In flowering plants, pollination,
transfer of pollen grains from the anther to the stigma, is a pre-requisite for
seed set and plays a critical role in their reproductive success. Over 85% of
the flowering plants are pollinated by animals (biotic pollination) and the
remaining are pollinated by wind or water. Amongst animals, insects are the
major pollinators. Birds and bats are the other important pollinators. Plant
pollinator interactions are largely mutualistic, but there are a good number of
species that achieve pollination by deceit. Biotic pollination essentially
involves a sedentary partner (plant) and a mobile partner (animal). This
imposes two conflicting demands on plants. 1) They have to develop effective
devices to attract animals to visit their flowers in a sustainable way and use
them effectively for pollination services. 2) They have to apply some degree of
discrimination to restrict the number of animal species visiting the flowers.
In the absence of such discrimination, all animal species that reside in the
habitat may visit all synchronously flowering plant species and bring about
extensive hetero-specific pollination. As pollination success depends on the transfer
of pollen to conspecific stigma, heterospecific pollination compromises
reproductive fitness of plant species. Most of the studies on pollination
ecology have so far concentrated on floral attraction; only limited studies
have been carried out on the details of restriction of floral visitors. This
chapter gives a brief introduction on the origin of biotic pollination and its
significance in diversification of flowering plants, and discusses our current understanding
on how plants have been able to achieve conflicting demands of attraction and
restriction of floral visitors for efficient pollination.
Flowers are the units of sexual
reproduction that involves a series of sequential events—production of functional
pollen grains (male partners) and ovules (female partners), transfer of pollen
grains from the anther to the stigma (pollination), pollen-pistil interaction
leading to the entry of pollen tubes into the ovules and delivery of male
gametes near the female gamete, fertilization, development of fruits and seeds,
dispersal of seeds, and growth of seedlings into adults. Pollination is one of
the most critical events in sexual reproduction of seed plants and plays a
crucial role in both fundamental and applied aspects of reproductive biology.
Pollination is the only means of gene flow between conspecific plants and
populations, and is thus the basis of recombination. Successful pollination is
a prerequisite for fruit and seed development, and thus plays an important role
in reproductive success of both cultivated and wild plant species. Pollination
limitation reduces the yield of cultivated species (Roubik 1995; Knight et al.
2005; James and Pitts-Singer 2008) and often acts as a driving force for
species vulnerability in natural habitats (Spira 2001; Wilcock and Neiland
2002; Biesmeijer et al. 2006; Potts et al. 2009; Shivanna 2012a; Burkle et al.
2013; Tylianakis 2013). Information on pollination ecology is essential for the
release of genetically transformed plants (Armstrong et al. 2005). Pollination
services are needed to sustain pollinators particularly those that depend
exclusively on floral resources (nectar/pollen).
Pollination is simply the deposition of
pollen grains from an anther to the stigma. Based on the source of pollen,
pollination is of three types: i) autogamy: transfer of pollen grains from the
anthers to the stigma of the same flower, ii) geitonogamy: transfer of
pollen grains from the anthers to the stigma of another flower of the same
plant or another plant of the same clone and iii) xenogamy: transfer
of pollen grains from the anther to the stigma of another non-clonal
plant.
Sexuality of the flower and of the plant
affects pollen flow within and between flowers/plants. The flowers may be
hermaphrodite (producing both functional pollen and ovules) or male (producing
only functional pollen) or female (producing only functional ovules). The plant
may be bisexual (producing only hermaphrodite flowers) or monoecious (each plant
producing both male and female flowers) or dioecious (each plant producing only
male or only female flowers). Thus, all three types of pollinations can occur
in plants producing hermaphrodite flowers; only geitonogamy and xenogamy can
occur in monoecious species while only xenogamy is possible in dioecious
species. Expression of male and female phases in hermaphrodite flowers may be
synchronous or show temporal (dichogamy) or spatial (herkogamy) separation.
When the female phase in dichogamous flowers is expressed earlier than the male
phase, the condition is called protogyny and when the male phase is expressed
earlier than the female phase, it is called protandry. In herkogamous flowers,
the anthers and the stigma are spatially separated and are located at different
levels in the flower. Herkogamy and dichogamy prevent autogamy but are not effective
in preventing geitonogamy. Many hermaphrodite species are self-incompatible that
prevents both autogamy and geitonogamy completely and permits only xenogamy.
Over 85% of the flowering plants are
pollinated by a variety of animals (biotic-pollination) and the remaining by
wind or water (Ollerton et al. 2011). Thus, biotic pollination provides one of
the crucial ecosystem services both in agricultural fields and natural
habitats. These services are threatened by habitat destruction and global
warming which lead to reduction of pollinator diversity and abundance. Several
recent studies have highlighted decline of pollinators and also parallel
decline of plant species (that depended obligatorily on biotic-pollination)
with their pollinators (Biesmeijer et al. 2006; Aguilar et al. 2006; Memmott et
al. 2007; Potts et al. 2009; Garibaldi et al. 2013; Burkle et al. 2013 see also
Tylianakis 2013).
Plant-pollinator interactions are largely
mutualistic and result in reciprocal benefits. It is a form of ‘biological
barter’ and involves exchange of resources of the plant such as pollen and
nectar with the services of the pollinator (Ollerton 2006). There are, however,
a good number of species that achieve pollination through deceit without
offering any rewards to the pollinators. The ultimate strategy of plants is to
deliver and receive conspecific pollen with minimum allocation of resources
while that of the pollinator is to harvest maximum reward with minimum use of
energy and time.
Evolution of biotic pollination provides
several advantages to plants over wind and water pollination: i) biotic-pollination
is more efficient as animals seek out conspecific flowers and often transport
pollen for longer distances, ii) it can thrive even in habitats with minimum
wind as in tropical forests with closed canopy and iii) plant species need to
allocate lesser resources for pollen production than wind/water-pollinated
species, as the latter involves extensive pollen wastage (see Pellmyr 2002). Many evidences indicate that abiotic
pollination by wind and water is a derived condition from biotic pollination:
i) Anemophily is present in families such as Poaceae, Cyperaceae, Betulaceae
and Juncaceae that are highly evolved and whose ancestry can be traced to
animal-pollinated species (Faegri and van der Pijl 1971). ii) Anemophily is
rare in tropical rain forests where pollinating animals are abundant. iii)
Several wind-pollinated species show a combination of wind- and
biotic-pollination. For example species of Salix produce nectar and
their flowers are pollinated by insects; they also produce large amount of
pollen that are carried by wind. (iv) Insect pollination seems to be ancestral
in basal angiosperms which represent the first flowering plants to diverge from
the ancestral angiosperms (Hu et al. 2012). Anemophily seems to have evolved as
an adaptation to overcome the scarcity of pollinators. Hydrophily seems to have
evolved in response to aquatic habitat which is considered to be a derived one
for higher plants (Faegri and van der Pijl 1971). Most of the aquatic plants in
which the flowers emerge above the water level are pollinated by animals
similar to their terrestrial ancestors. Only those aquatic species in which flowers
remain inside the water have developed devices to use water for pollen transport.
Two Conflicting Demands of Biotic Pollination: Attraction and Restriction
of Pollinators
Animal-mediated pollination essentially
involves a sedentary partner (plant) and a mobile partner (animal). This
imposes two conflicting demands on plants. 1) They have to develop effective
devices to attract suitable animals to visit their flowers in a sustainable way
and use them effectively for pollination services. This requires substantial
investment from plants in the form of attractants and rewards. 2) Plants have
to apply some degree of discrimination to restrict the number of animal species
visiting the flowers of each plant species. In the absence of such
discrimination, all animal species that are present in the habitat may visit
all synchronously flowering plant species. This would result in (i) unhealthy
competition between plant species, (ii) enormous wastage of pollen and (iii)
extensive heterospecific pollination (with pollen of other species). These
features seriously compromise reproductive fitness of plant species (see
Pellmyr 2002). Therefore, plants have to devise ingenious ways to achieve these
conflicting demands of attraction and restriction of floral visitors for efficient
pollination. Studies on pollination ecology so far have concentrated largely in
understanding the details of attraction; only limited studies have been carried
out to understand the details of restriction. Even the reviews and books on
pollination ecology hardly discuss the restriction aspect of pollination,
except some aspects of morphological filters (Pellmyr 2002; Roubik et al. 2005;
Dafni et al. 2005; Bronstein et al. 2006; Waser and Ollerton 2006; James and
Pitts-Singer 2008; Anonymous 2009; Willmer 2011; Patiny 2012). In this review
an attempt is made to give a brief introduction on the origin of biotic
pollination and its significance in diversification of flowering plants and
pollinators, and bring together available information on how the plants have been
able to achieve these conflicting demands of attraction and restriction of
pollinators to flowers. As the literature in the area is extensive, the
coverage tends to be subjective with an emphasis on recent studies.
Origin of Biotic-Pollination
Biotic pollination evolved in two groups
of Gymnosperms (Cycadales and Gnetales) as early as the Permian period (about
250 million yrs. ago) and is present even in several extant species of these
groups. Beetles, flies, thrips and wasps are the most common pollinators in
Gymnosperms (Seymour et al. 2004; Terry et al. 2007; Marler 2010). Fragrance is
the basis of attraction of pollinators. The chemical composition of their
fragrance is similar to general herbivore deterrents (Pellmyr and Thien 1987).
It is suggested that early attractants for pollinators evolved from herbivore
deterrents (Pellmyr et al. 1991). The pollinators frequently utilize male cones
for nursery purpose (for mating and obtaining food for larvae and adults) and
female cones mimic olfactory cues of male cones to attract pollinators. In some
species, the pollination drop present at the tip of the ovule may serve as a
reward for pollinators. Some cycads show obligate mutualism with their
specialist pollinators, and have evolved mechanisms to generate heat (4–12ÂșC
above ambient temperature) in the cones. The heat increases the emission of
volatiles and improves pollinators’ attraction (Terry et al. 2007; Marler
2010).
In Angiosperms, animal-mediated pollination
was prevalent from the beginning of their evolution in the early Cretaceous
period (over 100–120 million yrs. ago). The oldest fossil of the flower
discovered in the early Cretacieous (about 120 million yrs. ago) is related to
extant Nymphaeales. Another fossil
found in the upper Cretaceous (about 90 million yrs. ago) is similar to the
extant Victoria species. Based on molecular phylogeny, earliest angiosperms,
termed basal angiosperms, representing the first flowering plants to diverge
from the ancestral angiosperms, have been recognized (Soltis et al. 2000).
Pollination ecology of many species of basal angiosperms has been studied
(Pellymr and Thien 1987; Endress 2010, 2011; Thien et al. 2009). The flowers of
basal angiosperms are generally small, simple and radially symmetrical.
Bisexual flowers are more common and all of them are protogynous. Most of the
species show apocarpous (free carpels) condition and well-defined style is
generally absent. They seem to attract generalized pollinators prevalent in
animal-pollinated Gymnosperms and show many similarities to the pollination
system in Gymnosperms (Pellymr and Thien 1987). Beetles and flies are the major
pollinators and pollen is the major reward; many of them show floral thermogenesis
(use the search bar above for more about this). Bee pollination is found
only in Nymphaeaceae. Abiotic pollination is rare in basal angiosperms.
