Concepts of pollinator performance: is a

simple approach necessary to achieve a

standardized terminology?

Leandro Freitas

Brazilian Journal of Botany

ISSN 0100-8404

Braz. J. Bot
DOI 10.1007/s40415-013-0005-6

1 23
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 Author's personal copy
Braz. J. Bot (2013) 36(1):3–8
DOI 10.1007/s40415-013-0005-6
REVIEW PAPER
Concepts of pollinator performance: is a simple approach
necessary to achieve a standardized terminology?
Leandro Freitas
Received: 29 January 2012 / Accepted: 18 February 2013 / Published online: 5 April 2013
Ó Botanical Society of São Paulo 2013
Abstract Quantifying the importance of pollinators for
reproductive success of plants is a central question in
reproductive biology. However, the literature contains a
profusion of terms and sometimes conflicting definitions.
This inconsistency is a barrier to broad comparisons and
conceptual advances in different fields. In recent decades,
some widely disseminated studies have proposed recom-
mendations to foster greater standardization. Nevertheless,
the literature continues with little uniformity, and terms
such as ‘‘efficacy,’’ ‘‘efficiency,’’ and ‘‘effectiveness’’ of
pollinators are still used inconsistently. Previous studies
concerning conceptual and terminological uniformity pro-
vided a series of particular terms related to specific metrics
and/or strict definitions for these widely used terms. I here
propose comprehensive verbal definitions for the terms that
have historically been used by most specialists. Pollinator
performance in achieving reproductive success is defined
here as its effectiveness, which is, broadly, given by the
product of two components: pollinator efficacy and inten-
sity of visitation. In some approaches, a third component –
pollinator efficiency – is important for estimates of its
effectiveness. The definitions suggested here apply to dif-
ferent variables, parameters, and procedures for study, and
may refer to either individuals or populations of a polli-
nator species, or to functional groups of pollinators. This
terminology can be applied widely, as it is not constrained
by the scope, approach or scale of a study. A basic ter-
minology with simple definitions may facilitate consistent
use of these terms by specialists, particularly among
younger investigators, thus surmounting the first barrier to
L. Freitas (&)
Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 915, Rio de
Janeiro, RJ 22460-030, Brazil
e-mail: leandro@jbrj.gov.br
future proposals for conceptual and methodological unifi-
cation at larger scales.
Keywords Fitness
Pollinator effectiveness

