
foraging options for bats (Tschapka 2004). Up to
28% of the chiropterophilous plants found within
the home ranges of Glossophaga commissarisi in
Costa Rica were W. gladioliflora, making it the
most important plant resource for this bat
(Rothenwöhrer et al. 2011).
Conclusions and future directions
Chiropterophily has evolved in different lineages of the
Bromeliaceae family, with evidence for convergent
evolution occurring across different phylogenetic
clades. Key traits of chiropterophily, such as nocturnal
anthesis and the length of floral structures, allow bats
to act as the principal or occasionally the secondary
Figure 4. Bats identified as pollinators of Bromeliaceae: (a) Anoura caudifer (Glossophaginae subfamily), (b) Anoura geoffroyi
(Glossophaginae), (c) Glossophaga commissarisi (Glossophaginae), (d) Glossophaga soricina (Glossophaginae), (e) Hylonycteris
underwoodi (Glossophaginae), (f) Lichonycteris obscura (Glossophaginae), (g) Lonchophylla bokermanni (Lonchophyllinae), (h)
Artibeus lituratus (Stenodermatinae), (i) Pygoderma bilabiatum (Stenodermatinae), (j) Phyllostomus discolor (Phyllostominae).
Photographic credits: A, B, C, D, E, F, H: Marco Tschapka. G, I: Lena Geise. J: Pedro A. Aguilar-Rodríguez.
12 P. A. AGUILAR-RODRÍGUEZ ET AL.

pollinator of chiropterophilous species (Rosas-
Guerrero et al. 2014); however, most studies of such
species have not specifically evaluated the contribu-
tions of other floral visitors in terms of pollination
success. The short evolutionary time span of the bat-
bromeliad interaction has probably led to the main-
tenance of some ‘generalist’floral characteristics that
currently correspond to a bimodal pollination system
between primarily nocturnal and diurnal pollinators.
In a few clades, more specialised flowers seem to have
evolved relatively rapidly; for example, in Werauhia,
possibly the most specialised bat-pollinated genus in
the family, which is only ca.5mya(Givnishetal.2014).
Bat visitation has been reported in more than 40
species from four of the eight recognised bromeliad
subfamilies. Some bat-pollinated species may have
been overlooked in other subfamilies or presumed
to be moth-pollinated (Gardner 1986;Rauh1986,
1987,1990; Aguilar-Rodríguez et al. 2016). Only 24
(35%) of the references presented in Table S1 actually
represent in-depth studies on the reproductive biol-
ogy of Bromeliaceae. Of these, only seven (10%) were
conducted during the last 10 years, but even this
relatively small number of studies yielded five chir-
opterophilic species previously unreported in the
literature. This emphasises the importance of field-
work for determining the extent of the distribution of
this pollination syndrome within the family.
Pollination by vertebrates is considered to be an
important driver of speciation within the
Bromeliaceae (Givnish et al. 2014) and nectar-feed-
ing bats may therefore have played a significant role
in the origin of some species, although this remains
to be investigated in detail. The genus Werauhia,
with 92 species (Gouda et al. 2017), seems to be
particularly well adapted to bat pollination, (see also
Utley, 1983; von Helversen and von Helversen, 1975)
and offers interesting options for comparisons
between species from differing regions, elevations
and morphology; currently, detailed information on
the pollination system is only available for Werauhia
gladioliflora. In addition, the speciose genus
Stigmatodon, formerly included in Vriesea, shows
floral characteristics, including nocturnal anthesis,
pale and greenish petals and musty scent (Barfuss et
al. 2016), which suggest that all of its 18 species might
be bat-pollinated, although supporting field evidence
to date is limited.
As is the case with almost all plant-pollinator
interactions, only scarce information exists regard-
ing the contribution of bats to genetic population
structure within bromeliad species (i.e. Wendt et
al. 2002; Barbará et al. 2007; Paggi et al., 2007;
Lexer et al. 2016) or even their role in hybridisation
between species sharing habitats or pollinators
(Wendt et al. 2001; Palma-Silva et al. 2011;
Versieux et al. 2012; Queiroz et al., 2015). The
effect of pollinators on species cohesion could be
particularly important considering the lack of other
prezygotic reproductive barriers among many bro-
meliad species (Wendt et al. 2008, but see also
Matallana et al. 2016).
The presence of bat pollination among species
of the Bromeliaceae family is associated with envir-
onmental conditions and elevation (Kessler and
Krömer 2000 ; Kessler 2002) and most of the
reported species are epiphytic or lithophytic.
Borges et al. (2016), suggest that plant families
living in habitats with low water availability are
more likely to develop crepuscular or nocturnal
anthesis as a strategy to reduce nectar loss through
evaporation. In addition, species living in arid
regions (including Encholirium and Puya) and epi-
phytic species grow under environmental water
stress (Ruzana Adibah and Ainuddin 2011). In
this context, future work should focus on whether
high altitude and precipitation are truly associated
with pollination by bats among epiphytic species,
and whether drier environmental conditions
favour bat pollination in large bromeliad species
such as those of the genera Alcantarea and
Encholirium.
In order to understand the role of bat pollination in
abromeliadspeciesvisitedbyseveralpollinatorsover
its geographical distribution, it is important to quan-
tify the relative contribution of each pollinator species
to reproduction within local populations. If a brome-
liad flower has extended anthesis, lasting from after-
noon until early morning, it may be visited by animals
other than or in addition to bats. With regard to
nectar-feeding bats, different species may carry a spe-
cies-specificpollenload(Kingetal.2013)anddissim-
ilarities in size and behaviour might result in
differences in the relative contributions of each species
to seed set, and thus may ultimately modify the breed-
ing system of the species. There are bromeliad species
that seem to be self-incompatible and therefore
depend on pollinators for reproduction (e.g.
