There is no reason to believe that communication is any less important in the lives of invertebrates than of vertebrates. Invertebrates are well equfiped with means for the production and reception of chemical anct mechanical signals, and these seem to be important in those that have been studied. Optical signals, to be sure, are more restricted, generally to invertebrates with well-developed photoreceptors—Annelida, Mollusca, and Arthropoda—but significant in these. Unfortunately, studies on communication in invertebrates, except insects, are meager and scattered. In this survey, therefore, we can only review this spotty information and try to draw from the reports what implications seem justified.
To many biologists, Protozoa are simple animals, and seem to show little social organization. However, Protozoa are “simple” only in that they are generally tiny and have few observable body structures. Physiologically and behaviorally, they are not simple, carrying out all functions carried out by multicellular forms within a restricted framework. They have mechanoreceptors, chemoreceptors, and photoreceptors, the last usually unspecialized, but in some species reasonably well developed, even including lens-like structures. So far, studies on what can unequivocally be recognized as communication have been made only with chemical signals, and these in very few species.
At the time of conjugation in ciliates, or fusion of gametes in flagellates, two individuals come together, and this might suggest some form of mutual or individual attraction. In most cases, the meeting is apparently at random and the adhesion partakes more of an immunological reaction than a behavioral one (Kimball, 1943). However, for certain peritrichous ciliates, Finley (1952) has reported that the microconjugant, which is free-swimming, can identify the macroconjugant, which is sessile, by chemicals given off by the latter. When a microconjugant passes within one millimeter of a macroconjugant (a considerable distance in its size scale), it stops and undertakes a search until it finds the other. Furthermore, it can distinguish “young” macroconjugants from neuters and from “old” individuals. Similarly, Tsubo (1961) reported that, in Chlamydomonas moeicusii, which reproduces sexually by isogametes, + gametes are attracted by — gametes or even by cell-free medium that contained the latter. Four other species of this genus, however, did not show this. Tsubo tried to discover the nature of the attractive substance, basing most of his experiments on the fact that gametes of various algae are attracted by hydrocarbons, and found that coal-gas water was attractive, but he was not able to establish the identity of the material any further. These two examples certainly suggest that further studies involving behavioral types of observations, rather than mere mixture of conjugants or gametes, might well reveal other chemical communication systems.
The best-studied protistan communication system is that of cellular slime molds (Acrasiales). These organisms may be thought by some biologists not to be animal, but the matter is not clear-cut (Bonner, 1959b). They exist as amoeboid creatures during their feeding stages. For reproduction they fuse into a multicellular aggregation, which produces spores. It is during the aggregational phase that communication takes place, first demonstrated by Bonner (1947, 1959a) and since studied by a number of workers (Bonner, 1959b, gives references). Briefly, aggregation occurs in this way: one amoeba discharges a chemical, called by Bonner acrasin (this may be more than one compound), that initiates release of further acrasin by others nearby, setting up wave-like pulses of the material centrifugally. Acrasin not only induces acrasin discharge but also induces amoebae to stream toward the central producer, forming the aggregation.
Shaffer (1953, 1956a, b, 1957a, b, c) has extracted acrasin in cell-free medium and studied its properties. It is rapidly destroyed by the amoebae, apparently enzymatically. Thus a gradient is maintained. It is not, however, the gradient per se that orients the amoebae; instead it is the time sequence in which the relaying amoebae produce acrasin. In short, the pulse structure orients the amoebae, and may be specific. This is indeed a precise, yet simple system for the purpose.
Between Protozoa and the largest invertebrates—Annelida, Mollusca, and Arthropoda—is a wide array of phyla. Some of these—e.g., Platyhelminthes, Echinodermata—have been extensively studied taxonomically and morphologically, but little further; most have not. In terms of communication, studies are rare and scattered. We shall mention those that we have found.
Coelenterata, like Protozoa, have suffered from being considered simple animals. Recent studies on the nervous system and reactions of coelenterates (Bullock and Horridge, 1965) show, however, that their nerve nets are by no means simple in function. Certainly the pelagic life of jellyfish and sessile habits of most hydroids and sea anemones militate against elaborate systems of communication, and there are few cases reported so far. But attempts to find communication have been pathetically few.
