back to the past for pollination biology

Available online at www.sciencedirect.com

Back to the past for pollination biologyDanny Kessler and Ian T Baldwin

Manipulations of the interactions between plants and their floral

visitors remain the most successful path to an understanding of

floral traits, which may have been shaped by both herbivores

and pollinators. By using genetic tools in combination with old-

fashioned field work the dual protective/advertisement

functions of floral traits are being realized. The distinction

between wanted and unwanted floral visitors is blurring, and

plants with specialized pollination systems are being found

capable of using alternative pollinators if the specialized

pollinators fail to perform.

Address

Max-Planck-Institute for Chemical Ecology, Hans-Knoll Straße 8, 07745

Jena, Germany

Corresponding author: Baldwin, Ian T ([email protected])

Current Opinion in Plant Biology 2011, 14:429–434

This review comes from a themed issue on

Biotic interactions

Edited by Giles Oldroyd and Silke Robatzek

Available online 27th April 2011

1369-5266/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2011.03.023

IntroductionIn 1879, Kerner von Marilaun’s book ‘The Protective

Means of Flowers Against Unbidden Guests’ [1],

launched the conceptual and experimental analyses of

plant-pollinator interactions in an evolutionary context.

His book examined how flowers manage to balance the

attraction of mutualists and antagonists to maximize

their fitness and provided the first experimental tests

of insect-mediated pollination (Figure 1C), seed disper-

sal, and floral traits that afforded protection against

herbivores and nectar robbers [2]. Unfortunately this

approach was largely lost as the fear of ‘teleological

arguments’ stymied evolutionary thinking among Euro-

pean biologists [3]. It has taken biologists more than a

century to find their way back to the questions that

Kerner von Marilaun posed.

Simple manipulations of floral chemistryIn this first decade of the 21st century questions of how

plants attract pollinators while fending off herbivores or

micro-organisms are once again hot topics, and as is

commonly the case with research in ecology, theory

has rapidly outpaced the available data. Excellent theor-

www.sciencedirect.com

etical analyses and reviews by Adler [4,5] and Raguso [6]

have inspired a new generation of pollination biologists

who are grappling with how herbivores and pollinators act

together to shape floral traits [7�,8�] or understand the

origins of the cocktail of chemicals found in nectar, some

of which may originate from microbes inhabiting nectar

rather than the plant [9�], or that pollinators may even

vector the microbes that produce the scents [10,11].

Theory aside, simple manipulative experiments, coupled

with keen observations of the consequences of the manip-

ulation for the assembly of floral visitors, remains the most

frequently successful path to understanding the complex

chemical traits a plant uses to manipulate their visitors.

For example, Shuttleworth and Johnson [12��] found that

by only changing the sulphur compounds in the floral

headspace of Eucomis plants could shift the flower’s

pollination system from specialized carrion flies to pom-

pilid wasps. Similarly simple was Majetic et al. [13]

approach of scent augmentation; they used inflorescences

as scent emitters in different floral color backgrounds, an

augmentation that increased pollinator visitation rates.

The number of traits that plants use to attract pollinators

has increased with the addition of warm nectar [14] and

inflorescences that potentially hail pollinators by ‘waving’

[15] to the already long list of attractive traits.

Similarly simple manipulations of nectar constituents

[16–18] have proved equally illuminating. Irwin and

Adler [18], for example, discovered alkaloids in the nectar

of Gelsemium sempervirens, a bee-pollinated jessamine, and

demonstrated by addition experiments, that the alkaloids

functioned as repellents. There’s still much to learned

from experiments that manipulate the basic ingredients

of nectar, such as sugar composition [19] or nectar volume

[20], and these experiments underscore how small

changes can have very large effects on certain pollination

systems. The same simplicity of experimental approaches

can also provide compelling insights into the behavior of

pollinators, as Riffel et al. [21��] demonstrated with their

simple choice tests with naive or experienced moths

which demonstrated that hawkmoths use olfactory learn-

ing to feed from agave flowers.

