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Communication in spiders
Communication in spiders George W. Uetz and Gail E. Stratton As in other animals, the exchange of signals between spiders serves many purposes and in recent years it has been shown that they have evolved a very complex system. This includes the exchange of information by acoustic/vibratory mechanisms; by visual means; and by pheromones. This article reviews these systems and the circumstances in which they are brought into play. The mention of animal communication brings to mind numerous examples from everyday life: birds singing, crickets chirping, dogs wagging their tails, and so on. To biologists and others more familiar with animal behaviour, the subject brings to mind a number of examples of courtship display behaviours. parent-offspring recognition, social dominance interactions, and predator alarm calls, in a wide variety of animals. Even to those familiar with the subject, it might seem strange that the topic of communication in spiders would be the subject of an entire book. Spiders are Xi not thought of particularly communicative animals, but rather as solitary and silent predators. However. spiders have long been neglected as subjects of scientific research, when compared with vertebrates and insects, whose communication systems are widely known. There has developed, over the past few years, a body of information on the behaviour of these animals which shows them to be no less interesting than any of the larger animals that have attracted the attention of scientists and laymen alike. The recently published book [l] which has prompted the writing of this article, was the outcome of a svmposium at the 107s Inter-national George
W. Uetz, M.S., Ph.D.
Studied biology at Albion College, Michigan; galned a Master’s degree I” entomology at the University of Delaware; and a Doctorate in ecology from the University of Illinois. Currently. he is an Associate Professor of Biological Sciences at the University of Cincinnati. His research is centred on the behavioural ecology of spiders, particularly their courtshlp and social behavlour. Gall Stratton,
M.S.. Ph.D.
Received her undergraduate training at Carleton College, Minnesota, and her M.S. and Ph.D. at the University of Cincinnati. Her in the courtship are research interests behavlour and behaviour genetics of wolf spiders.
Endeavour. New Series, Volume 7. No. 1. 1983. (Cc, Pergamon Press. Printed in Great Britain1 0160.9327/63/010013-06 $03.00.
the Meeting of American Arachnological Society at Gainesville, Florida. In it, twelve biologists involved in research on diverse aspects of spider behaviour present a comprehensive review of previous and research on various current communicative interactions in spiders, the sensory modalities which underly them, and the nature of their ecological and evolutionary significance. This article will attempt to give a brief overview of the drawing topic, from the examples book, and borrowing to some extent its format. Spider communication: what is it? Communication in animals is typically an exchange of information in the form of direct interactions between individuals. A signal of some kind (that is, acoustic or visual display) is sent from one animal to another, and a signal or other change in behaviour occurs in response [2]. These signals may contain information on the behavioural state of the animals (level of aggression, sexual activity, etc.); their identity (species, sex); their relationship to others (mate, parent, offspring); and the nature of possible future actions (threat, receptivity). Communication may also be indirect, in that signals (that is, chemical pheromones), may be emitted without a specific target, and may persist in the environment long enough to elicit responses at a later time. in Communication spiders is fundamentally similar to that in other animals, with a few differences which relate to the nature of spiders themselves. Thus the various sensory organs which have evolved in spiders for detection of prey also serve in receiving signals from other spiders. Unlike most other predatory animals, which use keen vision or olfactory senses in locating prey, spiders use solid-borne mechanical cues (that is, vibrations) as their primary means of prey detection. Web-building spiders are well-adapted to detect prey vibrations in their webs, and are also recognizing capable of signals
transmitted through silk by conspecifics (for example, the plucking of silk strands by courting males). Not all spiders spin webs, however, and the sensory organs and hairs of wandering spiders, which provide information on prey insects crawling or flying nearby, are also used to detect the substrateconducted or airborne vibrations produced by other spiders in courtship or threat displays. Spiders use other sensory modalities, like vision and olfaction, in their predatory behaviour and communication as well. A limited number of spider families (for example, wolf spiders and jumping spiders (figure 1) ) possess well developed visual senses, and it is among these that visual signals play an important role in communication. Spiders also have olfactory senses, and although our understanding of chemosensory receptors and pheromones in spiders is nowhere near ah advanced as it is for insects, it is clear are that chemical signals important for spiders. In this article, we will examine the three main modes of communication in spiders (Acoustic/Vibratory, Visual, and Chemical) and their mechanisms. Then we will discuss the contexts of spider communication: the circumstances under which it occurs. and its ecological and evolutionary significance. It is hoped that this review will introduce the reader to an emerging area of biological research, and whet the appetites of those who desire more information, so that they may read the book. Acoustic/Vibratory communication As most spiders do not see well, it is probable that other senses provide them with much of the information they receive from their environment. Vibratory signals are of particular importance to spiders and other arachnids and are perceived through vibration receptors like trichobothria (‘thin hairs’), and slit sense organs. The trichobothria are elongate, slender hairs on the dorsal surface of the distal leg segments of many of the wandering
13
.I
Figure 1 A male jumping spider (fellenes courtesy Wayne P. Maddison.)