Some sea anemones exist in commensal relations with other species, and these seem to involve signals. Thus, certain reef fish sequester themselves within the tentacles of anemones, where they apparently are not stung, as other fish would be. This relationship develops rather slowly, with the fish at first gingerly flicking the tentacles and only gradually moving into the writhing mass. A number of persons have studied the means by which the fish become safe from the nematocysts of the anemones (reviews in Davenport, 1955; Graefe, 1964). The most recent studies continue with arguments started earlier. Davenport and Norris (1958) and Eibl-Eibesfeldt (1960) believe that the fish secretes a chemical onto its surface that suppresses nematocyst discharge. Absorption of some of this material onto a piece of sponge renders the sponge free from stinging; without the material the sponge is stung. Graefe (1963, 1964), however, believes that anemone fish, unlike other fish, lack the substances that induce stinging. His experiments showed that only smaller fishes were tolerated in the anemones, and that the fishes “snuggled” into the tentacles with characteristic motions. Thus, Graefe would have the communication in mechanical channels, while others would have it chemical.
Another symbiotic relationship of anemones is the classically famous one between the anemone Calliactis parasitica and various species of hermit crabs, which bear the anemones on the mollusk shells that they inhabit. Ross (1960) and Ross and Sutton (1961a, b) have studied this relationship and find it behaviorally rather complex. With the hermit crab Eupagurus bernhardus the anemone establishes the relationship without help from the crab by seizing the shell and somersaulting aboard. In Pagurus striatus, the crab stimulates the anemone by tugging at it with its claws, and the anemone then detaches and climbs onto the shell. In Dardanus arrosor, female crabs stimulate the anemones to release and then pick them up and transfer them to the shell. Male crabs generally do not do this; in this case, the anemones are alone active. The behavior of the anemone in moving onto a hermit crab’s shell is quite complicated, emphasizing, as Ross points out, that sea anemones are complex in their reactions. It involves recognition of the shell by the anemones, effected by a chemical in the shell, so-called shell factor. This is secreted by the mollusc that originally produces the shell. Shell factor can be removed by boiling the shell in strong alkali, and it seems to be fairly specific. This system thus involves a chemical secreted by an animal other than the one with which the commensal is ultimately associated. This may have been the original condition, according to Ross. Later, the crabs developed their own signaling system, involving special types of tactile stimuli applied to the bases of the anemones, that enabled them to remove the anemones and decorate their shells.
Sexual attraction or aggregation by chemicals has been reported for a free-living nematode, Panagrolaimus rigidus (Greet, 1964), a horsehair worm (Nematomorpha) Gordionus scaber (Müller, 1926), and rotifers of the genus Brachionus (Gilbert, 1963). The material in the nematode is water-soluble, diffuses through cellophane membranes, and is produced by both sexes, causing aggregation. That of the nematomorph is produced by females and apparently enables the males not only to distinguish females but also to determine the sexual state of the females, for fertilized females are unattractive to males. Both of these act as distance signals. The chemical in the case of the rotifers is produced by the females. It is not a protein, polysaccharide, or lipid, but seems to be a small molecule, probably with an aromatic or heterocyclic ring. Generally the males find the females accidentally, and the chemical stimulates contact receptors on the corona. However, extracts of the chemical in the medium induce males to twist and turn sharply, and this reaction can be used as a bioassay for the chemical. These three isolated examples indicate that similar studies with other invertebrates might lead to similar discoveries.
In invertebrates that discharge eggs and sperms into the sea, the spawning of males and females is usually synchronized. Induction of spawning by females in the presence of sperms released by males has been reported for isolated species of invertebrates (Thorson, 1946, 1950; Burdon-Jones, 1951), but with little evidence about the mechanisms involved. Perhaps some form of chemical signaling is implicated, as has been suggested for molluscs and annelids.
Marine polychaets establish commensal relationships with a variety of other invertebrates (Davenport, 1955). In most cases, there are specific chemicals emitted by the “host” species that attract the commensal. Since these are specific, enabling the commensals to distinguish among closely related species, it seems unlikely that they are merely metabolic end products (Lucas, 1947). Davenport and coworkers (1950, 1951, 1953a, b, 1960) and Hickok and Davenport (1957) have studied chemical attraction by and recognition of hosts in a variety of commensal polychaets; and they have found a number of situations ranging from almost perfect specificity to confusion of nearrelated species.
Perhaps attraction to such hosts is no more communication than attraction of an animal to its food plant or to a suitable settling place. Possibly the decision on this—if it is worth making at all—lies in whether or not the signal is merely a constant part of the attracting object—inherent chemical in a plant, or roughness in a substrate— or whether the attracting object produces the signal only in context. This obviously may be a difficult decision to make, and at present it is impossible for most situations studied. Consequently, we prefer to include these cases of commensal attraction as interspecific communication.
