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From: Franc¸ois J. Verheggen, Eric Haubruge, and Mark C. Mescher,
Alarm Pheromones—Chemical Signaling in Response to Danger.
In Gerald Litwack, editor: Vitamins and Hormones, Vol. 83,
Burlington: Academic Press, 2010, pp. 215-240
ISBN: 978-0-12-381516-3
© Copyright 2010 Elsevier Inc.
Academic Press.
CHAPTER NINE
Alarm Pheromones—Chemical
Signaling in Response to Danger
Franc¸ois J. Verheggen,*Eric Haubruge,*and Mark C. Mescher
†
Contents
I. Introduction 216
II. Alarm Pheromones in Insects 217
A. Aphids 221
B. Ants 223
C. Honeybees 225
D. Alarm pheromones used as kairomones by natural enemies 226
III. Alarm Pheromones in Marine Invertebrates 227
IV. Alarm Pheromones in Fish 228
V. Alarm Pheromones in Mammals 229
VI. Alarm Signals in Plants 230
VII. Conclusion: Potential Applications of Alarm Pheromones 231
References 232
Abstract
Many animals respond to the threat of predation by producing alarm signals that
warn other individuals of the presence of danger or otherwise reduce the success
of predators. While alarm signals may be visual or auditory as well as chemical,
alarm pheromones are common, especially among insects and aquatic organ-
isms. Plants too emit chemical signals in response to attack by insect herbivores
that recruit the herbivores’ natural enemies and can induce preparations for
defense in neighboring plants (or other parts of the same plant). In this chapter,
we discuss our current understanding of chemical alarm signaling in a variety of
animal groups (including social and presocial insects, marine invertebrates, fish,
and mammals) and in plants. We also briefly discuss the exploitation of alarm
pheromones as foraging cues for natural enemies. We conclude with a brief
discussion of the potential exploitation of alarm signaling to achieve the applied
goal of managing pest species. ß2010 Elsevier Inc.
Vitamins and Hormones, Volume 83 #2010 Elsevier Inc.
ISSN 0083-6729, DOI: 10.1016/S0083-6729(10)83009-2 All rights reserved.
* Department of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, Liege University,
Gembloux, Belgium
{
Department of Entomology, Center for Chemical Ecology, The Pennsylvania State University, University
Park, Pennsylvania, USA
215
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I. Introduction
In response to the approach of predators—or other rapid adverse
changes in the immediate environment—many organisms emit alarm signals
that can alert nearby individuals (conspecifics as well as others) of impending
danger. Alarm signaling has frequently been viewed as an evolutionary
puzzle because the fitness benefits to individuals receiving the signal are
usually apparent while signaling often appears costly for signalers (e.g.,
Taylor et al., 1990). Genuinely altruistic signaling can presumably evolve
where the benefits preferentially fall on conspecifics with higher than
average relatedness to the signaler (Sherman, 1977) as suggested by inclusive
fitness theory (Hamilton, 1964). But alarm signaling may also directly
benefit the fitness of the signaling individual itself, for example, if the
antipredator or escape behaviors induced by the call reduce the probability
of successful predation (Ho
¨gstedt, 1983; Sherman, 1985) or attract the
predator away from the signaling individual (Charnov and Krebs, 1974).
Alarm calls may also have delayed benefits for the signaler, for example, by
saving the lives of individuals who will reciprocate in the future (Trivers,
1971) or those of potential mates (Witkin and Fitkin, 1979) or other group
members in circumstances where group living is beneficial (Smith, 1986).
Alarm signals frequently have visual and auditory components, especially
in birds and mammals (e.g., Leavesley and Magrath, 2005; Seyfarth et al.,
1980; Sherman, 1977), but chemical alarm signals are also widespread
(Wyatt, 2003). Chemical signals involved in communication with other
conspecific individuals are called pheromones (from the Greek pherein,to
transfer) and are thus distinguished from hormones (hormon, to excite)
which mediate communication within an individual organism (Karlson
and Lu
¨scher, 1959). Most alarm pheromones likely have evolved from
compounds originally having other functions. Specifically, it has been
proposed that alarm pheromones may evolve either from chemicals
involved in defense against predators or from compounds released upon
injury (Wyatt, 2003). To the extent that these compounds serve as reliable
cues to the presence of predators, potential receivers should evolve to detect
them and respond in ways that enhance fitness. The acquisition of a true
signaling function then entails further evolutionary elaboration of the cue
specifically in response to selection acting on its role in communication
(Maynard Smith and Harper, 2003).