americanus:
family
Salticidae)
(Drawing
spiders. Each has 24 sensory cells at . The slit sense organs are unique to the arachnids, and have been shown to its base, which are triggered when the hair moves. They have been shown to be important receiving organs for respond to airborne stimuli, to air flow communication through vibration [4]. (their rough surface improves the A slit sense organ is comprised of a coupling with air), and to near-field hole in the exoskeleton, 5-200 pm acoustic signals. The importance of the long, 2 pm wide, covered by a thin trichbothria in prey localization has membrane (figure 2). The dendrites of a sensory cell attach to the membrane been demonstrated, but their relative and monitor movement or tension that importance in communication has not been experimentally verified [3]. occurs in the cuticle; thus, these organs function as ‘strain gauges’. Slit sense organs come in a variety of sizes and are mostly located on the extremities of the animal. One spider, Cupiennius salei, was found to have 3300 slit sense organs [5]! In some cases, slit sense organs occur in close parallel arrangements known as lyriform organs. Several slit sense or lyriform organs have been studied
Figure 2 Single slit sense organs in Cupiennius salei (family Ctenidae), involved in airborne sound and vibration detection. (a) Single slit (circle) on tarsus, sensitivetoairbornesound.Tr= trichobothrium;Sc=scopularhair.(b) Single slit in cuticle fold behind the tarsal claw, which is sensitive to substrateborne vibrations. (From Barth [4] by permission of Princeton University Press)
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electrophysiologically, and found to be very sensitive to solid-borne vibrations. A single large slit sense organ in the tarsus has been identified as a ‘hearing organ’ [6] and is sensitive to airborne sounds at some distance. Vibrations are important in the communication systems of many different kinds of spiders. Transmission of vibratory signals through silk is wellknown for a variety of web-building spiders. Males create signals on females’ webs by plucking, drumming, or use of stridulatory organs (a ‘file and washboard’ type of organ, similar to sound producing organs in other arthropods). Females respond by jerking the web or pulling on individual silk strands. Web vibrations during communication have been recorded by a number of investigators, and signals range in frequency from 2-150 Hz (figure 3). Many spiders are capable of making sounds and vibrations by drumming, stridulating, or vibrating the whole body [7]. Indeed, sound production may be quite common in spiders (26 families of spiders have members that appear capable of making sounds), although only a few species have been studied in any depth. Wolf spiders have been known to use percussion of palps to produce sound on leaves, plants, and the ground surface. The ‘purring’ sound of many wolf spiders was thought to be drumming, until a stridulatory organ in the palps was discovered by J. S. Rovner [8] (figure 4). This organ is located in the tibialtarsal joint with the scraper on one side of the joint and the file on the opposing surface. The sounds produced stridulation and associated by behaviours in wolf spiders have been studied [9], and figure 5 shows a sonogram of the sounds produced.
Figure 3 Web vibrations in.the courtship of a male Amaurobius Amaurobiidae);d=drummingwithpalps,k=strikeswithpalps;a=vibrationsof abdomen. (From Krafft (321 by permission of Princeton University
ferox (family Press)
Figure 4 Scanning electron microscope photo of palp of male wolf spider (Schizocosarovneri;familyLycosidae),showing locationofthestridulatoryorgan. (a)insidethejointofthetibiaandtarsus.(b)Theorganconsistsofafile,shownhere, and a scraper, which is rubbed against it to produce sound.
spiders, for crab spider Heteropoda venatoria, produce sound by vibration of their legs. These spiders use environmental surfaces like leaves as ‘sounding boards’ to amplify the airbourne component of the vibrations produced during courtship [lo]. Other example
wandering the giant
Visual communication
The Salticidae, or jumping spiders, stand apart among spiders in their development of visual acuity, and in the use of visual cues in both predatory and courtship behaviours. Jumping spiders, along with cephalopods and vertebrates, are considered to be one of the great evolutionary experiments in eyesight [I I]. Like most spiders.
salticids have four pairs of simple eyes. The arrangement of these eyes into three rows (figure 6) makes jumping spiders easy to recognize. This complement of eight eyes, each with particular strengths and abilities, gives these spiders the ability to perceive both form and movement. Row one, at the anterior end of the carapace, consists of two pairs of eyes, the anterior lateral eyes (ALE) and the anterior media1 eyes (AME); row two contains the very small posterior medial eyes (PME) whose function remains unknown; row three occurs about halfway back on the carapace and consists of the posterior lateral eyes (PLE). The eye structure of the Salticidae is the best studied of any spider. All the
eyes consist of a cornea (continuous with the cuticle on the carapace), a fixed lens, a vitreous body, and a retina. The AME, ALE, and PLE differ from each other in the structure of the retina and in the shape of the eye capsule, and have different capabilities based on these differences, affecting both the field of vision and the nature of visual perception [12]. The ALE and PLE have relatively and shallow capsules, eye corresponding broad fields of vision (figure 6). The lateral eyes are particularly capable of detecting movement. When movement is sensed somewhere in the visual field of the lateral eyes, the spider will swivel to face the moving object direction [ 11, 121. This then stimulates the AME, and will continue to stimulate the ALE (whose field of vision overlaps slightly directly in front of the spider). The large AME are unique in the animal kingdom. They have a very long focal length (the eye capsule is tube-shaped) and very fine receptor grain, which gives the jumping spiders visual acuity about 3 times that of the insect compound eye. The AME have a relatively small field of view. which is ;I ‘trade off’ and is compensated for by the ability of the retinae to move. The AME are used to identify stationary objects. which are first ‘fixated’ in the central area of the retinae, and then ‘scanned’ by the moving retinae. The good eyesight of jumping spiders correlates with their largely diurnal hunting habits; most do not build webs but rather pursue andlor stalk their prey. Salticid spiders make use of remarkable displays in visually Many mediated courtship. male salticids may be extravagantly marked with coloured setae, scales, and hairs (see cover), which in some cases may enhance the movements used in courtship. Many biologists have studied the behaviours of jumping spiders [13] and found a wide variety of different movements that function as visual signals (these include leg waving and raising, crouching, and other postures and movements). Lysocidae, or wolf spiders, are vagrant hunting spiders with relatively well- developed eyesight, but the visual system of this family is mainly adapted for detecting movement. This has been supported by behavioural studies, which have found movement of marked legs to be important in courtship [14]. Males of Schizocosa rovneri will not orient to females when they are not moving. In fact, a courting male might walk right past a female and apparently not ‘notice’ her until she moves. If she did, the male would orient to her and begin more vigorous courtship [15].
15
males of other species did not. It would appear that the relative importance of airborne and silk-borne chemical signals varies among spider species. Contexts
Figure 5 Sonagrams of sounds produced by male wolf spiders (a) Schizocosa ocreata; (b) Schizocosa rovneri.
