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Chemoecology
Evolutionary, Mechanistic and
Environmental Approaches to
Chemically-Mediated Interaction
 
ISSN 0937-7409
 
Chemoecology
DOI 10.1007/s00049-013-0140-3
Chemical aposematism
Paul J.?Weldon
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COMMENTARY
Chemical aposematism
Paul J. Weldon
Received: 8 July 2013 / Accepted: 29 July 2013
 Springer Basel 2013
Abstract Discussions of aposematism traditionally have
focused on the visual displays of prey that denote unpal-
atability or toxicity to predators. However, the construct of
aposematism accommodates a spectrum of unprofitable
traits signaled through various sensory modalities, includ-
ing contact and distance chemoreception. Aposematism,
involving learned aversions by signal receivers or selection
for their unlearned avoidances, arises in predator?prey or
other interspecific interactions where a mutually beneficial
avoidance of signal emitters by signal receivers exists.
Aposematism evolves by selection against signal receivers,
e.g., predators, imposed by signal emitters, e.g., unprofit-
able prey, and vice versa, where both nondiscriminating
signal receivers and unrecognized signal emitters are
imperiled. Chemical aposematism entails concurrent reci-
procal selection where signal emitters select for
chemosensory avoidance responses in signal receivers, and
where signal receivers select for the emission of identifi-
able (distinctive) chemicals in signal emitters.
Keywords Aposematism  Chemical defense
Charles Darwin and Alfred Russel Wallace, the celebrated
co-proponents of natural selection as a mechanism of
evolution, proffered different explanations for colorful
ostentation among animals. Darwin (1874) posited that
bright plumage and other conspicuous traits arise through
sexual selection, and are displayed chiefly by males ??to
charm the female??. However, he was puzzled by the gaudy
markings of some caterpillars, which, given their life stage,
could not plausibly be adorned for mate recognition
(Wallace 1867). Wallace (1867) suggested that these pat-
terns in caterpillars evolved as signals to potential
predators denoting unpalatability: ??? distaste alone would
be insufficient to protect a larva unless there were some
outward sign to indicate to its would-be destroyer that his
contemplated prey would prove a disgusting morsel, and so
deter him from attack??. Poulton (1890) coined the term
aposematism (Gr a?po?, away; rn?la?, sign) for the phenom-
enon postulated by Wallace, defining it as ??an appearance
which warns off enemies because it denotes something
unpleasant or dangerous??.
As Poulton?s definition of aposematism licenses, the
range of known or suspected features supporting the apo-
sematic status of signalers has been expanded beyond prey
unpalatability to embrace a spectrum of unprofitable traits,
including toxicity, pugnacity, and mechanical inaccessi-
bility. In addition, some authors have justly amended
Poulton?s definition to accommodate aposematism that is
manifest by means other than through appearance, i.e.,
where signals are perceived through non-visual sensory
channels.
Eisner and Grant (1980) proposed the idea of ??olfactory
aposematism??, whereby consumers associate odors with,
and hence refrain from attacking, toxic or otherwise nox-
ious animals and plants. Inspired by studies of conditioned
taste aversion, they hypothesized that predators and her-
bivores, using olfaction, learn to identify noxious
organisms, often responding to volatiles from them that are
unrelated to the toxins they harbor.
Since its inception, aposematic features have been por-
trayed as a prey?s ??warning?? to (chiefly vertebrate)
Handling Editor: Michael Heethoff.
P. J. Weldon (&)
Smithsonian Conservation Biology Institute, National Zoological
Park, 1500 Remount Road, Front Royal, VA 22630, USA
e-mail: weldonp@si.edu
Chemoecology
DOI 10.1007/s00049-013-0140-3 CHEMOECOLOGY
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Author's personal copy
predators. ??Warning?? here must be understood in a meta-
phorical sense; neither a signaler?s intent nor a responding
organism?s anticipation of danger necessarily is entailed. In
a parallel vein, many authors contend that learned avoid-
ance of predators, established in sub-lethal interactions
with conspicuous prey, is integral to the evolution of
aposematism; this notion was embraced by Eisner and
Grant (1980). However, the many demonstrated examples
of naive predators that avoid dangerous prey, or particular
aspects of prey organisms presented in stimulus control
experiments, affirm that aposematism is not invariably
predicated on learned aversions (see Lindstro?m et al.
1999). An operational construct of aposematism entails
merely a mutually beneficial avoidance of signal emitters
by signal receivers in interspecific interactions. In the
lexicon of chemical ecology, aposematic chemicals are
synomones.
A considered outlook on aposematism, then, acknowl-
edges signals denoting diverse kinds of unprofitability; a
panoply of sensory channels mediating them, including
various types of contact and distance chemoreception; and
different mechanisms by which phenotypic features
acquire iconic value. For chemical ecologists, aposematism
clearly has relevance beyond the visually conspicuous,
unpalatable caterpillars that captivated Darwin and Wal-
lace. For evolutionary biologists, in general, these
chemically mediated responses present opportunities to
examine participating taxa and trophic interactions not
conventionally entertained by those who study aposema-
tism, and from which new insights may be drawn.
Consider, for example, arthropod-vertebrate interactions
where the familiar roles of arthropods as aposematic sig-
nalers (prey) and vertebrates as aposematic signal
respondents (predators) are reversed. This occurs in some
cases involving nonhost odors (NHO) where mosquitoes,
ticks, and other nuisance arthropods use chemoreception to
avoid dangerous or otherwise unprofitable vertebrate hosts
(Weldon 2010). These semiochemicals, which typically
emanate from a nonhost?s integument, repel arthropods or
inhibit their attraction. Phytophagous insects similarly
respond to NHO from unpreferred plants (Andersson
2007).
Responses to NHO, on one hand, constitute a foraging
adaptation by host-seeking arthropods; arthropods that fail
to avoid unprofitable hosts are selected against. On the
other hand, the emission of NHO may constitute a defense
by unprofitable hosts whereby they avoid lethal attacks,
wounding, and tissue damage that could admit vectored
and opportunistic pathogens; hosts that fail to elaborate
identifiable chemicals are selected against. In this paradigm
of concurrent reciprocal selection?where signal receivers
select against signal emitters, and vice versa?both non-
discriminating signal receivers and unrecognized signal
emitters are imperiled. Chemical aposematism entails
selection by signal emitters for chemosensory avoidance
responses in signal receivers, and selection by signal
receivers for the emission of identifiable (distinctive)
chemicals in signal emitters. This proposition accords with
the premise that aposematic features arise by selection on
defended prey to avoid being confused with undefended
prey (e.g., Sherratt and Beatty 2003).
References
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Science, Swedish University of Agricultural Sciences, Alnarp,
pp 1?38
Darwin C (1874) The descent of man and selection in relation to sex.
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Eisner T, Grant RP (1980) Toxicity, odor aversion, and ??olfactory
aposematism??. Science 213:476
Lindstro?m L, Alatalo RV, Mappes J (1999) Reactions of hand-reared
and wild-caught predators towards warningly colored, gregari-
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Poulton EB (1890) The colours of animals: their meaning and use,
especially considered in the case of insects. D Appleton and Co,
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Sherratt TN, Beatty CD (2003) The evolution of warning signals as
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P. J. Weldon
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