A large literature addresses chemical identification of alarm pheromones
and their impact on the behavior of nearby individuals. In order to conclude
that particular compounds acts as an alarm pheromone, it is generally
considered necessary to demonstrate that (i) the chemical(s) is released
exclusively under exposure to hazard (e.g., predator attack), (ii) the signal
is perceived by conspecifics, and (iii) it induces in the receiving individuals
216 Franc¸ois J. Verheggen et al.
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behavioral reactions similar to those induced when directly exposed to the
same danger (Wyatt, 2003). The latter criteria is usually the most difficult to
demonstrate, as it is not enough to demonstrate a modification in the
behavior of the receiving individuals; the changes must clearly be appropri-
ate responses to danger specific threat. Generally, adaptive responses to the
reception of an alarm pheromone may be classified as evasive (e.g., receivers
flee from the pheromone releaser) or aggressive (receivers move toward the
signal and attack or harass the predator). Observed reactions can vary
according to the concentration of pheromone released and also with prior
experience of the receiver (Howse, 1998).
Alarm pheromones have documented in both vertebrate and nonverte-
brate animals (Wyatt, 2003), and similar types of signaling seem to occur
also in plants (Heil and Karban, 2010; Wittstock and Gershenzon, 2002).
The chemical composition of alarm pheromones is highly variable:
Table 9.1 presents a partial list of identified examples from animal systems.
Alarm signals may be as simple as a single molecule (e.g., citral in mites,
Kuwahara et al., 1979), but can also be complicated chemical mixtures,
whose activity is determined by their specific composition, the quantitative
proportion of the different compounds, and the stereoisomerism of the
dominating substances (Wadhams, 1990).
The remainder of this chapter reviews illustrative examples taken drawn
from the tremendous diversity of alarm signaling systems that occur in
presocial (aphids) and social (ants, termites, honeybees) insects, vertebrate
animals, and plants.
II. Alarm Pheromones in Insects
Alarm pheromones appear to be the second most commonly produced
class of chemical signals used by insects, after sex pheromones (Barbier,
1982). Alarm signaling has evolved in various Arthropod taxa in which the
individuals are proximate enough to each other to rapidly communicate.
Gregarious and social insects, including Hymenopterans and Hemipterans,
have developed a diverse array of chemical compounds that function as
releasers of alarm behavior (Table 9.1). Indeed, alarm pheromones appear to
be highly adaptive for species in which individuals form aggregates that can
exhibit a collective response to traumatic stimuli (Blum, 1985). In eusocial
species, for example, they allow colony resources to be rapidly and effi-
ciently deployed in response to specific threats. Insect alarm pheromones are
usually short molecules of low molecular weight and simple structure (e.g.,
terpenoids or aliphatic ketones and esters). They are thus highly volatile and
dissipate rapidly after emission as befits signals that operate over short time
frames and at localized spatial scales (Payne, 1974). Various organs can be
Alarm Pheromones 217
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Table 9.1 Some identified alarm pheromones in the animal kingdom
Animals Principal compounds
Typical behavioral
responses Additional observations References
Insects
Hymenopterans
Honeybees Isopentyl acetate
O
O
Recruitment and
aggression
Over 20 active compounds have been
identified in various bee species.
Guarding workers release alarm
pheromone in case of perturbation,
which leads to the recruitment of
nestmates and subsequent attack of the
intruder.
Boch et al. (1962),
Shearer and Boch
(1965)
2-heptanone
O
Ants n-undecane Fright reactions or
recruitment
and
aggression
All Formicidae species produce and use an
alarm pheromone whose secretion may
induce escape behaviors or the
recruitment of conspecifics and
aggressive reactions.
Hughes et al.(2001),
Stoeffler et al. (2007)
O
4-methyl-3-heptanone
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Homopterans
Aphids (E)-b-farnesene Fright reactions (E)-b-farnesene is the only active
component of the alarm pheromone of
most Aphidinae species. Receiving
individuals escape by running away from
the emitter or falling off the plant.
Edwards et al. (1973),
Bowers et al. (1977b)
Germacrene A
Fish
Ostariophysi Hypoxanthine-3-N-oxide
HN
OH
N
N
O–
N+
Fright reactions Ostariophysan fish exhibit antipredator
responses (increased shoaling and
decreased area of movement) when
exposed to compounds released from
the damaged skin of other individuals.
Exposure to low concentrations of
hypoxanthine-3-N-oxide induces
increase vigilance toward secondary
(visual) risk-assessment cues.
Brown et al. (2004)
(continued)
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Table 9.1 (continued)
Animals Principal compounds
Typical behavioral
responses Additional observations References
Cnidaria Anthopleurine
OH
OH
O
O–
N+
Fright reactions Anthopleurine was the first reported
cnidarian pheromone. The sea anemone
Anthopleura elegantissima, releases
anthopleurine from wounded tissues,
inducing rapid withdrawal in nearby
conspecifics.
Howe and Sheikh
(1975)
Mites
COH
Citral Fright reactions Several families of mites produce citral as
an alarm pheromone, whose perception
induces avoidance behavior along with
increased mobility.