Chemical communication channel The chemical
of communication is probably the most primitive one for animals in general. Chemical signals, called pheromones, are substances secreted by one individual and received by another which elicit a specific response (for example, sex pheromones secreted by females stimulate courtship behaviour in males). Spiders have a well developed tactochemical sense and are known to use pheromones in courtship situations. There is also evidence that several groups of spiders use airborne pheromones. However, the identity of the production sites of these chemicals is still unknown for spiders, as is the molecular spider structure of pheromones [ 161. Until recently, the actual identity of spider chemoreceptors was a topic of much speculation. R. F. Foelix (17) suggested that the curved, blunt-tipped sensilla concentrated on the distal parts of the legs (figure 7(a) ) are the chemoreceptors. This suggestion support from has received electrophysiological studies. Studies have revealed 19 dendrites (endings of nerve cells) running the length of the hairshaft as compared with 2-4 dendrites in insect sensilla. Thus, a spider could potentially discriminate many more types of chemical substances than insects do. These sensilla are probably contact chemoreceptors, and respond to pheromones deposited in spider silk or on environmental surfaces [IS]. 16
during
courtship.
Male orb-weaving spiders will begin characteristic courtship behaviour upon contacting a female’s web, even when the female is not present, and male wolf spiders will follow the dragline trails left by females (figure 7(b) ). W. J. Tietjen [19] suggests that a pheromone is necessary to start the ‘following behaviour’, but once started, tactile cues (from the silk) also become important. Tietjen found that males will occasionally follow male draglines, or imitation lines if the male is first following female silk. In many species of spiders, a pheromone, or a pheromone combined with tactile cues from silk, are sufficient to release courtship behaviour in males. Males of both Schizocosa ocreata and S. rovneri wolf spiders will court females of either species or their silk with equal indicating frequency, that the pheromone must be very similar for these two closely related species [20]. via Communication airborne chemical signals has been demonstrated in both web-building spiders and wandering spiders. Several studies have shown that males can find and orient to a female on her web over distances as great as 1 m [21]. Tietjen [22] tested several species of wolf spiders with an olfactometer, a device which tests the response of male spiders by circulating air across a hidden female into an arena. Males of several species responded by reducing their locomotory behaviour and approaching the female’s location while
of spider
communication
The communication systems used by spiders are interesting and diverse-in many cases different several communication modes are used simultaneously. Spiders are known to use visual, chemical, and acoustic/ vibratory courtship signals in behaviours, agonistic displays, and in a variety of other social interactions. One of the most important contexts of spider communication, and certainly the most studied, is that of courtship. The problem of getting the sexes together is compounded in- spiders by their cannibalistic tendencies, but is adequately overcome by the complex behaviours and fairly effective communication systems these animals have evolved. Finding a mate is often difficult for solitary animals dispersed in the environment. In general, mate location in spiders is accomplished using chemical cues. Silk-borne or airborne pheromones allow males to locate females by following draglines or searching surfaces for increasing concentrations of ‘sex scents’. Once a male comes into the vicinity of a female, he must be wary of her predatory instincts and give her advance notice of his identity and intentions, as well as ascertain her willingness to mate. These are usually accomplished by acoustic/vibratory communication or visual signalling. The leaves of a banana plant are used as a substrate for transmitting reciprocal courtship signals of Cupiennius safei [23]. A courting male can be identified by a female located on a separate leaf of the banana plant (out of sight of the male), and the male
Figure 6 Diagram of a horizontal/ frontal section through the eye region of a jumping spider, showing the field of vision of the different eye groups (see text for details). (from Forster (1 l] by permission of Princeton University Press)
can locate her, based on her responding vibratory signals to him, even when the airborne sound component is masked by a random noise generator. As they signal back and forth, the male moves closer, and eventually finds his mate. The substratum-borne importance of vibratory signals in the courtship of wolf spiders was demonstrated in a study in which a female spider was isolated first visually, then acoustically from the courting male [15]. Visual signals alone are not sufficient to elicit a receptive response in the female, but vibratory signals were both necessary and sufficient to elicit the receptive response. This study also showed that vibratory cues were essential to the reproductive isolation of these species. Although capable, these species do not interbreed because females will only respond receptively to species-specific vibrations from conspecific males. In many web-building spiders, males arrive at the edge of the female’s web and begin tapping. If the female responds receptively, the male enters her web and begins a more vigorous courtship, leading to tactile contact and mating. In many of the orb-weavers, whose intricate circular webs are particularly effective at transmitting vibrations, males use a slightly different male approach. The approaches the hub of the female’s web, and cuts a hole in her web and connects a mating thread to this area. He vibrates this thread by a variety of movements (bouncing, jerking, and tarsal rubbing), and if the female is receptive, she comes out on the thread, where mating occurs. If the female responds in a predatory fashion, the male cuts the thread and escapes [24]. The degree of visual sophistication which has evolved in jumping spiders has clearly influenced the diversity of behaviours exhibited by these spiders. Both the predatory behaviours and the courtship behaviours of jumping spiders make good use of the salticid visual system. As with all spiders, the courting male has the problem of not eliciting the predatory behaviour of the female he is courting. The approach tactics of a male jumping spider often include a zigzagging approach, in which the male moves widely from side to side as he approaches the female. This is coupled with species-characteristic movement of palps and legs (waving and tapping). These movements may rninimize the probability of eliciting chasing or stalking behaviour by the female, by keeping the male in the appropriate visual field [25]. Communication plays an important part in other aspects of the lives of spiders. For example, defence of webs is common among web-building