Animal Partners
Amongst animals, insects are the
principal pollinators. Hymenoptera (bees, wasps and ants), Lepidoptera
(butterflies and moths), Coleoptera (beetles) and Diptera (flies) are the major
orders of insects involved in pollination. In recent years, thrips
(Thysanoptera) have been reported to bring about pollination in a number of
species (Ananthakrishnan 1993; Williams et al. 2001; Garcia-Fayos and
Goldarazena 2008). Thrips are very small (< 1 mm long) and are poor flyers;
they can, however, be carried for long distances by the wind. Thrips largely
bring about autogamy and geitonogamy. Birds and bats are the other important
pollinators. They are generally confined to tropical and sub-tropical areas
that provide floral resources throughout the year. Bird-pollinated
(ornithophilous) species have been reported in over 60 families (see de Wall et
al. 2012). In the New World, hummingbirds are the principal bird pollinators and
in the Old World and Pacific regions, sunbirds and sugarbirds are the major
bird pollinators. In Australia the honeyeaters and in Hawaii the honeycreepers
are the main bird pollinators. Bird-pollinated species are more prevalent in
Australia when compared to other continents. According to an old survey (Ford
et al. 1979) 111 species of birds have been reported to visit flowers of about
250 species of plants. Only two families of bats, Pteropodidae which occurs
throughout tropical and subtropical regions of the Old World (including
Australia and Pacific islands) and Phyllostomidae which inhabits tropical and
subtropical regions of the New World contain species that are specialized in
nectar feeding (see Fleming et al. 2009). Old World bats are larger with
shorter tongues and do not hover whereas those of the New World are smaller with
longer tongues and hover. Bat-pollination (chiropterophily) has been recorded
in over 500 species belonging to 67 families and 28 orders of tropical and
semitropical plant species (Gibson 2001; Flaming et al. 2009). Bat and bird
pollinations are considered to be derived conditions and have evolved
independently in many advanced families of flowering plants. Some unusual
pollinators have also been reported in some plant species: cockroaches
(Nagamitsu and Inoue 1997—Uveria), mice (Wester et al. 2009 —Pagoda
lily), squirrels (Tandon et al. 2003—Butea), snails (Sarma et al. 2007—Volvulopsis)
and lizards (Olesen and Valido 2003; Ortega-Olivencia 2012—Scrophularia; Hansen
et al. 2006—Trochetia).
Bumblebees and honeybees have
trichromatic vision with UV, blue and yellow as primary colors and their
spectral range extend from about 550 nm to 336 nm. Human vision is also
trichromatic (blue, green and red as primary colors) and the spectral range is
confined to visible wavelengths (from 400 nm to about 700 nm). All Lepidoptera
and flies so far examined have the ability to see objects in UV range (see
Kevan 1983; Kearns and Inouye 1993). Those insects which can distinguish UV
from longer wavelengths have a separate UV absorbing pigment. Some butterflies
can see red while others cannot. Honeybees are also red-blind. Hummingbirds and
a few other birds also see in the near UV region of the spectrum (Chen et al.
1984). Bats are generally red-blind although they can distinguish white vs
black even in extremely low light (Gibson 2001).
Pollinating insects may be social or
solitary (Anonymous 2012). All species of ants and termites, and some species
of bees (honeybees, bumblebees and stingless bees) and wasps are social
insects. Truly social (eusocial) insects are characterized by: i) all
individuals of a colony share a common nest site, ii) reproduction in the
colony is restricted to only one or a few females, iii) the individuals of a
colony are made up of overlapping generations and iv) brood care within the
colony is a co-operative function. Most of the other bees involved in
pollination (such as Xylocopa, Megachile, Osmia and Nomia) are
solitary. Solitary bees do not form colonies. A solitary female constructs her
own nest, stores food for her brood in the form of pollen or nectar and then
dies or departs without further care to her offspring. The adult life of these
bees is generally short, spanning for a few weeks. They nest alone or in
aggregations.
Invertebrate pollinators have limited
memory and their visits are largely confined to just one type of flower at a
given time (Minckley and Roulston 2006). In a complex flower with hidden
rewards, insects have to learn by trial and error the best approach to harvest
the reward with minimum time. When they change host species, they have to learn
again to handle the second flower (Lewis 1986; see also Raine and Chitka 2007).
Pollen-collecting bees generally have a limited foraging range and frequently
commute between the nest and the host plants to unload the pollen sample. Bats
have stronger memory than bees. Nectar-feeding bats can retain up to 40 food locations
in their working memory, facilitating their foraging in tropical nocturnal
environments (Winter and Stich 2005). Vertebrate pollinators are homoeothermic
and need a continuous supply of food to maintain their high metabolic rate. They
are able to visit flowers even during low temperature conditions under which
insects are unable to fly. Insects, on the other hand, are able to survive long
periods of unfavorable conditions in larval stages or as hibernating adults.
Vertebrate pollinators and some butterfly species can cope with unfavorable
conditions during some parts of the year through local and regional migrations
(see Abrahamczyk et al. 2011).
Diversification of Flowering Plants and Pollinators
There was a dramatic increase in the
number of angiosperm species soon after their origin in the Cretaceous period.
Darwin recognized this increase and termed this diversification as an
“abominable mystery” (see Friedman 2009). Paleontological evidences indicate:
i) slow diversification of insect pollinator groups (although they arose in the
early Mesozoic or even before) until they became associated with angiosperms
and ii) rapid diversification of the angiosperms and pollinating insect groups
simultaneously in the latter half of the Cretaceous and tertiary period. On the
basis of these evidences evolutionary biologists suggested that biotic
pollination acted as a catalyst for reciprocal diversification of pollinating
insects and flowering plants in the latter half of the Cretaceous period (see
Crane et al. 2000; Pellmyr 2002; Magallon and Castillo 2009; Smith et al 2011).
A recent study suggests that the rise of bees coincided with the largest flowering
plant clade, the eudicots which comprises 75% of the flowering plants (Cardinal
and Danforth 2013; see also Cappellari et al. 2013).
Some evolutionary biologists, however,
argue that biotic pollination acted not as an exclusive factor but as a
co-factor in the diversification of angiosperms (Sanderson and Donoghue 1994;
see Pellmyr 2002). This argument is based on: i) angiosperm diversification
increased not at the beginning of their evolution when animal pollination arose
but rather at a later stage and ii) animal-pollinated Gymnosperm groups (such
as Zamia, Welwitschia and Gnetum) have not diversified more than
their wind-pollinated sister groups.
Several evidences indicate that apart
from biotic pollination, evolution of the flower and some of its innovations
seem to be the contributing factors for the evolutionary diversification of flowering
plants. The visual and fragrance components of the flower and the secretion of
the nectar as a carbohydrate-rich reward increased dramatically the attraction
of pollinators and their sustainability, thus increasing pollination efficiency
of flowering plants when compared to the cones of Gymnosperms. The other
innovations of the flower that seem to have contributed to the diversification of
angiosperms are the evolution of the carpel and floral zygomorphy. Evolution of
the carpel, as the result of covering of the ovule(s) with a sporophytic tissue
differentiated into the ovary (enclosing the ovules), style and stigma, had
profound effects on the operation of sexual reproduction of angiosperms. Unlike
in Gymnosperms, pollen grains in Angiosperms do not have direct access to the
ovules in which female gametes are located; they land on the stigma placed far
away from the ovules. Evolution of the pistil resulted in the addition of
another step in pre-fertilization events—growth of pollen tubes through the tissues
of the stigma and style—before pollen tubes enter the ovules and release the
male gametes for fertilization. All the carpels of the flower together are
referred to as the pistil. In most of the eudicots and monocots, all the
carpels of the flower are united (syncarpous) with a well-defined style. The
transmitting tissue (through which pollen tubes grow) of the styles of
individual carpels is also fused in syncarpous pistils enabling pollen tubes
originating from one carpel to cross-over to the ovules of other carpels (see
Armbruster et al. 2002; Endress 2010). Thus, pollen tubes originating from any
stigma or a part of the stigma can enter the ovules of all the carpels in
syncarpous pistils. This increases the efficiency of pollination and the extent
of seed set even under pollination constraint.
More importantly, the pistil screens
pollen grains for quality and compatibility before pollen tubes reach the
ovules (see Shivanna 2003). As the number of pollen grains that land on the
stigma is generally many times more than the number of ovules available for
fertilization, pollen grains are subjected to intense competition during pollen
germination and pollen tube growth in the pistil. Those pollen grains that
germinate early and pollen tubes that grow faster in the style, enter the
ovules earlier than the slow growing pollen tubes and effect fertilization.
Pollen grains which germinate later and pollen tubes with slower growth rate
are eliminated in this competition. Since cross-pollination takes place to a
limited or greater extent in most of the species, there is considerable genetic
variability in the pollen population on which pollen competition can operate.
There is no scope for such a competition among male gametes in lower groups of
plants including gymnosperms. The adaptive significance of pollen competition
in increasing the fitness of the progeny is documented in several species
through experimental manipulation of pollen competition (Mulcahy 1979; Mulcahy
and Mulcahy 1987; Davis et al. 1987; Schlichting et al. 1987; Tejaswini et al.
2001; Lankinen and Madjidian 2011). Seedlings resulting from intense pollen
competition show more vigorous and uniform growth when compared to those
resulting from no competition or limited competition.
The pistil also plays a critical role in
the breeding system of angiosperms. Self-incompatibility (SI) controlled by one
or a few genes, each with two or multiple alleles, is one of the common
outbreeding devices in plants (de Nettencourt 2001). When the SI allele present
in the male gamete matches that of the female gamete, fertilization is
prevented. In lower groups of plants where male and female gametes come in
direct contact with each other, SI cannot prevent completely the fusion of
gametes produced by the same individual. For example S1 and S2 gametes produced
by the S1 S2 self-incompatible individual can fuse although fusion of S1with S1
and S2 with S2 gametes is prevented (see Shivanna 2003). In flowering plants SI
recognition is established between the gametophytic pollen (each carrying one
of the S alleles) and the sporophytic tissues of the pistil (carrying both the
S alleles of the parent). In S1S2 plants, for example, pollen grains carrying
both S1 and S2 alleles are recognized and inhibited in the pistil. Evolution of
the pistil has made self-incompatible flowering plants the most efficient out-breeders
since all male gametes that originate from the same plant or any other plant with
the same genotype are effectively prevented from fertilization.
Yet another floral innovation that
appeared in some major lineages in Cretaceous period was the evolution of
bilateral zygomorphic flowers from radial actinomorphic flowers (Friedman 2009;
Mach 2012; Vamosi and Vamosi 2012). As zygomorphic flowers have one plane of
symmetry, effective pollen transfer depends on the accuracy in functional fitness
between the flower and the pollinator leading to specialized pollination systems
(Sargent 2004). Such specialized interactions facilitate reproductive isolation
and speciation. Phylogenetic analyses have shown that lineages with zygomorphic
flowers tend to contain more number of species than their actinomorphic sister
groups (Sargent 2004; see Vamosi and Vamosi 2012). Thus, biotic pollination
together with the evolution of the flower with the pistil and further floral
elaboration in the form of zygomorphy would have acted as catalysts for the
reciprocal diversification of flowering plants and pollinating insects.
The details of floral morphology in the
basal angiosperms are in agreement with the above concept (Thien et al. 2009).
As pointed out earlier, flowers in basal angiosperms are radially symmetrical
and the carpels are largely free (apocarpous) with ill-defined style. In
apocarpous species pollen grains that land on the stigma of a carpel cannot
cross-over to the ovules located in other carpels of the flower. This reduces
pollination efficiency and the extent of seed set under deficient pollination
environment as the seed set is confined only to pollinated carpel. Also, short
style prevalent in basal angiosperms is likely to be less effective in
screening pollen quality when compared to eudicots and monocots with
well-developed styles (see Mulcahy 1979; Armbruster et al. 2002). These floral
features explain limited diversification of basal angiosperms.
