Signalling and Reception Secondary article

Leena Lindstro¨m, University of Jyva¨skyla¨, Jyva¨skyla¨, Finland Article Contents Janne S Kotiaho, University of Jyva¨skyla¨, Jyva¨skyla¨, Finland . Introduction . What is Communication? Communication, a widespread natural phenomenon, occurs in both animals and plants. . Honesty of Signals Signals are evolved traits that transfer information from one individual (the signaller) to . Signal Design and Receiver Psychology another (the receiver); they can occur in any sensory modality. . Signalling in Plants

Introduction transmitted through a surrounding environment, and Communication is a widespread phenomenon in the received by a receiver. natural world, occurring not only in animals, but also in Signals can be either directed at conspecifics or at plants. Signals are traits that have evolved specifically to members of other species. Intraspecific signals (i.e. those transfer information from one individual (the signaller) to occurring between individuals in the same species) can be another (the signal receiver). They can occur in any sensory used to attract a mate, to deter rivals, to maintain social modality, and some signals are even sent in several sensory grouping, or to warn kin of approaching danger. Signals channels simultaneously. Signals have evolved to provide aimed at individuals of another species are often anti- useful information for receivers; a signaller provides this predator signals, for example, alarm calls, warning signals information in an attempt to manipulate a receiver’s and mimicry. Signals produced by plants are often aimed at behaviour to its own advantage. This conflict of interest animal receivers; for example, flowers attract insects or between signaller and receiver means that to be mutually birds to pollinate them, although, as we shall see, there is beneficial signals need to be honest, although under certain some evidence of communication between plants. How- circumstances, deceptive signals can evolve. The sensory ever, first we will consider animal communication in more and psychological capabilities of signal receivers have also detail. influenced signal design, and the signals that we see today are the product of selective pressures on both signal How do animals communicate? content and how efficiently that information can be transferred. Animals have evolved an incredibly diverse array of traits that they use for communication. Based on the sensory capabilities of the signal receivers, signals can be con- sidered to fall into three main categories: acoustic or What is Communication? vibrational signals; olfactory or chemical signals; and visual signals. In addition, electric signals are found in Communication is the process whereby individuals send some fish species that emit pulses from discrete electric and receive information about each other and their organs derived from modified muscle (Andersson, 1994). surroundings. Communication is achieved through the Acoustic signals, as well as all other vibrational signals, use of signals, traits that have specially evolved to transfer are mechanical stimuli that are transmitted through a information between one individual (the signaller) to medium such as air, water or a variety of solid materials. another (the signal receiver). Because signals have evolved Depending on the medium in which the signal is sent, these to transmit information, this distinguishes communication signals may be used for very short range communication from simple information acquisition. Psychologists often (e.g. plant stem vibrations produced by tropical wandering use the term ‘signal’ to describe any stimulus in an animal’s spiders), medium range communication (e.g. airborne bird environment that might alter its behaviour. For example, a song) and very long range communication (e.g. underwater tone might be a cue from which an animal learns to predict sounds and songs of whales). the arrival of food and move towards a food dispenser, but Olfactory and other chemical signals are transmitted the sound is not a signal in this evolutionary sense as it is an through a medium by diffusion, which can be a slow arbitrary cue designed by the experimenter. In addition to process if the viscosity of the medium is very high. communication between individuals, communication can Olfactory signalling is commonly used by mammals, where occur at other levels of cellular organization within it plays a potent role in their social organization. Olfactory individuals, for example in cell to cell signalling. However, communication is also widespread among insects: many here we focus only on those signals that are transmitted insects produce pheromones, a class of species-specific between individual animals and plants. These can be chemical compounds or molecules that are produced to characterized by the signals being produced by a signaller, communicate between members of the same species. In

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 1 Signalling and Reception addition, the use of scents or pheromones is not warn relatives of the presence of a predator. Interspecific uncommon even among birds, fish, amphibians and signals are perhaps less common, with signals that are reptiles. As with vibrational signals, olfactory signals can aimed at predators being the most well-studied. be very short range, localized signals (e.g. urine marking of many mammals) or can travel considerable distances (e.g. Sexual signalling moth pheromones). The purpose of sexual signals is either to attract mates of In addition to sounds and odours, animals produce a the opposite sex or to deter rivals of the same sex. variety of visual signals. These traits are usually extremely Ornaments are morphological traits that are used for mate striking (e.g. the bright plumage coloration of many