Kuwahara et al. (1980)
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involved in their production, including anal glands, mandibles, and stings.
Although commonly comprising mixtures of several compounds, alarm
pheromones tend to be less specialized than other types of pheromones,
and few are species specific (Blum, 1985). This relative nonspecificity may
be an advantage to species that are able to detect alarm signals of other
insects sharing vulnerability to a common threat.
In noneusocial insects the effects of alarm pheromones are generally
limited to causing dispersal. The response to alarm signals varies among
eusocial species, but commonly involves attraction/recruitment of conspe-
cific workers or soldiers and the adoption of aggressive postures. Below we
discuss alarm signaling in aphids, ants, and honeybees.
A. Aphids
Because aphids are important agricultural pests throughout the world, their
biology and behavior have been well studied. Aphid alarm signaling was first
characterized in the 1970s. In response to predation and other disturbances,
aphids secrete droplets from two cornicles situated on the upper surface of
the abdomen near the tail that emit an odor repellent to conspecifics (Kislow
and Edwards, 1972)(Fig. 9.1). This pheromone induces alate and apterous
Myzus persicae (Hemiptera, Aphididae) to stop feeding and move away from
the signaler or to drop from the host plant—waving their antennae before
and during these aversive behaviors. Variation in response to alarm phero-
mone occurs both within and between species and correlates with to the
relative risk of predation and the costs of escape (Pickett et al., 1992).
Figure 9.1 Top: In response to predation, aphids release an alarm pheromone from
their cornicles that induces escape behavior in surrounding conspecifics. Bottom: The
vetch aphid, Megoura viciae (Hemiptera, Aphididae), with arrows pointing to the alarm
pheromone releasing organs (cornicles). The site of (E)-b-farnesene production
remains unknown.
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The active component of the liquid secreted from the cornicles of
several economically important species of aphids was found to be a sesqui-
terpene (C
15
H
24
) named (E)-7,11-dimethyl-3-methylene-1,6,10-dodeca-
triene, or more commonly referred to as (E)-b-farnesene (Ebf) or trans-b-
farnesene (Bowers et al., 1972)(Table 9.1). This same compound was
subsequently identified in many other aphid species including the green
peach aphid M. persicae Sulzer (Edwards et al., 1973; Wientjens et al., 1973)
and the pea aphid Acyrthosiphon pisum (Wohlers, 1981).
Germacrene A (Table 9.1), a biogenetic precursor of many sesquiter-
penes, was later isolated from the alfalfa aphid and identified as an alarm
pheromone (Bowers et al., 1977b), though it appears to play this signaling
role only within the genus Therioaphis.Pickett and Griffiths (1980) found
Megoura viciae to synthesize additional monoterpenes, including a-pinene,
b-pinene, and limonene, with ()-a-pinene having the most significant
alarm activity. (Z,E)-a-farnesene and (E,E)-a-farnesene were also reported
in several aphid species (Gut and Van Oosten, 1985; Pickett and Griffiths,
1980), but did not show biological activity (Bowers et al., 1977a).
Recently, Francis et al. (2005) characterized the volatile emissions of 23
aphid species and reported that Ebf was the only volatile chemical emitted in
significant amounts by 16 of them. Ebf was a minor component of the volatile
emissions of five other species. The remaining two species, Euceraphis puncti-
pennis Zetterstedt and Drepanosiphum platanoides Schrank, did not release any
Ebf, though other terpenes were isolated. In addition to the species examined
by Francis et al. (2005), we have identified four additional aphid species that
appear to produce Ebf as their only volatile chemical: Rhopalosiphum maidis
Fitch, Aphis glycines Matsumura, Aphis spiraecola Pagenstecher, and Brachycau-
dus persicae Pesserini (Verheggen, unpublished data).
In M. persicae, the quantity and mode of action of the alarm pheromone
was found to vary with morph and age of aphids (Gut and Van Oosten,
1985). The quantities of Ebf in aphids also increase in relation to increasing
body weight (Byers, 2005), but its concentration declines exponentially
with increasing body weight. In A. pisum,Verheggen et al. (2009) found
that exposure to Ebf emitted by other individuals influences the levels of
Ebf produced by immature aphids during development.
In addition to its role as an alarm pheromone in aphids, Ebf is also a
common component of plant volatiles emissions—including both constitu-
tive volatile blends (e.g., Agelopoulos et al., 2000) and those induced by
herbivore feeding (e.g., Turlings and Ton, 2006) or mechanical damage (e.
g., Agelopoulos et al., 1999). And Ebf is a constituent of various essential oils
found in several plants family such as Asteraceae (Heuskin et al., 2009;
Reichling and Becker, 1978). It is thus tempting to speculate that Ebf
production by plants functions to repel or habituate aphids or to otherwise
interfere with alarm signaling, but there is currently little evidence that such
effects occur (Petrescu et al., 2001). Instead, it appears that the presence of
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other sesquiterpenes—like ()-b-caryophyllene—in plant volatile blends
allow aphids to distinguish the pure Ebf emitted by conspecifics from Ebfof
plant origin (Dawson et al., 1984). However, other terpenes like a-pinene
or isothiocyanates have been reported to enhance the dispersal-inducing
activity of Ebf, leading to an increased specificity of the alarm signal in
some aphid species (Dawson et al., 1987; Pickett and Griffiths, 1980).