Floral Attractants
Plants have to invest considerable
resources to attract pollinators and sustain their visits by providing rewards
to the visitors. Floral attractants advertise the presence of rewards that
provide motivation for animals to visit flowers in a sustainable way. Flowers
and inflorescences and their fragrance act as advertisers through visual and
olfactory cues (Dafni et al. 2005). Flowers exhibit a remarkable diversity in colors,
sizes, shapes, scents, and sexual systems; no other plant organ can match flowers
in their diversity. This has enabled them to attract a range of animals to the
flowers and use them for pollination services. A standard method used to study
differential effects of the color and fragrance in pollinator attraction is to
hide the color of the flower by covering the flowers/inflorescences with a
non-transparent material allowing the scent to escape through fine holes and
record pollinator responses to the fragrance (Dobson et al. 2005). To study the
effect of fragrance, the flowers/inflorescences are sealed with hermetic
transparent paper to prevent scent emission and study the responses of
pollinators to the color. The responses of the above two treatments are
compared with un-manipulated flowers (controls). Several investigators have
used artificial flowers to study the behavior of floral visitors (Kearns and
Inouye 1993; Johnson and Dafni 1998; Cresswell and Smithson 2005; Leonard and
Papaj 2011). Visual cues are prepared from colored paper folded suitably by incorporating
the landing area, if necessary; sugar solution is provided as the reward. Many
animals forage readily from artificial flowers with the most basic similarity
to actual flowers (Raguso et al. 2002).
Visual Cues
Visual cues are in the form of size,
shape and color of the pollination unit (flower/inflorescence). Floral colors
are essentially pigment-based; anthocyanins, anthoxanthins, carotenoids,
flavones, flavonols and betaxanthins impart a wide range of colors to the flowers
(see Pellmyr 2002). Amongst different floral organs, petals are the major
attractants; occasionally other parts of the flower such as bracts become
conspicuous.
Nectar guides. Flowers with hidden nectar generally have
contrasting patterns on the petals, termed nectar guides, pointing toward the
source of the nectar. The size and shape of nectar guides are highly variable
(Medel et al. 2003). Many studies have shown that nectar guides do help the
visitors to locate the source of nectar. A white mutant of blue-flowered Delphinium
nelsonii resulted in the loss of nectar guides. Bumblebees avoided such mutant
flowers; even when they visited such flowers, they took longer time to find the
nectar site (Waser and Price 1983). Flowers of Linum pubescens (Linaceae)
are pollinated by the bee-fly, Usia bicolor (Johnson and Dafni 1998). In
flower models with nectar guides, the pollinator tended to follow the lines
toward the center of the flower while on the plain models they showed
undirected behavior, often moving to the edge of the model. Similarly
bumblebees (Bombus impatiens) discovered the rewards more quickly on
artificial flowers with star-like pattern when compared to plain flowers
(Leonard and Papaj 2011).
In a recent study, using natural flowers,
Hansen et al. (2012) studied the role of nectar guides in an iris, Lapeirousia
oreogena. The flowers of this species have nectar guides in the form of
white narrow markings pointing towards the narrow entrance of the long corolla
tube and long-proboscid nemestrinid fly is its sole pollinator. Painting of the
nectar guides with ink that matched the color of the corolla background
dramatically reduced proboscis insertion into the corolla tube, although it did
not affect the approaches of the flies to the flowers from a distance. As
expected, removal of nectar guides significantly reduced pollen export as well
as fruit set.
Change of color in older flowers and its
role in pollinator attraction. In a number of species, older non-rewarding flowers change color
(instead of senescing) and are retained on the plant for several days. This
phenomenon has been reported in over 200 species belonging to 74 families (Gori
1983; Weiss 1991). In all the 26 such species investigated (Weiss 1991) fresh
flowers offered nectar and pollen rewards, and older flowers contained little
or no nectar and lacked pollen. Retention of older flowers increased plant’s
attractiveness to pollinators from a distance. However, the pollinator
discriminated the color of the flower from a close range and mostly visited
rewarding flowers. In Lantana camara, a classical example of
post-pollination changes in color, the flowers are yellow on the day of
anthesis and offer pollen and nectar to the pollinator. They turn orange and
then red on subsequent days. Red flowers are retained on the plant for several
days although they do not offer rewards. In a caged experiment, Weiss (1991)
reported that the pollinator butterfly (Agraulis vanilla) visited yellow
inflorescences significantly more often than red ones. Discriminating ability
of several pollinators (belonging to Diptera, Hymenoptera and Lepidoptera)
between rewarding and non-rewarding flowers was recorded in a number of other color-changing
plant species (Weiss 1991).
Olfactory Cues
Olfactory cues are in the form of
volatile fragrance compounds emitted by flowers. Floral fragrance, in most of
the species, is produced by petals but in several species other floral organs,
particularly pollen grains (Dobson 1988; Falara et al. 2013), also contribute
to the fragrance. The fragrance is in the form of complex mixtures of a large
number of volatile compounds, which give each species a characteristic
fragrance. Maximum emission of fragrance generally coincides with the
activities of their pollinators (Ando et al. 2001) and fragrance emission often
follows endogenous rhythm (Dudareva et al. 1999). For example, methyl benzoate
is one of the most abundant fragrance compounds in flowers of snapdragon,
tobacco and petunia. Its emission follows circadian rhythm (Kolosova et al.
2001); in diurnally pollinated snapdragon, maximum emission occurs during the
day coinciding with the forging activity of its pollinator (bumblebees) and in
nocturnal pollinated tobacco and petunia, maximum emission of methyl benzoate
is during the night. However, nocturnally pollinated flowers of Clarkia
breweri in which S-linalool (acyclic monoterpene) is a major component of
the fragrance (Dudareva and Pichersky 2000) and Dianthus inoxianus in
which aliphatic 2-ketones and sesquiterpenoids are the major components (Balao
et al. 2011) do not show such differences in emission rate between the day and night.
In Australian Chiloglottis orchids the levels of active compounds, chiloglottones,
remain stable not only during the day and night but also over the lifetime of
the flower lasting 2 to 3 wk. (Falara et al. 2013). In these orchids, UV-B
light is required for their synthesis (Falara et al. 2013).
In general, the fragrance acts as
long-distance attractant and at closer range both color and fragrance act
synergistically to guide the visitor to the flower. In an interesting study on
long-distance attraction of fragrance, (Ackerman 1983; see Williams 1983) took
a canoe on a lake in Costa Rica and exposed floral odor of an orchid species,
pollinated by a euglossine bee, at a distance of 50, 200 and 1000 m from the
shore, and recorded the arrival of euglossine bees up to 1000 m to the odor
source. For insects involved in nocturnal pollination, fragrance is the major
or the sole attractant (Jurgens et al. 2002; Balao et al. 2011).
Analysis of floral fragrance. The chemical composition of floral
fragrance is one of the most extensively investigated areas of floral biology
since long because of their commercial value in perfume industry. The role of
floral volatiles in pollinators’ attraction is comparatively recent. Earlier
studies on the composition of floral fragrance and the role of its constituents
in attracting pollinators have been reviewed by Williams (1983) and Knudsen et
al. (1993). The fragrance is generally extracted through headspace extraction
and analyzed using gas chromatography and mass spectrometry (GC-MS). In the
head-space extraction method (Dobson et al. 2005), the flower, intact on the
plant is sealed inside a glass chamber and its emitted volatiles are collected
by continually purging the glass chamber through a polymer mesh that binds the
volatiles. The volatiles are then extracted from the polymer with an organic
solvent.
There is great variation among species in
chemical composition of floral scents, and the number and relative
concentration of constituent volatiles. Floral scents are complex mixtures of
small volatile molecules largely made up of monoterpenoid (such as linalool,
limonene, myrcene, geraniol, cineole and menthol), sesquiterpenoid,
phenylpropanoid, and benzenoid compounds (see Williams 1983; Knudsen et al.
1993, 2006; Dudareva and Pichersky 2000). In many species, fatty acid
derivatives and a range of other chemicals containing nitrogen or sulphur are
also present.
In a number of species, the responses of
pollinators to various fragrance compounds have been analyzed by using either
electroantennogram, a technique commonly used to measure the output of the
antenna of an insect to the brain for the given odor and/or a bioassay. In the
bioassay, insects are exposed to floral scents or fractions of floral scents or
synthetic chemicals, and the responses of insects are studied in a cage of
suitable size. Chemicals are generally applied to filter paper discs which are
placed in glass vials. Some workers have used killed female insect dummies for
the assay in a few orchid species that show sexual deception (Ayasse et al.
2003). To remove innate odor from the dummies, they are Soxhlet-extracted in dichloromethane,
dried and fixed on insect pins. Such odorless dummies are impregnated with
various odor samples to be tested and offered to the pollinators (Ayasse et al.
2003).
The mixture of volatiles emitted by each
species is different; no two species, even if they are closely related, have
been shown to produce identical mixture of volatiles. The pollinator is
attracted to some of them but not to all of them. For example, Huber et al.
(2005) analyzed floral fragrance compounds in two closely related orchids, Gymnadenia
conopsea and G. odoratissima. They identified 45 volatiles in the flowers
of G. conopsea of which three were physiologically active. In G.
odoratissima, 44 volatiles were identified of which seven were physiologically
active. The specificity of fragrance of a species is established not by
individual fragrance compound but a combination of compounds. Insects are able
to distinguish complex mixtures of floral scent volatiles from different species
and respond accordingly. The emission of scent is markedly reduced after
pollination (Schiestl et al. 1997).
Only a limited number of studies have
been carried out on the fragrance of vertebrate-pollinated plants.
Bat-pollinated flowers generally emit strong fruity smell. Bats are sensitive
to odors of esters, alcohols, aldehydes and aliphatic acids (Gibson 2001).
Analysis of floral fragrance of 11 bat-pollinated species showed 49 compounds
of which 11 were sulphur compounds (Bestmann et al. 1997). In a recent study,
two aliphatic ketones, 3-hexanone and 1-hexane-3-one, have been shown to be
dominant compounds in the scent of a rodent pollinated species, Cytinus
visseri (Johnson et al. 2011). The aliphatic ketone-rich scent in
rodent-pollinated plants is in contrast to insect-pollinated plants in which
terpenoids, aromatic or non-ketone aliphatic compounds are the dominant scent
compounds (Bestmann et al. 1997).
In general, the response of pollinators
to floral scent is based on innate abilities of the pollinators superimposed by
learning experience (Andersson and Dobson 2003). The fragrance bouquets of flowers
elicit strong, innate species-specific attraction to pollinators. However, many
pollinators can learn the fragrance bouquets of other species through their
association with the reward (Riffell 2011). This learning ability provides a
means of flexibility to the pollinators in a changing floral habitat; it
enables pollinators to harvest alternative sources of rewards when their
preferred species are not in flowering (see Riffell 2011).
Floral Rewards
Flowers offer a range of rewards to
pollinators. These include food sources such as pollen, nectar and seeds as
well as specialized non-food rewards such as oils and resins, fragrance and
brood sites (see Armbruster 2012).
Pollen and Nectar
Pollen and/or nectar are the major
rewards for pollinators in most species of flowering plants. Many floral
visitors such as honeybees, bumblebees and stingless bees depend solely on floral
resources. For such bees, pollen and nectar serve as the exclusive food source
not only for adults but also for their larvae. For other floral visitors that
feed on other resources also, floral resources only complement their diet.
Pollen is highly nutritious and is a rich source of proteins, vitamins, amino
acids and minerals (Schmidt and Buchmann 1992; Roulston and Cane 2000). In
several species pollen grains, apart from serving as rewards, emit volatiles
and attract pollinators (Dobson 1988; Dobson and Bergstrom 1996, 2000). Pollen-foraging
insects use pollen odors not only to discriminate between plant species but
also between rewarding and non-rewarding flowers on the basis of pollen availability;
this enables pollinators to restrict their visits to the rewarding flowers
(Schmidt 1982; Dobson et al. 1999). For example, in nectarless Rosa rugosa pollinated
by bumblebees, application of pollen volatiles, particularly geranyl acetate to
emasculated, freshly opened flowers increased landing frequency of bees significantly
(Dobson et al. 1999). When anthers were exchanged between first-day flowers
(with pollen reward) and second-day flowers (without pollen reward), flowers
with first day anthers received more bee visits.