Encholirium spp.; Christianini et al. 2013;Hmeljevski
et al. 2017), while others are self-compatible and even
capable of autonomous self-pollination (T. hetero-
phylla;Aguilar-Rodríguezetal.2016,W. gladioliflora,
Tschapka and von Helversen 2007).
Finally, it is to be emphasised that the interaction
between bromeliads and nectar-feeding bats presents
amultitudeofinterestingecologicaland
PLANT ECOLOGY & DIVERSITY 13

evolutionary aspects, ranging from pollinator beha-
viour to local adaptations and population genetic
consequences. Bromeliad species occur in different
habitats all over the Neotropics, in high numbers and
often large population sizes. These characteristics
allow interesting studies that will help further our
understanding of wider patterns and ecological roles
within different habitats as well as the evolutionary
relationships that exist within the bromeliad family.
Acknowledgements
We are grateful to Marlies Sazima, Elton M. C. Leme, Stefan
Vogel, Michael Barfuss, Leonardo M. Versieux, Gustavo
Martinelli, Andrea Araujo, Marília Barros, Ana Paula Gelli
de Faria, Karina Hmeljevski, Leandro Freitas, Eric Gouda and
Lena Geise for providing information and references men-
tioned in this work, comments in the main text and about
bromeliad systematics, as well as some photos of Brazilian
bromeliads and bats. We thank Lilia Ruiz for preparing the
photo plates. We thank Keith MacMillan and six anonymous
reviewers to help improve this manuscript. This study was
funded by a CONACyT grant awarded to PAAR (No. 59406).
Disclosure statement
No potential conflict of interest was reported by the
authors.
Funding
This work was supported by the Consejo Nacional de
Ciencia y Tecnología (CONACyT) by the grant number
59406 awarded to P.A.A.-R.
Notes on contributors
Pedro A. Aguilar-Rodríguez recently completed his Ph.D.
on chiropterophilous bromeliads in Mexico.
Thorsten Krömer studies the diversity, distribution and
ecology of epiphytic plants and their conservation in tro-
pical montane forests.
Marco Tschapka studies the interactions between
Neotropical bats and their food plants, especially the role
of bats in pollination and resource partitioning among
nectarivorous bats.
José G. García-Franco is interested in the ecology of epi-
phytic and parasitic vascular plants, their reproduction,
host specificity and the biotic and abiotic factors that the
distribution of these plants is related to.
Jeanett Escobedo-Sarti studies plant-animal interactions in
relation to reproductive biology of selected taxa. She is also
interested in the evolution of key phylogenetic traits of
epiphytic plants, including bromeliads.
M.Cristina MacSwiney G. studies the ecology of bats and
rodents. She is interested in the composition of bat assem-
blage in different tropical habitats.
ORCID
Thorsten Krömer http://orcid.org/0000-0002-1398-8172
Marco Tschapka http://orcid.org/0000-0002-1398-8172
M.Cristina MacSwiney G. http://orcid.org/0000-0002-
9007-4622
References
Aguilar-Rodríguez PA, Krömer T, García-Franco JG,
MacSwiney GMC. 2016. From dusk till dawn: nocturnal
and diurnal pollination in the epiphyte Tillandsia hetero-
phylla (Bromeliaceae). Plant Biol. 18:37–45.
Aguilar-Rodríguez PA, MacSwiney GMC, Krömer T,
García-Franco JG, Knauer A, Kessler M. 2014. First
record on bat-pollination in the species-rich genus
Tillandsia (Bromeliaceae). Ann Bot. 113:1047–1055.
Araujo AC, Fischer E, Sazima M. 2004. As Bromélias na
região do Rio Verde. In: Marques O, Duleba W, editors.
Estação Ecológica Juréia-Itatins: ambiente físico, flora e
fauna. Ribeirão Preto: Holos; p. 162–171.
Ashworth L, Aguilar R, Martén-Rodríguez S,
Lopezaraiza-Mikel M, Avila-Sakar G, Rosas-Guerrero
V, Quesada M. 2015. Pollination syndromes: A global
pattern of convergent evolution driven by the most
effective pollinator. In: Pontarotti P, editor.
Evolutionary biology: biodiversification from genotype
to phenotype. Switzerland: Springer International
Publishing; p. 203–224.
Baker RJ, Bininda-Emonds ORP, Mantilla-Meluk H, Porter
CA, Van Den Bussche RA. 2012.Moleculartimescaleof
diversification of feeding strategy and morphology in New
World leaf-nosed bats (Phyllostomidae): A phylogenetic
perspective. In: Gunnell GF, Simmons NB, editors.
Evolutionary history of bats: fossils, molecules and morphol-
ogy. Cambridge: Cambridge University Press; p. 385–409.
Barbará T, Martinelli G, Fay MF, Mayo SJ, Lexer C. 2007.
Population differentiation and species cohesion in two
closely related plants adapted to Neotropical high-alti-
tude ‘inselbergs’,Alcantarea imperialis and Alcantarea
geniculata (Bromeliaceae). Mol Ecol. 16:1981–1992.
Barfuss M, Samuel MR, Till W, Stuessy TF. 2005.
Phylogenetic relationships in subfamily Tillandsioideae
(Bromeliaceae) based on DNA sequence data from seven
plastid regions. Am J Bot. 92:337–351.