birds), attraction and include the plumage and feather ornaments and often take conspicuous shapes and forms (e.g. the of many birds, the colour markings of some lizards and eyespots and enlarged fins of some fish). In addition to fish, and the leg tufts of certain species of spiders these morphological traits, some visual displays make use (Andersson, 1994). Traits produced in other sensory of foreign artefacts and construction. For example, modalities can also attract mates: bird song and the calls tropical bower birds, such as the Satin bower bird of crickets and frogs are examples of acoustic signals that (Ptinolorhynchus violaceus), adorn their bowers with animals use, and olfactory signals are also common, colourful objects that attract females. Male satin bower especially in insects. Other morphological traits and signals birds collect blue objects, ranging from flowers and bottle evolve in response to competition between members of one caps to colourful glass, with which to decorate their sex for access to mates in the other. These are used in bowers. Movement is often used in visual displays, perhaps contests between individuals where weaponry and threat to increase the detectability of morphological traits, as signals are produced to deter rivals. Perhaps the most these can only be received over relatively short distances. striking examples of these are traits that are used as This combination of movement with visual signals may be weapons, such as the antlers of many ungulates and the regarded as a behavioural display, which often incorpo- horns of some beetle species. rates signals from other sensory modalities. Social signalling Multicomponent signalling Social signals are used by conspecifics living in tight Many animals use complex signals that combine multiple groups. They can reveal the dominance and hierarchical components. Multicomponent signals may have evolved status of a particular individual within the group. Social because they allow more effective information transfer, or signals can also be cooperative when animals transfer convey more information than single component signals. information that benefits both signaller and receiver; for These signals may be potentially more reliable, or more example, small passerine birds use alarm calls to inform difficult to ‘eavesdrop’ (see below). Multicomponent individuals within the same flock of an approaching signals can be either unimodal, i.e. they are perceived in predator. Alarm calls benefit receivers as it provides them only a single sensory modality by the receiver, or they can with an opportunity to flee, but also protects the signaller be multimodal and produced in more than one sensory as it is less likely to be attacked in the flock than if it were to modality. For example, ladybirds (Adelia bipunctata) are flee on its own. aposematic, in that they taste unpleasant to birds and they signal this unpleasantness to birds using conspicuous Warning signalling colouring but also by releasing a strong pyrazine odour Not all communication occurs between conspecifics; when attacked. Birds learn to associate these multiple signals can also be directed at receivers in other species, signals with unpalatability, and association is most such as predators. Usually the function of signals that are effective when both the colour and the odour are present directed towards predators is to escape predation. Warn- (Marples et al., 1994). Many sexual signals also have ing signals, or aposematic signals, inform the predator that multiple components, and signallers often incorporate there is a cost of attacking the signaller. Usually this cost is movement in a vivid behavioural display. that the prey is unprofitable in some way; for example, the prey may contain chemicals that are unpalatable or are When do animals use signals? emetic. Some animals with warning colours, such as the yellow, red and black coral snakes or the redback spiders Animals use signals in situations where they need to convey (Latrodectus spp.), are deadly poisonous, and it is therefore information about themselves or their environment to in a predator’s interest to avoid these species. The most other animals. Signals are used in encounters between common and the best-studied warning signals are colour individuals of the same species (conspecifics), but also in patterns. A classic example of warning coloration is the interspecific interactions. Signals aimed at conspecifics black and yellow pattern of monarch butterfly larvae, and occur in a variety of social situations: for example, to their black and orange coloration as adult butterflies. In attract a mate, to defend a territory against a rival, or to this particular species of butterfly, the coloration functions

2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Signalling and Reception to warn predators that they contain cardiac glycosides. Siberia. In early spring, males advertise themselves to the These chemicals are emetic for most predators, and the females by drumming dry leaves with their abdomen. The recovery time after eating an adult butterfly may be up to a drumming is clearly audible to the human ear from several half an hour. metres. Male drumming rate is positively correlated with Many aposematic species also produce multicomponent male viability, and is highly condition-dependent (Kotia- warning signals (Rowe, 1999). For a long time, the different ho, 2000). Drumming has been found to be costly to components of these multicomponent signals, such as signallers, in that it takes considerable energy to produce odours, colours and behaviour, were thought to be directed and also increases the risk of predation. Moreover, at different groups of predators; for example, visual signals simultaneous manipulation of both the signalling rate were thought to be effective against