Manipulating the interactions with geneticallymodified plantsManipulation is the gold standard of proof for everything

in biology and was the standard that Kerner von Marilaun

set with his early work. But there are limitations to the

conclusions one can draw from the simple manipulations

described above. Spiking nectar with new constituents or

perfuming floral bouquets invariably fails to mimic the


mailto:[email protected]

http://dx.doi.org/10.1016/j.pbi.2011.03.023

430 Biotic interactions

Figure 1

Current Opinion in Plant Biology

(a) (c)

(b)

Plants solve the problem that floral advertisements attract herbivores as well as pollinators through a variety of morphological and chemical means. (A)

The opportunistic nectar foraging of day-active hummingbirds, Archilochus alexandri, makes this floral visitor the principle pollinator of the normally

night-flowering plant, Nicotiana attenuata, which is usually pollinated by night-active hawkmoths such as Manduca sexta (B) but produces morning-

open flowers when M. sexta larvae attack plants [35��]. (C) Pollination of Spartium scoparium by the carpenter bee Xylocopa violaceae elicits flower

closure after the flower plasters pollen on the under surface of the insect’s body described by Kerner von Marilaun 1895 [2]. A similar phenomena was

described by Willmer et al. [34��] in which the flowers of another legume species undergoes a color change if insufficiently pollinated, allowing the

flower to re-advertise for pollination services.

Illustration is taken from the book ‘The Natural History of Plants’, Vol. 2 by Kerner von Marilaun, 1894–1895.

kinetics and quantities of natural emissions, parameters of

likely functional importance. Recent advances in our

understanding of the biosynthesis of floral scents in model

and non-model plants has made it possible to genetically

manipulate floral bouquets [22], nectar composition [23],

or floral morphology [24].

When these genetic tools are combined with old-

fashioned field work and observational approaches, the

sophistication with which plants solve the ecological

challenges resulting from floral advertisement is

revealed. By genetically silencing benzylacetone pro-

duction, the main floral volatile component in the native

tobacco Nicotiana attenuata, by transforming plants with

RNAi constructs that targeted a floral chalcone synthase

gene, Kessler et al. [25��] were able to demonstrate the

centrally important role that this floral scent played in

attracting pollinating moths, which in turn increased the

fitness of the plant through both maternal and paternal


components. Conducting field work with such manipu-

lated plants allows for an unbiased analysis of the entire

floral visitor community, including nectar robbers or

florivores, in addition to pollinators [25��], information

that allows us to understand floral traits in their full

complexity. Moreover, by analyzing the phenotypes of

transformed plants in natural habitats allow researchers

to use the behavior of floral visitors to indentify plant

traits that otherwise might have been overlooked. Bezzi

et al. [16] demonstrated that silencing an important leaf

defense gene that codes for the production of trypsin

proteinase inhibitors (TPIs), substantially altered how

plants interact with their floral insect visitors. Silencing

TPIs in N. attenuata changed the processing and

secretion of nectar proteins, which in turn increased

the levels of nectar H2O2, and made the nectar repellant

to floral visitors. Had the floral visitors not pointed out the

change in nectar properties, the researchers would not

have noticed this on their own.


Back to the past for pollination biology Kessler and Baldwin 431

In addition to manipulating plant traits thought to be

important for pollinator interactions, molecular tools

have also been used to enhance the observational and

more descriptive components of the interaction. For

example, Wilson et al. [26] developed a PCR-based

method to identify pollen collected by wild bees. This

method allows for high throughput analyses of mixed

pollen loads of particular pollinators and could help to

quantify the host range as well as efficiency of different

pollinators. Microsatellite markers have the potential to

distinguish pollen donors among closely related individ-

uals [27] and may become a useful tool for pollination

biologists eager to measure pollen flow in native popu-

lations.

