AMER. ZOOL., 41:1215-1221 (2001) Vibrational Communication and the Ecology of Group-Living, Herbivorous Insects1 REGINALD B. COCROFT2 Division of Biological Sciences, 105 Tucker Hall, University of Missouri, Columbia, Missouri 65211 SYNOPSIS. Communication among members of a colony is a key feature of the success of eusocial insects. The same may be true in other forms of insect sociality. I suggest that substrate-borne vibrational communication is important in the suc- cess of group-living, herbivorous insects. I examine three challenges encountered by herbivorous insects: locating and remaining in a group of conspeciflcs; locating food resources; and avoiding predation. Studies of groups of immature treehop- pers, sawflies and butterflies suggest that vibrational communication can be im- portant in each of these contexts, enhancing the ability of these group-living her- bivores to exploit the resources of their host plants. INTRODUCTION The ecological importance of eusocial in- sects such as bees, ants and termites is due in part to their remarkable ability to monitor changing resources in their environment (Holldobler and Wilson, 1990; Seeley, 1995; Shellman-Reeve, 1997). The ability of an insect colony to efficiently exploit un- predictable resources is, in turn, based on elaborate systems of communication among colony members. Accordingly, one of the hallmarks of the eusocial insects is that col- ony members communicate in relation to important features of their environment (Seeley, 1995). The eusocial insects, how- ever, represent only one end of a broad spectrum of insect sociality. Analogous communication systems can exist in very different forms of insect society, as shown, for example, by studies of trail-marking pheromones in group-living lepidopteran and sawfly larvae (Fitzgerald, 1995; Costa and Louque, 2001). Here I will suggest that for some (and perhaps many) group-living insects that feed on plants, substrate-borne vibrational communication is an important component of their ability to exploit host plant resources. I focus on three challenges faced by group-living, herbivorous insects. First, be- 1 From the Symposium Vibration as a Communi- cation Channel presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3-7 January 2001, at Chicago, Illinois. 2 E-mail: CocroftR@missouri.edu cause there often are considerable benefits to individuals of living in groups, one chal- lenge is to locate and remain with other in- dividuals. Second, because the location of high-quality feeding sites will vary over time within a host plant, another challenge is to locate currently profitable feeding sites. Finally, herbivorous insects must avoid predation. I will suggest that, in many species, vibrational communication among group members is important for solving each of these challenges. BENEFITS OF GROUP LIVING Although there are inherent disadvantag- es to group living, such as increased com- petition and risk of disease (Alexander, 1974), plant-feeding insects may benefit in various ways from being in a group. Pro- tection against predators has been proposed to be one of the most general factors se- lecting for group living (Hamilton, 1971; Alexander, 1974; Vulinec, 1990; Mooring and Hart, 1992). In insects, this might oc- cur, for example, through dilution effects (Foster and Treherne, 1981) or through en- hancement of chemical defenses (e.g., Ad- rich and Blum, 1978). For some herbivo- rous insects, feeding efficiency is increased by the presence of conspeciflcs (Ghent, 1960; Kalin and Knerer, 1977; Lawrence, 1990), resulting in faster growth rates and/ or greater survivorship. Other benefits of grouping can include increased water up- take (Lockwood and Story, 1986), slower 1215 1216 REGINALD B. COCROFT water loss (Friedlander, 1965), and en- hanced thermoregulation (Seymour, 1974). Indeed, Costa and Pierce (1997) suggest that there may often be sufficient direct benefits of group living that grouping is fa- vored whether or not the individuals are ge- netically related. One line of evidence sup- porting this view is that, in many species, groups that encounter each other merge into a larger group composed of individuals from different family groups, species, or genera (Came, 1962; Wood, 1984, 1993). LOCATING AND REMAINING IN A GROUP In some cases, the individuals on the same plant may be in groups from the start, if they hatch from eggs laid in a cluster. However, in other cases, groups are com- posed of individuals hatching from eggs de- posited in different locations (e.g., the tree- hopper Vanduzea arquata; [Fritz, 1982]). Furthermore, groups may move from one location to another (e.g., Carne, 1962). Consequently, individuals will often be faced with the challenge of locating or re- joining a group. Several lines of evidence suggest that this task can be accomplished by means of vibrational communication. First, is it possible for a small