Pollinator performance
Plant reproductive success
Introduction
In recent decades, pollination biology has incorporated an
extensive new body of theoretical background and proce-
dures for data gathering and analysis, as well as interac-
tions with other disciplines, and applications to questions
of wide interest, such as environmental services and bio-
diversity conservation, and responses to global climatic
changes, habitat conversion, and biological invasions
(Kearns and Inouye 1994; Dafni et al. 2005; Traveset and
Richardson 2006; Aizen et al. 2008; Mitchell et al. 2009;
Mayer et al. 2011). For instance, the debate on the validity
of the concept of pollination syndromes and on special-
ization versus generalization in pollination systems has
remained intense since it began in the mid-1990s (Waser
et al. 1996; Fenster et al. 2004; Ollerton et al. 2007, 2009).
In addition, the use of the interacting-webs approach has
opened new avenues for research in the last decade, in
particular for community-based studies (Memmott 1999;
Vázquez et al. 2009). As expected in such a lively scenario,
concepts in pollination biology have been refined or
expanded, new terms have been formulated, and the old
ones are employed in new ways (Inouye et al. 1994).
However, these innovations are spread over many articles,
and the inconsistent and ambiguous use of terms among
them inhibits the development of a common terminological
and conceptual framework.
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4 L. Freitas
Although, strictly, pollination proceeds from the release
of pollen from the anthers to its deposition on a conspecific
stigma (Faegri and van der Pijl 1979; Inouye et al. 1994),
for a more comprehensive understanding of pollination it is
necessary to evaluate its effects on subsequent (‘‘post-
pollination’’) processes (Herrera 2000), such as pollen
germination and pollen-tube growth, ovule fertilization,
fruit and seed set, and seeds sired on other plants. Also,
pollination encompasses a wide diversity of traits of both
flowers and pollinators (Endress 1994). The completion of
the process (i.e., the contribution to male and female
reproductive success) is also affected by the architecture
and size, and the population structure and dynamics of the
plant species (Karron and Marshall 1990; Murcia and
Feinsinger 1996; Ollerton and Lack 1998; Kato and Hiura
1999), as well as by the abiotic component of the envi-
ronment and the composition and structure of the flora and
fauna (Herrera 1988; Pellmyr and Thompson 1996; Kearns
et al. 1998; Thompson and Cunningham 2002; Ollerton
et al. 2007; Mitchell et al. 2009; Mayer et al. 2011).
Most angiosperm species are pollinated by animals
(Ollerton et al. 2011), and in the great majority of cases,
pollination is carried out by different species belonging to
one or more taxonomic groups (Waser et al. 1996; Kearns
et al. 1998; Freitas and Sazima 2006) that differ in their
pollination ability (Faegri and van der Pijl 1979; Fenster
et al. 2004). Thus, the contribution of pollinators to plant
reproductive success is an increasingly important topic for
studies on floral evolution and the ecology of mutualistic
interactions (Mitchell et al. 2009), and also important
because of emerging needs for risk assessment in conser-
vation and sustainable agriculture that require multi-year
and multi-site comparisons across studies (Ne’eman et al.
2010). However, this topic is a fair example of the con-
sequence of application of many different procedures and
inconsistent use of terminology.
This latter question has attracted the attention of some
authors, in particular those who were engaged in writing
about methods in pollination biology. For instance, the
question was highlighted in the two most important text-
books on the topic: Kearns and Inouye (1994), who
reproduced the proposals by Inouye et al. (1994), and Dafni
et al. (2005) in chapters by Caroline L. Gross, Peter
Bernhardt, Judith Slaa and Koos Biesmeijer. These two
books are fundamental sources for novice fieldworkers in
pollination biology, and are well regarded among experi-
enced pollination biologists. More recently, Ne’eman et al.
(2010) presented an extensive and updated review on
metrics and use of terms for pollinator performance, in
addition to proposing equations and terminology within a
modular system. The aim of this latter study was to provide
standard field protocols, metrics, and definitions to facili-
tate broad comparisons of pollinator performance. Despite
123
the robustness and visibility of these proposals, the litera-
ture on the topic seems to have remained as unstandardized
as before.
In this contribution, I provide verbal definitions for the
concept of pollinator performance, based on the division of
two components: pollinator efficacy and intensity of visi-
tation. Pollinator performance results from both of these
components in a simple conceptual model, and expresses
the pollinator’s effectiveness in contributing to the male
and female components of plant reproductive success.
Although some quotations are provided as examples, the
intention is to provide a basic terminology and general
definitions for broad application, rather than to exhaus-
tively present a compilation of past studies. Analyses and
descriptions of specific procedures and metrics are avail-
able in the syntheses of Kearns and Inouye (1994), Inouye
et al. (1994), Dafni et al. (2005), and Ne’eman et al. (2010).
Terminology and definition of concepts
Floral visitors and pollinators
Every floral visitor is not necessarily a pollinator. Although
this idea is conceptually simple, the categorization of a
floral visitor as a pollinator is not straightforward in many
cases. The identification of pollinators may be mistaken, in
particular when it is based on the expected pollinator that
fits on a certain floral phenotype (i.e., ‘‘pollination syn-
drome approach’’) (Hingston and McQuillan 2000; Oller-
ton et al. 2009). False positives are generated due to low
accuracy of naturalistic observations or field experiments,
as well as insufficient knowledge of the study system, for
example, when visiting time is decoupled from the stig-
matic receptivity (Kishore et al. 2012) or when visitors
forage on a single plant of self-incompatible species, as
some pollen-collecting insects do in massive-flowering
trees (Kevan and Baker 1983). False negatives are mainly
