Karel Kleisner and Timo Maran
30 Visual communication in animals:
Applying a Portmannian and Uexküllian
biosemiotic approach
Abstract: In modern biology, the appearance of organisms is largely understood
as an adaptation serving the survival function. Here we advance a biosemiotic
perspective inspired by the works of Adolf Portmann and Jakob von Uexküll. From
this perspective, the visual dimension of every living being can be understood as
a representation of the evolutionary experience of a species. In the study of animal
displays, biosemiotics focuses on the qualitative perspective in both the logic
behind the emergence of such signs as well as their perception and interpretation
by perceiving animals. In this study, we claim that convergence of the animal
surface patterns that stem developmentally from different ontogenetic precursors
should be taken as evidence for congruence in biological meaning. As a specific
example, the article discusses the development, perception, and evolution of
semantic organs such as eyespots on butterfly wings and vertebrate eyes.
1 Diversity of visual communication in animals
Studying visual communication in non-human animals always means taking a
comparative perspective. Visual communication channels, i.e. organs of perception and expression, remain invariant in human visual communication; but
between differing species, the specifics and effects of these can differ to a large
extent. And so to focus on any singular trait, or even to build up a typology based
on any single criterion, produces a simplified picture of animal visual communication. For this reason we claim in this chapter that the Portmannian and Uexküllian
biosemiotic approach is potentially useful in studying animal visual communication as it provides a holistic understanding by incorporating several causal mechanisms, taking the specifics of living systems into account, and also including
within it the animal’s subjective perspective.
On a purely physical level, the range of perceivable light-waves differs
between taxonomical groups: many birds and insects are able to perceive ultraviolet patterns whereas many reptiles sense infrared wavelengths. This means that
human perception of the visual communication of other species may be biased
due to our own physiological capacities. For instance, many differences or similarities that are significant to the members of other species remain outside our visual
range. Thus, we do not sense the different coloring of the head cap of the male
and female blue tits in UV, which is an important marker in their interspecific
communication (Andersson et al. 1998), and it is easy for us to distinguish between
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Karel Kleisner and Timo Maran
the colors of orchid red helleborine and bellflowers, which are undistinguishable
for certain bees for whom these form a mimicry of resemblance (Nilsson 1983).
In addition to the simple range of wavelength, visual perception may differ
for different animal species in many other aspects. It appears that we humans, as
well as many other primates, have exceptionally good color vision when compared
to other mammals, whereas other mammalian taxa, cats in particular, may have
sharper eyesight in low-light conditions. Also, the ways in which animal eyes organize the color information can be rather different. Our visual apparatus consists
of three types of retinal cells that distinguish between base colors – green, blue,
and red – and renders all hues as a combination of these; birds have four types
of color receptors (one of which is suited to perceive UV wavelengths) and accordingly, for birds, four base colors exist. When the many evolutionary pathways
and the variety of anatomies of visual perception organs from simple unicellular
structures capable of distinguishing light from non-light to the compound eyes of
insects which have a large field of vision but relatively low resolution (though
even here there are exceptions, as for instance dragonflies) are added to all the
varieties of eyes in vertebrates, one can see that taking the comparative perspective
to animal visual communication is a real necessity.
Looking at visual signals themselves, one can distinguish between several
types based on a formal criterion. One possibility would be to pose the question:
how do colors emerge? This would allow a distinction between the visual signals
of emitted colors (as in fireflies Photuris) and reflected colors, whereas the latter
type could be further divided between embodied visual signals, those that exist
within an animal’s body structure, and detached signals, which would include
territorial markings, tracks, nests, feathers, and other environmental signs of the
animal’s presence. Based on the physical mechanisms of color generation, embodied visual signals could in turn be divided between physical colors (blue, green,
and metallic tones that are caused by color diffraction in the microstructures of
body integuments) and pigmental colors (mostly brown, black, yellow and red
tones that are caused by selective light absorption in chemical compounds).
Finally, specific body structures exist through which messages of visual communication are expressed in animals, and which vary greatly (including outgrowths,
spikes, outer ears, horns, feather structures, tales, among others).
In addition to such purely formal description, any analysis of specific cases of
visual communication in animals should pay attention to the spatial or temporal
organization of the signals of a given species. Depending on taxonomical group,
colors in animals can form patterns and specific indexical signs, for example the
pale “follow-me” sign below the tail of many ungulates. Visual signals can also
form repertoires of behavioral acts with a communicative function, e.g., the facial
gestures or body postures of many group-living birds and mammals that are
depicted in ethology as ethograms. In temporal means, visual signals can form
specific sequences of ritual behavior, e.g., “wedding dances” and other forms of
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courtship behavior. In their full species-specific complexity, animal signals can be
dynamically employed in dialogic or polylogic encounters between the members
of one and the same or different species, and they can be described as conveying
meaning or function based on codes that organize specific acts of communication.