birds, while odours and the condition of individuals has shown that drumming warned nocturnally hunting mammals. Recent studies of rate is more costly to those individuals in poor condition multicomponent signalling have, however, revealed that in than for those in good condition (Kotiaho, 2000). These fact more than one signal may be directed at a single results clearly show that, in H. rubrofasciata, male predator (Marples et al., 1994). Thus, by having more that drumming rate is an honest signal. one warning signal, prey can increase their chance of H. rubrofasciata females use male drumming signals to survival against a particular predator (Marples et al., 1994; choose their mate, and prefer those males with the highest Rowe and Guilford, 1996). drumming rates (Kotiaho et al., 1996). The females do not derive direct benefits from their mates, but the information that females receive from male signals may reveal heritable Honesty of Signals viability, in that the offspring of males with high drumming rates survive better than those of males with low drumming A fundamental component of signalling systems where rates (Alatalo et al., 1998). there is a conflict of interest between the signaller and the receiver is the maintenance of honesty in the signal. The question is, what prevents signallers from cheating or Deceptive signals giving misleading information in their signals? This We all know the story of the boy who ‘cried wolf’ when question is particularly pertinent because theoretically an there was no wolf around, who was then eaten by a wolf individual can benefit from giving false information (see because no one believed him when he was telling the truth. discussion on deception and mimicry below). Signal In the same way as the boy in the story, false signallers are honesty was first appreciated through the idea of the ignored and are selected out in nature. There are, however, ‘handicap principle’ (Zahavi, 1975; Johnstone, 1995). The some signals that are deceptive, in that they cause the handicap principle was introduced in the context of sexual receiver to behave in a way that is beneficial only to the selection and mate choice, but it is also applicable to many signaller. This can occur when the deceivers are very rare other signalling systems: for example, signals from prey to compared with honest signallers, or when the cost of predators, from offspring to parents, and between oppo- ignoring the signal, whether honest or not, is sufficiently nents in agonistic contests. The handicap principle high that the receiver should always pay attention to the proposes that signals are used by an intended receiver signal. because they convey honest information about the signaller; however, signal honesty can only be maintained if two conditions are fulfilled. First, signals must be costly Batesian mimicry: an example of a dishonest signal to produce or maintain for the signaller; and, second, the Prey use warning signals to inform predators that they are cost must be dependent on the condition of the signaller, inedible. It is advantageous for both predators and prey to such that signallers in good condition can withstand the use these signals, as the prey avoid being eaten and the cost of signalling at a given level better than a signaller in predators avoid eating prey that have detrimental fitness poor condition (Johnstone, 1995). The differential costs effects, and could be deadly poisonous. Thus the cost of between high-quality and poor-quality individuals is vital ignoring these signals is potentially very high for predators, for the maintenance of honest signals by the handicap which allows some species to display warning signals principle; however, in some cases, for example if there is no without being unpalatable. This phenomenon was first conflict of interest between the signaller and the receiver described by the nineteenth century naturalist Walter and the communication is cooperative, the signal may Bates, who described a striking similarity between different convey reliable information even if signalling is cost-free. species of conspicuous butterflies in the Amazon basin (Bates, 1862). By copying the same colourful warning An example of an honest signalling system patterns of unpalatable species (referred to as ‘models’), palatable ‘Batesian mimics’ escape predation, because Hygrolycosa rubrofasciata is a small lycosid spider which predators learn to avoid the unprofitable models and occurs in bogs throughout northern Europe and western cannot discriminate between them and the mimics. In this

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 3 Signalling and Reception way, the receiver is deceived, as Batesian mimics are survival by being designed to be easily detected, learned potentially edible prey. However, if the mimics become too and avoided by predators. abundant, predators are likely to sample both edible and The perceptual abilities of receivers have a significant inedible species while learning to avoid them, and the signal impact on signal design. First, the signal has to be sent will lose its meaning to receivers; therefore, Batesian within the sensory limits of the receiver in order for it to be mimics should always be rare relative to the abundance of perceived at all. The sensory systems of animals vary: for their models. example, birds can perceive ultraviolet wavelengths of light to which humans, and most other mammals, are blind and Audience effect cannot see. In fact, avian visual systems are more sensitive to colour than those of many mammals, which may explain One other interesting influence that changes signaller why birds often use colourful signals, whereas many behaviour is the size of its potential audience. The audience mammals use olfactory or acoustic signals. Second, signals of a signaller includes the intended