Barfuss MHJ, Till W, Leme EMC, Pinzón JP, Manzanares
JM, Halbritter H, Samuel R, Brown GK. 2016.
Taxonomic revision of Bromeliaceae subfam.
Tillandsioideae based on a multi-locus DNA sequence
phylogeny and morphology. Phytotaxa. 279:001–097.
Barros MAS, Rui AM, Fabián ME. 2013. Seasonal variation
in the diet of Anoura caudifer (Phyllostomidae:
Glossophagine) at the Southern limit of its geographic
range. Acta Chiropterologica. 15:77–84.
14 P. A. AGUILAR-RODRÍGUEZ ET AL.

Beaman RS, Judd WS. 1996.SystematicsofTillandsia sub-
genus Pseudoalcantarea (Bromeliaceae). Brittonia. 48:1–19.
Benzing DH. 2000. Bromeliaceae. Profile of an adaptive
radiation. Cambridge: Cambridge University Press.
Bestmann HJ, Winkler L, von Helversen O. 1997.
Headspace analysis of volatile flower scent constituents
of bat-pollinated plants. Phytochemistry. 46:1169–1172.
Bolzan DP, Pessôa LM, Peracchi AL, Strauss RE. 2015.
Allometric patterns and evolution in Neotropical nec-
tar-feeding bats (Chiroptera, Phyllostomidae). Acta
Chiropterologica. 17:59–73.
Borges RM, Somanathan H, Kelber A. 2016. Patterns and
processes in nocturnal and crepuscular pollination ser-
vices. Q Rev Biol. 91:389–418.
Burck W. 1892. Wandelingen door den Botanischen Tuin.
T Treub’s Lands Plantentuin te Buitenzorg. Leipzig:
Batavia.
Canela MBF, Sazima M. 2005.ThepollinationofBromelia
antiacantha (Bromeliaceae) in Southeastern Brazil: ornitho-
philous versus melittophilous features. Plant Biol. 7:411–416.
Cascante-Marín A, Oostermeijer JGB, Wolf JHD, Dennijs
JCM. 2005. Reproductive biology of the epiphytic bro-
meliad Werauhia gladioliflora in a premontane tropical
forest. Plant Biol. 7:203–209.
Christianini AV, Forzza RC, Buzato S. 2013. Divergence on
floral traits and vertebrate pollinators of two endemic
Encholirium bromeliads. Plant Biol. 15:360–368.
Cirranello A, Simmons NB, Solari S, Baker RJ. 2016.
Morphological diagnoses of higher-level phyllostomid
taxa (Chiroptera: Phyllostomidae). Acta Chiropterologica.
18:39–71.
Corbet S. 2003. Nectar sugar content: estimating standing
crop and secretion rate in the field. Apidologie. 34:1–10.
Cordero-Schmidt E, Barbier E, Vargas-Mena JC, Oliveira
PP, Santos FDAR, Medellín RA, Rodríguez-Herrera B,
Venticinque EM. 2017. Natural history of the Caatinga
endemic Vieira’sflower bat, Xeronycteris vieirai.Acta
Chiropterologica. 19:399–408.
Cox AC. 1984. Chiropterophily and ornithophily in
Freycinetia (Pandanaceae) in Samoa. Plant Syst Evol.
144:277–290.
Crayn DM, Winter K, Smith JAC. 2004. Multiple origins of
crassulacean acid metabolism and the epiphytic habit in
the Neotropical family Bromeliaceae. Proc Nat Acad Sci.
101:3703–3708.
Cunningham SA. 1995. Ecological constraints on fruit
initiation by Calyptrogyne ghiesbreghtiana (Arecaceae):
floral herbivory, pollen availability and visitation by pol-
linating bats. Am J Bot. 82:1527–1536.
Darriba D, Taboada G, Doallo R, Posada D. 2012.
jModelTest 2: more models, new heuristics and parallel
computing. Nat Methods. 9:772.
Dobat K, Peikert-Holle T. 1985. Blüten und Fledermäuse
(Chiropterophilie). Frankfurt: Waldemar Kramer Verlag.
Edgar R. 2004. MUSCLE: multiple sequence alignment
with high accuracy and high throughput. Nucleic Acids
Res. 32:1792–1797.
Escobedo-Sarti J, Ramírez I, Leopardi C, Carnevali G,
Magallón S, Duno R, Mondragón D. 2013. A phylogeny
of Bromeliaceae (Poales, Monocotyledoneae) derived
from an evaluation of nine supertree methods. J Syst
Evol. 51:743–757.
Fabián ME, Rui AM, Waechter JL. 2008.Plantasutilizadas
como alimento por morcegos (Chiroptera, Phyllostomidae)
no Brasil. In: Reis NR, Peracchi AL, Santos GASD, editors.
Ecologia de morcegos. Londrina: Technical Books Editora;
p. 51–70.
Faegri K, van der Pijl L. 1979. The principles of pollination
ecology. Toronto: Pergamon Press.
Fischer EA. 1994. Polinização, fenologia e distribuição
espacial de Bromeliaceae numa comunidade de Mata
Atlântica, Litoral Sul de São Paulo [Master´s Thesis].
São Paulo (Brazil): Universidade Estadual de
Campinas.
Fleming TH. 2004. Nectar corridors: migration and the
annual cycle of lesser long-nosed bats. In: Nabhan GP,
editor. Conserving migratory pollinators and nectar cor-
ridors in western North America. Tucson: University of
Arizona Press; p. 23–42.
Fleming TH, Geiselman C, Kress WJ. 2009. The evolution
of bat pollination: a phylogenetic perspective. Ann Bot.