A well-known example of spatially and temporally complex visual communication
systems in animals is claw movements in signaler crabs, which are used in speciesspecific sexual and territorial communication. Another much studied case is the
“dance language” honeybees use to communicate information about the position
of a food source or other resource, relative to the bee-hive and the position of the
sun. In its particulars, this appears to be a well-organized communication system
that allows the conveyance of referential information about environmental objects
(thus matching much of the criteria specific to human language e.g., Hockett
1960).
Concerning the function of visual signals of animal communication, contemporary evolutionary biology mostly tries to establish that specific animal signals
have selection value for the given animal species, thus contributing to its survival.
Such outcome may relate to the effect of natural selection, for instance where the
warning coloration of an insect species announces that it is unpalatable or poisonous. Alternatively, such an outcome can be related to sexual selection, as where
vivid red and yellow colors in the plumage of the males of some passerine birds
supposedly reveal their health and diet to the females. Given the variety of visual
communication systems in animals, the function or meaning of a particular message can also be much more concrete. For instance, the German theoretical biologist Günter Tembrock (1971: 56) has described the basic categories of meaning that
are transmitted in intraspecific communication as follows: (1) identity of the sender
(species, group, age, sex, and individuality); (2) motivation (physiological status
such as hunger and behavioral status such as intention to fly); (3) other living
beings (dangerous and non-dangerous animals), things, territory, food, meteorological conditions. To present a typology does not mean to imply that all the colors
in animal body surfaces necessarily have meaning or function. It is plausible to
assume that there are also many aspects in animal body coloration that have no
special meaning or function. In other cases, it is more adequate to talk about
meaning complexes that can include several actualized or potential meanings, as
we are about to show in the following semiotic excursion into animal appearances.
2 Introducing Portmannian and Uexküllian
biosemiotics
Biosemiotics generally studies the semiotic processes (e.g. recognition, communication, and interpretation) that are considered to exist in a variety of forms down
to the simplest living organisms and to the lowest levels of biological organization.
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Karel Kleisner and Timo Maran
Biosemiotics can focus on codes and coding in biological systems, biological functions of semiotic processes, typology and evolution of sign usage, etc. (see Kull et
al. 2008). Compared to mainstream Darwinian biology, the biosemiotic and especially Portmannian-Uexküllian biosemiotic approach is closer to many treatments
of visual communication in the humanities and social sciences. This is because
Portmannian-Uexküllian biosemiotics combines structural descriptions of the ecologies, physiologies, and development of animals with a subject-centered focus.
Many of Uexküll’s basic concepts such as building plan (Bauplan), form-shaping
rule, functional cycle (Funktionskreis), and counterpoint (Kontrapunkt) can be
interpreted as tools of structural description; and both Portmann and Uexküll
emphasize the subjective perspective by treating animals as perceiving, expressing, and communicating creatures (e.g. Uexküll’s analysis of animal Umwelten
and Portmann’s concepts of self-representation and inwardness). It can be
assumed that Portmannian-Uexküllian biosemiotics is more capable at describing
qualitative aspects of the specific appearances in animal species.
The Swiss zoologist Adolf Portmann (1897–1982, born and died in Basel)
belongs in any list of the most original thinkers of twentieth-century biology. His
originality was not founded by any new radical invention, but rather by elaborating the classical ideas of German romantic science. Portmann’s ideas were highly
influenced by a tradition of continental speculative philosophy; perhaps this is
why, with a few exceptions, philosophers and social scientists have appreciated
his work, rather than biologists (see Gould 1977: 349). Adolf Portmann understood
organic form as something of value in itself which should be studied as such. In
his thinking, the external surface of an organism has its own formal value and a
certain kind of autonomy over other life-sustaining functions. He was convinced
that this outermost aspect of an organism informs us about the innermost dimensions as these surface manifestations reflect the inner self-experience of every living being. He stated that the only way to get closer to understanding the existence
of other living creatures is by a sensitive interpretation of the outermost organic
surfaces (Portmann 1960a, 1960b, 1965, 1969: 315). Though Portmann’s views may
seem part of German idealistic biology, his approach does take animal appearance
into account as a whole, making it very suitable for studying the complex visual
patterns of an animal.1
 This tradition of biology was common in German intellectual space, i.e. besides Germany it was
especially common in Switzerland, Holland, Austria, the former Czechoslovakia, Estonia, and St.