recipients, and also all have to be detected by the receiver against environmental other individuals that can potentially receive and use the background noise; for example, acoustic signals need to be signal (see also Eavesdropping, below). A good example of heard over other sounds, perhaps the running water of a the audience effect is where signallers only signal if river or the wind rustling the vegetation. Many signals are conspecifics are present. Experiments investigating alarm therefore highly conspicuous, which increases the like- calling in male chickens show that males are more likely to lihood of the intended receiver detecting the signal, but of give alarm calls in response to aerial predators if there are course also increases the risk of other animals also conspecifics present than if they are alone. This suggests receiving the signal. The level of detectability of a signal that, because of the risk of being attacked, it is only may be considered a trade-off between ensuring the advantageous for these males to make this call when there signaller’s target receives the message while reducing the are receivers to hear it, especially if those animals are chance that the information gets into the wrong hands (see related. The audience effect may influence other beha- Eavesdropping, below). Finally, once the signal has been viours of an individual, and consequently this term does detected, the receiver has to recognize the signal and not refer exclusively to signalling situations. For example, discriminate between signals that are similar. This may male budgerigars have been found to be more likely to involve the receiver having to learn and remember the engage in extra-pair courtship and copulation when their meaning of the signal, so, again, features of a signal that are mates are not observing such behaviour. Thus, the easily remembered will be selected for by receivers. behaviour of the signalling individual can be influenced Receivers exert strong selection pressures on signallers by which receivers are present. The next section considers to produce signals that they can readily perceive, and the role of receivers in the evolution and design of signals in signallers benefit from their signals being more effective at more detail. producing the desired response from receivers; however, as mentioned above, it is not only the intended receivers that affect signal design, but also those animals that eavesdrop. Signal Design and Receiver Psychology Eavesdropping So far, we have only considered the ‘strategic’ design of a signal, i.e. how a signal transfers information to receivers, The Concise Oxford Dictionary defines ‘eavesdrop’ as to and how that information is, on the whole, reliable and ‘listen secretly to private conversation’. Of course, this honest. There is another aspect to signalling, as signals are definition applies to human communication, but the term also designed to transfer this information in an efficient eavesdropping is used in a similar way to describe the way, i.e. in a way that makes it easy for an intended receiver situation where a third animal (neither the signaller nor the to perceive the signal. This has been termed signal ‘efficacy’ intended receiver) receives the signal and obtains informa- (Guilford and Dawkins, 1991), and it can be thought of as tion from it. Eavesdroppers can be conspecifics but, being how the signal is designed to transfer its message. To perhaps more commonly, eavesdroppers are from other understand the evolutionary pressures acting on signal species, and indeed are often predators or parasites using efficacy, we need to consider the environment in which a signals to locate their victims. A good example of this has signal is emitted, but also the sensory systems and been found in studies of Gryllus field crickets and their psychology of receivers. ‘Receiver psychology’ is likely to parasitoids. Male field crickets produce acoustic signals by have been important in signal evolution, selecting for those stroking their modified forewings together, which serve as signals that are easier to detect, recognize, discriminate, sexual signals to attract females. Field crickets are learn and remember (Guilford and Dawkins 1991). A good parasitized by parasitoid flies (Ormia spp.) and it has been example of signals that enhance their efficacy are conspic- shown that these flies find their cricket hosts by acoustically uous warning signals that increase the chance of prey orienting towards their song (Zuk et al., 1998). Thus, the

4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Signalling and Reception parasitoid flies are eavesdropping on the male sexual transferred between flowers, ensuring their reproductive signals that are intended for the female crickets. In cases success. In most cases the signal of nectar availability is where eavesdropping is costly for the signaller, as in this honest, but there are some plants that deceive pollinators example, signallers have evolved adaptations that mini- and do not have nectar (Nilsson, 1992). mize the chance of signal detection by eavesdroppers, or There are some other well-known cases of deceptive prevent it altogether. One good way to do this is to use a signalling in plants; for example, carnivorous pitcher signal that their predators cannot perceive; for example, plants (Rafflesiaceae) use ultraviolet and olfactory signals nestlings of bird species that are prone to nest predation use to deceive insects into approaching them, when they are higher frequency and lower amplitude pecking calls than then trapped and digested. Another interesting example is other species. These acoustic features make it much more found in some orchids (Orchidaceae) which produce difficult for the predator to find the nest. flowers that resemble the body and crossed wings of a particular