due to insufficient sampling (see Case and Bradford 2009).
Furthermore, the categorization of a certain species as a
pollinator of a plant species may not be discrete. Pairwise
interactions are dynamic and may fluctuate at environ-
mental, temporal, and spatial scales (e.g., Fishbein and
Venable 1996; Wilcock and Neiland 2002; Herrera 2005;
Aizen et al. 2008; Brunet 2009; Irwin et al. 2010; Gowda
and Kress 2013), ranging from intensive use of floral
resources and no contribution to reproductive success, to
highly effective and efficient pollination. There are also
tradeoffs on the pollinator contribution to male and female
success (e.g., Campbell 1989; Stanton et al. 1991).
The terms described below and summarized in Table 1
are applied only to those floral visitors that transfer pollen
with potential effects on plant reproductive success (i.e.,
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Pollinator performance
pollinators), so they exclude visitors involved in floral
larceny (sensu Inouye 1980; but see Irwin et al. 2010).
Pollinator efficacy
Efficacy is the capacity of pollinators to effect the transfer
of pollen from the stamen to the target stigma, so that this
can result in seed production. Its operational definition is
the contribution that each pollinator provides to the plant
reproductive success after a pollination event, i.e., after a
single visit to the flower, inflorescence or plant, or to
another unit of measurement in the analysis.
Efficacy may be estimated by measuring different
variables such as the amount of pollen removed from the
anthers or deposited on the stigma, and the number of
fertilized ovules; and by parameters such as fruit and seed
set (e.g., Levin and Berube 1972; Motten 1986; Sahli and
Conner 2007; Avila and Freitas 2011; Kishore et al. 2012).
It can be presented in proportions, for example, in relation
to the number of ovules or the maximum capacity of seed
set. The measurement of efficacy is independent of polli-
nator efficiency and intensity of visitation (Herrera 1987,
1989). However, although it may seem to be a phenomenon
that is intrinsic to an individual, a species or a group of
pollinators in relation to a certain plant species, actually
pollinator efficacy is highly dependent on characteristics of
the sampled plant population (e.g., density, size and
aggregation of individuals, and flowering dynamics) and
interactions among floral visitor species (e.g., reduced
efficacy due to depletion of pollen by other visitors or by
agonistic interactions) (e.g., Murcia and Feinsinger 1996;
Kato and Hiura 1999; Wilcock and Neiland 2002; Gómez
et al. 2009; Mitchell et al. 2009; Maruyama et al. 2012).
Intensity of visitation
From the perspective of contribution to reproductive suc-
cess, the intensity of visitation expresses the number of
independent pollination events provided by a certain pol-
linator. In practice, it is measured by the number of visits
per time unit (i.e., visitation rate). As with pollinator effi-
cacy, visitation rates may be estimated in different ways,
using a flower, inflorescence or branch, the whole plant, or
a plant patch as the unit of observation and/or measurement
(e.g., Herrera 1989; Sahli and Conner 2007; Avila and
Freitas 2011). Intensity may also be transformed to pro-
portions, for example by the relative frequency of different
pollinators. Intensity of visitation is theoretically indepen-
dent of the efficiency and local abundance of the pollinator
(Jennersten 1984), although they may be correlated.
Visitation rates can be measured indirectly (Parker and
Haubensak 2002); however, this may be biased if an
efficacy component is embedded in these measurements
5
(see Engel and Irwin 2003). Last, the intensity of visitation
is also subject to many influences, which are difficult to
control in field studies, for example, the spatiotemporal
pattern of resource availability, local assemblage of floral
visitors, plant density, and existence of competing flowers
(Kearns and Inouye 1994).
Pollinator efficiency
The common-sense idea of efficiency, as well as its tech-
nical definitions, are based on performing a task as cheaply
as possible, i.e., this idea takes into account the energy cost
to generate the desired effect. Pollinator efficiency is clo-
sely linked to pollinator foraging strategies, and there is a
clear dichotomy between animal and plant expectations
(e.g., Borrell 2007; Fishbein and Venable 1996, respec-
tively). Thus, from the perspective of the contribution to
plant reproductive success, pollinator efficiency can be
defined as the pollinator efficacy in relation to floral
resource consumption and pollen wastage. Similarly to the
other parameters, pollinator efficiency is influenced by
many factors and may be measured in several ways
(e.g., Galen and Stanton 1989; Harder and Thomson 1989;
Young and Stanton 1990; Arroyo and Dafni 1995; Conner
et al. 1995; Pellmyr and Thompson 1996; Sahli and Conner
2007).
Accurate measurements of pollinator efficiency are hard
to obtain in the field, and this difficulty may preclude its
inclusion as a parameter in mechanistic models of polli-
nator effectiveness (but see Keys et al. 1995; Canto-
Aguilar and Parra-Tabla 2000). Finally, it is common in the
literature (e.g., Hargreaves et al. 2012) to use the term
efficiency in relation to another concept, in general coined
as ‘‘pollination efficiency,’’ which deals broadly with the
probability that any given unfertilized ovule will be fer-
tilized, in relation to the total production of pollen and/or
ovules. This latter concept is strictly plant based—although
it may be measured in relation to particular pollinators—
and should not be confounded with the concept of
pollinator efficiency as treated above.
Pollinator effectiveness
Pollinator effectiveness is given by the total contribution to
plant reproductive success, and thus, it reflects pollinator
efficacy and intensity of visitation in a simple conceptual
model. It may refer to the contribution of an individual or
population of a species of pollinator or a functional group
of pollinators (e.g., Arroyo and Dafni 1995; Fishbein and
Venable 1996; Avila and Freitas 2011). Different proce-
dures, operational variables, and equations can be applied
to measure pollinator effectiveness as proposed here
(see Inouye et al. 1994), but it primarily reflects the product
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6 L. Freitas