Interestingly, Ebf is present in trichomes of wild potato plants where its
release under aphid infestation does appear to cause dispersal (Gibson and
Pickett, 1983).
The behavioral effect of alarm pheromone on aphids varies across species
and also with the amount of pheromone encountered by receiving indivi-
duals. Typical responses range from the cessation of feeding and removal of
the stylet from host plant tissues to walking, jumping, or falling away from
the source of emission (Braendle and Weisser, 2001; Chau and Mackauer,
1997; Clegg and Barlow, 1982; Edwards et al., 1973; Losey and Denno,
1998; Montgomery and Nault, 1977a,b, 1978; Phelan et al., 1976; Roitberg
and Myers, 1978; Shah et al., 1999; Wientjens et al., 1973; Wohlers, 1980).
In the sugarcane woolly aphid, Ceratovacuna lanigera Zehntner (Homoptera,
Pemphigidae), the alarm pheromone reportedly elicited aggressive behavior
from conspecifics (Arakaki, 1989). Ebf has also a repellent effect on the
landing behavior of alate aphids, which can cause them to choose an
alternative host plant (Lambers and Schepers, 1978; Phelan and Miller,
1982; Wohlers, 1982). Field experiments confirmed dispersal behavior of
aphids subjected to their alarm pheromone in 41 species (Xiangyu et al.,
2002). Kunert et al. (2005) also found that Ebf exposure increased the
production of winged individuals specialized for dispersal. Once Ebf con-
centrations decrease, aphids commonly reinfest host plants (Calabrese and
Sorensen, 1978). Because the amounts of alarm pheromone emitted by an
individual under natural conditions might be too low to warn all nearby
conspecifics, two recent studies tested the hypothesis that aphids might
amplify the alarm signal by emitting additional Ebf in response to the
alarm signals of other individuals but found no evidence for such an effect
(Hatano et al., 2008; Verheggen et al., 2008b).
In addition to serving as an alarm signal to conspecifics and other aphids,
Ebf is exploited as a foraging cue by predators and parasitoids that feed on
aphids. Details are presented in Section D.
B. Ants
The first published observation of an ant alarm pheromone was probably
that of Goetsch (1934) who noted that crushed organs were capable of
causing aggressive reactions in workers. Following this original observation,
all Formicid species were subsequently found to produce and use an alarm
pheromone (Ho
¨lldobler and Wilson, 1990), whose secretion may alert or
Alarm Pheromones 223
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recruit conspecifics and often stimulates aggressive reactions (Blum, 1985
and references therein). Although behavioral responses can differ drastically
among ant species, alarm pheromones generally serve two distinct functions
(Wilson and Regnier, 1971). The response to ‘‘aggressive alarms’’ is char-
acterized by rapid movements oriented toward the emitter and by aggressive
attitudes ranging from mandible and gaster movements to biting or stinging
the antagonist (Fig. 9.2). Recruitment of more workers and intensified
attacks on intruders are also observed. Responses to ‘‘panic alarms’’ entail
escape, dispersion, and flight behaviors. Workers’ displacement speed is
increased, as well as the frequency of direction changes. The type of reaction
was found to correlate with differences among species in the size and density
of colonies, with species having larger and denser colonies being more
prone to aggressive responses. For example, Lasius fuliginosus forms large
subterranean colonies and the general response workers to the alarm phero-
mone, n-undecane (Table 9.1), entails running toward the pheromone
source with mandibles opened (Stoeffler et al., 2007). In contrast, workers
of Hypoponera opacior and Ponera pennsylvanica, which have small colony
sizes, drastically increase their mobility but do not run toward the emitter
when exposed to the main constituent of their alarm pheromone, 2,5-
dimethyl-3-isopentylpyrazine (Duffield et al., 1976).
A variety of natural products and associated behaviors have been high-
lighted in the different formicid genera, with production sites including
mandibular, pygidial, metapleural, and Dufour’s glands. Ant alarm phero-
mones are usually aliphatic carbon chains shorter and more volatile than
those characteristic of trail pheromones. These include ketones, alcohols,
esters, aldehydes, alkylpyrazines, terpenes, short aliphatic hydrocarbons, and
formic acid. As with aphid alarm signals, the alarm pheromones used by ants
are thus well suited chemically for their role in mediating effective responses
to threats that are highly localized in space in time. Different chemicals often
Figure 9.2 Two common alarm postures in Formicidae. Formicid ants respond to
alarm pheromone with either aggressive or escape behaviors.