There is a wide variety of spawning and mating patterns in annelids: from release of eggs and sperms freely into the sea to internal fertilization and production of egg cocoons. Among those that release eggs and sperms there are generally mechanisms for synchronization of the release. Environmental factors, such as tides, temperatures, etc., are usually involved, but these only fix the times within hours or days. For more precise synchronization, in many species, the release of gametes by one sex causes the others to spawn. As Thorson (1950, p. 7) put it:
Remarks in the prefaces of papers in the widespread literature dealing with the embryology of marine invertebrates seem, however, when compiled, to give a solid basis for a biological rule of the greatest interest, namely, that among marine invertebrates shedding their eggs and sperm freely in the water the males are the first to spawn, thus stimulating the females to shed their eggs, which, shed directly into a suspension of sperm of their own species, have espedaily good chances of being fertilized.
He then cited a number of examples of annelids, other marine “worms,” echinoderms, mollusks, etc. that support this rule. Duncan (1960), however, found that, in Arenicola marina, the females spawn first and the males are then induced to spawn. While undoubtedly various patterns will be found when enough species have been studied, precise synchronization of spawning in many marine invertebrates is controlled by chemicals in seminal fluids or on the gametes.
There is remarkably little evidence for recognition of sexes in marine annelids. Reish (1957) reports that in Neanthes caudata males and females are attracted to each other and that fighting occurs between animals of the same sex but not of opposite sex. This is not the case, however, in the territorial behavior of Nereis pelagica (Clark, 1959).
Mating partner recognition and attraction in terrestrial annelids (mostly hermaphroditic) have been little studied. Certainly one might expect some chemical recognition marks. In land leeches, Leslie (1951) has reported an isolated observation on mechanical signaling. He heard leeches tapping on leaves and noticed that a male approached a tapping female and set up a duet with her. The two alternately tapped and curled the front ends of the bodies together, ultimately leading to copulation.
Other than this, there have been almost no studies on mechanical stimuli as communication mechanisms in annelids, although one might be inclined to assume that these would be important. The annelids certainly are equipped generally with a wide variety of mechanoreceptors. Mangold (1924) reported that captive earthworms (LumbriÎ eus terrestris) produced sounds that were not merely due to feeding or moving about. They seemed to have definite structured sequences: a series of dots (“de, di, da”) and dashes (“drrrrrrt”) in specific patterns. He believed that a special pharyngeal “tongue” might be involved in the production of these sounds and that the sounds were possibly important as signals to the worms. This report was picked up by the popular press and the sounds were described as “singing.” Confirmatory notes were published by Ruedeman (1927) and Walton (1927), the latter stating that he thought that stridulation might be involved, but that the “songs” were so faint and puny that those of insects were as symphonic poems alongside them. Mangold stated that he expected to study these sounds in detail later, but apparently did not, and they remain thus as rather casually reported possible communication signals in these animals.
There are many marine annelids and other invertebrates that are luminescent. The possible communicative significance of luminescence will be discussed below. We may just note here that, in at least one marine annelid, a signaling system using luminescence has been described. Galloway (1908) and Galloway and Welch (1911) reported that in a Bermudan polychaet, Odontosyllis enopla, which swarms at certain seasons, the females rise to the surface of the sea, there forming a glowing mass. The males are attracted to this and rise to mate with the females. If the females stop glowing, the males signal by flashing, and the females resume their light. This is one of the few cases in which luminescence is known to be involved in mating, and it certainly suggests that studies upon other luminescent annelids would be of interest.
While there have been a number of studies on chemoreception and chemotactic behavior in molluscs (Kohn, 1961a), our knowledge is still unsatisfactory. Yet chemical sensitivity of molluscs is undoubted, and these animals are well equipped with glands to produce chemicals of many sorts. Studies on chemical communication in this group are badly needed.
There are a few reports of commensal attraction, as with annelids. Morton (1962) found that a bivalve, Montacuta ferruginosa, is attracted to and orients toward its host, a heart urchin, even under unnatural conditions. The attractive factor is a chemical given off by the urchin. Similarly, Wear (1966) found that another bivalve, Arthritica bifurca, is attracted to its host, a tubicolous polychaet, by a chemical in the water coming from the tube.
Many marine molluscs have free-swimming larvae, although the adults are sessile or nearly so. It is obvious that aggregation of the adults would facilitate fertilization. There are, however, only a few reported cases of specific aggregation. Nagabhushanam (1962) found that larvae of the wood-boring molluscs Martesia striata and Teredo furcillatus are attracted to wood that is already infested with members of the same species. Kohn (1961b) noted that, in Conus, males and females form spawning aggregations, apparently being attracted chemotactically. For Crepidula, a sessile gastropod, Gould (1919, 1952) and Coe (1953) found that a chemical given off by settled females attracts swimming larvae or newly settled juveniles of the same species and induces them to become males. This can be transmitted through several millimeters of sea water and causes piling up of males on the female, assuring fertilization of the eggs.