Figure 7 (a) Scanning electron microscope photo of chemosensory hairs on the palp of a male wolf spider (Lycosa punctulata). (b) A male wolf spider following a silk dragline left by a female. ( (a) courtesy W. J. Tietjen; (b) courtesy J. S. Rovner) spiders, and it is apparent that ritualistic combat behaviours serve this function without serious loss of life or limb to the combatants. In the extensively studied desert funnel web spider, Agelenopsis aperta, the intensity of conflict and the sequence of behaviours involved in contests over web sites vary with the quality of the web site and the size difference between resident and intruder. In these interactions, disputes are settled primarily by visual and vibratory signalhng between spiders [26]. Other examples of spider communication in the context of territoriality may involve defence of female’s webs by males [27] or the maintenance of spacing between individuals relative to food availability [28]. In both of these situations, communicative interactions serve to mediate disputes. Interactions of this type are particularly important among the web-building spiders living in social
groups. Communication through web vibration has been suggested as a preadaptation for sociality in some groups, and serves to mediate spacing, facilitate feeding, and warn colony members of danger from predators [291. Communication in social interactions is not limited to web-building spiders. Social hierarchies may exist among the vagrant wolf spiders, and provide the successful competitors preferential accessto food or mates, even where a territorial space is not involved. W. P. Aspey [30] found a diversity of agonistic display in behaviours Schizocosa ocreata which were used in establishing and maintaining dominance-subordinance relationships among males. Many spiders exhibit some degree of maternal care of their young, and this appears to depend in part on complex interactions between parent and offspring, which serve to prevent cannibalism and allow coordination of activities. Communication can play an important role in these interactions. Female wolf spiders, for example, tear open egg sacs when they detect vibrations indicating that the young are ready to move from the egg sac on to the abdomen of the female, where they will be carried for several days. The young spiders cling to specialized hairs on the female’s abdomen [31] and travel with her. When the female is not moving, the spiderlings may climb down off her abdomen and explore the environment, drink water, and wander about, always connected to the mother by silk draglines attached to the abdominal hairs. When danger threatens, or a change in location is imminent, changes in the tension of those silk lines due to erection of hairs signal the young to return to the female’s abdomen. Stimulation of mechanoreceptor hairs on the female as the result of activity of the spiderlings also suppresses cannibalistic tendencies in their mother. Tolerance of young spiders on the web of some female spiders is facilitated by recognition of offspring through communicative interactions involving tactile contact, web vibration, or chemical signals. However, some web-building spiders exhibit maternal care beyond tolerance and protection of young. When a female of Theridion saxatile captures prey, she tugs on the threads of the web in a jerking fashion, warning spiderlings to hide in a protected area. Once the prey is subdued, she slowly pulls on the thread, and the young emerge to share in the kill [32]. In other Theridiid spiders, the young actively request feeding by tapping their legs on the palps and legs of their mother. The 17
female regurgitates digested food for the spiderlings, but regulates the rate of their feeding and their access by communicative leg movements. Even among those species whose young hatch from egg sacs left behind without parental care, communication between spiderlings is important to survival. Encounters between spiderlings on communal webs involve vibratory communication through the web, or leg tapping behaviours, which allow spiderlings to recognize and coexist with each other [33]. As spiderlings grow older, the mechanisms of mutual tolerance present in iuvenile aggregations disappear. Young- spiders snin individual webs. and after this -r ~~~ stage are more likely to exhibit agonistic or predatory behaviours conspecifics. The towards interactions which communicative govern the relations between spiders during the juvenile communal and dispersal phases are still largely unknown. It is, however, probable that these behaviours may form the basis for development of adult behaviours, and have some role in the evolution of social behaviour in some of the groupliving spider species. Conclusion
Questions concerning communication and the evolution of communicatory signals are perhaps particularly interesting in spiders because these animals are mostly solitary, predatory, and potentially cannibalistic. In many cases, behaviours that serve in prey detection and localization have been only slightly modified to function in communication. We would, therefore, expect intense selection pressure for effective communication. The result of
18
this pressure has been the evolution of the tremendous behavioural diversity that makes spiders such fascinating creatures.
References [l] Witt, P. N. and J. S. Rovner (Eds.), ‘Spider Communication: Mechanisms and Ecological Significance.’ Princeton Univ. Press. 1982. [2] Wilson, E. 0. ‘The Insect Societies.’ Harvard Univ. Press. 1971. [3] Reissland, A. and P. Gorner. Mechanics of trichobothria in orbweaving spiders. J. Camp. Physiol., 123; 59. 1978
[4] Barth, F. G. ‘Spiders and Vibratory Signals: Sensory Reception and Behavioral Significance’ in Witt & Rovner, pp. 67-122. 1982. [S] Ibid. [6] Ibid.
[7] Uetz, G. W. and G. E. Stratton. ‘Acoustic Communication and Reproductive Isolation in Spiders.’ in Witt & Rovner, pp. 123-159, 1982. !8] Rovner, .I. S. Science, 190, 1309. 1975. [9] Stratton, G. E. and G. W. Uetz. Science. 214. 575. 1981.
[lo] Rovner, J: S. J. Arachnof., 8, 201, 1980. [ll] Forster, L. M. ‘Visual communication in jumping spiders (Salticidae)’ in Witt & Rovner, pp. 161-212, 1982. [12] Forster, L. M. Amer. Scientist, 70, 165, 1982.
[13] Jackson, R. L. ‘The behavior of communicating in jumping spiders (Salticidae).’ in Witt & Rovner, pp. 213-247. 1982.
[14] Rovner, J. S. Anim. Behav. 16, 358, 1978. [15] Stratton, G. E. and G. W. Uetz. Communication via substratumcoupled stridulation and reproductive isolation in wolf spiders (Araneae: Lycosidae). Anim. Behav. (in press). [16] Tietjen, W. J. and J. S. Rovner. ‘Chemical communication in lycosids and other spiders.’ in Witt & Rovner, pp. 249-279, 1982. [17] Foelix, R. F. J. Morph., 132, 313, 1970. [18] Foelix, R. F. and I. W. Chu-Wang. Tissue & Cell, 5, 461, 1973. 1191Tietjen, W. J. and J. S. Rovner. Anim. behav.,28,735,1980. 1201 Uetz. G. W. and G. Denterlein. J. Akzchnof., 7, 121, 1979. [21] Blanke, R. 2. Tierpsychol., 37, 62, 1975. [22] Tietjen, W. J. J. Arachnol., 6, 197, 1979. [23] Rovner, J. S. and F. G. Barth. Science, 214, 464, 1981. [24] Robinson, M. H. and B. Robinson. Symp. Zool. Sot. London., 42, 17, 1978. [25] Jackson, op. cit. L
1
[26] Reichert, S. E. ‘Spider interaction strategies: communication vs. coercion.’ in Witt & Rovner, pp. 281-315, 1982. [27] Rovner, J. S. Z. Tierpsychologie, 25, 232,1968. [28] Reichert, S. E. Symp. Zool. Sot. Lond., 42, 211, 1978. [29] Burgess, J. W. and G. W. Uetz. ‘Social spacing strategies in spiders.’ in
Witt & Rovner, pp. 317-351, 1982. [30] Aspey, W. P. Behaviour, 62, 103, 1977. [31] Rovner, J. S., G. A. Higashi and R. F. Foelix. Science, 182, 1153, 1973. [32] Krafft, B. ‘The significance and
complexity of communication in spiders.’ in Witt and Rovner, pp. 15-65, 1982. [33] Krafft, B. Ibid.