104:1017–1043.
Fleming TH, Muchhala N. 2008. Nectar-feeding bird and
bat niches in two worlds: pantropical comparisons of
vertebrate pollination systems. J Biogeogr. 35:764–780.
Fleming TH, Muchhala N, Ornelas JF. 2005. New World
nectar-feeding vertebrates: community patterns and pro-
cesses. In: Sánchez-Cordero V, Medellín RA, editors.
Contribuciones mastozoológicas en homenaje a
Bernardo Villa. México City: Instituto de Biología e
Instituto de Ecología-UNAM; p. 161–184.
García-Franco JG, Martínez-Burgoa D, Pérez TM. 2001.
Hummingbird flower mites and Tillandsia spp.
(Bromeliaceae): polyphagy in a cloud forest of
Veracruz, Mexico. Biotropica. 33:538–542.
Gardner CS. 1986. Inferences about pollination in
Tillandsia (Bromeliaceae). Selbyana. 9:76–87.
Geiselman CK, Defex TI. 2015. Bat eco-interactions data-
base. [accessed 2016 Jan 15]. www.batplant.org.
Gentry AH. 1974. Flowering phenology and diversity in
tropical Bignoniaceae. Biotropica. 6:64–68.
Gilmartin AJ, Brown GK. 1987. Bromeliales, related mono-
cots, and resolution of relationships among
Bromeliaceae subfamilies. Syst Botany. 12:493–500.
Givnish TJ, Barfuss M, Van Ee B, Riina R, Schulte K,
Horres R, Gonsiska P, Jabaily R, Crayn D, Smith J, et
al. 2011. Phylogeny, adaptive radiation, and historical
biogeography in Bromeliaceae: insights from an eight-
locus plastid phylogeny. Am J Bot. 98:1–24.
Givnish TJ, Barfuss M, Van Ee B, Riina R, Schulte K,
Horres R, Gonsiska P, Jabaily R, Crayn D, Smith J, et
al. 2014. Adaptive radiation, correlated and contingent
evolution, and net species diversification in
Bromeliaceae. Mol Phylogenet Evol. 71:55–78.
PLANT ECOLOGY & DIVERSITY 15

Givnish TJ, Millam KC, Berry PE, Sytsma KJ. 2007.
Phylogeny, adaptive radiation, and historical biogeogra-
phy of Bromeliaceae inferred from ndhf sequence data.
Aliso. 23:3–26.
Givnish TJ, Millam KC, Evans TM, Hall JC, Pires JC, Berry
PE, Sytsma KJ. 2004. Ancient vicariance or recent long-
distance dispersal? Inferences about phylogeny and
South American-African disjunction in Rapateaceae
and Bromeliaceae based on ndhF sequence data. Int J
Plant Sci. 165:S35–S54.
Gomes LAC, Maas ACS, Godoy MSM, Martins MA, Pedrozo
AR, Peracchi AL. 2018. Ecological considerations on
Xeronycteris vieirai: an endemic bat species from the
Brazilian semiarid macroregion. Mastozoología Neotrop.
25:81–88.
Gonzalez-Terrazas TP, Martel C, Milet-Pinheiro P, Ayasse
M, Kalko EKV, Tschapka M. 2016. Finding flowers in
the dark: nectar-feeding bats integrate olfaction and
echolocation while foraging for nectar. R Soc Open Sci.
3:160199.
Gouda EJ, Butcher D, Gouda CS. 2017. Encyclopedia of
bromeliads, version 3. University botanic gardens,
Utrecht. [accessed 2017 Jan 27]. http://encyclopedia.flor
apix.nl/.
Grant JR. 1995. The resurrection of Alcantarea and
Werauhia, a new genus. Tropische und Subtropische
Pflanzenwelt. 91:7–57.
Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W.
2008. GEIGER: investigating evolutionary radiations.
Bioinformatics. 24:129–131.
Hilo de Souza E, Massarioli AP, Moreno IAM, Souza FVD,
Ledo CAS, Alencar SM, Martinelli AP. 2016. Volatile
compounds profile of Bromeliaceae flowers. Revista de
Biología Tropical. 64:1101–1116.
Hmeljevski K, Wolowski M, Forzza R, Freitas L. 2017. High
outcrossing rates and short-distance pollination in a
species restricted to granitic inselbergs. Aus J Bot.
65:315–326.
Hodges SA. 1993. Consistent interplant variation in nectar
characteristics of Mirabilis multiflora. Ecology. 74:542–
548.
Hornung-Leoni C, Sosa V. 2006. Morphological variation
in Puya (Bromeliaceae): an allometric study. Plant Syst
Evol. 256:35–53.
Howell DJ, Burch D. 1974. Food habits of some Costa
Rican bats. Rev Biol Trop. 21:281–294.
Jakobsen HB, Kritjánsson K. 1994.Influence of tempera-
ture and floret age on nectar secretion in Trifolium
repens L. Ann Bot. 74:327–334.
Janzen DH. 1971. Euglossine bees as long distance pollina-
tors of tropical plants. Science. 171:203–205.
Kaehler M, Varassin IG, Goldenberg R. 2005. Polinização
em uma comunidade de bromélias em floresta atlântica
alto-montana no estado do Paraná, Brasil. Braz J Bot.
28:219–228.
Kessler M. 2002. Environmental patterns and ecological
correlates of range size among bromeliad communities
of Andean forest in Bolivia. Botl Rev. 68:100–127.
Kessler M, Krömer T. 2000. Patterns and ecological corre-
lates of pollination modes among bromeliad commu-
nities of Andean forests in Bolivia. Plant Biol. 2:659–669.