The nectar is an aqueous solution made up
of sugars (largely of sucrose, fructose and glucose) generally ranging from 15
to 45% and small amounts of amino acids (see Nicolson and Thornburg 2007; Heil
2011). Secondary metabolites such as alkaloids and phenolics are also present
in the nectar of a range of species (Baker 1977). The nectar contains bacteria
(Fridman et al. 2012; Alvarez-Perez et al. 2012) or yeast (de Vega et al. 2009;
Herrera et al. 2009) in a number of species. Yeast metabolism in the nectar is
thought to contribute to the floral scent (Pozo et al. 2009). Interestingly,
the proportion of plant species that contain yeasts in the nectar was found to
be highest in those pollinated by birds while those visited only by Hymenoptera
showed the lowest values (de Vega et al. 2009). Recently de Vega and Herrera
(2013) reported significant changes on sugar composition in flowers visited by nectarivorous
ants; it contained significantly more glucose and fructose, and less sucrose
when compared to the nectar of ant-excluded flowers. These changes were
correlated with the density of yeast cells in the nectar indicating that
changes in nectar composition is brought about by yeasts transported by ants.
As the nectar and pollen are harvested by
visiting animals, the quality and quantity of available rewards get depleted during
the life of the flower. Many pollinators are able to discriminate nectar
rewarding flowers from non-rewarding flowers by making use of floral cues that
honestly indicate nectar availability. Change of color of older flowers
mentioned earlier is one such cue. The nectar in many species is colored and
has so far been documented in 67 taxa belonging to a wide taxonomic and
geographic ranges (Hansen et al. 2007). The color as well as its intensity is
highly variable between species. Pollinators can assess the presence and
quantity of nectar in the flowers based on visual cues. Dark brown nectar of Aloe
vryheidensis is due to the presence of phenolic compounds (Johnson et al. 2006).
Dark purple nectar of Leucosceptrum canum has been shown to be due to
the presence of an anthocyanidin, 5-hydroxyfl avylium (Zhang et al. 2012). As
5-hydroxyfl avylium inhibits the growth of bacteria and fungi, it may have a
role in preventing growth of bacteria and fungi in the nectar of long-lived flowers
(96 h in this species). Two Mauritian plant species, Trochetia boutoniana and
T. blackburniana, with colored nectar are pollinated by Phelsuma
ornata and P. cepediana geckos, respectively (see Hanson et al. 2006).
P. ornata geckos prefer colored nectar over clear nectar in artificial flowers
(Hanson et al. 2006). Thus, the colored nectar in these species increases its
visibility and acts as a foraging signal to increase pollination efficiency.
Floral nectar of several species is
scented (Raguso 2004). Nectar-foraging bees are able to discriminate between flowers
that contain nectar from nectar-depleted flowers based on nectar fragrance. In
a study on solitary Osmia bees on Penstemon flowers, Howell and
Alarcon (2007) reported that nectar-containing flowers received several times
more bee visits when compared nectar-depleted flowers. Bees in which antennae
were covered with non-toxic silicon (which blocked the olfactory capabilities
of bees) did not discriminate between the two types of flowers indicating that
bees are able to discriminate nectar-rewarding flowers from nectar-depleted flowers
based on nectar volatiles.
Many other pollinator species are able to
discriminate nectar-containing and nectar-depleted flowers on the basis of
other floral cues. The flowers of Datura wrightii pollinated by a
hawkmoth (Manduca sexta) show above ambient emissions of up to 200 ppm
CO2 peak at dusk soon after they open (when the flowers are rich in nectar) but
floral CO2 diminishes rapidly after pollinator visit, although
visual and fragrance cues persist for a much longer time (Guerenstein et al
2004). The pollinator moth seems to detect such differences with their CO2
sensing organ. In a dual choice assay using artificial flowers, moths preferred
to feed from the flowers emitting higher levels of CO2 over those emitting
ambient level of CO2 (Thom et al. 2004). Another instance of such floral cue
that honestly indicates nectar availability has been reported in night blooming
Oenothera cespitosa pollinated by another species of hawkmoth (Hyles
lineate). The relative humidity of the headspace of the flowers of this
species reaches about 4% above ambient relative humidity during the first 30
min after flower opening, although the other floral traits such as visual and
fragrance cues may persist for up to 24 h (von Arx et al. 2012). As floral
humidity gradients are largely produced by the evaporation of the nectar, these
gradients indicate the amount of reward available to floral visitors. Hawkmoth
pollinators can distinguish the differences in RH; they consistently visited flowers
with higher humidity levels when compared to those with ambient humidity levels
(von Arx et al. 2012). These abilities of pollinators to discriminate rewarding
flowers from non-rewarding flowers increase the fitness of both the plants and
pollinators.
Fragrant Compounds
Many Neotropical orchids (over 600 spp.)
produce fragrant compounds largely terpinoids and aromatics to attract as well
as reward male euglossine bees (over 130 spp.). Euglossine bees collect
fragrant compounds and store them in their modified hind legs (Dressler 1982).
The bees are thought to use these compounds to produce sex pheromones that are
released to attract females. Attraction is species-specific in many of these
orchids. Species of Bulbophyllum orchid which do not produce nectar are
pollinated by fruit flies (Bactrocera spp.) (See Tan 2006). Methyl
eugenol is a major fragrance compound in several Bulbophyllum spp.
Methyl eugenol attracts its pollinator, male Bactrocera fruit flies,
even at a very low concentration. The number of flies visiting the flowers in
the morning hours was high and the number dwindles in the afternoon. This is
correlated with the release of high methyl eugenol peak in the morning and
absence of detectable peak from 14.00 hr. onwards in the afternoon (Tan et al.
2002; Tan 2006). Methyl eugenol is eventually converted into sex pheromone and
is released by males to attract females (see Tan 2006). Thus, the fragrance in
these orchids acts as an attractant as well as a reward. Apart from orchids,
fragrance has been reported to act as attractant as well as reward in some six
other Neotropical species such as Anthurium (Araceae), Gloxinia (Gesneriaceae)
and Crinum (Liliaceae) (Dresler 1982; Pellmyr 2002; Armbruster 2012).
Oils and Resins
Several plants belonging to some 11
families such as Malpighiaceae, Krameriaceae and Scrophulariaceae provide oils
as reward. Solitary bees harvest oils and use them for nest building and as a
provision for their larvae (Buchmann 1987; Steiner and Whitehead 1991; Pauw
2006; Renner and Schaefer 2010; Armbruster 2012). Species of Dalechampia (Euphorbiaceae)
and Clusia (Clusiaceae) and a few orchids produce resins as rewards.
Solitary bees use them for nest building and for antifungal purpose (Pemberton
and Liu 2008; Armbruster 2012).
Young Seeds
Many species reward pollinators with
nutrients for their larvae in the form of seeds. Fig and fi g wasps, and Yucca
and yucca moths are classical examples of providing seeds as rewards for
pollinators (nursery pollination). Pollination in Ficus and Yucca is
highly specialized; each plant species is generally pollinated by a specific
species of insect (see Cook and Rasplus 2003; Machado et al. 2005). These
pollination systems are examples of obligate relationships as neither the plant
nor the pollinator is able to reproduce without the other. They represent
insect-plant co-evolution. A few exceptions to this obligate mutualism in figs,
however, have been reported recently (see Cruaud et al. 2012; Wang et al.
2013). Senita cactus (Lophocereus schottii) and Senita moth (Upiga
virescens) is another example of nursery pollination; it is not, however,
an obligate system as two species of halictid bees also bring about pollination
of Senita cactus to a lesser extent (Fleming and Holland 1998). Seed reward has
also been reported in a few other species (see Armbruster 2012). In nursery
pollination systems the pollinators lay their eggs in the ovary of a proportion
of flowers and the larvae consume developing seeds after they emerge. Viable
seeds develop from uninfected ovaries/ovules.
Extensive studies have been carried out
on the fig and fig-wasp mutualism. Most of the Ficus species produce
monoecious flowers in special inflorescences called syconia. The female wasps
enter the receptive syconium through the terminal pore, termed ostiole; they
bring about pollination with pollen collected from male flowers of the syconium
visited earlier, and lay their eggs in a proportion of female flowers. The
larvae of the wasp feed on the gall formed in oviposited flowers and the
remaining pollinated flowers develop into seeds. The emergence of adult wasps
developed from the larvae coincides with the maturation of male flowers. The
wingless male wasps are short-lived; they mate with the females and cut an exit
hole in the syconium for the females to escape. The females loaded with pollen come
out through the exit tunnel and enter another receptive inflorescence (which is
in the female phase) through the ostiole to reproduce; they bring about
pollination during their movement inside the syconium. The trees in receptive phase generally occur
at low densities. As the adult female wasps live only for a few days, it is
critical that the female wasps fly to a receptive syconium usually of a
different tree within a short time. Reproductive success of both fi g and wasp
depends on transmission of a very strong signal by receptive syconia (Harrison
and Shanahan 2005). Several studies have shown that volatile compounds emitted
by the receptive syconia are responsible for attraction of their specific
pollinator (Khadari et al. 1995; Proffit et al. 2008, 2009). The syconia emit
volatile compounds attractive to pollinating wasps only during the period of receptivity.
Pentane extracts of receptive syconia of Ficus carica have been shown to
attract its pollinator Blastophaga psenes from distances of at least 5 m
in the field (Hossaert-McKey et al. 1994). Even non-receptive syconia when
their ostioles were painted with pentane extracts of receptive syconia elicit
the entry of pollinator wasps (Hossaert-McKey et al. 1994).
Several studies have shown
species-specificity of fragrant compounds and their role in attracting specific
pollinators. The fragrance emitted by receptive figs of three sympatric Ficus
species, namely, F. hispida, F. racemosa, and F. tinctoria
could be clearly distinguished by the composition of their fragrance (Proffit
et al. 2008, 2009). Specific odors of these three species were tested for
attraction of the pollinator (Ceratosolen solmsi marchali) of one of the
fig species, F. hispida. Behavioral bioassays showed that the pollinator
was attracted only to the specific odor of F. hispida but not to the
fragrance of other Ficus species (Proffit et al. 2009). In another
dioecious fi g, Ficus semicordata. 4-methylanisole was shown to be the
predominant (94–98%) volatile compound emitted by receptive male and female
syconia (Chen et al. 2009). This compound was absent in receptive volatiles
emitted by two other sympatric fi g species, F. racemosa and F.
hispida. 4-methylanisole attracted its pollinator, Ceratosolen gravelyi,
in a wide range of concentrations. The fragrance was totally absent in the
volatiles emitted by syconia 4 days after pollination. Chemical blends lacking
4-methylanisole were unattractive to C. gravelyi. Receptive syconia of
two non-host fi g species, F. racemosa and F. hispida, repelled C.
gravelyi. These results on different fi g species clearly indicate that
active volatiles are the species-specific signal compounds that attract their
obligate pollinator to the host syconia at the receptive stage.
Recent studies of Wang et al. (2013) have
indicated that apart from long range volatiles, contact cues after the wasp
lands on the syconium also plays a role in determining pollinator specificity.