Petersburg in Russia, but some of its adherents also lived in France and England. Idealistic biology
crystallized in the works of German Naturphilosophen towards the end of the eighteenth and beginning of the nineteenth century. It stresses the concepts of form, metamorphosis, and different kinds
of holistic organization. Individual development (ontogeny) was often taken as co-logical with
evolution. The rapid development of idealistic biology in the first half of nineteenth century was
impaired by various subsequences of Darwin's appearance (1859), though in continental Europe it
survived in various diasporas until the second world war. The foremost representatives of this
intellectual line were L. Oken, J. W. Goethe, K. E. v. Baer, E. G. Saint-Hilaire, R. Owen, W. Troll,
and A. Naef.
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Jakob J. von Uexküll (born 1864 Estonia, died 1944 Italy) developed an original
semiotic theory of nature that emphasizes meaning as the organizing force of animal physiology as well as individual relations with the living and non-living environment (Uexküll 1982). His work was inspired by the philosophies of Immanuel
Kant and J. Wolfgang von Goethe and, in turn, influenced the latter ethological
studies of Konrad Lorenz and Nikolaas Tinbergen. In the context of the present
paper, we focus particularly on Uexküll’s notion that the specific form of an animal – its features and ontological development, the functional relations it has with
others of its own species, especially its mates, but also with representatives of
other species, physical forces etc – is interconnected by meanings.
3 Semantic organs
The exposed surfaces of organisms play a crucial role in visual communication.
It is largely through these that animals recognize each other’s species, sex and
individuality, and these are the primary displays with which an animal can express
its intentions and moods. Let organic appearances that may potentially enter the
Umwelten of other living beings be called semantic organs (“semes” in short;
Kleisner and Markoš 2005; Kleisner 2008b). In formal language, semantic organs
can be defined as semiautonomous relational entities dependent on Umwelt-specific interpretation (Kleisner 2008a). It is remarkable that semantic organs can be
defined neither by listing solely their anatomical, morphological, developmental
or genetic components nor by unambiguous attribution of a particular signaling
function. More precisely, every semantic organ exists at the interface between the
expression of bodily features and their meaning within the Umwelt of a receiver.
Semantic organs come into existence through semiotic cooption and semiotic
selection. Semiotic selection occurs because semiosis literally operates through
perception, interpretation and feedback, being thus an evolutionary derivative of
Uexküll’s Funktionskreis (Maran 2008: 177; Maran and Kleisner 2010). Semiotic cooption happens when a trait expressed by an organism is recognized as meaningful by another organism (Kleisner 2011). It does not matter whether the co-opted
trait was shaped to serve some specific function or had no function at all. In this
respect, semiotic cooption is a kind of exaptation operated by the sensory channels
and cognitive sphere of an organic subject (on exaptation, see Gould and Vrba
1982; Weible 2012).
In our following exposition, we take eyespots as an example of semantic
organs par excellence. Though eyespots take on immense diversity of form and
color, still they bear something in common: the meaning of an eye. Eyespots are
found in almost all kind of ecosystems whether underwater, in the air, or on terra
firma. These iconic signs (i.e. signs based on resemblance) occupy the bodies of
organism living nowadays as well as of those that were fossilized long before
mammals first appeared.
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Karel Kleisner and Timo Maran
By focusing on this specific case, we hope to demonstrate the methodology
and argumentation characteristic to the Portmannian-Uexküllian biosemiotic
approach. Throughout the following exploration we highlight the complex nature
of the visual appearances in animals that needs to be maintained to the final
conclusions of our study. Our methodological approach is to analyze and finally
synthesize the following aspects of animal appearance:
1. distribution and diversity across species and groups;
2. array of the possible functions of the phenomenon (eyespots in the present
study);
3. evolutionary history of the particular appearance and the species involved;
4. developmental background of the individual;
5. behavioral activities of the animal (i.e. which behaviors are needed to make
the appearance function as a message in the given communicative situation);
6. interpretations of appearances by other species (e.g. predatory species), their
feedback and further effects.
We address these methodological points in pairs in the following sub-chapters:
1 and 2 in “Eyespots – their distribution, morphological diversity and functions”;
3 and 4 in “Eyespots in evolution and development”; 5 and 6 in “Behavioral components do matter”. The following survey should lead us to a complex model of
animal visual communication systems that is qualitative (e.g. by preferring the
concept of appearance over signals, inter alia), sees the semiotic faculty (meanings
and signification) as a main organizing force of communication, and highlights
the interplay between meanings in communication and evolutionary history.