King C, Ballantyne G, Willmer PG. 2013.Whyflower visita-
tion is a poor proxy for pollination: measuring single-visit
pollen deposition, with implications for pollination net-
works and conservation. Methods Ecol Evol. 4:811–818.
Knudsen JT, Tollsten L. 1995. Floral scent in bat-pollinated
plants: a case of convergent evolution. Bot J Linnean Soc.
119:45–57.
Kowalski VS, Tardivo RC. 2015. O grupo Vriesea platy-
nema Gaudich. (Bromeliaceae: Tillandsioideae) no
estado do Paraná, Brasil. Rodriguésia. 66:465–475.
Krömer T. 2003. Fledermausbestäubung (Chiropterophilie)
bei Bromelien der Gattung Guzmania in Bolivien. Die
Bromelie. 3:60–63.
Krömer T, Espejo A, López-Ferrari AR, Acebey A. 2005.
The presence of Werauhia nutans in Mexico. J
Bromeliad Soc. 55:280–284.
Krömer T, Espejo A, López-Ferrari AR, Acebey A. 2007.
Werauhia noctiflorens (Bromeliaceae), una nueva especie
del sureste de México y Belice. Novon. 17:336–340.
Krömer T, Espejo-Serna A, López-Ferrari AR, Ehlers R,
Lautner J. 2012.Taxonomic and nomenclatural status
of the Mexican species in the Tillandsia viridiflora com-
plex (Bromeliaceae). Acta Botánica Mexicana. 99:1–20.
Krömer T, Kessler M, Herzog SK. 2006. Distribution and
flowering ecology of bromeliads along two climatically
contrasting elevational transects in the Bolivian Andes.
Biotropica. 38:183–195.
Krömer T, Kessler M, Lohaus G, Schmidt-Lebuhn AN.
2008. Nectar sugar composition and concentration in
relation to pollination syndromes in Bromeliaceae.
Plant Biol. 10:502–511.
Leme EM. 1995. Contribução ao estudo da seção Xiphion
(Vriesea)–I. Studies of the section Xiphion (Vriesea)−1.
Bromélia. 2:24–28.
Lexer C, Marthaler F, Humbert S, Barbará T, de la Harpe
M, Bossolini E, Paris M, Martinelli G, Versieux LM.
2016. Gene flow and diversification in a species complex
of Alcantarea inselberg bromeliads. Bot J Linnean Soc.
3:505–520.
Macías-Rodríguez MA, Sahagún-Godínez E, Lomelí-
Sención JA. 2007.Pitcairnia abundans L.B.SM.
(Bromeliaceae): supplementary description, range exten-
sion and conservation status of an endemic mexican
plant. Polibotánica. 23:93–100.
Maguiña Conde NR. 2016. Nectar bats and their flowers
across cloud forests of Ecuador and the effect of artificial
nectar feeders [Master´s Thesis]. Missouri: University of
Missouri-St. Louis.
Maguiña R, Amanzo J. 2016. Diet and pollinator role of the
long-snouted bat Platalina genovensium in Lomas eco-
system of Peru. Tropl Conserv Sci. 9:1-8. October-
December.
Maguiña R, Amanzo J, Huamán L. 2012. Dieta de
murciélagos filostómidos del valle de Kosñipata, San
Pedro, Cusco-Perú. Revista Peruana de Biología.
19:159–166.
Mantilla-Meluk KH, Baker RJ. 2010. New species of
Anoura (Chiroptera: Phyllostomidae) from Colombia,
with systematic remarks and notes on the distribution
of the A. geoffroyi complex. Occ Papers Museum Texas
Tech. 292:1–19.
16 P. A. AGUILAR-RODRÍGUEZ ET AL.

Mantilla-Meluk KH, Jiménez-Ortega AM, Baker RJ. 2009.
Range extension of Anoura aequatorialis and notes on
distributional limits of small Anoura in Colombia.
Investigación, Biodiversidad y Desarrollo. 28:107–112.
Marques JS, Tagliati MC, Faria APG. 2015.Diurnalversus
nocturnal pollination success in Billbergia horrida Regel
(Bromeliaceae) and the first record of chiropterophily for
the genus. Anais da Academia Brasileira de Ciências.
87:835–842.
Martinelli G. 1994. Reproductive biology of Bromeliaceae in
the Atlantic rainforest of southeastern Brazil [PhD Thesis].
Saint Andrews (UK): University of Saint Andrews.
Martinelli G. 1997. Biologia reprodutiva de Bromeliaceae
na Reserva Ecológica de Macaé de Cima. In: Lima HC,
Guedes-Bruni RR, editors. Serra de Macaé de Cima:
diversidade Florística e Conservação em Mata
Atlântica. Brazil: Instituto de Pesquisa Jardim Botânico
do Rio de Janeiro; p. 213–250.
Matallana G, Godinho MAS, Guilherme FAG, Belisario M,
Coser TS, Wendt T. 2010.Breedingsystemsof
Bromeliaceae species: evolution of selfing in the context of
sympatric occurrence. Plant Syst Evol. 289:57–65.
Matallana G, Oliveira PE, Da Silva PRR, Wendt T. 2016.Post-
pollination barriers in an assemblage of Bromeliaceae in
south-eastern Brazil. Bot J Linnean Soc. 181:521–531.
Miller M, Pfeiffer W, Schwartz T. 2010. Creating the
CIPRES Science Gateway for inference of large phyloge-
netic trees. New Orleans (LA): Gateway Computing
Environments Workshop (GCE).