W. Uetz, M.S., Ph.D.
Studied biology at Albion College, Michigan; galned a Master’s degree I” entomology at the University of Delaware; and a Doctorate in ecology from the University of Illinois. Currently. he is an Associate Professor of Biological Sciences at the University of Cincinnati. His research is centred on the behavioural ecology of spiders, particularly their courtshlp and social behavlour. Gall Stratton,
M.S.. Ph.D.
Received her undergraduate training at Carleton College, Minnesota, and her M.S. and Ph.D. at the University of Cincinnati. Her in the courtship are research interests behavlour and behaviour genetics of wolf spiders.
Endeavour. New Series, Volume 7. No. 1. 1983. (Cc, Pergamon Press. Printed in Great Britain1 0160.9327/63/010013-06 $03.00.
the Meeting of American Arachnological Society at Gainesville, Florida. In it, twelve biologists involved in research on diverse aspects of spider behaviour present a comprehensive review of previous and research on various current communicative interactions in spiders, the sensory modalities which underly them, and the nature of their ecological and evolutionary significance. This article will attempt to give a brief overview of the drawing topic, from the examples book, and borrowing to some extent its format. Spider communication: what is it? Communication in animals is typically an exchange of information in the form of direct interactions between individuals. A signal of some kind (that is, acoustic or visual display) is sent from one animal to another, and a signal or other change in behaviour occurs in response [2]. These signals may contain information on the behavioural state of the animals (level of aggression, sexual activity, etc.); their identity (species, sex); their relationship to others (mate, parent, offspring); and the nature of possible future actions (threat, receptivity). Communication may also be indirect, in that signals (that is, chemical pheromones), may be emitted without a specific target, and may persist in the environment long enough to elicit responses at a later time. in Communication spiders is fundamentally similar to that in other animals, with a few differences which relate to the nature of spiders themselves. Thus the various sensory organs which have evolved in spiders for detection of prey also serve in receiving signals from other spiders. Unlike most other predatory animals, which use keen vision or olfactory senses in locating prey, spiders use solid-borne mechanical cues (that is, vibrations) as their primary means of prey detection. Web-building spiders are well-adapted to detect prey vibrations in their webs, and are also recognizing capable of signals
transmitted through silk by conspecifics (for example, the plucking of silk strands by courting males). Not all spiders spin webs, however, and the sensory organs and hairs of wandering spiders, which provide information on prey insects crawling or flying nearby, are also used to detect the substrateconducted or airborne vibrations produced by other spiders in courtship or threat displays. Spiders use other sensory modalities, like vision and olfaction, in their predatory behaviour and communication as well. A limited number of spider families (for example, wolf spiders and jumping spiders (figure 1) ) possess well developed visual senses, and it is among these that visual signals play an important role in communication. Spiders also have olfactory senses, and although our understanding of chemosensory receptors and pheromones in spiders is nowhere near ah advanced as it is for insects, it is clear are that chemical signals important for spiders. In this article, we will examine the three main modes of communication in spiders (Acoustic/Vibratory, Visual, and Chemical) and their mechanisms. Then we will discuss the contexts of spider communication: the circumstances under which it occurs. and its ecological and evolutionary significance. It is hoped that this review will introduce the reader to an emerging area of biological research, and whet the appetites of those who desire more information, so that they may read the book. Acoustic/Vibratory communication As most spiders do not see well, it is probable that other senses provide them with much of the information they receive from their environment. Vibratory signals are of particular importance to spiders and other arachnids and are perceived through vibration receptors like trichobothria (‘thin hairs’), and slit sense organs. The trichobothria are elongate, slender hairs on the dorsal surface of the distal leg segments of many of the wandering
13
.I
Figure 1 A male jumping spider (fellenes courtesy Wayne P. Maddison.)
americanus:
family
Salticidae)
(Drawing
spiders. Each has 24 sensory cells at . The slit sense organs are unique to the arachnids, and have been shown to its base, which are triggered when the hair moves. They have been shown to be important receiving organs for respond to airborne stimuli, to air flow communication through vibration [4]. (their rough surface improves the A slit sense organ is comprised of a coupling with air), and to near-field hole in the exoskeleton, 5-200 pm acoustic signals. The importance of the long, 2 pm wide, covered by a thin trichbothria in prey localization has membrane (figure 2). The dendrites of a sensory cell attach to the membrane been demonstrated, but their relative and monitor movement or tension that importance in communication has not been experimentally verified [3]. occurs in the cuticle; thus, these organs function as ‘strain gauges’. Slit sense organs come in a variety of sizes and are mostly located on the extremities of the animal. One spider, Cupiennius salei, was found to have 3300 slit sense organs [5]! In some cases, slit sense organs occur in close parallel arrangements known as lyriform organs. Several slit sense or lyriform organs have been studied
Figure 2 Single slit sense organs in Cupiennius salei (family Ctenidae), involved in airborne sound and vibration detection. (a) Single slit (circle) on tarsus, sensitivetoairbornesound.Tr= trichobothrium;Sc=scopularhair.(b) Single slit in cuticle fold behind the tarsal claw, which is sensitive to substrateborne vibrations. (From Barth [4] by permission of Princeton University Press)
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electrophysiologically, and found to be very sensitive to solid-borne vibrations. A single large slit sense organ in the tarsus has been identified as a ‘hearing organ’ [6] and is sensitive to airborne sounds at some distance. Vibrations are important in the communication systems of many different kinds of spiders. Transmission of vibratory signals through silk is wellknown for a variety of web-building spiders. Males create signals on females’ webs by plucking, drumming, or use of stridulatory organs (a ‘file and washboard’ type of organ, similar to sound producing organs in other arthropods). Females respond by jerking the web or pulling on individual silk strands. Web vibrations during communication have been recorded by a number of investigators, and signals range in frequency from 2-150 Hz (figure 3). Many spiders are capable of making sounds and vibrations by drumming, stridulating, or vibrating the whole body [7]. Indeed, sound production may be quite common in spiders (26 families of spiders have members that appear capable of making sounds), although only a few species have been studied in any depth. Wolf spiders have been known to use percussion of palps to produce sound on leaves, plants, and the ground surface. The ‘purring’ sound of many wolf spiders was thought to be drumming, until a stridulatory organ in the palps was discovered by J. S. Rovner [8] (figure 4). This organ is located in the tibialtarsal joint with the scraper on one side of the joint and the file on the opposing surface. The sounds produced stridulation and associated by behaviours in wolf spiders have been studied [9], and figure 5 shows a sonogram of the sounds produced.