female insect, tricking male insects into ‘copu- Sensory exploitation and sensory bias lating’ with the flower. The orchids have evolved not only a visual resemblance to female insects but the flowers also Although receiver psychology can influence the design of a emit chemical compounds that are identical to those signal, it can also be ‘exploited’ by signallers. ‘Sensory produced in the pheromonal secretions of the receptive exploitation’ occurs when signallers take advantage of female insects (Nilsson, 1992). The insect does not gain preexisting sensory properties or biases that have evolved anything from the orchid but with the fraudulent signalling in receivers for reasons unrelated to communication. This the orchid may achieve pollination. has been proposed as a mechanism by which sexually Animals may not be the only receivers of plant selected traits might evolve, with a preference for a signals: there is some evidence of signalling between particular trait occurring in females before it actually plants. For example, when sagebrush plants are evolves in males; obviously such a trait will have a strong experimentally clipped, they release a pulse of a chemical selective advantage through female choice (Ryan, 1998). In that functions as a volatile signal capable of inducing theory, there are good reasons why sensory exploitation resistance to herbivory in neighbouring undamaged wild should be common, but as yet we have not enough tobacco plants (Karban et al., 2000). Although this does empirical evidence to assess the general importance of not show that these chemicals have explicitly evolved as sensory exploitation in the evolution of signalling systems signals, it does show that plants can potentially perceive (Johnstone, 1995). One of the best examples for sensory and respond to chemical cues from other plants. These exploitation comes from studies on the tu´ ngara frog examples show that signalling and communication are (Physalaemus pustulosus) species complex. In this group common phenomena not only among animals but also of frogs, some species produce calls consisting of two among plants. different components, while others produce calls with only one component. If the mating call of a male from a species that has only one component is digitally mastered to contain two components, females now prefer the new call with the additional component. Thus it would appear that References females prefer a call with more components if it were to Alatalo RV, Kotiaho J, Mappes J and Parri S (1998) Mate choice for evolve in this species. In fact, if we look at the evolutionary offspring performance: major benefits or minor costs? Proceedings of history of this group of frogs, the male calls become the Royal Society of London. Series B: Biological Sciences 265: increasingly complex as the species evolve. This confirms 2297–2301. the results of the experiments, and gives strong support for Andersson M (1994) Sexual Selection. Princeton: Princeton University preexisting sensory biases in females and sensory exploita- Press. tion by males (Ryan, 1998). Bates HW (1862) Contributions to the insect fauna of the Amazon valley (Lepidoptera: Heliconidae). Transactions of the Linnean Society of London 23: 495–556. Guilford T and Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Animal Behaviour 41: 1–14. Signalling in Plants Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biological Review 70: Communication is often thought to be characteristic of the 1–65. animal kingdom but signalling also occurs in plants; for Karban R, Baldwin IT, Baxter KJ, Laue G and Felton GW (2000) example, the colours and scents of flowers in animal Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125: pollinated plant species are clear signals that have evolved 66–71. to attract pollinators. The flowers offer pollen and nectar Kotiaho JS (2000) Testing the assumptions of conditional handicap rewards to foraging pollinators, while at the same time theory: costs and condition dependence of a sexually selected trait. benefiting from these foraging animals when pollen is Behavioural Ecology and Sociobiology 48: 188–194.

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Kotiaho J, Alatalo RV, Mappes J and Parri S (1996) Sexual selection in a Zuk M, Rotenberry JT and Simmons LW (1998) Calling songs of field wolf spider: male drumming activity, body size and viability. Evolution crickets (Teleogryllus oceanicus) with and without phonotactic 50: 1977–1981. parasitoid infection. Evolution 52: 166–171. Marples NM, van Veelen W and Brakefield PM (1994) The relative importance of colour, taste and smell in the protection of an aposematic insect Coccinella septempuncata. Animal Behaviour 48: 967–974. Further Reading Nilsson LA (1992) Orchid pollination biology. Trends in Ecology and Evolution 7: 255–259. Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford: Rowe C (1999) Receiver psychology and the evolution of multi- Clarendon Press. component signal. Animal Behaviour 58: 921–931. Guilford T and Dawkins MS (1993) Receiver psychology and the design Rowe C and Guilford T (1996) Hidden colour aversion in domestic of animal signals. Trends in Neurosciences 16: 430–436. chicks triggered by pyrazine odours of insect warning displays. Nature Hauser MD (1997) The Evolution of Communication. Cambridge, MA: 383: 520–522. MIT Press. Ryan MJ (1998) Sexual selection, receiver biases, and the evolution of sex Krebs JR and Davies NB (eds) (1991) Behavioural Ecology. An differences. Science 281: 1999–2003. Evolutionary Approach, 3rd edn. Cambridge: Blackwell Science. Zahavi A (1975) Mate selection – a selection for a handicap. Journal of Majerus MEN (1998) Melanism. Evolution in Action. New York: Oxford Theoretical Biology 53: 205–214. University Press.

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