Morales RAE. 2016. Dieta, actividad y reproducción de los
murciélagos Anoura geoffroyi ySturnira hondurensis en
el bosque Nublado del Parque Nacional Montecristo, El
Salvador [Bachelor´s Thesis]. San Salvador (El Salvador):
Universidad de El Salvador.
Moras LM, Bernard E, Gregorin R. 2013. Bat assemblages
at high-altitude area in the Atlantic forest of southeast-
ern Brazil. Mastozoología Neotrop. 20:269–278.
Moratelli R, Dias D. 2015. A new species of nectar-feeding
bat, genus Lonchophylla, from the Caatinga of Brazil
(Chiroptera, Phyllostomidae). ZooKeys. 514:73–91.
Morgan GS, Czaplewski NJ. 2012. Evolutionary history of
the neotropical chiroptera: the fossil record. In: Gunnell
GF, Simmons NB, editors. Evolutionary history of bats.
Cambridge: Cambridge University Press; p. 105–161.
Moseley HN. 1870. Notes by a naturalist on the challenger.
London: Macmillan.
Mosti S, Friedman CR, Pacini E, Brighigna L, Papini A.
2013. Nectary ultrastructure and secretory modes in
three species of Tillandsia (Bromeliaceae) that have dif-
ferent pollinators. Botany. 91:786–798.
Moura RL, Costa AF. 2014. Taxonomic notes on Vriesea
sect. Xiphion (Bromeliaceae) with descriptions of three
new species. Syst Botany. 39:791–803.
Muchhala N. 2007. Adaptive trade-offin floral morphology
mediates specialization for flowers pollinated by bats and
hummingbirds. Am Nat. 169:494–504.
Muchhala N, Caiza A, Vizcete JC, Thomson JD. 2008.A
generalized pollination system in the tropics: bats, birds
and Aphelandra acanthus. Ann Bot. 103:1481–1487.
Muchhala N, Jarrín-V P. 2002.Flowervisitationbybats
in cloud forest of western Ecuador. Biotropica.
34:387–395.
Muchhala N, Mena VP, Albuja VL. 2005. A new species of
Anoura (Chiroptera: Phyllostomidae) from the
Ecuadorian Andes. J Mammal. 86:457–461.
Muchhala N, Thomson JD. 2009. Going to great lengths:
selection for long corolla tubes in an extremely specialized
bat–flower mutualism. Proc Rl Soc B. 276:2147–2152.
Muchhala N, Thomson JD. 2012. Interspecific competition
in pollination systems: costs to male fitness via pollen
misplacement. Funct Ecol. 26:476–482.
Müller F. 1897. Einige Bemerkungen über Bromeliaceen.
IX-XIII. Flora. 83:455–473.
Nachev V, Stich KP, Winter C, Bond A, Kamil A, Winter
Y. 2017. Cognition-mediated evolution of low-quality
floral nectars. Science. 355:75–78.
Ollerton J, Alarcón R, Waser NM, Price MV, Watts S,
Cranmer L, Hingston A, Peter CI, Rotenberry J. 2009.
A global test of the pollination syndrome hypothesis.
Ann Bot. 103:1471–1480.
Ortega-García S, Guevara L, Arroyo-Cabrales J, Lindig-
Cisneros R, Martínez-Meyer E, Vega E, Schondube JE.
2017. The thermal niche of Neotropical nectar-feeding
bats: its evolution and application to predict responses to
global warming. Ecol Evol. 7:6691–6701.
Paggi GM, Palma-Silva C, Silveira LCT, Kaltchuk-Santos E,
Bodanese-Zanettini MH, Bered F. 2007. Fertility of
Vriesea gigantea Gaud. (Bromeliaceae) in southern
Brazil. Am J Bot. 94:683–689.
Palma-Silva C, Leal BSS, Chaves CJN, Fay MF. 2016.
Advances in and perspectives on evolution in
Bromeliaceae. Bot J Linnean Soc. 181:305–322.
Palma-Silva C, Lexer C, Paggi GM, Barbará T, Bered F,
Bodanese-Zanettini MH. 2009. Range-wide patterns of
nuclear and chloroplast DNA diversity in Vriesea gigan-
tea (Bromeliaceae) a Neotropical forest species.
Heredity. 103:503–512.
Palma-Silva C, Wendt T, Pinheiro F, Barbará T, Fay MF,
Cozzolino S, Lexer C. 2011. Sympatric bromeliad species
(Pitcairnia spp.) facilitate test of mechanisms involved in
species cohesion and reproductive isolation in
Neotropical iselbergs. Mol Ecol. 20:3185–32101.
Paradis E, Claude J, Strimmer K. 2004. APE: analyses of
phylogenetic and evolution in R language.
Bioinformatics. 20:289–290.
Patterson BD, Pacheco V, Solari S. 1996. Distributions of
bats along an elevational gradient in the Andes of south-
eastern Peru. J Zool (London). 240:637–658.
Porsch O. 1932. Das Problem Fledermausblume. Anzeiger
der Akademie der Wissenschaft Wien, Mathematisch-
Naturwissenschaftliche Klasse. 69: 27–28.
Porsch O. 1934.SäugetierealsBlumenausbeuterunddieFrage
der Säugetierblume. III. Mit 1 Abbildung im Text. 4:1–21.
Queiroz JA, Quirino ZGM, Lopes AV, Machado IC. 2016.
Vertebrate mixed pollination system in Encholirium
spectabile: A bromeliad pollinated by bats, opossum,
and hummingbirds in a tropical dry forest. J Arid
Environ. 125:21–30.