Where eggs and sperms are released freely into sea water, the rule noted by Thorson (1950) applies in many cases. In the oyster (Crassostrea virginica) Galtsoff (1938, 1940, 1961) has shown that males release sperms when stimulated by temperature changes and by the presence of eggs or sperms from a number of species of invertebrates not even closely related. Females release eggs when stimulated by a chemical in the sperms, a material that is thermolabile and insoluble in water, perhaps taken in by the female by ingesting the sperms. Thus, the male is unspecific and releases sperms upon being excited by many stimuli, whereas the female releases eggs only when sperms are present.
As with annelids, there have been few studies in molluscs on mechanoreceptive channels of communication. Elaborate courtship behavior patterns of land snails and slugs, involving slime trail feeding, mutual titillation by special organs, such as the sarcobellum of slugs, and the use of so-called love darts (pointed, calcareous structures fired into mating partners), have been described in detail for a number of species (Gerhardt, 1933a, b, 1934, 1935, 1936, 1937; Karlin and Bacon, 1961). Most of these studies are descriptive and give little information about the physiology of communication. These behavior patterns would seem to lend themselves excellently to analysis of the channels and signals involved.
Probably only cephalopods have well enough developed eyes for optical communication to be significant, unless luminescent molluscs signal by flashing. This could be detected even by the simple eyes of gastropods and some lamellibranchs. Certainly there are many luminescent species, but there is no direct evidence on the use of this luminescence.
In the squid Loligo pealii, Drew (1911) and Arnold (1962) have described aggressive and courtship behavior of males involving characteristic swimming patterns and development of specific colored areas at the bases of the arms. In Sepioteuthis sepioidea, a squid from the Bimini area, Arnold (1965) found that the male assumes a definite color pattern to ward off other males from a female he has selected and to court the female. The female is mostly passive, but also adopts a characteristic pattern. This behavior is closely similar to courtship patterning in the cuttlefish (Sepia officinalis) as described by Tinbergen (1939). In Sepia, the male adopts both a special position and a zebra pattern when he accosts another cuttlefish. If the second is a male, it too adopts this habit, and no copulation is attempted. If it is a female, it does not adopt it, and copulation occurs. Males court models of females. Thus recognition of sex and readiness to mate is signaled in these cephalopods by visual displays and not by chemicals.
Octopods, with their well-developed eyes, would seem to be well adapted for visual displays, but there have been few studies. Young (1962) reported for a reef-inhabiting species, Octopus horridus, that the male displays special vertical stripes to the female during courtship. This is, as Young admits, an isolated observation, and he notes that it seems strange, in view of the remarkable ability of octopods to change color. Perhaps, he notes, they have gone over to the use of displays of special suckers on the arms, as described by Packard (1961, 1963) for Octopus vulgaris. These suckers, of especially large size and contrasting color, are displayed in aggressive encounters and during courtship.
The greatest number of studies on communication in invertebrates have been made on members of this gigantic phylum, particularly Insecta (covered in other chapters of this book), Crustacea, especially marine species, and Arachnida, especially spiders. Other groups in the phylum, like the majority of invertebrates, have been given only scattered attention.
Most work has been done on crabs, particularly fiddler crabs (Uca spp.), spiny lobsters (Panulirus spp.), and snapping shrimp (Alpheus spp. and Synalpheus spp.). Fresh-water and terrestrial Crustacea are almost unstudied. General reviews of earlier works may be found in Balss (1944), Schone (1961), Wynne-Edwards (1962), and Carthy (1965). Reviews on acoustic communication are given by Guinot-Dumortier and Dumortier (1960), Hazlett and Winn (1962), Moulton (1963, 1964), and Frings (1964). The present review will deal mainly with recent studies.
Chemical communication signals—in nonsexual contexts—have been reported for barnacles, crayfish, and a few species of crabs. Knight-Jones (1953, 1955) and Knight-Jones and Stephenson (1950) showed that a material in the shells of settled barnacles induces cyprid larvae of the same species to settle and attach. If cyprids are kept from contacting attached animals, they do not settle for long periods of time. The material seems to be quite specific, and Knight-Jones (1955) suggested that the settling reaction of cyprids could be used as an index of systematic affinity, for cyprids of Balanus balanoides settle near conspecific adults to a much greater extent than near other species.
