REVIEW PAPER

Concepts of pollinator performance: is a simple approachnecessary to achieve a standardized terminology?

Leandro Freitas

Received: 29 January 2012 / Accepted: 18 February 2013 / Published online: 5 April 2013

� Botanical Society of Sao 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

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;

Vazquez 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.

L. Freitas (&)

Jardim Botanico do Rio de Janeiro, R. Pacheco Leao 915, Rio de

Janeiro, RJ 22460-030, Brazil

e-mail: leandro@jbrj.gov.br

123

Braz. J. Bot (2013) 36(1):3–8

DOI 10.1007/s40415-013-0005-6

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

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.,

4 L. Freitas

123

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; Gomez

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

(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

Pollinator performance 5

123

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

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 (Vazquez 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).

Conclusions

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

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

a conspecific

stigma, with potential effects on the plant reproductive

success

Individuals or population of an animal species

Functional groups

Pollinator efficacy Contribution of each pollinator to the plant reproductive success after

a pollination event. In practice, it is measured after a single visit of

a pollinator to the flower, inflorescence or plant, or to another

unit of measure in the analysis

The quantity of pollen removed from the

anthers or deposited on the stigma

The number of fertilized ovules

Fruit and seed set

Intensity of visitation The number of independent pollination events provided by a certain

pollinator. In practice, it is measured by the visitation rate

The number of visits to a flower, inflorescence

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

resource consumption and pollen wastage

Rate of deposited pollen or seed set/pollen

removed

Rate of nectar consumption

Pollinator

effectiveness

Total contribution by a certain pollinator to male and female

components

of reproductive success

A pollinator may be efficacious but not effective. This happens

if its efficiency and intensity of visitation are low. Similarly,

less efficacious pollinators may be among most effective due to

a high frequency of visits to flowers

The product of pollinator efficacy and its

intensity of visitation

Pollen deposited on stigma, pollen tubes or

seed set after treatments with differen

exposure times of flowers

6 L. Freitas

123

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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