‘Specialist’ and ‘generalist’ pollinatorsSince the time when Kerner von Marilaun wrote his

treatise, biologists are no longer being trained in natural

history observation skills, but this has not noticeably

slowed the number of different taxa whose visits to

flowers have been shown to vector pollen. In the past

two years, pollination by mice [28], crickets [29], ants [30],

thrips [31] or different flies [32,33] has been reported.

Given the diversity of different pollinator taxa, the emer-

ging chemical complexity of floral scents and nectar

metabolites should come as no surprise. Plants will

require a lot of sophisticated chemistry to winnow the

wanted pollinators from the unwanted floral visitors.

But even this distinction, between wanted and unwanted

visitors is blurring in more recent research, particularly in

apparently specialized pollination systems, where plants

appear to have back-up plans if the main pollinators fail to

perform or simply ‘misbehave’. The conflation of ‘flower

visitor’ and ‘pollinator’ is a major problem for pollination

biologist and plant alike, as nicely illustrated in the

research by Willmer et al. [34��] on the flowers of the

legume Desmodium setigerum. These flowers are ‘tripped’

by bee floral visitors, and undergo a color change, provid-

ing a signal to pollinators that visitation has occurred.

However if the visitor turns out to be an inadequate

pollinator, the flowers reverse the color change, signaling

that further visits by other pollinator guilds later in the

day are invited to improve pollination effectiveness.

Similarly, the night flowering tobacco N. attenuata seeks

pollination services from other opportunistic floral visi-

tors, yet for another reason. This plant normally produces

flowers that open at night and release benzyl acetone

(BA) to attract night-active hawkmoth pollinators

(Figure 1B), which are both herbivores and pollinators.

When plants are attacked by the larvae of pollinating

hawkmoth adults, the plants produce flowers with

reduced BA emissions that open in the morning and

are preferentially pollinated by day-active humming-

birds (Figure 1A; [35��]). Hence by switching pollinators,

the plant avoids the ovipositions that frequently accom-

pany nectaring by the adult moths.


One of the liabilities of relying on specialized pollinators

is that they are not always present, and when this hap-

pens, secondary floral visitors can benefit from the unused

nectar rewards welling up in the corolla to provide limited

pollinator services [36]. Detailed observational analyses

of bird pollinated flowers has shown that opportunistic

floral visitors can provide successful pollination services in

specialist flowers [37].

The distinctions are also blurring for plants with apparent

‘generalist’ floral traits, which turn out to have highly

specialized pollination systems on closer examination.

The African milkweed, Pachycarpus grandiflorus, for

example, produces open flowers with copious amounts

of exposed nectar that would appear to be available to all

floral visitors. However the nectar is highly unpalatable

and the flowers are cryptically colored producing a very

special scent which appears to exclude most potential

floral visitors and attract a specialist wasp species for

pollination [38].

While most plants use scents which are floral-specific to

attract or manipulate the behavior of floral visitors, some

plants use scents that are characteristically released by

leaves in their floral bouquet, scents which function as

indirect defenses of leaves. The flowers of the orchid

Epipactis helleborine use green-leaf volatiles (GLVs), usually

emitted from damaged plant tissues and known to guide

parasitic and predatory wasps to their hosts, to lure these

parasitic wasps for pollination services [39��]. The deceit-

ful use of leaf indirect defenses to lure carnivores for

pollination services is just another example in a long line

of deceitful strategies used by orchids to acquire pollina-

tion services. Another example is an orchid whose flowers

produce volatiles similar to alarm pheromones of aphids to

attract aphid feeding hoverflies that provide pollination

services [40]. Other orchids were found to produce bee

pheromones to attract bee-hunting predacious wasps [41].

Lastly, some pollinators have been shown to provide both

defense and pollination services, as is the case with Crotonsuberosus (Euphorbiaceae) were a predacious wasp both

pollinates and defends flowers against florivores [42].