Crisp (1961) and Crisp and Meadows (1962) found that the chemical, which they named settling factor, is nondialyzable and heatstable and is active at extreme dilutions when contacted by the cyprids. They pointed out that for tiny animals such as cyprids, distance chemical attraction is likely to be impractical, for their small size makes it difficult for them to sense gradients. As a test for settling factor, they extracted bodies or shells of barnacles and applied the extracts to otherwise clean slates. These were then submerged among barnacle cyprids, and the degree of settlement on these and untreated slates was determined. This case, like some cited above, is a borderline situation, for the material may be arthropodin (Crisp and Meadows, 1962), and this is a regular constituent of the exoskeleton of the animals, not a specially produced signaling material.
Recognition of species by chemical means seems to occur in certain crayfish (Bovbjerg, 1956). Antennal contact, as well as visual contact, between two crayfish of the same species can initiate fighting. Similarly, chemical attractive materials involved in attraction and recognition of hosts by commensal pinnotherid crabs have been reported by Johnson (1952) and Sastry and Menzel (1962).
Sexual attraction and recognition by chemical signals have been reported for a number of species. The term pheromones (Karlson and Butenandt, 1959), widely used for insect chemical signaling agents, has been applied to these chemicals also. This is a rather unfortunate term, for it intentionally suggests a relationship with hormones that is questionable and sunders this class of signals from other communication signals as if they were somehow different, whereas they act in exactly the same ways as do the others. Unfortunate or not, however, the term has become established—even suffering the fate of many such terms—misspelling (pherormone, for instance) and inappropriate reference to chemical materials with quite different origins and actions. On the positive side, the coining of the term has apparently given impetus to studies in this field. Most of the reviews of chemical communication signals deal almost exclusively with insects: Karlson and Butenandt (1959), Karlson (1960), Wilson (1963), Wilson and Bossert (1963), and Jacobson (1965). Only recently has the possible importance of these for marine Crustacea been recognized.
Carlisle and Knowles (1959) noted that, in many marine Crustacea, the molt in which the female is transformed from an immature into a nubile adult is special; they call it the copulatory molt. Females just before or at the time of this molt seem to be recognized by males, which often seize the females and hold them for mating. Copulation occurs almost immediately after the molt in many cases. Carlisle and Knowles pointed out that the Crustacea studied so far seem to fall into two classes: those in which the male is attracted from a distance to the premolt female and those in which the male must make antennal contact with the female for recognition to occur. The reasons given by Crisp and Meadows (1962) for the inappropriateness of distance chemical stimuli for small aquatic animals are probably pertinent here, although not all species having distance reactions are large, and vice versa. Too few species have been studied so far to make generalizations safe.
For Crustacea in which the male detects the premolt or freshly molted female at a distance, the earliest report seems to be that of Parker (1901) for a copepod, Labidocera aestiva. Later reports are by Williamson (1953) for some talitrids (Amphipoda); Hughes and Matthiessen (1962) for the lobster Homarus americanus; Hazlett and Winn (1962) for a snapping shrimp, Synalpheus hemphilli; Knudsen (1964) for a crab, Hemigrapsus oregonensis; and Ryan (1966) for another crab, Portunus sanguinolentus. In all these, the chemical attractants seem to be fairly specific. Ryan (1966) has shown that the chemical is given off in the urine of the female, but its nature and means of production are unknown.
Of Crustacea in which contact by the antennae of the male with some part of the female is necessary for recognition, the earliest reference seems to be that of Hay (1905) for Callinectes sapidus, with later reports by Höglund (1943) and Forster (1951) for Leander squilla, Veillet (1945) for Carcinus maenas, Burkenroad (1947b) for Palaemonetes vulgaris, and Carlisle (1959) for Pandalus borealis. In no case is the chemical structure of the material known.
Communication by mechanical stimuli apparently is common among Crustacea, although few species have been studied. A number of species are known to produce sounds by a variety of sound-producing methods—tapping, bubbling, stridulation, etc. The latter may involve many parts of the body, with a file-like structure on one part and a tooth-like structure that is drawn over the file on another. Details of structure and classification of types may be found in Guinot-Dumortier and Dumortier (1960) and Dumortier (1963). Brief reviews of possible communication uses of the sounds are given by Hazlett and Winn (1962), Moulton (1963, 1964), and Frings (1964). Recent studies on sound production by Crustacea—the communication function, if any, however, is questionable or unknown—include those of Moulton (1957) on Panulirus argus, Busnel and Dziedzic (1962) on barnacles, Hazlett and Winn (1962) on Panulirus sp.; Gonodactylus sp., Alpheus sp., and Synalpheus sp., and Hazlett (1966) on the land crab, Coenobita clypeatus.