4 Eyespots – their distribution, morphological
diversity and function
Different spots and eyespots may be found in a number of animals of different
phylogenetic origin such as squids, octopuses, turtles, sharks, rays, fishes,
amphibians, reptiles, birds, and especially insects. The various eyespots on the
surfaces of animals were traditionally considered representations of eyes. One may
suggest this is only imaginative, resulting from subjective “anthropomorphic” projections that have nothing to do with modern science. Here we do not follow such
an ultimate purification of the meaning of these iconic signs. We would rather ask
whether the similarity between eyespots and eyes reflects a common principle that
exceeds the range of human cognition and touches the other living beings in a
similar way.
In the most general sense, eyespots are mostly considered to be survival devices that deter enemies. Eyespots on the wings of butterflies especially represent
the most intensively studied semantic system. The experimental approach is con-
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tinuously perfected to bring more reliable results. There are two major explanations for the protective function of eyespots. The first represents an “intimidation”
hypothesis according to which the function of the eyes is to deter predators, and
prevent an attack. The usual reasoning here is that eyespots intimidate predators
because they represent an imitation of vertebrate eyes: this is the “eye mimicry”
hypothesis (Blest 1958). Recently, this hypothesis has been strongly criticized,
especially by authors who perform field behavioral experiments (Stevens et al.
2007, 2009). In this view, eyespots serve an antipredation function, not because
they are representations of eyes but because they are conspicuous. The fact that
many of them resemble a vertebrate eye to a human observer arguably has nothing
to do with their warning function. Eyespots effectively intimidate the predator’s
attack because they are simply conspicuous and highly contrasting, not because
they imitate vertebrate eyes. This understanding led Stevens et al. to abandon the
term “eyespots” as anthropocentric while proposing the term “wingspots” for these
structures in butterflies, “finspots” in fishes, etc. This hypothesis is based on the
deflection of a predator’s attack away from the vital body parts, e.g. the head, to
less vulnerable ones, e.g. the wing margins. Current support for the deflection
hypothesis remains equivocal (Lyytinen et al. 2003; Hill and Vaca 2006; Vlieger
and Brakefield 2007). Eyespots have yet other functions such as playing a signaling role in sexual selection. In the butterfly Bicyclus anynana (Nymphalidae), for
instance, the dorsal wing pattern is supposed to partake in female mate choice
whereas the ventral pattern serves a camouflaging and/or predator-deflecting role
(Brakefield and Reitsma 1991; Lyytinen et al. 2004; Stevens 2005).
Despite the current research progress in the behavioral ecology of antipredation signals, there are still some questions that transcend the focus of the mainstream adaptationist agenda. Our concern with eyespots occurs prior to formulating and testing a hypothesis. We assume that some pre-understanding to “what is
an eye?” is always present when we approach objects that are conspicuous, circular, and concentric. One should ask: do eyespots enter the Umwelten of nonhuman animals as representations of an eye? May eyespots represent vertebrate
eye mimicry? How has it come about that different circular objects are experienced
as eyes? And, how have various representations of the eye come into existence?2
In the following, we will argue that neither the “eye mimicry” hypothesis nor
the “conspicuous signal” hypothesis represents an appropriate explanation of the
evolution of eyespots. Here, we propose a third perspective which differs from the
previous “either … or” scenario and, at the same time, remains compatible with
recent findings.
 For a more detailed application of the semiotic methodology to the study of animal communication, see Maran 2010.
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5 Eyespots in evolution and development
There are two major hypotheses on the evolution of eyespots in butterflies. The
first proposes that eyespots originated from the undifferentiated row of elements
(border ocelli) – each occupying a single wing compartment (or wing cell) – that
became further individuated and diversified in number and morphology. According to the second scenario, eyespots originally appeared as single autonomized
compartmental elements that were duplicated and repeatedly co-opted by other
wing compartments (Monteiro 2008). Morphologically, the wings of satyrid and
nymphalid butterflies often bear a row of eyespots that are homologous to the
border ocelli within the generalized wing pattern of the nymphalid ground plan
(Süffert 1927; Nijhout 1991); see Figure 1. By contrast, the eyespots on the hindwings of some sphingid moths originate from elements of the central symmetry
system, that is, from a different part of the nymphalid groundplan.
Inasmuch as the element of border ocelli consists of an array of eyespots, the
whole system has a modular character similar to that of the vertebrate backbone.
In the ancestral state, the eyespots were presumably highly coupled, both genetically and developmentally. However, during the course of evolution, acting adaptive forces led to their genetic decoupling, favoring individuation and independent
diversification of single eyespots (Beldade and Brakefield 2003). Artificial selection
Fig. 1: Generalized ground plan of wing patterns of family Nymphalidae according to Süffert
(1927).