Although generalized pollinator-plant systems are

thought to be more common in the plant kingdom than

specialized ones [43,44], the majority of researchers have

focused on the specialist systems. We are just beginning

to explore the complexities of generalized pollination

systems to understand how flowers manage the larger

number of different floral visitors [34��,45–48], as well as

to better understand the selective forces which result in

specialized pollination systems [47,49].

When flowers attract herbivores andpollinatorsKerner von Marilaun described flower traits, including

trichomes, glandular hairs, strategically positioned on



floral organs, or scents, to ensure the visitation by a

pollinating species rather than herbivores and nectar

robbers. However since this work, herbivory and pollina-

tion have been studied by different researchers with little

exchange between the research communities. That sec-

ondary metabolites in nectar or floral scents can deter

nectar robbers and florivores was only recently demon-

strated [4,25��] and is likely another reason for the diver-

sity of floral scents. Similarly, it has only recently been

shown that nectar robbers [50] or herbivores [51–53] can

negatively influence the pollinating community due to

the activation of systemic induced defense mechanisms

in the plant. Chemical changes in the floral tissue after

herbivory may reduce pollinator attraction in some

species [8], but the effects may not be all negative, as

recently shown in Cucurbita pepo subsp. texana where

herbivory increased floral volatile production in male

flowers [54�].

Many insect species have life stages with opposing fitness

effects for plants: the adult function as pollinators, while

the larval stages are herbivores, frequently on the same

plant. Bronstein et al. [55�] examined this conflict in

Datura wrightii, a highly self-compatible Solanaceous

species, in which an herbivorous pollinator depositing

either outcrossed or self pollen almost doubled fruit and

seed set compared with unvisited flowers. This suggests

that enhanced pollination services selects for the toler-

ance of this herbivorous pollinator. However plants still

have additional possibilities to cope with herbivorous

pollinator larvae by secondary defenses, switching the

opening time of flowers [35��], or aborting fruit, as is the

case with the well described Yucca-Tegeticula moth mutu-

alism.

Learning from extrafloral nectarRecent research on extrafloral nectar, as with floral nectar,

has revealed that nectar is chemically more complex than

originally thought. By coupling functional studies of extra-

floral nectar with a phylogenetic approach, researchers

have discovered that Acacia trees harboring facultative

and obligate ant mutualists produce extrafloral nectar with

an amino acid composition capable of shaping the structure

of the ant–plant mutualism [56]. Moreover, this extrafloral

nectar is also replete with antimicrobial proteins and

enzymes which preserve the nectar for the intended mutu-

alists [57,58]. Comparisons of extrafloral nectar defense

strategies and their consequences for the community of

floral visitors are likely to be illuminating [59].

ConclusionsThe past few years have witnessed a resurgence of theory

which promises to unite functional analyses of plant–pollinator and plant–herbivore interactions. The theor-

etical developments have far out-paced the available data,

and few of the functional analyses are able to quantify the

effects of the traits in a fitness currency. The manipula-


tive power of molecular biology is only slowly being

applied to these questions, partly due to the regulatory

challenges posed by pollination experiments with geneti-

cally modified plants. What Kerner von Marilaun stated in

his book is as true today as it was in 1879: ‘Most research-

ers give priority to what seems at the time to be most

important; and . . . the functional significance of morpho-

logical characters is often not deemed important.’

References and recommended readingPapers of particular interest, published within the annual period ofreview, have been highlighted as:

� of special interest

�� of outstanding interest

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3. Hartmann T: The lost origin of chemical ecology in the late 19thcentury. Proceedings of the National Academy of Sciences of theUnited States of America 2008, 105:4541-4546.

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7.�

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Phylogenetic analyses of 44 plant-insect networks demonstrated thatherbivores interact with plant species that are more closely related toeach other than pollinators are supporting the generalization that plantphylogeny constrains pollinators less than herbivores.

8.�

Kessler A, Halitschke R: Testing the potential for conflictingselection on floral chemical traits by pollinators andherbivores: predictions and case study. Functional Ecology2009, 23:901-912.