Among the most studied of crustacean sounds are those made by snapping shrimps (Alpheidae). During World War II? the sounds made by these animals became important to naval authorities, for they interfered with sonar. This led to a number of studies on the physical nature of the sounds and mechanisms of production and a few attempts to determine their functions. Snapping shrimp produce loud cracks by closure of a highly specialized large claw. There has been considerable debate about the origin of the snap, but recent studies by Hazlett and Winn (1962) and Knowlton and Moulton (1963) show that it results from the collision of movable and fixed parts of the appendage, as Volz (1938) postulated. The function of the snapping, however, is still uncertain. Volz (1938) believed that the purpose of the claw closure was to produce a jet of water which acted as a mechanical signal to others of the same species and that the noise was incidental to this and of no significance in itself. The MacGinities (1949) reported seeing small fish and other small organisms stunned by the sound, and they believed that its function is to stun prey. Since the snapping occurs in certain well-defined diurnal time patterns, Johnson et al. (1947), Everest et al. (1948), Hiyama (1953), and Fish (1964) postulated that it might be involved in territorial or sexual signaling, or both. So far, however, no clear-cut evidence of any such use has been forthcoming. We briefly discuss these shrimp here because we believe that future work will show that these special sounds, produced by such highly specialized appendages, are used for communication.
The use of acoustic signals in territorial situations has been documented for some species. Volz (1938) and Hazlett and Winn (1962) believe that the snapping of snapping shrimp and mantis shrimp is used to mark territories. Lindberg (1955) and Moulton (1957) regard the stridulation of Panulirus as probably territorial in function also. In none of these cases, however, is the matter settled. Male fiddler crabs (Uca spp.) thump their large claws on the ground: this apparently has a territorial function (Dembowski, 1925; Altevogt, 1957, 1964; Crane, 1943, 1957). Furthermore, Uca spp. males thump on the substrate in male-female interactions leading to courtship behavior (Burkenroad, 1947a; Crane, 1943, 1957; Altevogt, 1957; Salmon and Stout, 1962; Salmon, 1965).
There are many luminescent marine Crustacea, particularly in the depths. There has been considerable discussion about the functions of light production by these, as well as other, invertebrates. Among recent publications, the matter is discussed by Dennell (1955), Nicol (1960), Buck (1961), Harvey (1961), and Clarke (1963). The possible functions include blinding prospective predators; acting as a “burglar alarm,” the victim giving the alarm to others; aggregational attraction and recognition; sexual attraction and recognition; and countershading. Obviously, only alarm, recognition, and attraction involve communication, and no clear-cut evidence for any of these exists.
Visual recognition of species or sex has been reported by Bovbjerg (1956) for crayfish and (1960) for a crab, Pachygrapsus crassipes; by Schöne and Schöne (1963) for Goniopsis cruentata; and by Hazlett (1966) for Coenobita clypeatus. Reese (1962) described the adoption of a submissive posture in hermit crabs when a dominant individual raises its large, strikingly marked, left cheliped. The communication system involved in these aggressive interactions has been analyzed statistically by Hazlett and Bossert (1965).
By far, the best studied of visual courtship displays in Crustacea are those of the fiddler crabs (Uca spp). Males have a large claw, often brightly marked; females have not. This claw is used by most species in a series of ritualized posings and movements to signal territorial rights—male to male—or to court—male to female. Detailed comparative descriptions of the behavior patterns of many species of Uca have been published by Peters (1955), Altevogt (1955, 1957, 1959), Crane (1943, 1957, 1958), and Gordon (1958). Sounds are also used in these activities by some species, as Salmon and Stout (1962) and Salmon (1965) have shown. The basic pattern involved is waving of the large cheliped in what has been called beckoning or challenging. Actually, it has both functions. The body may be raised, and curtsying or sidling may occur. As summarized by Crane (1957, p. 81).
Two basic patterns of display have been distinguished during field studies of more than fifty species of fiddler crabs (Uca). The first pattern is characteristic of a group of species with narrow fronts. It is distinguished by a simple, more or less vertical gesture (“wave”) made with the major cheliped of the male, and by the male’s pursuit of the female toward her burrow . . . The second pattern is typical of broad-fronted species in the genus. It is characterized as follows: the cheliped is unflexed laterally, rather than vertically elevated, and sometimes completes a circular motion in returning to rest position; there is in addition a distinct second stage of display which is usually elicited by the approach of a female and which depends both on special movements of the various appendages and on an increased tempo of waving ... A few species with intermediate types of behavior have been observed, especially in the Indo-Pacific.