There is an optimum balance between the
number of wasps that enter a syconium and available resources. Entry of too
many wasps into the syconium results in oviposition in most of the ovaries;
this would lead to eventual collapse of the syconium due to the development of
very few or no seeds, compromising the fitness of the plant as well as the wasp
species. Several hypotheses have been put forward to explain the stability of
this mutualism by preventing wasps from overexploiting the figs (see Dunn et
al. 2008). According to one of the hypotheses, the wasps seem to have developed
mechanisms to discriminate wasp load in the syconium on the basis of the number
of wings left behind by the wasps that have already entered the syconium at and
around the ostiole (Ramya et al. 2011). In F. benghalensis and F.
microcarpa, Ramya et al. (2011) have reported a strong correlation between
the wing load on the ostiole and the wasp load in the syconium. The wasps
preferentially entered those syconia from which the wings were removed rather
than those on which the wings were retained. Adding wings artificially to the
empty syconia also deterred the wasps from entering them, suggesting that
residual wings serve as negative feedback regulators for the entry of wasps. In
another fi g species, F. racemosa, however, wasps did not use leftover
wings as cues. A rapid post-pollination decrease in pollinator attractant as
has been reported in some other species may act as a cue and limit pollinator
visits, thus minimizing overexploitation of ovaries by mutualistic wasps.
The fi g-fi g wasp pollinator mutualism
is also exploited by several parasites of pollinating fi g wasps. The parasites
generally do not enter the syconium but insert their ovipositors into the
syconium from outside and deposit their eggs in some of the flowers; the
offspring of the parasites feed pollinator larvae already present in the galls.
For more information on pollinator and parasitoid interaction in figs please
refer Nedft and Compton (1969); Dunn et al. (2008); Jousselin et al. (2008) and
Ghara et al. (2011) and references therein.
Similarly, each species of yucca is
pollinated by a specific species of moth (Tegeticula or Parategeticula)
(see Powell 1992; Pellmyr and Huth 1994; Pellmyr 2003). The scent from virgin
flowers of the host Yucca glauca was sufficient to attract its obligate
pollinator Tegeticula yuccasella (Svensson et al. 2011). A female yucca
moth mates with a male in yucca flower and collects pollen in its specialized
mouthparts. She carries pollen to another flower, lays its egg in the ovary
wall and deposits pollen grains on the stigma. The larva after its emergence in
the ovary consumes only a proportion of the seeds from the developing fruit and
the remaining seeds develop normally. After the fruits dehisce, the larvae drop
to the ground, burrow into the soil and construct cocoons. The larvae remain in
cocoons during the winter. Following spring rains, adult moths emerge from the
cocoon. By this time yucca plants would be in flowering and initiate new
pollination cycle. Some pupae may remain dormant in the soil for more than a
year.
Nocturnal Pollination
In a number of species, pollination takes
place at night. As visual attraction is not reliable during the night,
nocturnally pollinated species relay more on olfactory cues. Nocturnally
pollinated flowers are generally drab in color but emit strong smell. Some
species show both diurnal and nocturnal pollination (Young 2002; Dar et al.
2006; Muchhala et al. 2009; Dafni et al. 2012). Moths and bats are the most
important nocturnal pollinators. Moths have superposition compound eyes, where
each rhabdom receives light through a wider aperture consisting of hundreds of
facets. This increases the number of photons caught in dim-light conditions and
thus facilitate nocturnal vision (Warrant 2004).
Bees in general are diurnal; their
foraging activity begins at dawn and ends at dusk. However, several bees have
developed abilities to forage in dim light. Many of them such as Xenoglossa
fulva (Linsley et al. 1955), Xylocopa tabaniformis (Janzen 1964),
Ptiloglossa guinnae (Roberts 1971) and Megalopta genalis (Warrant et
al. 2004) are able to forage during crepuscular (twilight) periods. Some bee
species such as Apis dorsata and Apis mellifera (Dyer 1985) have
been reported to forage nocturnally on moonlit nights. However, Xylocopa
tranquebarica has been shown to be a true nocturnal bee (Somanathan and
Borges 2001; Kelber et al. 2006; Somanathan et al. 2008); it can fly and
navigate even during the moonless parts of nights and so far is the only known
bee to be able to do so. Unlike typical nocturnal insects such as moths which
have superposition compound eyes, all bees including the nocturnal species,
have apposition compound eyes that are well adapted to diurnal vision. X.
tranquebarica has also been shown to exhibit color vision under moonlight,
twilight, and even starlight conditions and is the only insect with apposition
eyes to exhibit color vision under such dim light conditions. Opposition eyes
of X. tranquebarica are larger with large facets and very wide rhabdoms
which make them very sensitive to dim light (Somanathan et al. 2009).
Bats involved in pollination generally
have longer tongues when compared to insectivorous species. Bat-pollinated flower
syndrome includes nocturnal anthesis, drab coloration and musty, fetid odor.
Their flowers are generally placed away from the foliage at the tips of
branches or are borne directly on the trunk or branches (cauliflory). In many
deciduous trees flowering is initiated after defoliation. Flowers of
bat-pollinated species may be tubular or radially symmetrical and produce
relatively large amounts of hexose-rich nectar (Flemings et al. 2009). In flowers
of bat-pollinated Ochroma species as much as 7–15 ml of nectar has been
reported (Faegri and van der Pijl 1971). Amongst floral traits, nocturnal
anthesis, placement of flowers away from foliage and production of larger amount
of nectar are found in almost all bat-pollinated flowers (Fleming 2009). Bats
are long distance pollen dispersers. They use vision, olfaction and
echolocation to locate flowers. They have keen sense of smell that helps in
long-distance location of flowers. Bat-pollinated species generally occur in
low density and bats play a crucial role in maintaining genetic continuity of
their population (Fleming et al. 2009). New World Bats (Phyllostomidae) can
produce ultrasonic sound to locate flowers. The sound is reflected by the
petals of bat-pollinated flowers and bats have the ability of recognize this
reflected sound (echolocation). The erect petals of the flowers of many species
such as Mucuna holtonii have been shown to reflect sound pulses produced
by echolocation bats that visit the flowers for their copious nectar (von
Helversen and von Helversen 1999). Echolocation ability is not developed in
most of the old world bats (Pteropopodidae); they depend largely on olfactory
and visual cues to locate the flowers. The eyes of all bats are well adapted to
low illumination. Old World fruit bats have color vision whereas New World bats
can see only in black-and-white.
Pollination by Ants: A Rare and Ineffective Pollination Syndrome
Ants are among the most abundant insects
on earth and visit flowers frequently. Also, the fossil record shows that ants
were present during the explosive radiation of the angiosperms in the late
cretaceous period even before the presence of bees (Beattie 1985).
Surprisingly, ant pollination has not evolved as a major pollination syndrome
in angiosperms. So far, ant pollination has been documented in less than 20
species of herbs and shrubs (Shivanna 2010). Although ants are active 24 hr. a
day, ant-pollination does not seem to have evolved in any of the night blooming
plant species (Beattie et al. 1984; Beattie 1985; Sharma et al. 2009; see
Shivanna 2010). Interestingly, ant-pollination has not been reported so far in
any tree species. The following are some of the hypotheses put forward to
explain the rarity of ant pollination: 1. Ants bring about largely
geitonogamous self-pollination as their movements are usually restricted to
within the plants. 2. Secretion of antibiotics from metapleural glands present
in most of the ant species (as a defense against bacteria and fungi) reduces
pollen viability. 3. Pollen transfer is not efficient as their body surface is
smooth and pollen grains do not adhere well to their bodies. 4. Ants groom
their bodies too frequently with the result very little pollen is left on the
body for transfer to the stigma.
Most of the observations recorded in
various plant species do show that the movements of ants are restricted within
the plant and most of the pollinations are geitonogamous. They may move between
plants and bring about cross-pollination infrequently only in small herbaceous
species that grow in high density in small patches (Hickman 1974). Studies on
the effects of antibiotics show differential potency among ant species and
differential sensitivity among pollen species (Beattie et al. 1984). Thus,
inhibition of pollen function by exposure to the surface of ants may provide
only a partial explanation for the rarity of ant pollination systems.
Smoothness of the body surface of ants is not universal. Many ant species are
as hairy as bees or are covered with bristles suitable for carrying pollen
load. Although pollen load recorded on ants are generally low (10–30), pollen
load of over 200 grains per ant has been recorded in a few species. Many investigators
have discounted the suggestion that ants groom their body frequently since bees
also groom their body frequently (Beattie et al. 1984). Thus, available evidences
support, to some extent, the first two hypotheses to explain the rarity of ant
pollination.
There is very little information on floral
attractants for which ants are responsive. Although some investigators have
suggested that floral scent could play a key role as floral attractant, there
are no experimental evidences. The nectar acts as the reward for ants. For most
of the species, ants are not exclusive pollinators; they share pollination
services with several winged insects. For example, Balanophora flowers
are visited by a variety of flying insects besides ants (Peakall and Beattie 1989).
However, specialized, exclusive ant-pollination has been reported in two
Australian orchids. Leporella fimbriata (Peakall 1989) is exclusively
pollinated by male winged ants of Myrmecia urens. The other orchid, Microtis
parviflora (Peakall and Beattie 1989) is pollinated by flightless worker
ants of Iridomyrmex gracilis, through sexual deceit.
Non-Mutualistic Pollinations
In a number of plant species, pollination
is achieved through non-mutualistic interaction (Dafni 1984; Renner 2006;
Bernklau 2012). Such plants advertise the presence of reward without offering
the reward and achieve pollination through deceit. Non-mutualistic interactions
have evolved in all major groups of flowering plants. Orchids form the most
important group of non-mutualistic pollination; about one third of the orchids
(over 10,000 species) are estimated to be deceptive (Renner 2006; Jersakova et
al. 2006). Most of the species producing reward-less flowers are pollinated by
insects; however, two of the reward-less species have been reported to be
bird-pollinated and one bat-pollinated (Renner 2006). Many animal visitors also
harvest the rewards of the flower without effecting pollination. Such visitors
are referred to as pollen or nectar robbers. Nectar robbers generally enter the
flower from the side by piercing the corolla tube and harvest the nectar
without coming in contact with the anthers and stigma. Pollen robbers forage
the pollen from the anthers but do not come in contact with the stigma.
Food Deception
Plants of non-rewarding species (mimic)
coexist with rewarding species (model) and the flowers of the mimic resemble
those of the model. Floral visitors draw rewards from the model but do not
discriminate against non-rewarding flowers of the mimic. Food deceptive orchids
generally attract both male and female pollinators. In many food deceptive
orchids, floral color seems to play more dominant role than the extent of
morphological similarity of the model and the mimic (Gigord et al. 2002;
Streinzer et al. 2010). A South Africa orchid, Disa ferruginea (Johnson
1994; Newman et al. 2012), for example, depends on a butterfly species, Aeropetes
tulbaghia for pollination. In the Cape Province (western part of its range)
a red flowered form of this orchid occurs and attracts butterfly visits by
imitating red, nectar-producing flowers of Tritoniopsis triticea (Iridaceae).
The butterfly does not discriminate between the nectarless orchid flower and
the nectar-producing model flower in sympatric populations. Interestingly, in
the Langeberg Mountains (eastern part of its range) an orange-flowered form of D.
ferruginea occurs and mimics the orange, nectar-producing flowers of Kniphofia
Uvaria (Asphodelaceae). The pollinator butterfly preferred red flowers in
the western part where its main nectar model has red flowers while in the east
it preferred orange flowers, where its main model has orange flowers. These
results indicate that the flower color in D. ferruginea is adaptive and
driven by local color preference of its pollinator. Several studies have
indicated that the food deception is largely mediated by visual signals and
olfactory signals do not seem to play any major role. Studies of Galizia et al.
(2005) on a food deceptive orchid, Orchis israelitica and its model Bellevalia
flexuosa (Liliaceae) showed that fragrance compounds in the mimic were
quite different and weak when compared to the model. The odor of the model and
the mimic elicited distinct activity patterns in the brain of its pollinator
bee, indicating that the bee can easily distinguish the flowers of the model
and the mimic on the basis of their odors. As the bee does not discriminate
between the flowers of the two species, odor obviously does not play any role
in signaling. In another study in which both the mimic and the model are
orchids, Salzmann et al. (2007) reported that both the model (Anacamptis
coriophora) and the mimic species (A. morio) emit complex odor
bouquets. Several components of the fragrance of the model triggered electrophysiological
responses in olfactory neurons of honey-bees and bumble-bees. The scent of the
mimic, however, was too weak to elicit any electrophysiological responses
(Salzmann et al. 2007), negating the role of olfactory signals in deception.