Figure 3 Web vibrations in.the courtship of a male Amaurobius Amaurobiidae);d=drummingwithpalps,k=strikeswithpalps;a=vibrationsof abdomen. (From Krafft (321 by permission of Princeton University
ferox (family Press)
Figure 4 Scanning electron microscope photo of palp of male wolf spider (Schizocosarovneri;familyLycosidae),showing locationofthestridulatoryorgan. (a)insidethejointofthetibiaandtarsus.(b)Theorganconsistsofafile,shownhere, and a scraper, which is rubbed against it to produce sound.
spiders, for crab spider Heteropoda venatoria, produce sound by vibration of their legs. These spiders use environmental surfaces like leaves as ‘sounding boards’ to amplify the airbourne component of the vibrations produced during courtship [lo]. Other example
wandering the giant
Visual communication
The Salticidae, or jumping spiders, stand apart among spiders in their development of visual acuity, and in the use of visual cues in both predatory and courtship behaviours. Jumping spiders, along with cephalopods and vertebrates, are considered to be one of the great evolutionary experiments in eyesight [I I]. Like most spiders.
salticids have four pairs of simple eyes. The arrangement of these eyes into three rows (figure 6) makes jumping spiders easy to recognize. This complement of eight eyes, each with particular strengths and abilities, gives these spiders the ability to perceive both form and movement. Row one, at the anterior end of the carapace, consists of two pairs of eyes, the anterior lateral eyes (ALE) and the anterior media1 eyes (AME); row two contains the very small posterior medial eyes (PME) whose function remains unknown; row three occurs about halfway back on the carapace and consists of the posterior lateral eyes (PLE). The eye structure of the Salticidae is the best studied of any spider. All the
eyes consist of a cornea (continuous with the cuticle on the carapace), a fixed lens, a vitreous body, and a retina. The AME, ALE, and PLE differ from each other in the structure of the retina and in the shape of the eye capsule, and have different capabilities based on these differences, affecting both the field of vision and the nature of visual perception [12]. The ALE and PLE have relatively and shallow capsules, eye corresponding broad fields of vision (figure 6). The lateral eyes are particularly capable of detecting movement. When movement is sensed somewhere in the visual field of the lateral eyes, the spider will swivel to face the moving object direction [ 11, 121. This then stimulates the AME, and will continue to stimulate the ALE (whose field of vision overlaps slightly directly in front of the spider). The large AME are unique in the animal kingdom. They have a very long focal length (the eye capsule is tube-shaped) and very fine receptor grain, which gives the jumping spiders visual acuity about 3 times that of the insect compound eye. The AME have a relatively small field of view. which is ;I ‘trade off’ and is compensated for by the ability of the retinae to move. The AME are used to identify stationary objects. which are first ‘fixated’ in the central area of the retinae, and then ‘scanned’ by the moving retinae. The good eyesight of jumping spiders correlates with their largely diurnal hunting habits; most do not build webs but rather pursue andlor stalk their prey. Salticid spiders make use of remarkable displays in visually Many mediated courtship. male salticids may be extravagantly marked with coloured setae, scales, and hairs (see cover), which in some cases may enhance the movements used in courtship. Many biologists have studied the behaviours of jumping spiders [13] and found a wide variety of different movements that function as visual signals (these include leg waving and raising, crouching, and other postures and movements). Lysocidae, or wolf spiders, are vagrant hunting spiders with relatively well- developed eyesight, but the visual system of this family is mainly adapted for detecting movement. This has been supported by behavioural studies, which have found movement of marked legs to be important in courtship [14]. Males of Schizocosa rovneri will not orient to females when they are not moving. In fact, a courting male might walk right past a female and apparently not ‘notice’ her until she moves. If she did, the male would orient to her and begin more vigorous courtship [15].
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males of other species did not. It would appear that the relative importance of airborne and silk-borne chemical signals varies among spider species. Contexts
Figure 5 Sonagrams of sounds produced by male wolf spiders (a) Schizocosa ocreata; (b) Schizocosa rovneri.
Chemical communication channel The chemical
of communication is probably the most primitive one for animals in general. Chemical signals, called pheromones, are substances secreted by one individual and received by another which elicit a specific response (for example, sex pheromones secreted by females stimulate courtship behaviour in males). Spiders have a well developed tactochemical sense and are known to use pheromones in courtship situations. There is also evidence that several groups of spiders use airborne pheromones. However, the identity of the production sites of these chemicals is still unknown for spiders, as is the molecular spider structure of pheromones [ 161. Until recently, the actual identity of spider chemoreceptors was a topic of much speculation. R. F. Foelix (17) suggested that the curved, blunt-tipped sensilla concentrated on the distal parts of the legs (figure 7(a) ) are the chemoreceptors. This suggestion support from has received electrophysiological studies. Studies have revealed 19 dendrites (endings of nerve cells) running the length of the hairshaft as compared with 2-4 dendrites in insect sensilla. Thus, a spider could potentially discriminate many more types of chemical substances than insects do. These sensilla are probably contact chemoreceptors, and respond to pheromones deposited in spider silk or on environmental surfaces [IS]. 16
during
courtship.