Species can readily be distinguished, even by man, by their displays, which are quite specific, causing sympatric species to be behaviorally isolated. So far, chemical signals have not been reported for Uca. With such a complex system of visual, mechanical, and acoustic signals in their territorial and mating behavior, perhaps chemicals are not needed. One is inclined to suspect that similar detailed studies on other species of Crustacea would reveal similarly complex situations.
Among the most intensively studied of communication patterns in invertebrates are the courtship procedures of spiders. These have aroused interest since antiquity (Bonnet, 1945, gives references). In general, female spiders are considerably larger than males. All spiders are ferocious, with poison chelicerae, and pounce upon and bite any moving body of appropriate size. If males could not identify themselves to the females, they might be quickly killed and eaten. Two sets of adaptations have evolved that enable the male to overcome this difficulty. First, he transfers the sperm by special palpal tips, which are loaded with semen taken up from a sperm web. These palpi enable the male to reach around the female, or through her web, thus not bringing his body close to her chelicerae. Second, males generally exhibit some form of courtship behavior which may be remarkably elaborate. These courtship displays are often similar to male-male displays involved in territoriality, but the reactions in the two cases are quite different. It is interesting to note that, although males can kill each other, they rarely do—ritualized fighting, through displays, generally replaces actual combat.
The courtship displays and performances of male spiders have been described in detail by a number of authors: McCook (1890), who covers older works; Montgomery (1903, 1910); Savory (1928); Berland (1932); Bristowe (1939-1941, 1958); and Cloudsley-Thompson (1958). Bristowe (1958), particularly, gives excellent descriptions and pictures of courtship displays in many families of spiders.
There has been considerable discussion about the significance and function of these displays. The Peckhams (1890) favored the Darwinian idea of sexual selection, believing that females select the handsomest males. Montgomery (1910), on the other hand, took the view of Wallace that the male is driven to display by his excitement and need for self-defense. Bristowe and Locket (1926) and Bristowe (1929) emphasized the specific differences in the displays and felt that the most clear-cut signalers among males were most successful, thus fixing specific patterns. Savory (1928) concluded, rather unconvincingly, that the whole affair is instinctual. Berland (1932) believed that the function is to arouse sexual readiness in the female. Crane (1949b) and Drees (1952) postulated that the male displays excite the females, causing them to lose their aggressiveness.
It seems quite probable that the male’s behavior is related to his normal behavior in an encounter with any other spider of the same or nearly related species—an aggressive display. This changes, upon the nonmale reaction of the female, into repetition and alteration of the unit patterns that form the courtship display. The female seems thus to be rendered nonaggressive and sex-ready. In many species, the female becomes almost cataleptic immediately before and during copulation. Since displays are different with different species, it is likely that selection favors those males that are most clearly marked or carry out the displays in the most distinctive fashion.
Extensive comparative studies on mating behavior have been carried out by Montgomery (1903), Gerhardt (1911, 1921, 19231933-a, b), and Bristowe (1929). Studies on special groups have been made by Buchli (1962) on trap-door spiders (Ctenizidae); Bristowe and Locket (1926) and Kaston (1936) on wolf spiders (Lycosidae); Peckham and Peckham (1889), Crane (1948, 1949a, b), and Drees (1952) on jumping spiders (Salticidae); Kaston (1936) on crab spiders (Thomisidae); and Locket (1926), Meyer (1928), and Dabelow (1958) on various web-spinning species.
Mating occurs in three interrelated phases: first, finding of the female by the male; second, precopulatory behavior; and third, copulation. Spiders differ from group to group in each of these. Because of the wealth of data now available, some generalizations are possible.
The means by which a male spider finds a female are determined by the habits and sensory abilities of the species. In snaring spiders, which spin webs or live in lairs, the female is sedentary and both sexes usually have poor vision. The male generally finds the female by chemical signals: her web is usually scented with a specific odor. The male wanders about until he blunders onto the web. He is capable of determining the species and sex, but generally not the sexual readiness of the female. In hunting spiders the female is on the move, and both sexes usually have good vision. The male finds the female either by sight or by the scent of her dragline which she lays down as she walks. In most cases, a chemical signal enables the male to determine the species and sex, except for some jumping spiders (Salticidae) with well-developed eyes.
Precopulatory behavior depends upon whether the female is in a web or not. If she is, the male generally uses vibrations of the web as signals. These may be taps of the lair in trap-door spiders or purse-web weavers or plucks of the threads of the web in orb weavers. If the female is still immature or already fertilized, her reaction is clearly aggressive and the male departs. If she is mature and sexually acceptant, she signals back or remains passive; the male enters the web and mating occurs. If the female is a wandering hunter or lurker, the male may, in some families, be larger than she and simply master her or, in other families, smaller and perform a courtship “dance.” This usually involves specific movements of the legs, palpi, and body. In some lycosids, special hairs or colored areas on the legs are erected. In some salticids, the color of the eyes changes. These courtship dances are specific and act as isolating mechanisms. Table 1, from Crane (1949b), illustrates the specific details for one group of spiders, the family Salticidae.