Table 1 Terms, verbal definitions, and the most common variables/metrics for some general concepts of pollinator performance
Terms Definitions Common variables/metrics

Pollinators Floral visitors that transfer pollen from the anthers to Individuals or population of an animal species
a conspecific Functional groups
stigma, with potential effects on the plant reproductive
success
Pollinator efficacy Contribution of each pollinator to the plant reproductive success after The quantity of pollen removed from the
a pollination event. In practice, it is measured after a single visit of anthers or deposited on the stigma
a pollinator to the flower, inflorescence or plant, or to another The number of fertilized ovules
unit of measure in the analysis
Fruit and seed set
Intensity of visitation The number of independent pollination events provided by a certain The number of visits to a flower, inflorescence
pollinator. In practice, it is measured by the visitation rate or plant (or other unit of measure) per unit
time
Relative frequency of visits
Pollinator efficiency Pollinator contribution to reproductive success in relation to floral Rate of deposited pollen or seed set/pollen
resource consumption and pollen wastage removed
Rate of nectar consumption
Pollinator Total contribution by a certain pollinator to male and female The product of pollinator efficacy and its
effectiveness components intensity of visitation
of reproductive success Pollen deposited on stigma, pollen tubes or
A pollinator may be efficacious but not effective. This happens seed set after treatments with differen
if its efficiency and intensity of visitation are low. Similarly, exposure times of flowers
less efficacious pollinators may be among most effective due to
a high frequency of visits to flowers