Antagonistic pleiotropic interactions can result from the use of the samechemistry in the protection of leaves and flowers; experiments andliterature review suggests that inducibility by herbivore attack can alle-viate some of the fitness costs of these chemical interactions.

9.�

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Floral nectar from 130 species in 44 plant families was examined micro-scopically for the presence of yeast cells, which occurred regularly andsometimes attained extraordinary densities.

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12.��

Shuttleworth A, Johnson SD: The missing stink: sulphurcompounds can mediate a shift between fly and wasppollination systems. Proceedings of the Royal Society B-Biological Sciences 2010, 277:2811-2819.

By comparing floral scent bouquets and experimentally manipulatingfloral scents of field-grown plants, the production or suppression ofsulphur compounds (dimethyl disulphide and dimethyl trisulphide) inthe fragrance bouquet was shown to account for the shift between waspand fly pollination systems in four Eucomis congeners.


Back to the past for pollination biology Kessler and Baldwin 433

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14. Norgate M, Boyd-Gerny S, Simonov V, Rosa MGP, Heard TA,Dyer AG: Ambient temperature influences australian nativestingless bee (Trigona carbonaria) preference for warmnectar. PLoS ONE 2010, 5:e12000.

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16. Bezzi S, Kessler D, Diezel C, Muck A, Anssour S, Baldwin IT:Silencing NaTPI expression increases nectar germin,nectarins, and hydrogen peroxide levels and inhibits nectarremoval from plants in nature. Plant Physiology 2010,152:2232-2242.

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21.��

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25.��

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34.��

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35.��

Kessler D, Diezel C, Baldwin IT: Changing pollinators as a meansof escaping herbivores. Current Biology 2010, 20:237-242.

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39.��

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53. Torres I, Salinas L, Lara C, Castillo-Guevara C: Antagonists andtheir effects in a hummingbird-plant interaction: fieldexperiments. Ecoscience 2008, 15:65-72.

54.�

Theis N, Kesler K, Adler LS: Leaf herbivory increases floralfragrance in male but not female Cucurbita pepo subsp.texana (Cucurbitaceae) flowers. American Journal of Botany2009, 96:897-903.

The experimental leaf damage in Cucurbita pepo subsp. texana leads toincreased fragrance production in male but not female flowers.

55.�

Bronstein JL, Huxman T, Horvath B, Farabee M, Davidowitz G:Reproductive biology of Datura wrightii: the benefits of aherbivorous pollinator. Annals of Botany 2009, 103:1435-1443.

Pollination systems are typically complex, involving moths (here, Manducasexta) that visit the flowers of multiple species of plants (here, Datura wrightiiand Agave palmeri) but also deposit eggs on one of the plants (D. wrightii),and yet these complexities are rarely studied. For this system, despite thepotential costs of herbivory and mixed pollen loads, Manduca visitationswhich deposited either outcross or self pollen on Datura stigmas, almostdoubled fruit and seed set compared with unvisited flowers.

56. Gonzalez-Teuber M, Heil M: The role of extrafloral nectar aminoacids for the preferences of facultative and obligate antmutualists. Journal of Chemical Ecology 2009, 35:459-468.

57. Gonzalez-Teuber M, Eilmus S, Muck A, Svatos A, Heil M:Pathogenesis-related proteins protect extrafloral nectar frommicrobial infestation. The Plant Journal 2009, 58:464-473.

58. Gonzalez-Teuber M, Pozo MJ, Muck A, Svatos A, Adame-Alvarez RM, Heil M: Glucanases and chitinases as causalagents in the protection of Acacia extrafloral nectar frominfestation by phytopathogens. Plant Physiology 2010,152:1705-1715.

59. Hernandez-Cumplido J, Benrey B, Heil M: Attraction of flowervisitors to plants that express indirect defence can minimizeecological costs of ant–pollinator conflicts. Journal of TropicalEcology 2010, 26:555-557.


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