Male orb-weaving spiders will begin characteristic courtship behaviour upon contacting a female’s web, even when the female is not present, and male wolf spiders will follow the dragline trails left by females (figure 7(b) ). W. J. Tietjen [19] suggests that a pheromone is necessary to start the ‘following behaviour’, but once started, tactile cues (from the silk) also become important. Tietjen found that males will occasionally follow male draglines, or imitation lines if the male is first following female silk. In many species of spiders, a pheromone, or a pheromone combined with tactile cues from silk, are sufficient to release courtship behaviour in males. Males of both Schizocosa ocreata and S. rovneri wolf spiders will court females of either species or their silk with equal indicating frequency, that the pheromone must be very similar for these two closely related species [20]. via Communication airborne chemical signals has been demonstrated in both web-building spiders and wandering spiders. Several studies have shown that males can find and orient to a female on her web over distances as great as 1 m [21]. Tietjen [22] tested several species of wolf spiders with an olfactometer, a device which tests the response of male spiders by circulating air across a hidden female into an arena. Males of several species responded by reducing their locomotory behaviour and approaching the female’s location while
of spider
communication
The communication systems used by spiders are interesting and diverse-in many cases different several communication modes are used simultaneously. Spiders are known to use visual, chemical, and acoustic/ vibratory courtship signals in behaviours, agonistic displays, and in a variety of other social interactions. One of the most important contexts of spider communication, and certainly the most studied, is that of courtship. The problem of getting the sexes together is compounded in- spiders by their cannibalistic tendencies, but is adequately overcome by the complex behaviours and fairly effective communication systems these animals have evolved. Finding a mate is often difficult for solitary animals dispersed in the environment. In general, mate location in spiders is accomplished using chemical cues. Silk-borne or airborne pheromones allow males to locate females by following draglines or searching surfaces for increasing concentrations of ‘sex scents’. Once a male comes into the vicinity of a female, he must be wary of her predatory instincts and give her advance notice of his identity and intentions, as well as ascertain her willingness to mate. These are usually accomplished by acoustic/vibratory communication or visual signalling. The leaves of a banana plant are used as a substrate for transmitting reciprocal courtship signals of Cupiennius safei [23]. A courting male can be identified by a female located on a separate leaf of the banana plant (out of sight of the male), and the male
Figure 6 Diagram of a horizontal/ frontal section through the eye region of a jumping spider, showing the field of vision of the different eye groups (see text for details). (from Forster (1 l] by permission of Princeton University Press)
can locate her, based on her responding vibratory signals to him, even when the airborne sound component is masked by a random noise generator. As they signal back and forth, the male moves closer, and eventually finds his mate. The substratum-borne importance of vibratory signals in the courtship of wolf spiders was demonstrated in a study in which a female spider was isolated first visually, then acoustically from the courting male [15]. Visual signals alone are not sufficient to elicit a receptive response in the female, but vibratory signals were both necessary and sufficient to elicit the receptive response. This study also showed that vibratory cues were essential to the reproductive isolation of these species. Although capable, these species do not interbreed because females will only respond receptively to species-specific vibrations from conspecific males. In many web-building spiders, males arrive at the edge of the female’s web and begin tapping. If the female responds receptively, the male enters her web and begins a more vigorous courtship, leading to tactile contact and mating. In many of the orb-weavers, whose intricate circular webs are particularly effective at transmitting vibrations, males use a slightly different male approach. The approaches the hub of the female’s web, and cuts a hole in her web and connects a mating thread to this area. He vibrates this thread by a variety of movements (bouncing, jerking, and tarsal rubbing), and if the female is receptive, she comes out on the thread, where mating occurs. If the female responds in a predatory fashion, the male cuts the thread and escapes [24]. The degree of visual sophistication which has evolved in jumping spiders has clearly influenced the diversity of behaviours exhibited by these spiders. Both the predatory behaviours and the courtship behaviours of jumping spiders make good use of the salticid visual system. As with all spiders, the courting male has the problem of not eliciting the predatory behaviour of the female he is courting. The approach tactics of a male jumping spider often include a zigzagging approach, in which the male moves widely from side to side as he approaches the female. This is coupled with species-characteristic movement of palps and legs (waving and tapping). These movements may rninimize the probability of eliciting chasing or stalking behaviour by the female, by keeping the male in the appropriate visual field [25]. Communication plays an important part in other aspects of the lives of spiders. For example, defence of webs is common among web-building
Figure 7 (a) Scanning electron microscope photo of chemosensory hairs on the palp of a male wolf spider (Lycosa punctulata). (b) A male wolf spider following a silk dragline left by a female. ( (a) courtesy W. J. Tietjen; (b) courtesy J. S. Rovner) spiders, and it is apparent that ritualistic combat behaviours serve this function without serious loss of life or limb to the combatants. In the extensively studied desert funnel web spider, Agelenopsis aperta, the intensity of conflict and the sequence of behaviours involved in contests over web sites vary with the quality of the web site and the size difference between resident and intruder. In these interactions, disputes are settled primarily by visual and vibratory signalhng between spiders [26]. Other examples of spider communication in the context of territoriality may involve defence of female’s webs by males [27] or the maintenance of spacing between individuals relative to food availability [28]. In both of these situations, communicative interactions serve to mediate disputes. Interactions of this type are particularly important among the web-building spiders living in social