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applied to eyespots had a rapid effect on size, location and color composition of
the eyespots, whereas much lower heritability was reported for eyespot shape during selection for elliptical eyespots in the anteroposterior and proximodistal axes
(Monteiro et al. 1997a; Monteiro et al. 1997b). As a result, it seems evident that
when compared to other parameters, the circular shape of the eyespots is strongly
constrained. This is probably because of developmental-mechanistic reasons during the formation of the eyespot such as the response of the surrounding epidermis
to radial diffusion of a signal from a central focus point (Nijhout 1980, 1991; French
and Monteiro 1994). However the same explanation can hardly be applied to
instances where the eyespots do not originate from material homologous to border
ocelli. The eyespots on the forewings of peacocks (Inachis io, Nymphalidae) represent a composite of neighboring elements of color pattern. The eyespots originated
by fusion; integrations of different parts of a centrally symmetric system are frequent, for instance within sphinx moths, but also some mantids bear eyespots
formed from spiralized stripes, etc.
The suggestion of Stevens (Stevens et al. 2007: 526) that the high frequency of
circles compared to the other shapes may be explained by “[…] the radial diffusion
of a morphogen outward forming a concentration gradient, with the epidermal
cells producing specific pigments depending on the morphogen concentration” is
thus valid only for a limited number of eyespots, namely those derived from the
marginal ocelli. But eyespots tend to be circular even when generated from noncircular precursors. Alternatively, “the circularity of these elements are favored
because they increase the probability that the eyespots will be perceived as “eyelike” by a majority of possible receivers and thus attract the sight of predators”
(Kleisner 2008a: 215). In other words, specific developmental mechanisms do not
appear to fully explain the existence of generalized forms that are present in many
species and groups. Within most studies, eyespots serve as a model system of
development. Particular phenotypic changes in eyespot parameters provide information on the functioning of developmental mechanisms and genetic underpinnings. For such approaches, eyespots are an excellent experimental model, but
this does not help us understand their close resemblance to vertebrate eyes. Again,
one wonder how these eyespots became “eye-like” and how are they maintained
as such during evolution.
5.1 Eyespots in fossils
The role eyespots play in communication between and within species has a long
evolutionary history. Eyespots are well evidenced from insect fossils. For example,
members of the Eurasian family Kalligrammatidae were large insects from the
Jurassic period that belonged to the order Neuroptera. Their conspicuously patterned wings, often with large eyespots on hind- and fore-wings, are well preserved
in the fossil record. As nicely stated by Grimaldi and Engel:
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Kalligrammatids were the “butterflies” of the Jurassic. Their densely setose and patterned
wings and bodies and their long palpi gave them the superficial appearance of large moths
or butterflies, despite occurring 60–90 MY before the first papilionoid fluttered […] It is tantalizing to speculate how the eyespots of kalligrammatids served a similar function of startle
defense. It is equally interesting as to what peculiar Jurassic vertebrates kalligrammatids might
have been mimicking, perhaps some small, insectivorous reptile or even an archaeopterygid
bird? (Grimaldi and Engel 2005: 347).
Edmunds’ (1976) mention of eyespots found on the wings of the carboniferous
insects from the order Protodiamphipnoa represents another example from an even
older geological period. If these eyespots functioned as recent ones, the only possible vertebrate receivers of these signals would have been amphibians and/or
reptiles (Komárek 1989). One should ask, however, whether or not these eyespots
represented an imitation of the eyes of some particular animal group. The question
whether there were any eyespots on the surfaces of animals from the period that
preceded the evolutionary origin of the ventricular eye cannot be answered easily.
Nevertheless, the eyespots found within the fossil record seem to be of the same
forms and shapes as recent ones. The simplest explanation is that the eyespots
probably did not represent an imitation of eyes, neither of a particular vertebrate
species nor a vertebrate class. For now, we would rather say that eyespots generally do not imitate the eyes of any particular kind of vertebrate.