224 Franc¸ois J. Verheggen et al.
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composed the alarm pheromone blend of a single ant species and these
components can elicit different behaviors in receiving individuals. More-
over, because of differences in volatility, and perhaps also due to differences
in the sensitivity of receiving individuals, the areas over which specific
compounds induce active responses can also vary.
Minor workers of Pheidole embolopyx respond to encountering intruders
of other species by secreting trail and alarm pheromones produced by the
pygidial gland (Wilson and Ho
¨lldobler, 1985). In combination, these signals
announce the presence of the enemy and lead to the recruitment of major
workers who mount a sustained attack on the intruders.
The different components of the Camponotus obscuripes (Formicinae)
alarm pheromone are produced in Dufour’s gland and in the poison gland
(Fujiwara-Tsujii et al., 2006). The first gland contains a mixture of aliphatic
carbon chains of which n-undecane represents 90%. Formic acid, a com-
pound commonly used by ants for defense, trail marking, and recruitment,
appears to be the only volatile chemical produced in the poison gland. In
response to danger, C. obscuripes releases a mixture of these substances, each
having a different volatility and function. Formic acid, perceived at longer
distances, informs other colony members of the presence of a threat
and helps them to locate the source of the emission. At shorter range,
n-undecane and other associated saturated hydrocarbons induce aggression
toward antagonists.
Among leaf cutting ants in the genus Atta, the mandibular gland secre-
tions of most species contain mixtures of volatile, low-molecular-weight
alcohols and ketones, which elicit the alarm response (Blum, 1968). The
main volatile components of the mandibular glands of major workers are
4-methyl-3-heptanone (Table 9.1) and 2-heptanone (Hughes et al., 2001),
with the former being most active in eliciting alarm responses (Moser et al.,
1968). The latter chemical also occurs commonly in other ant genera
(Feener et al., 1996).
C. Honeybees
A vital role in honeybee colony defense is played by so-called guard bees,
which patrol the nest entrance and represent the first line of defense. These
guards are also specialized for the production of alarm pheromone which
they release to recruit nestmates from the interior of the colony in case
of danger (Boch et al., 1962; Collins et al., 1982). The perception of the
pheromone increases workers movement and promotes aggression. Indeed,
beekeepers are well acquainted with the banana-like odor released by
stressed colonies, and with the fact that one bee sting is likely to be followed
by others unless one rapidly moves away from the colony or uses smoke to
sedate it. Although there is a striking variation in the intensity of their
response (in docile colonies, only a few bees may respond while thousands
Alarm Pheromones 225
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of stinging individuals may attack in more aggressive colonies), only guard-
ing workers produce the alarm pheromone (Alaux et al., 2009; Vander Meer
et al., 1998).
The possibility that an alarm signal, of then unknown nature and origin,
could act to alert honeybee workers was first suggested in the early 17th
century (Butler, 1609, cited by Wilson, 1971). The signal was later proposed
to be an odorant by Huber (1814), who noticed that presenting a honeybee
worker’s sting (attached to a forceps) to conspecifics changed their behavior
from ‘‘quiet’’ to ‘‘aggressive.’’ He concluded that ‘‘some odors incite honey-
bees to flee.’’ It was later established that the honeybee alarm pheromone is
produced in the mandibular as well as in the Koshewnikov gland associated
with the sting apparatus (Boch et al., 1962; Shearer and Boch, 1965)—though
pheromone emission does not require that the sting be used.
Boch et al. (1962) first identified isopentyl acetate (previously called iso-
amyl acetate) (Table 9.1) as a biologically active alarm pheromone associated
with the sting (The use of smoke by beekeepers suppresses the activation of
antennal receptors of isopentyl acetate, and therefore reduces nestmate recruit-
ment.) (Visscher et al., 1995). Subsequently, over 20 additional volatile ali-
phatic and aromatic active compounds of low molecular weight have been
identified in the alarm pheromone blend (Hunt, 2007). In addition to isopentyl
acetate, (Z)-11-eicosen-1-ol is thought to play an essential role (Boch et al.,
1962; Pickett et al., 1982). Although both these compounds individually
induce alarm responses in bee workers, when presented together they elicit
behavioral responses comparable to the intact sting (Pickett et al., 1982). Not all
components of the pheromone blend in honeybees induce alarm behavior,
some have other specialized functions including flight induction (e.g., benzyl
acetate), and recruitment (e.g., 1-butanol, 1-octanol, hexyl acetate), while
others play multiple roles (e.g., 1-hexanol, butyl acetate, isopentyl acetate,
2-nonanol) (Wager and Breed, 2000). Shearerand Boch (1965) reported alarm
activity of 2-heptanone (Table 9.1) isolated from honeybee mandibularglands.