insect to detect the location of a vibration source? In many cases, the answer is yes. There is ex- tensive evidence that insects can locate a vibration source to one of two stems at a branching point (Latimer and Schatral, 1983; Steidl and Kalmring, 1989; Ota and Cokl, 1991; Roces etal, 1993; Pfannenstiel et al., 1995). This ability is not surprising, given the large number of taxa in which males localize receptive females by means of plant-borne vibrations (Michelsen et al., 1982; Markl, 1983; Claridge, 1985; Gogala, 1985; Henry, 1994; Stewart, 1997). There is also indirect evidence that some insects can determine whether a vibration source is in front them or behind them on a single, unbranched stem (Cokl et al., 1999; see dis- cussion in Cocroft et al., 2000). What evidence is there that insects use plant-borne vibrational cues to locate a group of conspecifics? Observations sug- gest that group-living sawfiy larvae use vi- brational signals to rejoin a moving group from which they become separated. In the Australian sawfiy Perga dorsalis, larvae (sometimes called "spitfires") form groups that move not only within a single tree, but also from one tree to another. According to Carne (1962), individual P. dorsalis larvae in migrating groups continually assess the presence of nearby individuals by "tap- ping" with a hardened sclerite at the end of their abdomen: "If an individual strays from the moving column and fails to make contact with another larva, it manifests dis- turbance by an abrupt increase in its rate of tapping. The larvae in the main body of the colony respond immediately by uncoordi- nated tapping for a period of 10?15 sec. There is usually an "answering" signal from the stray, then further tapping on the part of the colony. It seems certain that this is a form of communication for it invariably results in the individual rejoining its colo- ny." Once the individual rejoins the colony, tapping activity subsides. Carne (1962) fur- ther suggests larvae respond not to the air- borne sound, but to the vibration produced by tapping. Evans (1934) suggested that tapping occurs in a similar context during group movements in other species in the ge- nus Perga. A strikingly similar pattern has been ob- served in the chrysomelid beetle Polychal- ma multicava (D. Windsor, personal com- munication). In this species, groups of lar- vae migrate from resting positions at the base of small plants to feeding areas at the tips. When individuals become separated at a branching point, the two groups re-aggre- gate after back-and-forth bouts of substrate tapping. Vibrational signaling during group movements may occur in the tingid bug Corythucha hewitti, in which groups of nymphs are attended by a female. Faeth (1989) observed that disturbance of the leaf containing an aggregation of C. hewitii caused a nymph to stop feeding and move away, "occasionally stopping and vibrating its abdomen in the vertical plane. Other nymphs in the brood followed." Because such abdominal vibrations are involved in signal production in other insects (e.g., Henry, 1994), and because such movements will unavoidably produce a vibration in the substrate, these observations suggest the COMMUNICATION IN HERBIVOROUS INSECTS 1217 N O g. 5 - A B C 3 - 't 1 - .?=? ,--. .?? iiiti|iiiiiiiiii, i I i i i Time (s) FIG. 1. Audiospectrograms of plant-borne vibrational signals. (A) A signal produced by a nymph of the tree- hopper Calloconophoru pinguis after having located a high-quality feeding site; (B) A coordinated, group sig- nal from an aggregation of nymphs of the treehopper Umbonia crassicornis, produced in response to the ap- proach of a predator; (C) A series of signals produced by an (unidentified) ant-attended lycaenid caterpillar. production of vibrational signals in the con- text of group movement. LOCATING A FOOD RESOURCE In the membracid treehoppers Callocon- ophora caliginosa and C. pinguis, nymphs develop to adulthood in tight aggregations, accompanied at least in the early nymphal stages by their mother (Wood, 1978 [as Gu- ayaquila compressa]; R.B.C., unpublished data). These treehopper groups have a no- madic foraging pattern, in which the entire group moves from one feeding site to an- other. In C. pinguis, aggregated nymphs on a stem whose nutritional quality is declin- ing (such as a maturing stem or a cut stem) eventually leave the group and explore the rest of the plant, probing with their mouth- parts. When a nymph encounters a suitable feeding site (a new, growing shoot), it stops and produces a long series of vibrational signals (see Fig. 1A). These signals are used by other individuals to locate the new feeding site (R.B.C., unpublished data). In- dividuals in the dispersing group alternate periods of walking toward the source with periods of quiescence: they wait until a sig- nal is perceived, then walk, then wait for another signal. Individuals that arrive at