5.2 Eyespots underwater
The different physical and physiological constraints of an aquatic environment do
not prevent the communicational function of eyespots in inhabitants of marine
and freshwater ecosystems. Various eyespots (or just spots) occur in many fish
species. The most striking examples involve the presentation of the eyespots (finspot) on the caudal part of the body, while a dark band conceals the real eye, as
seen in some species of butterfly fish (Chaetodontidae). As a result, the caudal part
of the body fulfils the role of a false head. The entire effect is sometimes supported
by movement opposite to body direction (backward in relation to real head). The
coloration of the whole fish body, the concealed eyes and caudal fin-spots,
together with associated behavior, together generates a context within which the
spots carry the meaning of an eye and the caudal region that of a false head. The
location of the eyespot and false head may be supposed to misdirect the attack of
predator to less vital parts of the animal body as described by the misdirection
hypothesis (Cott 1957; Neudecker 1989; Meadows 1993; Winemiller 1990). This
hypothesis assumes that the eyespots should imitate the real eye in size and structural composition, while differing in position. Nevertheless, the caudal eyespots
of many fish, for instance the four-eye butterfly fish (Chaetodon capistratus), markedly exceed the size of natural eyes. The larger size of the eyespots appears to
refer to the presence of a larger animal, thus they would be more effective in
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intimidating a predator (the intimidation hypothesis). The occurrence of dislocated
and large sized eyespots may also be explained by the “reaction-distance hypothesis” which assumes that the larger size of eyespots may induce predators to initiate an attack from too great a distance, thus giving a temporal advantage to the
prey and potentially thwarting the attack. According to this hypothesis, the predators use the angular extent of the eyelike pattern on their retina as a cue to trigger
the attack. Moreover, the oval or elliptic shape of the eyespots may confuse the
predator about its actual angle of approaching trajectory and thus misdirect the
attack (Meadows 1993). These examples show that explaining the particular
appearance of the eyespots may require taking into account the interpreter’s perceptual specifics and behavioral preferences.3 It would be extremely interesting to
test these ideas in the context of insect eyespots, as we often find therein either a
series or single eyespots of different sizes and sometimes spatially warped shapes.
It is worth noting that the eyes themselves appeared to be a very conspicuous
signal within the newly discovered red fluorescence of reef fishes. Red fluorescent
eye rings were reported in 30 species from four families (Gobiidae, Tripterygiidae,
Blenniidae, Syngnathidae). The frequent occurrence of this feature indicates that
fluorescent eyes may potentially function as a presence indicator or deceptive gaze
signal (Michiels et al. 2008). We return to the importance of the conspicuousness
of the animal eyes in the final part of our discussion.
6 Behavioral components do matter
In addition to the structural diversity and the developmental and evolutionary
history of animal appearance, its dynamical and behavioral aspects must also be
taken into account. The comparison of effectiveness of deimatic coloration in two
models of butterflies shows that the behavioral component can play a crucial role.4
Vallin et al. (2007) performed an experiment in which hawkmoths (Smerinthus
ocellatus) and peacocks (Inachis io) were subjected to attack by birds (great and
blue tits). As a result, the birds killed more hawkmoths than peacocks. This is
surprising because both species have similarly sized eyespots, which were suspected of having a similar intimidating effect on bird predators. Both peacocks
and hawkmoths are palatable and non-poisonous. It is worth noting, that hawkmoths are a much larger prey item, which should be easier to attack than the
smaller peacocks. However, when peacocks are disturbed not only do they open
their wings with the eyelike ornaments, they also start to flick their wings and
 The recent research on coral reef fish Pomacentrus amboinensis also indicates the possible role
of eyespots in social interactions (Gagliano 2008). The eyespots may take a role in rapid recognition
of conspecifics, thus bringing a selective advantage to the species (Zaret 1977).
 Edmunds (1974) used the term deimatic behaviors for all forms of displays, postures and sounds
taken up by prey with the apparent purpose of intimidating an attacking predator.
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allegedly turn around to follow the movement of the attacking bird (Vallin et al.
2007). The protective behavior of hawkmoths also involves “eyespots flickering”
but this may seem especially impressive to human (mammalian) observers, while
seen as more static and less frightening to birds. This is supposedly related to
differences between the perceptual worlds (Umwelten) of humans and birds, the
reaction times and temporal perception being generally much faster in the latter.
A different species of hawkmoth, the tobacco hornworm (Manduca sexta),
which has dorsal black and yellow bands on its abdomen, gives other example of
correspondence between behavior and warning coloration. The abdominal pattern
of Manduca somewhat imitates a wasp-like pattern. When Manduca sexta is irritated (attacked), it starts to move with its abdomen in a way that simulates the
stinging behavior of aculeate hymenopterans (Evans 1983). The wasp-like coloration followed by an imitation of aculeate abdominal movements makes an overall
expression quite intimidating for a potential receiver.
The intimidating effectiveness of such deimatic displays thus depends on the
behavioral repertoire of a bearer. Quite probably it could be the behavioral component that makes the eyespots a more effective anti-predation signal than the other
conspicuous forms examined by the experimental design of these British behavioral ecologists. In other words, eyes and eye-marks should not be isolated as
merely static displays, but considered in a way that emphasizes their dynamical
and functional being – that is, within the context of activities such as looking,
eye-blinking, head-turning, etc. However difficult it would be to test this possibility
in the field, further research that integrates behavioral components with deimatic
coloration is needed.