With increasing age, the size of the gland and the amount of 2-heptanone
increases (Vallet et al., 1991). When filter paper treated with 2-heptanone is
placed at the hive entrance, bees nearby become greatly agitated, assuming a
characteristic aggressive posture and running toward the emission source in
jerky circles or short zigzags. Contrary to longstanding expectations, the
honeybee alarm pheromone blend does not seem to be implicated in target
localization (Free, 1961; Wager and Breed, 2000).
D. Alarm pheromones used as kairomones by
natural enemies
Semiochemicals provide a powerful way for organisms to communicate and
coordinate their behaviors. But they also represent opportunities for other
organisms to intercept and exploit such signals. Indeed, there are numerous
226 Franc¸ois J. Verheggen et al.
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examples of natural enemies having learned or evolved to use the phero-
mones of their prey as foraging cues (Vet and Dicke, 1992).
For example, aphid natural enemies rely on semiochemicals, especially
the aphid alarm pheromone, to locate aphid colonies (Fig. 9.3). Previous
studies have demonstrated this phenomenon in lady beetles, Coccinella sp.,
Adalia sp., and Harmonia sp. (e.g., Francis et al., 2004; Nakamuta, 1991;
Verheggen et al., 2007); hoverflies (e.g., Almohamad et al., 2009;
Verheggen et al., 2008a, 2009); ground beetles (Kielty et al., 1996); lacew-
ings (Boo et al., 1998; Zhu et al., 1999); and parasitic wasp adults and larvae
(Beale et al., 2006).
Ant parasitoids also use alarm pheromone components to locate their
specific hosts. Individuals of Apocephalus paraponerae (Diptera: Phoridae),
which parasitizes workers of the giant tropical ant Paraponera clavata (Hyme-
noptera: Formicidae), locate fighting or injured workers of this host species
by using 4-methyl-3-heptanone and 4-methyl-3-heptanol (Feener et al.,
1996). The cursorial spider Habronestes bradleyi (Araneae, Zodariidae), a
specialist predator of the meat ant Iridomyrmex purpureus, likewise locates
workers of its prey by using their alarm pheromone, which consists mainly
of 6-methyl-5-hepten-2-one and is frequently released during territorial
disputes among conspecifics (Allan et al., 1996).
III. Alarm Pheromones in Marine Invertebrates
Alarm behaviors in aquatic invertebrates are also commonly mediated
by chemical signals, and a growing number of aquatic organisms have been
shown to display antipredator behavior in response to injury-released
Figure 9.3 Like many natural enemies, aphid predators and parasitoids have evolved
to perceive and exploit the alarm pheromones of their prey.
Alarm Pheromones 227
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chemical cues from conspecifics, including mollusks (e.g., Spinella et al.,
1993), flatworms (e.g., Wisenden and Millard, 2001), annelids (e.g., Watson
et al., 2005), and echinoderms (e.g., Vadas and Elner, 2003).
The first report of a chemical alarm cue in a platyhelminth was the
demonstration that predator avoidance behavior in a free-living flatworm,
Dugesia dorotocephala, could be induced by chemical cues released from
injured conspecifics (Wisenden and Millard, 2001). Despite their relatively
simple nervous system, Planaria are apparently also capable of learned risk
association, as following simultaneous exposure to the conspecific alarm
signal and sunfish odor cues, they subsequently respond to the sunfish odor
alone as an indicator of danger (Wisenden and Millard, 2001). Green sea
urchins, Lytechinus variegates, employ a two-phased response to cues from
damaged conspecifics entailing an initial rapid but ephemeral alarm response
followed by a more sustained flight phase, which induces urchins to disperse
(Vadas and Elner, 2003). Chemical alarm substances have also been docu-
mented in Gastropods. The snail Littorina littorea, common periwinkle,
shows crawl-out responses (i.e., movement out of the water) in response
to chemical stimuli from injured individuals ( Jacobsen and Stabell, 1999).
The first cnidarian pheromone to be documented was anthopleurine
(Table 9.1), which is released from wounded tissues of the sea anemone
Anthopleura elegantissima—for example, during attack by the nudibranch
Aeolidia papillosa—and evokes rapid withdrawal in nearby conspecifics
(Howe and Sheikh, 1975).