groups. Communication through web vibration has been suggested as a preadaptation for sociality in some groups, and serves to mediate spacing, facilitate feeding, and warn colony members of danger from predators [291. Communication in social interactions is not limited to web-building spiders. Social hierarchies may exist among the vagrant wolf spiders, and provide the successful competitors preferential accessto food or mates, even where a territorial space is not involved. W. P. Aspey [30] found a diversity of agonistic display in behaviours Schizocosa ocreata which were used in establishing and maintaining dominance-subordinance relationships among males. Many spiders exhibit some degree of maternal care of their young, and this appears to depend in part on complex interactions between parent and offspring, which serve to prevent cannibalism and allow coordination of activities. Communication can play an important role in these interactions. Female wolf spiders, for example, tear open egg sacs when they detect vibrations indicating that the young are ready to move from the egg sac on to the abdomen of the female, where they will be carried for several days. The young spiders cling to specialized hairs on the female’s abdomen [31] and travel with her. When the female is not moving, the spiderlings may climb down off her abdomen and explore the environment, drink water, and wander about, always connected to the mother by silk draglines attached to the abdominal hairs. When danger threatens, or a change in location is imminent, changes in the tension of those silk lines due to erection of hairs signal the young to return to the female’s abdomen. Stimulation of mechanoreceptor hairs on the female as the result of activity of the spiderlings also suppresses cannibalistic tendencies in their mother. Tolerance of young spiders on the web of some female spiders is facilitated by recognition of offspring through communicative interactions involving tactile contact, web vibration, or chemical signals. However, some web-building spiders exhibit maternal care beyond tolerance and protection of young. When a female of Theridion saxatile captures prey, she tugs on the threads of the web in a jerking fashion, warning spiderlings to hide in a protected area. Once the prey is subdued, she slowly pulls on the thread, and the young emerge to share in the kill [32]. In other Theridiid spiders, the young actively request feeding by tapping their legs on the palps and legs of their mother. The 17
female regurgitates digested food for the spiderlings, but regulates the rate of their feeding and their access by communicative leg movements. Even among those species whose young hatch from egg sacs left behind without parental care, communication between spiderlings is important to survival. Encounters between spiderlings on communal webs involve vibratory communication through the web, or leg tapping behaviours, which allow spiderlings to recognize and coexist with each other [33]. As spiderlings grow older, the mechanisms of mutual tolerance present in iuvenile aggregations disappear. Young- spiders snin individual webs. and after this -r ~~~ stage are more likely to exhibit agonistic or predatory behaviours conspecifics. The towards interactions which communicative govern the relations between spiders during the juvenile communal and dispersal phases are still largely unknown. It is, however, probable that these behaviours may form the basis for development of adult behaviours, and have some role in the evolution of social behaviour in some of the groupliving spider species. Conclusion
Questions concerning communication and the evolution of communicatory signals are perhaps particularly interesting in spiders because these animals are mostly solitary, predatory, and potentially cannibalistic. In many cases, behaviours that serve in prey detection and localization have been only slightly modified to function in communication. We would, therefore, expect intense selection pressure for effective communication. The result of
18
this pressure has been the evolution of the tremendous behavioural diversity that makes spiders such fascinating creatures.
References [l] Witt, P. N. and J. S. Rovner (Eds.), ‘Spider Communication: Mechanisms and Ecological Significance.’ Princeton Univ. Press. 1982. [2] Wilson, E. 0. ‘The Insect Societies.’ Harvard Univ. Press. 1971. [3] Reissland, A. and P. Gorner. Mechanics of trichobothria in orbweaving spiders. J. Camp. Physiol., 123; 59. 1978
[4] Barth, F. G. ‘Spiders and Vibratory Signals: Sensory Reception and Behavioral Significance’ in Witt & Rovner, pp. 67-122. 1982. [S] Ibid. [6] Ibid.
[7] Uetz, G. W. and G. E. Stratton. ‘Acoustic Communication and Reproductive Isolation in Spiders.’ in Witt & Rovner, pp. 123-159, 1982. !8] Rovner, .I. S. Science, 190, 1309. 1975. [9] Stratton, G. E. and G. W. Uetz. Science. 214. 575. 1981.
[lo] Rovner, J: S. J. Arachnof., 8, 201, 1980. [ll] Forster, L. M. ‘Visual communication in jumping spiders (Salticidae)’ in Witt & Rovner, pp. 161-212, 1982. [12] Forster, L. M. Amer. Scientist, 70, 165, 1982.
[13] Jackson, R. L. ‘The behavior of communicating in jumping spiders (Salticidae).’ in Witt & Rovner, pp. 213-247. 1982.
[14] Rovner, J. S. Anim. Behav. 16, 358, 1978. [15] Stratton, G. E. and G. W. Uetz. Communication via substratumcoupled stridulation and reproductive isolation in wolf spiders (Araneae: Lycosidae). Anim. Behav. (in press). [16] Tietjen, W. J. and J. S. Rovner. ‘Chemical communication in lycosids and other spiders.’ in Witt & Rovner, pp. 249-279, 1982. [17] Foelix, R. F. J. Morph., 132, 313, 1970. [18] Foelix, R. F. and I. W. Chu-Wang. Tissue & Cell, 5, 461, 1973. 1191Tietjen, W. J. and J. S. Rovner. Anim. behav.,28,735,1980. 1201 Uetz. G. W. and G. Denterlein. J. Akzchnof., 7, 121, 1979. [21] Blanke, R. 2. Tierpsychol., 37, 62, 1975. [22] Tietjen, W. J. J. Arachnol., 6, 197, 1979. [23] Rovner, J. S. and F. G. Barth. Science, 214, 464, 1981. [24] Robinson, M. H. and B. Robinson. Symp. Zool. Sot. London., 42, 17, 1978. [25] Jackson, op. cit. L
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[26] Reichert, S. E. ‘Spider interaction strategies: communication vs. coercion.’ in Witt & Rovner, pp. 281-315, 1982. [27] Rovner, J. S. Z. Tierpsychologie, 25, 232,1968. [28] Reichert, S. E. Symp. Zool. Sot. Lond., 42, 211, 1978. [29] Burgess, J. W. and G. W. Uetz. ‘Social spacing strategies in spiders.’ in
Witt & Rovner, pp. 317-351, 1982. [30] Aspey, W. P. Behaviour, 62, 103, 1977. [31] Rovner, J. S., G. A. Higashi and R. F. Foelix. Science, 182, 1153, 1973. [32] Krafft, B. ‘The significance and
complexity of communication in spiders.’ in Witt and Rovner, pp. 15-65, 1982. [33] Krafft, B. Ibid.