The fragrance of the model, however, may still play a role in long distance
attraction of the pollinators to the location where the model and the mimic
grow.
Sexual Deception
A large number of orchids achieve
pollination by sexual mimicry. Most of the species showing sexual mimicry are
pollinated by species of Hymenoptera. Pollination through sexual deception is
often highly specific and attracts a particular species of pollinator. Odor
signal plays a dominant role in sexual mimicry (see Galizia et al. 2005). Flowers
of non-rewarding species mimic visual, olfactory and tactile cues of conspecific
females of the pollinator. Olfactory cues are similar to sex pheromones of
receptive females. For example, sexually deceptive Australian orchid, Chiloglottis
trapeziformis attracts males of its pollinator wasp, Neozeleboria
cryptoides, by emitting a unique volatile compound,
2-ethyl-5-propylcyclohexan-1, 3-dione which is also produced by female wasps as
a sex pheromone (Schiestl et al. 2003). The visitor lands on deceptive flowers
and tries to copulate (pseudo-copulation) and during this process, brings about
pollination. In sexual deception, pollinators are first attracted to the
fragrance signals from a distance but in close vicinity they seem to be guided
exclusively by visual signals (Streinzer et al. 2009).
Kullenberg (1956) was the first to show
the role of fragrance in sexual deception in orchids. Until then it was thought
that sexual mimicry in orchids was mediated only by visual cues. Kullenberg
(1956) covered the flowers Ophrys lutea with a piece of cloth for a few
hours and showed that the cloth attracted its pollinator, Adrena bees.
Subsequent studies confirmed that both visual and volatile chemicals are
involved in attraction of male bees. Flowers showing sexual mimicry produce
complex odor bouquets of a large number of volatiles that are similar to those
produced by the females of their pollinators (see Ayasse et al. 2003). Ophrys
is one of the well-investigated orchids showing sexual mimicry. Different
species of Ophrys produce distinctive qualitative and quantitative
blends of floral fragrance compounds. The fragrance compounds produced by Ophrys
flowers of several species have been shown to be similar to those found in
the mandibular and/or Dufour’s glands of their pollinators (see Williams 1983;
Borg-Karlson 1990). Ayasse et al. (2003) studied the details of fragrance in
the flowers of O. speculum and its pollinator, Campsoscolia ciliata. In
field trials, they used female dummies as control. The male insects hardly
responded to odorless female dummies but were attracted in high frequency to
freeze-killed virgin females and intact O. speculum flowers; Labellum
extracts of O. speculum flowers and cuticular extracts of virgin females.
They identified eight electro-physiologically active compounds. Of these,
9-hydroxydeconic acid was the major one in both the labellum and the insect. In
Ophrys sphegodes, pollination has been shown to result in changes in odor
components (Ayasse et al. 2000; Schiestl et al. 1997, 2003) and thus the attractiveness
of pollinated flowers to its pollinator male bees (Andrena nigroaenea)
decreases. Pollinated flowers showed a significant increase in farnesyl
hexanoate. Flowers treated with farnesyl hexanoate were found to be less
attractive to males indicating that this chemical acts as a repellent and guides
pollinators to un-pollinated flowers (Schiestl and Ayasse 2001). In another
study (Stokl et al. 2009), the odor compounds were analyzed in three
species of Ophrys, O. lupercalis, O. bilunulata, and O. fabrella. All
the species grow sympatrically and are pollinated by three species of Andrena.
These Ophrys species use the same odor compounds for pollinator
attraction, but in different proportions. Thus a change in the concentration of
the constituents of floral odor can result in the attraction of a new
pollinator species that acts as an isolation barrier towards other sympatrically
occurring Ophrys species (Stokl et al. 2009).
Brood Site Deception
Several species mimic brood sites and
attract insects whose larvae feed or lay their eggs on decaying organic matter
such as dung, decaying feces and carrion. Brood site mimicry has been
documented in species belonging to some ten families such as Annonaceae,
Araceae and Aristolochiaceae (see Wiens 1978; Bernclau 2012). Their flowers
mimic the odors of dung and/ or carrion to attract coprophilous beetles and flies
that oviposit or feed on dung or carrion. These odors are very unpleasant to
humans. The odors are composed of sulfide compounds, ammonia, alkylamines,
cadaverine and putrescine. Fecal-like odors are also produced by skatole and
indole compounds (Meeuse 1978; Dettner and Liepert 1994).
In many species showing brood site mimicry,
the odors are enhanced by the production of heat (thermogenesis). Floral
thermogenesis appears to be more common in basal angiosperms and Eumagnoliids
when compared to other angiosperms. It has been reported in 3 families (Nymphaeaceae,
Schisandraceae and Illiciaceae) of basal angiosperms, 6 families (Annonaceae,
Araceae, Arecaceae, Aristolochiaceae, Cyclanthaceae and Magnoliaceae) of
Eumagnoliids, and only 2 families (Nelumbonaceae and Refflesiaceae) of Eudicots
(see Thien et al. 2009). Detailed studies have been carried out on Victoria
amazonica, a thermogenic basal angiosperm (Prance and Arias 1975) in which
beetles are the major pollinators. Flowers are protogynous; they are in the
female phase on day 1 and in the male phase on day 2. Flower buds open in the
evening of day 1, and produce heat (>11ÂșC above ambient) and strong odor
that attract beetles. Flowers close by the next morning trapping the beetles
followed by gradual loss of heat and odor. The flowers gradually turn from
white to deep purplish-red. By evening of day 2, the stamens release pollen and
the flowers reopen. The escaping beetles pick up pollen and fly to another flower
of day 1 which is thermogenic and scented. When beetles are trapped inside the flowers,
they consume starchy stylar appendages. High temperature inside the flower also
seems to act as an energy reward for the beetles in maintaining their body
temperature at endothermic level (Seymour and Matthews 2006). In general,
thermogenesis and trapping mechanism are associated with food deceptive species
which do not provide any rewards to the visitor. But in N. amazonica the
flowers seem to provide rewards in the form of nutrients and heat energy
(Seymour and Matthews 2006).
In species of Aristolochia (Murugan
et al. 2006; Trujillo and Sersic 2006) the flowers are differentiated into an
expanded limb, a long narrow tube of various lengths and a basal expanded
utricle. The inner surface of the tube is lined with downward-pointed hairs
which facilitate the entry of insects into the floral chamber where the sexual
organs are located but not their exit. The flower produces an odor similar to
decaying plant tissues, mimicking the natural oviposition substrate of their
pollinators. Flowers are protogynous and the stigma is receptive at the time of
flower opening. The pollinators (mostly Dipterean flies) are attracted by the
color and odor of the flower, enter the floral chamber through the narrow tube
and are entrapped for 24–48 h as the downward-pointed hairs on the inner
surface of the floral tube prevent their exit. By the time anthers dehisce and
the insects get coated by the pollen, the hairs in the tube become flaccid and
start senescing allowing the flies to escape. The flies, coated with pollen
enter freshly opened flower with receptive stigmas and bring about pollination.
The flowers of some species of
Aristolochiaceae, Araceae, Orchidaceae and Saxifragaceae are pollinated by
fungus gnats. The flowers or floral parts of many such species mimic
oviposition sites (gill fungi) of fungus gnats (the larvae of which feed on
gill fungi) (Vogel and Martens 2000; Okuyama et al. 2004 and references
therein). Some of them also have trap mechanism. The visual mimicry in
combination with emission of odor characteristic of fungi attracts fungus gnats
which oviposit and bring about pollination. The pollination in Mitella (Saxifragaceae)
species differs from other fungus gnat-pollinated species in that the fungus
gnats do not lay their eggs in the flower and seem to consume small amount of
the nectar available (Okuyama et al. 2004).
Aphidophagus hoverflies (Syrphidae)
generally lay their eggs in places of aphid infestation as their larvae feed on
aphids. The orchid Epipactis veratrifolia is exclusively pollinated by
five species of aphidophagous hoverflies (Ivri and Dafni 1977) and the authors
suggested that the flowers in this species mimic the shape and color of aphids
to attract syrphid flies. However, recent studies (Stokl et al. 2010) have
shown that the flowers produce α- and ÎČ-pinene, ÎČ-myrcene and ÎČ-phellandrene
(which are similar to the alarm pheromone released by several aphid species).
The pheromones attract aphidophagus hoverflies. The flies bring about
pollination during egg deposition and nectar feeding. As these pheromones are
not species specific (they attract several species of syrphid flies) and also
the flies consume nectar, Stokl et al. (2010) prefer to call it generalized
mimicry rather than typical mimicry. Evolution
of rewardless flowers and their stability has been discussed by some
investigators (Pellmyr 2002; Renner 2006). Pollinators constantly encounter
rewardless flowers during most of the foraging bouts even within the rewarding
species. This regularity in encountering rewardless flowers makes pollinators
follow flexible foraging. Because of this foraging flexibility pollinators do
not discriminate more strongly against rewardless species (Pellmyr 2002; Renner
2006). It has been suggested that transiently rewardless flowers may have
facilitated the evolution of rewardlessness as a stable strategy because their
presence lowers the strength of selection on pollinators to consistently
discriminate against lack of rewards (Renner 2006).
Restriction of Pollinators
Any natural community is made up of a
number of plant species and a range of animal species, many of which are
potential pollinators. However, each plant species attracts only a proportion
of potential pollinators to visit its flowers in a sustainable way and use them
for pollination services but prevents the visit of several others present in
the community. So far studies on pollination ecology have largely been on floral
attractants and rewards. However, for an efficient pollination system,
restriction of visits to a reasonably limited number of pollinator species is
important to ensure their visits to largely conspecific flowers. Although there
are several studies on the factors which act as filters to prevent the visits
of some animal species, there is hardly any discussion on this aspect in
reviews on pollination ecology. Available evidence indicate that restriction of
floral visitors may act at different levels—morphology of the flowers,
species–specific fragrance, and quantitative and/or qualitative features of the
nectar and of pollen.
Morphological Filters
The role of morphological elaboration of
floral traits that permit some species of pollinators (and prevent some others)
was known since long. Faegri and van der Pijl (1971) referred to such
adaptations that permit only a particular group of animals as ‘harmony’ between
the visitor and the flower. Lack of harmony prevents floral visitors. One such
floral elaboration is the evolution of bilateral symmetry. It enables the flowers
to guide the approach pattern of the visitors to harvest the rewards efficiently.
Flowers of such species are visited only by those animal species that are able
to find and harvest the rewards. Another type of elaboration is the evolution
of the flowers with a long corolla tube or a spur in which nectar is located.
Plant species with such flowers are very common. In southern Africa for
example, long-tube flowers have been reported in about 200 spp. of at least 10
families. A large number of orchids have spurs of various lengths often up to
40 cm. In flowers with long corolla tubes, only insects that have the proboscis
of matching length or birds with matching beak length can harvest the reward. Pollinator
species with different tongue lengths tend to specialize on plant species with
matching spur/corolla tube lengths. Such correlation has been highlighted in
several studies on plant-pollinator communities (Pleasants 1983; Pellmyr 2002;
see also More et al. 2007; Santos-Gally et al. 2013). In a bumblebee community
with different tongue lengths (short, medium and long), a relationship between
the corolla length of the plant species and the tongue-length of the bees that
visit them has been reported even in earlier literature (Pleasants 1983). Such
plant-pollinator relationship reduces competition by restricting the visits of
the bees of various tongue lengths to flowers of matching corolla length. The
bees with tongue-length shorter than corolla length would not visit the flowers
of long corolla tubes since they cannot reach the nectar. Avoidance of the bees
with long tongue-length to visit the flowers with shorter corolla tubes has
been explained on the basis of less efficient foraging (of long-tongued bees on
short corolla tubes) when compared to those with appropriate tongue length.