IV. Alarm Pheromones in Fish
Many fishes use alarm pheromones to warn conspecifics of potential
threats in the surrounding environment (reviewed by Smith, 1992). The
first suggestion that Ostariophysan fishes (the second largest superorder of
fish) might exhibit a fright reaction in response to some signal from
wounded conspecifics, and that this might reduce the receivers’ vulnerabil-
ity to subsequent predation, was made by von Frisch (1938).Pfeiffer (1963,
1977, 1978) subsequently documented alarm signaling in several Ostario-
physan species. The secretion of the signals involves specialized epidermal
cells that contain the alarm pheromone. When these cells are broken, as
during predation events, this substance is released into the surrounding
water (Fig. 9.4). Thus, senders cannot actively release their alarm substance
(Smith, 1992), but the restricted context in which they are emitted reliably
informs conspecifics of the presence of a predator. Fathead minnows (Pime-
phales promelas) and finescale dace (Chrosomus neogaeus) also exhibited signif-
icant antipredator responses (increased shoaling and decreased area of
movement) when exposed to conspecific skin extract (Brown et al.,
228 Franc¸ois J. Verheggen et al.
Author's personal copy
2000). Similar reactions were observed in response to hypoxanthine-3-N-
oxide (Table 9.1), one of several molecules thought to function as a
chemical alarm signal in Ostariophysan species (Brown et al., 2000). Com-
plementary studies subsequently found that exposure to low concentrations
of hypoxanthine-3-N-oxide may cause fish to increase vigilance toward
secondary (i.e., visual) risk-assessment cues, leading to an increased alarm
response in case of predator attack (Brown et al., 2004). The fish fright
reaction can also be detected visually by other nearby individuals leading to
the rapid propagation of the alarm response through a group (Smith, 1992).
In the Percid fishes, physical injury also appears to be required for release
of the active alarm pheromone component, and exposure to water that
previously contained an injured individual leads to reduced movement
(‘‘freezing’’) and periods of inactivity in the receiver (Crane et al., 2009).
Fish alarm pheromones do not appear to be species specific, and usually
induce equivalent alarm responses in other species (Smith, 1982). For exam-
ple, the pumpkinseeds, Lepomis gibbosus (Acanthopterygii), exhibit antipre-
dator responses when exposed to hypoxanthine-3-N-oxide, the putative
Ostariophysan alarm pheromone (Golub et al., 2005). This similarity of
intra- and interspecific reactions in fishes, suggests corresponding similarities
in signaling chemistry and reception mechanisms. This has led to some
controversy as to whether alarm signals in fish should strictly be classed as
pheromones or as allelochemicals (Burnard et al., 2008).
V. Alarm Pheromones in Mammals
Mammals make wide use of pheromones to mark territories, attract
mates, and coordinate group behavior. Chemical alarm signaling also
occurs, but though many territorial and sexual pheromones have been
Figure 9.4 Ostariophysan fish species release an alarm signal when their skin is
damaged, and receiving individuals exhibit fright reactions including increased shoaling
and decreased area of movement.
Alarm Pheromones 229
Author's personal copy
identified in mammals, relatively little progress has been made in the
chemical identification and functional analysis of mammal alarm phero-
mones (Hauser et al., 2005). It is commonly thought that mammal alarm
pheromones are volatile, and it is hypothesized that they may be low
molecular weight compounds, such as fatty acids or steroids. The perception
of these alarm signals seems to be mediated by an auxiliary olfactory sense
organ called the vomeronasal organ (VON), or Jacobson’s organ (Dulac and
Axel, 1998).
Although, infochemicals appear to play a smaller role in communication
between humans than in other mammals, the ability to produce and per-
ceive pheromones has also been demonstrated in humans (McClintock,
1998). The existence of a human alarm pheromone has not been demon-
strated, but it has been suggested that humans can detect differences
between a neutral scent and a scent associated with frightened individuals
(Ackerl et al., 2002).
Chemical alarm signaling has been demonstrated in mice (Rottman and
Snowdown, 1972). When exposed to the odor of a stressed conspecific,
mice behaved aversively to the source of the odor, even though they
responded positively to the sender’s odor prior to the introduction of the
stress. Stressed male Wistar rats release a volatile alarm pheromone, from the
perianal region that elicits defensive and risk-assessment behavior in receiv-
ing individuals, characterized by hyperthermia, increased freezing, sniffing,
and walking as well as a decreased resting behavior (Inagaki et al., 2009;
Kikusui et al., 2001). So far, the chemical structure of this pheromone has
not been elucidated.
Odor-induced fear responses have also been documented in cattle and
shown to be at least partly mediated by olfactory cues in the urine of stressed
individuals (Boissy et al., 1998).
VI. Alarm Signals in Plants
Plants actively respond to damage induced by infesting arthropods by
inducing direct defenses such as toxins and antifeedants (Gatehouse, 2002).