With the danger facing most male spiders (although it is now known that females usually do not eat the males), prompt and clearcut identification is necessary. In this case, displaying before females of the wrong species is particularly inappropriate biologically. Thus, natural selection would tend to evolve males with clearly marked, distinctive behavior patterns. Dabelow (1958) has found that different European geographic races of the spider Scytodes thoracica are different enough in behavior that cross-breeding does not occur, even when members of the races are artificially brought together. This is a good illustration of a type of behavioral isolation that could be important in evolution.
Of possible communication significance in spiders is the ability of some to produce sounds by various stridulatory devices. Chrysanthus (1953), Legendre (1963), and Dumortier (1963) give descriptions of the types of stridulatory apparatus, and Bristowe (1929), Savory (1928), and Berland (1932) discuss the possible significance. In most cases, both males and females stridulate. This has caused some workers to argue against a communicative function, particularly in sexual activities. The general consensus, however, is that stridulatory sounds either ward off prospective predators or are used for sexual signaling. In Steatoda spp., where only the adult male has a stridulatory organ, the sounds are known to be involved in courtship. Otherwise, the matter is still open to question.
The second group of arachnids whose courtship has been studied is the scorpions. This group was described in detail by Fabre (1905) and has been studied since by a number of workers, including Serfaty and Vachon (1950), Vachon (1953), Southcott (1955), Angermann (1955, 1957), Alexander (1956, 1957, 1959), Shulov (1958), Shulov and Amitai (1959), and Rosin and Shulov (1963). The male, who can apparently distinguish a female from males, probably chemically, seizes the female by her claws, and the two perform a promenade back and forth, often with the male vibrating his body in a movement called juddering. The male clears an area and deposits a spermatophore of special hooklike shape on the substrate, then pulls the female over it, hooking it into her genital opening. Earlier workers failed to note the spermatophore and believed that copulation occurred after the dance.
There may be, in certain species, other patterns of movement. In terms of communication, the procedure seems to consist of a special set of mechanical signals, with chemical signals initiating it. Some scorpions are known to stridulate, but Alexander (1958, 1960) believes that, since they have no obvious sound receptors, the sounds are almost certainly not important in sexual signaling. She believes that they are used to deter predators. In view of the well-developed vibration sense of scorpions, as indeed of all invertebrates, and the physical contact of male with the female in courtship, there is no reason why stridulatory vibrations might not be transmitted from one individual to another, but proof remains to be obtained.
Other arachnids have been reported with communication systems, but the reports are scattered and fragmentary. Sturm (1958) and Alexander (1962a, b) have described courtship and mating in a few Pedipalpi, involving tapping in special fashion and spermatophore transfer like that of scorpions. Kew (1912), Levi (1953), and Weygoldt (1966), among others, have described courtship in pseudoscorpions, which resembles that of scorpions except that certain species have special eversible organs, the ram’s-horn organs, which are displayed in threat and courtship.
Welsh (1930, 1931) found that a parasitic water mite, Unionicola ypsilophorus, which is usually positively phototactic, becomes negatively phototactic when in the presence of a chemical given off by its host, a fresh-water calm. This brings it into the shell of the host. The chemical material given off by the host is quite specific, and it may then be classed with other materials involved in host-finding. Mitchell (1957) reported that male pionid water mites do not produce spermatophores until they touch a female. He believes that the signals are both chemical and tactile. The female apparently can distinguish males of her own species, for she rejects others that grasp her. Böttger (1962) found, with three species of water mites, that each has its own pattern of sexual distinction. In Arrenurus globator, the male locates the female tactually from vibrations produced as she moves. In Fiona modata, the male distinguishes the female only upon contact by chemical means. In Eylais infundibulifera, recognition is entirely tactile; no chemical signals are involved.
Other than for insects, data are almost nonexistent. Certain centipedes and millipedes are known to stridulate (Dumortier, 1963), but the significance is unknown. Klingel (1959, 1960) has described courtship in various centipedes, involving tapping and specific positions and movements, with sperm transfer brought about by the male’s putting the sperms on a web and drawing the female over the deposit. These scattered references indicate clearly the vast amount of work needed before secure generalizations about communication in arthropods as a group will be possible.
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