Another reason put forward to explain this avoidance is the lower net profit to
long-tongued bees in visiting flowers of short corolla tube as they have to
compete with short-tongued bees which would reduce the nectar reward to unprofitable
levels (see Pleasants 1983; More et al. 2007).
Pollination Syndromes
The role of morphological traits of flowers
and their relationship to the pollinators has been elaborated in the form of
pollination syndromes (Faegri and van der Pijl 1971). Since the time of Darwin,
the traditional concept on the evolution of pollination systems has been toward
specialization leading to a greater refinement in making the pollinator and the
flower mutually inter-dependent. Various pollination syndromes such as
beetle-pollinated, bee-pollinated, butterfly-pollinated and bird-pollinated
were identified and described (Table 1). A syndrome is a combination of
phenotypic traits associated with attraction and utilization of specific types
of animals for Pollination syndromes do not form closed compartments and do not
represent exclusiveness of the respective pollinators to the flowers of a
particular syndrome. They also do not indicate the presence of all the specific
traits of a syndrome in all plant species of that syndrome. Pollination
syndromes simply represent traits that are over-represented in flowers that
attract specific types of pollinators; they do not exclude other visitors
(Faegri and van der Pijl 1971; Pellmyr 2002).
Specialization in floral traits leading
to pollination syndromes was explained on the basis of selection pressure
exerted by the pollinators. Different pollination syndromes are often present
in closely related species. For example, Petunia axillaris (flowers
white, nocturnally scented) is pollinated by nocturnal hawkmoth (Manduca sp.)
while P. integrifolia (flowers colored and unscented) is pollinated by
diurnal bee (Hexantheda sp.) (Ando et al. 2001). Similarly, unrelated
plants also show similarities in floral traits; such similarities are
attributed to evolutionary convergence resulting from selection by shared types
of pollinators (Faegri and van der Pijl 1971).
Many recent studies have shown that in a
majority of species, flowers are visited by a number of animal species and the
advanced level of specialization is seen only in a limited number of species.
Based on these studies traditional concept of pollination syndromes has been
questioned (Waser et al. 1996; Waser and Ollerton 2006). However, many
pollination biologists (Pellmyr 2002; Fenster et al. 2004; Bronstein et al. 2006;
Fleming et al. 2009; Mitchell et al. 2009) argue that the concept of
pollination syndromes helps in understanding the mechanisms of floral diversification
and the convergence of floral form across angiosperms pollinated by similar pollinators.
The concept of generalization and specialization is used in terms of the number
of pollinators a plant species attracts. Most of the plants are pollinated by
two or more species, indicating selection against excessive specialization;
this gives pollination assurance even under spatio-temporal variation in
pollinator abundance.
One of the major limitations of assessing
the number of pollinators of a given plant species is the lack of data on
actual pollinators based on pollen transfer. In some plant species, the number
of animal species visiting the flowers is quite large. Over 70 species of
insects have been reported to visit the flowers of Andira inermis (Fabaceae)
(Frankie et al. 1976; see Bawa 1990). In such plant species true pollinators,
on the basis of pollen transfer, are likely to be much less. Some of them may
be casual visitors to explore the availability of resources and some others may
predate on insects that visit the flowers; and yet others may rob the pollen
and/or nectar without bringing about pollination. Further, the frequency of
some of the visitors may be too low to have any impact on pollination efficiency
of the plant species. The number of effective pollinators on the basis of
pollen transfer has been documented only in a limited number of species. In one
of the Syzygium species, S. heyneanum, out of 23 species of floral
visitors’ only three species turned out to be effective pollinators (Giby
Kuriokose, P.A. Sinu and K.R. Shivanna, unpublished). In the absence of such
detailed information, records of the number of visitors to flowers may be
misleading in assessing the number of pollinators of plant species and the
extent of its specialization/generalization. In most of the plant species with
unusually large number of visiting species, the number of pollinators is likely
to be much less than the number of visitors reported. Generalization and
specialization also applies to pollinators. Generalists are those that forage
the flowers of a number of plant species and specialists are those that forage
the flowers of a limited number of species. Specialization is not generally in the
evolutionary interest of flower-visiting animals. Many animal species
specialize when their preferred species is flowering but in the absence of
their preferred species, utilize a wide range of plant species.
Co-evolution
Guided by Darwin’s concept of
co-evolution (reciprocal selection between plant and pollinator), earlier
pollination biologists interpreted most of the diversification of plants and
pollinators as the result of co-evolution. Subsequently it became apparent that
co-evolution is largely restricted to a limited number of species which show
obligate relationship between plant species and its pollinator such as figs and
fi g-wasps, yucca and yucca-moths (Pellmyr 2002; Bronstein et al. 2006), and
several orchids. In these highly specialized pollination systems in which each
plant species is pollinated by just one animal species, the specificity of
pollinators is apparently the result of mutual adaptation of the plant and
pollinator species. Attraction of species-specific pollinator is largely
mediated through morphological elaboration of the flower and/or species-specific
fragrance. Other species do not visit the flowers because these lack matching
flower structure or specific fragrance.
The well-recognized example of
co-evolution, first proposed by Darwin, is the length of floral spurs, and the
length of insect tongues and beaks of birds (see Pellmyr 2002). While
explaining the exceptionally long nectar spur (40–50 cm) of the star orchid in Madagascar,
Angraecum sesquipedale, Darwin proposed that a co-evolutionary ‘race’
(between spur length of flowers and tongue length of insects) acted as a
driving force for the directional increase in the length of plant’s spur (where
the nectar is concealed) and the tongue of its pollinator. Floral visitors
whose proboscis is longer than the length of the spur/corolla tubes of its host
flower, rob the nectar without effecting pollination (as the insect need not
push the proboscis deep enough to bring its mouthparts in contact with the
anthers and the stigma). For effective pollination it is advantageous for the
plant if the length of the spur/corolla tube exceeds the length of its
pollinator tongue so that the pollinator is forced to push the proboscis deep
into the spur thus bringing the mouthparts in contact with the anthers and the
stigma. This would induce directional selection for longer spurs in the
population. Evolution of deeply concealed nectar induces reciprocal selection
in tongue length in the pollinators. This process can continue as long as
genetic variation is available in both the partners. Correlation of plant fitness
with the length of the spur was supported by studies of Nilsson (1988) in an
orchid, Platanthera bifolia, in which spur length ranges from 30 to 50
mm. He shortened spur length by pushing the nectar upward and tying the spur
with a thread and studied the responses of its pollinator moth. When the spur
length was shorter than the length of the proboscis, the moths pushed the
proboscis only up to the level of the spur necessary to forage the reward;
their mouth parts did not come in contact with the sexual organs of the flower
which is necessary for the removal of pollinaria and its deposition on the
stigma. Shortening of the length of the spur proportionately reduced both the
removal of pollinaria (male fitness) and their deposition on the stigma (female
fitness) of visited flowers. Longer the spur length better was the removal of
pollinaria and their deposition.
In contrast to many examples documenting
the effects of selection pressure exerted by pollinators on plants,
plant-mediated selection on pollinators is limited except in those highly
specialized obligate pollination systems. This is largely because of the
difficulty of measuring life-time fitness of pollinators which are mobile. Also
plant-mediated selection on animals is indirect since the plants do not exert
direct effects on the pollinator’s gene flow but only on their food intake (see
Pellmyr 2002). However, plant-mediated selection on animals has been correlated
to differences in bill length and shape in male and female individuals of the
purple-throated Carib (Eulampis jugularis) (Temeles et al. 2000). In
this species the female has significantly longer and curved bill when compared
to the male. The males primarily visit nectar-rich patches of Heliconia
caribaea which has short, straight flowers corresponding to their bills,
whereas females are the primary visitors to flowers of Heliconia bihai, which
has long, curved flowers matching the size and shape of their bills. On the
basis of these studies sexual dimorphism in E. jugularis has been
suggested to have evolved in response to differences in the floral traits of
their primary floral resources. Because of this partitioning, heterospecific
pollen transfer is avoided. Their subsequent studies provided evidence to
indicate that differences in bill length and curvature between sexes in hermit
hummingbirds are also associated with differences in their food plants (Temeles
et al. 2010).
Strong selection on bill size has also
been documented in Hawaiian honeycreeper in response to dietary shift (Smith et
al. 1995). The honeycreeper, Vestiaria coccinea, used its long curved
beak to access nectar in tubular lobelias. These lobelias have now become
extinct or very rare. The bird has now changed its diet to the nectar of Metrosideros
polymorpha, the flowers of which lack corolla. Comparison of the museum
specimens of V. coccinea collected before 1902 with the extant
individuals revealed a significant reduction in bill length in extant
specimens.
Restriction of Pollinators in ‘Open Flowers’
In ‘open flowers’, which are generally
symmetrical without any structural elaboration, pollen and nectar are exposed
and practically any animal that visits such flowers can harvest both pollen and
nectar rewards. Even in such open flowers, there is some degree of specificity;
all animals present in the habitat do not visit the flowers. Syzygium
cuminii (our unpublished observations) for example has a typical open flower.
Apis dorsata and one species of ant are the major visitors to the flowers;
a few other insects such as Apis cerana, Trigona sp., a few wasps
and a butterfly make occasional visits but their frequency is too low to have
any impact on pollination efficiency of the species. Flowers of Passiflora spp.
also have brightly colored open flowers with exposed pollen and nectar.
However, the number of floral visitors reported in different species of Passiflora
is also limited (Varassin 2001; Shivanna 2012b). In a study on pollination
ecology of annual weeds, Shivanna (unpublished observations) observed that Apis
cerana was a regular and frequent visitor to the open flowers of Triumfetta
rhomboidea for pollen, but they never visited open flowers of Abutilon
indicum, Urena lobata and Melochia corchorifolia, which were flowering
sympatrically next to T. rhomboidea. These studies and several others
clearly show that although the rewards in such open flowers are accessible to
any visitor, only a limited number of animal species visit the flowers in spite
of the presence of a large number of insets in the habitat. In many such
species, the number of animal species visiting flowers may not be more than
those flowers with some structural specialization. In such species with open flowers,
morphological filters do not operate; however, they have other filters to
restrict the number of visiting species. Several studies have shown that the
fragrance, nectar and even pollen may act as filters to restrict the number of
species to visit their flowers. These filters may operate in specialized flowers
also.
Fragrance Filters
Most of the studies on floral fragrance
are concerned with their role in attracting floral visitors. As pointed out
earlier, the composition of fragrance is unique to each plant species and
attracts a specific pollinator or a group of pollinators. The fragrance acts as
a filter in many plant species as their flowers lack suitable fragrance to
attract other species. As pointed out earlier, in species with obligate
specialization, fragrance appears to be the main filter. Several studies have
highlighted the role of fragrance in repelling some floral visitors. Omura et
al. (2000) reported that only a few species of insects visit the flowers of Osmanthus
fragrans despite their strong scent and vivid coloration. A butterfly, Pieris
rapae, a potential visitor, never visits the flowers of this species. They
showed that isopentane fraction of floral volatiles, particularly
Îł–decalactone, is a strong repellent to this butterfly. Willmer et al. (2009)
have reported that floral volatiles act as repellents to ants in some species
of Acacia. A meta-analysis of 18 studies on the response of animals to
floral scents by Junker and Bluthgen (2010) have also highlighted the dual
function of floral scents; obligate floral visitors are attracted to floral
scent while those which are facultative and antagonists are repelled by floral
scents.