of these two components (efficacy and visitation). It can be Conclusions

estimated directly from the seed set (female component) or
from the proportion of seeds sired on other plants (male
component); or indirectly, for example, by measuring
pollen deposition on stigma or pollen removal from anthers
(reviewed by Ne’eman et al. 2010), which are usually
proxies for female and male fitness (Vázquez et al. 2005,
but see Pellmyr and Thompson 1996).
Alternatively, effectiveness can be estimated by com-
bining efficacy and visitation (e.g., experiments that restrict
the access to flowers by some visitors, followed by some
measure of success; Young 2002). In the latter cases,
researchers cannot know whether a given pollinator is more
effective because it is more efficacious, or more frequent,
or because of a combination of these factors. The decision
to estimate effectiveness by quantifying the two compo-
nents separately or together depends on the specific ques-
tions of a study, but their segregation is essential to propose
mechanistic models of selection of floral traits (e.g., Aigner
2001; Philipp et al. 2009), pollinator management for
agriculture (Rader et al. 2012), and effects of invasive
species of plants and flower visitors (Moragues and Tra-
veset 2005; Aizen et al. 2008). Similarly, pollinator effi-
ciency is not a mandatory component for evaluating its
effectiveness in pollination at a coarse scale, although it
has received less than its due attention and its estimation is
important for a deeper comprehension of these topics (see
Mitchell et al. 2009; Mayer et al. 2011).
Numerous expressed or implied definitions, in part con-
flicting, have been provided for the most common terms for
pollinator performance in thousands of standard papers
concerning specific study systems. This situation motivated
studies related to standardizing the terminology and con-
ceptual framework; at one extreme, Inouye et al. (1994)
proposed that the terms effectiveness and efficacy be
abandoned. Despite the quality of these previous articles to
standardizing, authors continue to use these terms, and
none of the strict definitions has gained wider support.
The excess of more-limited terms and concepts is a pos-
sible reason for the low adherence to these standardization
proposals. In this context, simple definitions for wider con-
cepts regarding pollinator performance are suggested here. I
believe that these terms can be applied in any study of the
subject, whatever the approach, scale, and procedures for
data collection and analysis. The idea is that heuristic defi-
nitions for common terms reflecting a simple conceptual
model may encourage more-consistent use of terms in the
literature. A parallel can be drawn to the concept of floral
larceny. In an equivalent situation of proliferation of terms
and definitions (although on a smaller scale), the classic work
of Inouye (1980) achieved great success in proposing a basic
terminology for visitor behavior regarding the use of floral
resources. Terms such as primary and secondary thieves and
robbers (Inouye 1980) have spread consistently in the

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Pollinator performance
literature since then, and this has facilitated the advancement
of the theoretical framework on the subject (reviewed by
Irwin et al. 2010). Thus, the motivation for this proposal is
based on the belief that achieving uniformity in the use of
more-general terms can facilitate debate regarding more
precise and accurate definitions of the concepts, as well as
recommendations for particular and general procedures.
From the theoretical viewpoint, the definitions suggested
here acknowledge the concept of qualitative and quantita-
tive components of pollinator contribution to reproductive
success by Lindsey (1984) and Herrera (1987, 1989). This
concept is firmly established in the area. It is the basis,
although implicit in some cases (e.g., Keys et al. 1995), for
ideas and methodological procedures used in most case
studies on pollinator performance (e.g., Sahli and Conner
2007; Avila and Freitas 2011; Rader et al. 2012) and also in
synthesis papers (e.g., Mitchell et al. 2009). Finally, I also
attempted to propose definitions that are closer to the
established usage of these terms in industrial engineering,
business, and economics, which have been applied in other
scientific areas (e.g., Cunningham 2001).
More than half of the ca. 300,000 species of flowering
plants that are pollinated by animals occur in tropical
environments (Ollerton et al. 2011). For the vast majority
of these species, little or nothing is known about their
pollination ecology beyond pollination syndromes or
anecdotal records of flower visitors. For instance, data that
allow estimating pollen limitation exist for only 1 %
(Wolowski et al. Unpublished data) of the ca. 13,000
species of angiosperms that occur in the Brazilian Atlantic
Forest (Stehmann et al. 2009), one of the most studied
Neotropical ecosystems (e.g., Laurance 2009). Case studies
that measure pollinator effectiveness are a necessary first
step to understanding plant–pollinator interactions, in par-
ticular in the lesser-known biodiversity hotspots (Watts
et al. 2012). Such studies are time consuming, and their
space is progressively diminishing in high-impact journals.
To join international debates on the topic and to close the
gaps in basic knowledge of plant–pollinator interactions is
a challenge for the next generations of pollination biolo-
gists in the tropics. I hope that this contribution may
stimulate them to go beyond these present constraints.
Acknowledgments The author thanks Faperj (Jovem Cientista) and
CNPq (PQ) for Research Fellowships and JW Reid for improving the
English.
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