7 How a spot becomes an eyespot?
Both theoretical arguments and experimental evidence have challenged the “vertebrate eye mimicry” hypothesis (e.g. Stevens et al. 2007). When we discard the
concept of “eyespot” for the more or less neutral concept of “wingspot” – as suggested by Stevens and co-authors – we simultaneously abolish the question as to
why some wingspots resemble eyes to us and perhaps also to other non-human
receivers. Therefore, we should ask how wingspots become eyespots, or how a
circular structure becomes an iconic sign that stand for an eye. Another source of
criticism may point to the fact that experiments use an artificial design to examine
the functioning of the anti-predatory role of eyespots – not butterflies themselves.
This means that the possible active role of the prey in this prey-predator interaction is abandoned a priori. We have already shown that the behavior of the potential prey does influence a signal’s effectiveness, as probably do the specific features and capacities of the receiver, its response and co-action with the prey.
We learn that different eyespots (wingspots, finspots) function because they
are conspicuous, not because of their imitation of vertebrate eyes. It is also pos-
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Visual communication in animals
671
sible, however, that they refer to an eye as a general model, since the eyes themselves are usually conspicuous structures (as shown in the previous examples in
fish).5 Therefore, we suggest that if the conspicuousness hypothesis attempts to
explain the functioning of eyespots it should consider the question of why vertebrate eyes themselves are often conspicuous. Very likely, vertebrate eyes are mimicked because they are conspicuous structures marking the position of the animals’
heads. Vertebrate eyes are in fact headspots, to use Stevens’ (2005) vocabulary.
But also the eyes of some vertebrate species became conspicuous secondarily, only
after they have adopted a signaling function. Usually only conspicuous parts of
other animals deserve to be imitated, as one can see in the frequent cases of partial
mimicry (e.g. false heads, eyespots).
It is in principle impossible to describe the evolutionary origin of complex
eyespots on the wings of butterflies without any reference to the interpretative act
(the signification) on the part of predator that gives a meaning of “vertebrate eye”
to the primarily raw structures on butterfly wings. Only after such prospectively
eye-like structures acquire the meaning of the eye in the Umwelt of the animal
interpreter, can selection act to make them more and more similar to the representation of a vertebrate eye in a predator’s Umwelt, and thus ultimately become
closely similar to real vertebrate eyes (Kleisner 2008b). Moreover, the morphological diversity of complex eyespots on the wings of insects may hypothetically be
explained by differing Umwelt-specific interpretations of predators that have acted
as selective agents. In this sense, one can also think about the attempt to infer the
predator’s inner representation of an “eye” from eye-like ornaments exposed on
the wings of his potential insect prey (Hinton 1977). In other words, if one wants
to discover the meaning of an eye in the Umwelt of a particular interpreter it will
potentially be helpful to look at the eyespots on the wings of its potential prey.
We conclude this section with a couple of questions. Can conspicuousness
partly explain the evolution of eyespots’ aversive function? Yes. Does conspicuousness suffice to elucidate the evolution of eyespots? No. Eventually we suggest
that only wing spots, fin spots and other spots that are semiotically co-opted as
representing eyes in the Umwelt of a particular animal interpreter should be
named eyespots. Spots that are not so involved in any animal Umwelten should
rather be considered as structures with an existing but yet-unrevealed semiotic
potential.
8 Theoretical implication of semantic morphology
One may question the need for new concepts such as semantic organs, appearance,
co-option and others when contemporary biology already has such terms as signal
 “Mimicry of snakes by insects appears to be analogous to mimicry of vertebrate eyes by many
species of insects. Many of these false eyes are very like the eyes of vertebrates: the incorporate
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672
Karel Kleisner and Timo Maran
and cue by which to label organic appearances. We insist, however, that the
vocabulary of signals and cues, and the biological rationale underlying these terms,
does not fit many of the situations that we find within the animal world. A sender
emits a signal to directly affect a particular receiver, i.e. a signal is a sign that
serves manipulative purposes. Cues, on the other hand, are not specific to living
organisms and could also be present and perceived within inanimate objects. What
is wrong with these terms is that the concepts of cues and signals are rather used
to denote specific features of an animal body or an environment, and not the animal body as a whole. By contrast, when considering the whole surface of an organism as derived meaningfully in the function of a living body, and self-display as a
revelation of the otherwise inaccessible innermost potential of an organism (i.e. as
representation of organic inwardness, in Portmann’s terms), a new terminology is
needed. These concepts should, on the one hand, describe animal appearances as
meaningfully organized wholes and, on the other, make a clear distinction between
living and non-living surfaces. The apparent feature of all exposed organic surfaces
is their uniqueness in relation to other bodily structures.