Nectar Filters
Studies on nectar have highlighted
largely the role of its nutritive components, sugars and amino acids, as
rewards for the visitors. The amount of nectar present in the flower and its
sugar concentration are, to some extent, correlated with the type of animals
visiting the flowers (Baker and Baker 1983). Bee-visited flowers generally have
lower amount of nectar with higher sugar concentration while bat- and
bird-visited flowers have higher nectar volume with lower sugar concentration.
These features are well recognized and form a component of pollination
syndromes.
Although the presence of non-nutritive
metabolites such as alkaloids and phenolics in the nectar was known since long
(Baker 1977), only limited number of studies are available on their role in
attracting or repelling floral visitors (Stephenson 1981; Adler 2000; Adler and
Irwin 2005; Raguso 2004; Wright et al. 2013). In an earlier study Stephenson
(1981, 1982) showed that secondary compounds of the nectar of Catalpa
speciosa are effective in filtering the visitors. The floral nectar of this
species contains iridoid glycosides, catapol and catalposide, which adversely
affected potential nectar thieves (ants and a skipper butterfly, Ceratomia
catalpa). The legitimate diurnal bee pollinators were not affected by these
glycosides. Some South African species of Aloe produce dark brown nectar
with a bitter taste because of the presence of phenolic compounds in high
concentration (1.2–1.5 mg/ml). Detailed studies of Johnson et al. (2006) on one
such species, A. vryheidensis clearly indicated that the main effect of
phenolics in the nectar is to repel inefficient-/non-pollinators. Bulbuls and
white eye, which are effective pollinators are not affected by the bitter taste
of nectar. Bees and sunbirds which are not effective pollinators do not even approach
the flower as they do not like dark brown nectar. Naive honeybees and sunbirds,
however, approach nectar during initial visits but avoid it completely in subsequent
visits. Thus, the dark phenolic component of the nectar functions as a floral
filter by attracting some animals and deterring others by its taste. In another
study Liu et al. (2007) have shown that buck wheat nectar phenolics in
combination with 15–35% sugar syrups attracted Apis cerana but acted as
deterrents below or above this sugar concentration range. Such synergism
between phenolics and sugar may provide a novel mechanism for plants to
preferentially select some pollinators and to reduce energy investment in
nectar.
Presence of alkaloids in plants is quite
common and they act largely as deterrents to herbivores. As mentioned earlier,
the nectar of some species contains alkaloids such as nicotine and caffeine. In
Nicotiana atenuata pollinated by a moth and hummingbirds, presence of
nectar nicotine decreased visitation time and the volume of nectar removed for
both the pollinators, but increased the number of their visits (Kessler and
Baldwin 2006). Interestingly, pollinators removed nearly 70% more nectar from nicotine-silenced
plants (through genetic transformation) in which nectar lacked nicotine
completely when compared to control plants. On the basis of these results they
hypothesized that nectar repellents optimize the number of visits per volume of
nectar produced, allowing plants to keep their nectar volumes small. The flowers
of Coffee and Citrus contain low concentration of caffeine which
does not deter their pollinator bees (Wright et al. 2013; see also Chittka and
Peng 2013). Interestingly, the presence of caffeine in the nectar has been
shown to significantly enhance the memory of bees; honeybees rewarded with
caffeine were three times more likely to remember the reward when compared to
honeybees rewarded with sucrose alone.
Floral nectar of several species is
scented. The nectar scent compounds in some species have been shown to be a
subset of the compounds emitted by the surrounding floral tissues, while in
some others they contain unique scent compounds compared to the floral tissues
(Raguso 2004). In a detailed study, Kessler and Baldwin (2006) analyzed
secondary metabolites in floral and nectar fragrance of Nicotiana atenuata and
studied their responses on their pollinators (one moth and two hummingbird
species) and a nectar robber (one ant species). Various components of the
fragrance showed positive or negative effects on different animals tested.
Compounds from the same biosynthetic class tended to evoke similar responses.
Benzyl acetone attracted the pollinators (moth and hummingbirds). Methyl
salicylate repelled hummingbirds and ants but attracted moths. Although studies
on nectar filter so far are limited, they have clearly shown that the nectar
can act as one of the effective filters favoring some floral visitors and
deterring others (Kessler and Baldwin 2006, 2011).
Pollen Filters
Nutritional quality of pollen is highly
variable; some of them lack several essential nutrients and some are poor in
proteins (Roulston and Cane 2000; Rasmont et al. 2005) and yet others contain
secondary compounds which are repellent or toxic to insects (Pimentel De
Carvalho and Message 2004; see Hargreaves et al. 2009; Sedivy et al. 2011).
There is much evidence to indicate that pollen can act as a filter to select floral
visitors.
Several studies have analyzed pollen
loads of bee species to check the extent of their host specificity. Pollen load
analyses of 35 species of the genus Chelostoma (Megachiledae) revealed
that 33 species to be pollen specialists at the level of plant family or genus
(Sedivy et al. 2008). In another study on pollen load analyses, Muller and
Kuhlmann (2008) reported that 26 species of the genus Colletes (Colletidae)
out of the 60 species analyzed, were specialists at the level of plant family,
subfamily or genus and the remaining 34 species were pollen generalists to varying
degrees, visiting the flowers of up to 15 plant families. Fourteen of the
specialist species were found to harvest exclusively or predominantly the
pollen of Asteroideae. However of the 34 pollen generalist species Asteroid
pollen formed a very small proportion (<3 27="" a="" acids.="" adaptations="" although="" amino="" and="" asteroideae="" at="" based="" be="" bees="" bl="" both="" bumblebees.="" bumblebees="" choices="" collected.="" collected="" colonies="" constrained.="" contain="" content="" developed="" did="" differed="" digest="" digestibility="" essential="" feeding="" flowers.="" foragers="" generalist="" generally="" have="" higher="" honeybees="" host="" hosts="" in="" investigated="" leonhardt="" load="" loads="" located="" majority="" may="" more="" not="" nutritional="" o:p="" obviously="" of="" on="" only="" patterns="" physiological="" physiologically="" plant="" pollen.="" pollen="" protein="" quality="" range="" recent="" remaining="" same="" seems="" select="" seven="" site="" species="" study="" the="" their="" they="" thgen="" this="" those="" thus="" to="" unfavorable="" use="" visited="" were="" which="" with="">
Several experimental studies have shown
that bees, when offered pollen of several species, prefer pollen of some
species over others. In one of the early studies, Schmidt (1982) reported that
honeybee species, Apis mellifera, preferred pollen of almond over desert
broom, saguaro (Carnegiea sp.), and Creosote (Larrea sp.). In
another set of experiments, the pollen of maple was preferred over that of
cottonwood (Populus sp.), dandelion (Taraxacum sp.) and pine. The
amount of pollen removed by A. mellifera from preferred species was significantly
higher when compared to pollen of others. Thus this intrinsic ability of the floral
visitors to discriminate pollen of different species can act as a filter.
Some studies have been carried out on the
effects of feeding host and non-host pollen to bee species on the development
of their larvae. Pollen of Sinapis arvensis (Brassicaceae) and Echium
vulgare (Boraginaceae) failed to support larval development of Colletes bee
species specialized on pollen of Campanula (Praz et al. 2008a).
Similarly, pollen of Asteraceae and Ranunculaceae permitted larval growth of
only those bee species that are specialized to harvest pollen from plants
belonging to these families; their pollen failed to support larval growth of
other bee species. Recognition of host pollen in specialized species seems to be
genetically determined (Praz et al. 2008b). They compared the floral
preferences of one of specialized bee species, Heriades fruncorum (Megachiledae,
specialized on Asteraceae pollen), reared on host and non-host pollen. Bees
restricted pollen collection to host flowers irrespective of whether they were
reared on host or non-host pollen. Recently, Sedivy et al. (2011) studied
larval performance of two generalist solitary bees, Osmia bicornis and O.
cornuta on pollen diet of four plant species. The larvae of O. bicornis developed
well on pollen diet of Ranunculus but failed to develop on Echium pollen;
it was the reverse for the larvae of O. cornuta. Larvae of both the
species developed well on pollen of Sinapis, but failed to develop on
pollen of Tanacetum vulgare (Asteraceae). These studies clearly indicate
that palatability of pollen can act as an effective filter to restrict the
number of floral visitors. Pollen of non-host species may hamper the digestion
of the larvae and the bees seem to have adapted their metabolism to digest
pollen of their host species.
Concluding Remarks
Enormous information has accumulated over
the years on pollination ecology but our understanding on several aspects in
this field is far from complete (Mayer et al. 2011). Although biotic
pollination evolved in a few gymnosperms and is present in several extant
species, it is not refined and may not be more efficient than wind pollination
prevalent in a majority of gymnosperms. Lack of specialization in attracting a
wider range of pollinators resulting in inefficient pollination may be one of
the primary reasons for lack of diversification in entomophilous gymnosperms.
Evolution of the flower in angiosperms with nectar as a reward enhanced floral
attraction leading to marked improvement in the frequency and consistency of
the pollinators’ visits. Apart from enhanced pollination efficiency, other
innovations of the flower particularly the pistil, and evolution of zygomorphy
with its further elaboration leading to floral specialization seems to have
contributed to reproductive success and dramatic diversification of
angiosperms.
The central focus on biotic pollination
is the ability of plants to achieve conflicting demands of attraction and
restriction of animal species for pollination services. A major limitation of
the enormous data accumulated on biotic pollination is the lack of clear
distinction between the pollinator(s) and floral visitors in most of the
investigations. It is important for pollination biologists to confirm
pollinators and their efficiency amongst floral visitors on the basis of pollen
transfer to the stigma. Also, biotic pollination is dynamic and shows temporal
and spatial variations. It is desirable to study pollination at different
locations and during the entire duration of the flowering period for a clear
understanding of pollinators’ variability in time and space and its impact on
pollination success. Studies on biotic pollination have become more complicated
in the light of the reports that many insect pollinators, in the absence of
preferred flowers in the habitat, are able to exploit other floral resources by
associative learning of floral odors and/or colors with the reward (Riffell
2011). There are even reports of honeybees visiting the flowers of
wind-pollinated species to harvest their nutritive pollen source when insect
pollinated plants are not available (Keller et al. 2005; Hocheri et al. 2012).
Our understanding on various floral
attractants and their role in pollinators’ attraction, and the details of
various floral rewards is comprehensive. Considerable information is also
available on deceptive pollination. Restriction of floral visitors is as
important as their attraction for an efficient pollination system to work. The
role of morphological and fragrance filters in specialized flowers that limit
the number of animal species with matching features to harvest the reward and
consequently eliminate others that are incapable of harvesting the rewards are
well documented. The factors responsible for restricting the number of visitors
to ‘open flowers’ seems to be more subtle. Although several recent studies have
indicated the role of fragrance, nectar and pollen acting as filters in restricting
animal visitors, such studies are limited and they need to be extended to a
larger number of species. The role of nectar components particularly the
secondary metabolites, which was largely ignored so far, needs to be
investigated with more vigor. The role of pollen, its quality, digestibility
and toxicity seem to play an important role in attracting/ restricting
potential pollinators. Interestingly most of the pollen species that have been
found to be unfavorable for the development of larvae of several bee species
happen to have flowers with fully accessible pollen (Sedivy et al. 2011 and
references therein) indicating that pollen filter may be primarily responsible
for limiting the number of visitors to open flowers. Available evidence clearly
indicates that a combination of floral traits —floral morphology, its
fragrance, the quality and quantity of both nectar and pollen rewards—seem to
be involved in achieving the dual function of attraction and restriction of floral
visitors. The role of each of these may vary between species. Hopefully future
studies would try to dissect these functions with appropriate techniques for a
better understanding of the role of different components of the flower, the
most innovative organ of angiosperms, in achieving the dual functions.
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