PLANT ECOLOGY & DIVERSITY 17

Queiroz JA, Quirino ZGM, Machado IC. 2015. Floral traits
driving reproductive isolation of two co-flowering taxa
that share vertebrate pollinators. AoB Plants. 7:plv127.
doi:10.1093/aobpla/plv127
R Core Team. 2016. R: A Language and Environment for
Statistical Computing. Vienna (Austria): R Foundation
for Statistical Computing.
Ramírez N, Seres A. 1994. Plant reproductive biology of
herbaceous monocots in a Venezuelan tropical cloud
forest. Plant Syst Evol. 190:129–142.
Rauh W. 1986. Bromelienstudien. I. Neue und wenig
bekannte Arten aus Peru und anderen Ländern (18
Mitteilung). Tropische und Subtropische Pflanzenwelt.
58:715–773.
Rauh W. 1987. Bromelienstudien. I. Neue und wenig
bekannte Arten aus Peru und anderen Ländern (19
Mitteilung). Tropische und Subtropische Pflanzenwelt.
60:907–1004.
Rauh W. 1990. Bromelien, Tillandsien und andere
kulturwürdige Bromelien. 2nd ed. Ulmer: Stuttgart.
Rodríguez-Peña N, Stoner KE, Flores-Ortiz CM, Ayala-
Berdón J, Munguía-Rosas MA, Sánchez-Cordero V,
Schondube JE. 2016. Factors affecting nectar sugar com-
position in chiropterophilic plants. Revista Mexicana De
Biodiversidad. 87:465–473.
Rojas D, Vale A, Ferrero V, Navarro L. 2011.Whendidplants
become important to leaf-nosed bats? Diversification of
feeding habits in the family Phyllostomidae. Mol Ecol.
20:2217–2228.
Rojas D, Warsi OM, Dávalos LM. 2016. Bats (Chiroptera:
Noctilionoidea) challenge a recent origin of extant
Neotropical diversity. Syst Biol. 65:432–448.
Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S,
Ashworth L, Lopezaraiza-Mikel M, Bastida JM,
Quesada M. 2014. A quantitative review of pollination
syndromes: do floral traits predict effective pollinators?
Ecol Lett. 17:388–400.
Rothenwöhrer C, Becker NI, Tschapka M. 2011. Resource
landscape and spatio-temporal activity patterns of a
plant-visiting bat in a Costa Rica lowland rainforest. J
Zool. 283:108–116.
Ruzana Adibah MS, Ainuddin AN. 2011. Epiphytic plants
responses to light and water stress. Asian J Plant Sci.
10:97–107.
Salas D. 1973.Una bromeliácea costarricense polinizada
por murciélagos. Brenesia. 2:5–10.
Sazima I, Vogel S, Sazima M. 1989. Bat pollination of
Encholirium glaziovii, a terrestrial bromeliad. Plant Syst
Evol. 168:167–179.
Sazima M, Buzato S, Sazima I. 1995. Polinização de Vriesea
por morcegos no Sudeste brasileiro. Revista de
Sociedade Brasileira de Bromélias. 2:29–37.
Sazima M, Buzato S, Sazima I. 1999. Bat-pollinated flower
assemblage and bat visitors at two Atlantic forest sites in
Brazil. Ann Bot. 83:705–712.
Schmid H. 2000.Puya nitida (Bromeliaceae): Generalist für
Chiropterophilie und Ornithophilie [Thesis]. Bayreuth
(Germany): Universität Bayreuth.
Schmid S, Schmid VS, Zillikens A, Harter-Marques B,
Steiner J. 2011. Bimodal pollination system of the bro-
meliad Aechmea nudicaulis involving hummingbirds
and bees. Plant Biol Suppl. 1:41–50.
Scultori da Silva HCS. 2009.Comunidadedemorcegos,
interações com flores e estratifição vertical em Mata
Atlântica do Sui do Brasil [Master´s Thesis]. São
Paulo (Brazil): Universidade Estadual de Campinas.
Seres A, Ramírez N. 1995. Biología floral y polinización de
algunas monocotiledóneas de un bosque nublado
Venezolano. Ann Mo Bot Gard. 82:61–81.
Shivanna KR, Tandon R. 2014. Breeding systems. In:
Shivanna KR, Tandon R, editors. Reproductive ecology
of flowering plants: a manual. New Delhi: Springer; p.
107–123.
Shockey BJ, Salas-Gismondi R, Baby P, Guyot JL, Baltazar
MC, Huamán L, Clack A, Stucchi M, Pujos F, Emerson
JM, et al. 2009. New Pleistocene cave faunas of the
Andes of Central Peru: radiocarbon ages and the survi-
val of low latitude, Pleistocene DNA. Palaeontologia
Electronica. 12:1–15.
Silva Jorge J, Silva Rocha LH, Silva Jorge JP, Pierote Sousa
PH, Xavier Freire EM. 2018. Floral visitors and potential
pollinators of a rupicolous bromeliad (Pitcairnioideae)
in the Brazilian semiarid. Neotropl Biol Conserv.
13:101–110.
Simmons NB. 2005. Order Chiroptera. In: Wilson DE,
Reeder DM, editors. Mammal species of the world. A
taxonomic and geographic reference. Baltimore: Johns
Hopkins University Press; p. 312–529.
Siqueira Filho JA. 2003.Fenologia da floração, ecología da
polinização e conservação de Bromeliaceae na Florest
Atlâantica Nordestina [PhD Thesis]. Recife (Brazil):
Universidade Federal de Pernambuco.