Everything that comes into being could be potentially perceived by someone,
therefore being existent means being somewhat apparent. Being existent as animate supposes that appearance has inner causes, for organisms build themselves.
If you remove the surface layer of a rock, you will usually find the same pattern
beneath. This is because the appearance of a rock does not represent the result of
activity stemming from the rock’s centrality, i.e. from the rock itself. Looking under
the coat of a mammal produces a quite different experience. Although this basic
fact is evident even to children, most of today’s biologists seems behave as if they
are unaware of it. These differences between inner and outer lie at the core of the
division between life/non-life.
Living beings have an inwardness that can be interpreted in evolutionary terms
as an evolutionary experience gathered by a lineage during the temporally vast
period of evolutionary history. This deeply anchored dimension of living beings
simply cannot be erased, forgotten, or overwritten. For the same reason, neither
can it be wholly imitated. When thinking in terms of semantic organs, we simultaneously refer to these innermost dimensions of living. While a sign is a representation of something other, the semantic organs are self-representations of organisms
(thus coming close to “proper names” in a semiotic typology of the signs). In identifiably particular ways, they reveal the evolutionary experience of a lineage and
thus also their specificity and individuality. To talk about organisms in terms of
semantic organs means to take their ontological wholeness into consideration.
There is one important point stemming from the logic of semantic organs. One
could admit that the exposed surfaces of an organism are often imitated, and
eccentric circles and an apparently reflective high-light from a moist cornea. They can be astonishingly realistic, but they do not resemble the eyes of any particular vertebrate.” (Pough 1988: 81).
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673
because many organic surfaces can be conceived as semantic organs, so too
semantic organs must be subjects of imitation. Imitation is indeed ubiquitous in
the living world, but semantic organs cannot be imitated easily. What we mean by
this is that such an imitation would never be safe for the mimic (the imitating
organism). As semantic organs are tightly related to organic inwardness (and living
experience), changing a semantic organ will also change that being’s inwardness.
We should now correct the former statement that “semantic organs cannot be
imitated easily” to suggest that “semantic organs cannot be imitated ‘superficially’”.
For example, take numerous cases of mimicry where a model is imitated by
one or more mimic species. In the case of Batesian mimicry, the model is protected
(unpalatability, sting, poison etc.), whereas the mimics have no protection. It is
apparent that mimicking organisms gain a selective advantage by adopting the
semantic organs (semes) of a model. In classical neo-Darwinian exposition, the
story ends at this point. We suggest that advantage in survival is necessarily connected with a less apparent disadvantage in terms of self-representation. This is
the loss of species-specific semes. This is what a mimic must pay for increased
reproductive success, or in other words, for hiding behind a model. The most
obvious example of this is the necessity for new types of intraspecific communicative mechanisms to arise, as imitating other species may cause previous speciesspecific communicative mechanisms to collapse. But this lead to crucial consequences as:
[…] self-representation of mimic does not longer stand for the presentation of the self, but it is
the presentation of the semes of a model on the body of the mimic. In other words, bodies of
the mimics serve as a projecting screen for the semes of the model. So, in fact, the display of a
mimic represents the “self”-representation of the model (Kleisner and Markoš 2009: 305–306).
By analogy from human society, losing face is also conceived as a dramatic event
with non-trivial consequences for an individual. The other example can be seen
when someone aims to ‘clear’ his or her family name; simply adopting a new
“false” family name is usually not considered a satisfying solution.
Some of the ideas presented in this chapter remain unacceptable in mainstream biological thought. However, without taking the “self” of living beings
seriously as a representation of evolutionary experience gathered into a lineage
by its unique evolutionary history, we will be in danger of erroneous reasoning
about evolution. For the humanities and social sciences, biological treatment of
communication may appear predominantly focused on evolutionary history and
functionality in message conveyance. In this context, the Portmannian-Uexküllian
biosemiotic approach attempts to introduce greater awareness about the historical
and communicative contexts of meanings and the roles of the sender and the
interpreter in bringing forth and shaping the messages in communication.
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674
Karel Kleisner and Timo Maran
Acknowledgments: We thank David Machin for the kind invitation to contribute
to this volume. Karel Kleisner was supported by Czech Grant Agency project GACR
P505/11/1459, and by Charles University in Prague project UNCE 204004, Timo
Maran’s research was supported by European Union through the European
Regional Development Fund (Centre of Excellence CECT, Estonia) and by Estonian
Science Foundation Grant No 7790.
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