But, they also typically release blends of volatile compounds from damaged
tissues—as well as systemically—that appear to play a variety of signaling
functions (Farmer, 2001). For example, these herbivore-induced plant
volatiles can directly repel foraging herbivores, such as ovipositing butter-
flies and moths and host-seeking aphids (Dicke and Vet, 1999). Herbivore-
induced volatiles also serve as key foraging cues for natural enemies of the
feeding herbivores, including insect predators and parasitoids (e.g., Turlings
et al., 1998) and even for insectivorous birds (Ma
¨ntyla
¨et al., 2008). More-
over, these signals can convey complex and highly specific information
230 Franc¸ois J. Verheggen et al.
Author's personal copy
about the status of emitting plants. For example, the highly specialized
parasitoid wasp Cotesia congregata can consistently distinguish among volatile
blends elicited by the feeding of two closely related caterpillar species and
preferentially responds to the odors of plants infested by its host (De Moraes
et al., 1998).
There has been a longstanding debate about the extent to which dam-
age-induce plant volatiles might also be important in signaling between
neighboring plants (Farmer, 2001; Heil and Karban, 2010; Karban, 2008),
but a number of recent studies suggests that these compounds play an
important role in signaling between damaged and undamaged tissues of
individual plants (e.g., Arimura et al., 2000; Dolch and Tscharntke, 2000;
Engelberth et al., 2004; Karban and Maron, 2002; Karban et al., 2003), and
particularly in overcoming potential constraints on the internal (vascular)
transmission of wound signals imposed by plants’ modular architecture
(Frost et al., 2007; Heil and Silva Bueno, 2007; Karban et al., 2006;
Rodriguez-Saona et al., 2009).
VII. Conclusion: Potential Applications
of Alarm Pheromones
In addition to obviously intriguing questions about the evolution of
alarm signaling within individuals species and differences in the way they
function between taxa, understanding this class of semiochemical-mediated
interactions also has potential for application to the management of pest
species. Sex pheromones, mainly of Lepidopteran insects, have frequently
been incorporated into management strategies (Copping, 2001). While few
alarm pheromones have been employed in this context, some efforts have
been made to incorporate them in push–pull strategies as behavior-mani-
pulating stimuli to make the protected resource unattractive to the
pest (Cook et al., 2007). And honeybee alarm pheromone can be used to
repel Apis mellifera from oilseed rape before insecticide applications
(Free et al., 1985).
A good deal of research has addressed the potential use of aphid alarm
pheromone as a control mechanism. Following identification of the aphid
alarm pheromone—Ebf in most species of Aphidinae—researchers began
discussing the possibility of using this semiochemical to repel aphids
(Bowers et al., 1972), encouraged by the relative ease of extracting and
purifying Ebf from plant material (Heuskin et al., 2009). Early attempts to
employ Ebf in the field were unsuccessful, however, as aphids recolonized
host-plants very rapidly following exposure (Calabrese and Sorensen, 1978).
Later, slow-release formulations of Hemizygia petiolata (Lamiaceae) contain-
ing high levels of Ebf were successfully employed to reduce pea aphid
Alarm Pheromones 231
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populations in field experiments (Bruce et al., 2005). The increased aphid
mobility induced by Ebf exposition could also increase aphid exposure to
insecticides and fungal control agents (Griffiths and Pickett, 1980). Simi-
larly, application of farnesol and nerolidol, components of the two-spotted
mite (Tetranychus urticae) alarm pheromone, increased mite mobility and
subsequent exposure to coapplied acaricides, leading to enhanced control
relative to the application of acaricides alone (Copping, 2001).
Studies on the role of Ebf in interspecific interactions in natural systems
also suggest its potential application to the control of aphid population
mechanisms. As noted above, Gibson and Pickett (1983) demonstrated
the ability of wild potatoes to repel aphids by naturally releasing Ebf from
their glandular trichomes. And work on the perception of the aphid alarm
pheromone by predators highlights of its potential to increase aphid appa-
rency to natural enemies (Almohamad et al., 2008; Du et al., 1998;
Verheggen et al., 2007, 2008a; Zhu et al., 1999). Beale et al. (2006) exploited
this potential by incorporating an Ebf synthase gene into the genome of
Arabidopsis thaliana, and demonstrated increased attraction of aphid para-
sitoids to the modified plants.
Because alarm pheromones can be attractants for certain organisms, they
also have potential for use in baits or traps. Hughes et al. (2002) showed that
an alarm pheromone produced by grass-cutting ants, 4-methyl-3-hepta-
none, has significant potential to improve the efficacy of baits used for the
control of these insects, since individuals receiving the signal tend to move
toward the source of emission.
Far fewer studies have addressed practical applications of non-insect
alarm pheromones. However, alarm signals might well have applications in
the control of aquatic pests. For example, the search for a method to decrease
the decline of Britain’s native white-clawed crayfish (Austropotamobius
pallipes) caused by the presence of the induced signal crayfish (Pacifastacus
leniusculus), originally from North America, has given rise to speculation that
P. leniusculus pheromones (including sex, stress, and alarm pheromones)
might improve the efficiency of existing baits (Stebbing et al., 2003).
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