Soriano PJ, Ruiz A, Arends A. 2002. Physiological
responses to ambient temperature manipulation by
three species of bats from Andean cloud forests. J
Mammal. 83:445–457.
Stewart A, Dudash MR. 2016.Differential pollen placement
on an Old World nectar bat increases pollination effi-
ciency. Ann Bot. 117:145–152.
Stewart AB, Dudash MR. 2017. Field evidence of strong
differential pollen placement by Old World bat-polli-
nated plants. Ann Bot. 119:73–79.
Terry RG, Brown GK, Olmstead RG. 1997. Examination of
subfamilial phylogeny in Bromeliaceae using compara-
tive sequencing of the plastid locus ndhF. Am J Bot.
84:664–670.
Tripp EA, Manos PS. 2008.Isfloral specialization an
evolutionary dead-end? Pollination system transitions
in Ruellia (Acanthaceae). Evolution. 62:1712–1737.
Tschapka M. 2004. Energy density patterns of nectar
resources permit coexistence within a guild of neo-
tropical flower-visiting bats. J Zool (London). 263:7–
21.
Tschapka M, Dressler S. 2002. Chiropterophily: on bat-
flowers and flower bats. Curtis Bot Mag (Series 6).
19:114–125.
18 P. A. AGUILAR-RODRÍGUEZ ET AL.

Tschapka M, Gonzalez-Terrazas TP, Knörnschild M. 2015.
Nectar uptake in bats using a pumping-tongue mechan-
ism. Sci Adv. 1:e1500525.
Tschapka M, von Helversen O. 2007.Phenology,nectar
production and visitation behaviour of bats on the
flowers of the bromeliad Werauhia gladioliflora in
Costa Rican lowland rain forest. J Tropical Ecol.
23:385–395.
Utley J. 1983.ArevisionoftheMiddleAmericanthecophylloid
Vrieseas (Bromeliaceae). Tulane Stud Zool Bot. 24:1–81.
van del Pijil L. 1961. Ecological aspects of flower evolution.
II. Zoophilous flower classes. Evolution. 15:44–59.
van der Niet T, Johnson SD. 2012. Phylogenetic evidence
for pollinator driven diversification of angiosperms.
Trend Ecol Evol. 27:353–361.
Varadarajan GS, Brown GK. 1988. Morphological variation
of some floral features of the subfamily Pitcairnioideae
(Bromeliaceae) and their significance in pollination biol-
ogy. Bot Gaz. 149:82–91.
Versieux LM, Barbará T, Wanderley MGL, Calvente A, Fay
MF, Lexer C. 2012.MolecularphylogeneticsoftheBrazilian
giant bromeliads (Alcantarea,Bromeliaceae):implications
for morphological evolution and biogeography. Mol
Phylogenet Evol. 64:177–189.
Versieux LM, Wanderley MGL. 2015. Bromélias-gigantes
do Brasil. Natal: Capim Macio & Offset.
Vogel S. 1958. Fledermausblumen in Südamerika.
Oesterreichische Botanische Zeitschrift. 104:491–530.
Vogel S. 1969. Chiropterophilie in der neotropischen Flora-
Neue Mitteilungen III. Flora. 158:289–323.
von Helversen D, Holderied MW, von Helversen O.
2003. Echoes of bat-pollinated bell-shaped flowers:
conspicuous for nectar-feeding bats? J Exp Biol.
206:1025–1034.
von Helversen D, von Helversen O. 1975.Glossophaga
soricina (Phyllostomidae) Nahrungsaufnahme (Lecken).
Encyclopaedia Cinematographica E. 1837/1975.
von Helversen O 1993.Adaptationsofflowers to the
pollination by glossophagine bats. In: Barthlott W,
Naumann CM, Schmidt-Loske K, Schuchmann KL,
editors. Animal-Plant Interactions in tropical envir-
onments. Results of the Symposium of the German
Society for Tropical Ecology held at Bonn; 1992 Feb
13–16; Bonn: Museum Koenig; p. 41–59.
von Helversen O, Reyer HU. 1984. Nectar intake and
energy expenditure in a flower visiting bat. Oecologia.
63:178–184.
von Helversen O, Winkler L, Bestmann HJ. 2000. Sulphur-
containing “perfumes”attract flower visiting bats. J
Comp Physiol A. 186:143–153.
von Helversen O, Winter Y. 2003. Glossophagine bats and
their flowers: costs and benefits for plants and pollina-
tors. In: Kunz TH, Fenton MB, editors. Bat ecology.
Chicago: The University of Chicago Press, Chicago; p.
346–397.
Wendt T, Canela MBF, Klein DE, Rios RI. 2002. Selfing
facilities reproductive isolation among three sympatric
species of Pitcairnia (Bromeliaceae). Plant Syst Evol.
232:201–212.
Wendt T, Coser TS, Matallana G, Guilherme FAG.
2008. An apparent lack of pre-zygotic reproductive
isolation among 42 sympatric species of Bromeliaceae
in southeastern Brazil. Plant Syst Evol. 275:31–41.
Wendt T, Ferreira CMB, Gelli de Faria AP, Iglesias-Rios R.
2001. Reproductive biology and natural hybridization
between two endemic species of Pitcairnia
(Bromeliaceae). Am J Bot. 88:1760–1767.
Willmer P. 2011. Pollination and floral ecology. Princeton
(NJ): Princeton University Press.
Zwickl D. 2006. Genetic algorithm approaches for the
phylogenetic analysis of large biological sequence
datasets under the maximum likelihood criterion
[PhD Thesis]. Austin (TX): The University of Texas.
PLANT ECOLOGY & DIVERSITY 19