the site begin to signal in unison with the in- dividuals already there. The alternation of walking and waiting to detect a signal was also observed in sawHy larvae locating a group (Carne, 1962). This signaling system FIG. 2. An aggregation of nymphs of the treehopper Umbonia crassicornis on a host plant stem. appears to allow sibling groups to take ad- vantage of changing nutritional resources on the plant. It also shows that locating a feeding site can, in some circumstances, be essentially the same task as locating a group. The only additional requirement for food recruitment is that group-location sig- nals are produced at an appropriate feeding site. Hograefe (1984) reported that larvae of the sawHy Hemichroa crocea, which live in groups on birch and alder, communicate while feeding. A signal is produced as the end of the abdomen is repeatedly scraped against the leaf surface in a characteristic rhythmic pattern. Signaling is more fre- quent when larvae are on new, undamaged leaves, which represent high-quality feed- ing sites, and less frequent when larvae are on already heavily damaged leaves. Larvae eventually move from low to high quality sites, apparently orienting by means of the vibrational signals. Again, orientation to a group and to a feeding site are closely re- lated. DEFENSE AGAINST PREDATORS: PARENT- OFFSPRING INTERACTIONS In the membracid treehopper Umbonia crassicornis, females defend their nymphal offspring from predators. Nymphs develop to maturity in a dense aggregation of up to 100 individuals encircling a host plant stem (Fig. 2). In their exposed position near the tip of a growing shoot, the nymphs are preyed upon by a diverse array of inverte- brates such as predatory Hemiptera, syrphid fly larvae, coccinellid beetle larvae, spiders, 1218 REGINALD B. COCROFT and wasps (Wood, 1974, 1976, 1983; Dow- ell and Johnson, 1986; McKamey and Deitz, 1996; Cocroft, 2002). Females de- fend their offspring by approaching the predator from their position outside the group, fanning their wings, and kicking with their hind legs (Wood, 1976, 1983; Dowell and Johnson, 1986; Cocroft, 19996). Maternal defense is an important resource for offspring: the female is their only protection against invertebrate preda- tors, and if she disappears the nymphs' chances of survival are low (Wood, 1976; Dowell and Johnson, 1986; Cocroft, 2002). When a predator approaches, nymphs of U. crassicornis produce vibrational signals (Cocroft, 1996, 1999a, b). The signal of one nymph is a brief series of pulses, last- ing about 50 msec. However, the nymphs within an aggregation coordinate their sig- nals (Fig. IB). Signaling usually begins on one end of the aggregation (e.g., where the predator first contacts a nymph) and travels across the group in a rapid wave as indi- viduals respond to the signals of their neighbors. As a result, signals of individu- als merge into a characteristic group display that is longer and higher in amplitude than the signal of a single nymph (Cocroft, 1999a). Females respond to these coordi- nated signals by quickly moving into the aggregation. In one field study, the combi- nation of signaling nymphs and defending females was successful in repelling about 3 out of 4 attacks by predatory wasps (Co- croft, 2002). The coordination of signals among nymphs is necessary to elicit the fe- male's response (Cocroft, 1996). Because obtaining the benefits of maternal defense requires collective effort, this signaling be- havior contains an element of cooperation. DEFENSE AGAINST PREDATORS: ANT MUTUALISM Many species of membracid treehoppers, especially in the tropics, have mutualistic relationships with honeydew-harvesting ants (Wood, 1984, 1993). This relationship can have important consequences for mem- bracid survival, because at least some ant species greatly reduce treehopper mortality from other predatory insects (McEvoy, 1979; Fritz, 1982). Ant-mutualism may have important consequences for membra- cid social behavior: it is correlated with, and enhanced by, aggregating as opposed to solitary behavior (McEvoy, 1979). Mutualism with ants, then, will often se- lect for aggregating behavior by treehop- pers. In the Neotropics, groups often consist of more than one species (Wood, 1984), again highlighting the likely importance of direct benefits to the grouped individuals. We might expect, then, that ant-attended species will have signals used in the for- mation and maintenance of groups. Such signals appear to be present in at least some membracid species that form mutualisms with ants (e.g., species in several genera in the subfamily Membracinae; R.B.C., un- published data). Vibrational communication is an impor- tant component of the mutualism of lycaen- id and riodinid butterfly larvae with ants (Fig. 1C; deVries, 1990; Travassos and Pierce, 2000). The signals of larval and pu- pal lycaenids appear to function in attract- ing and maintaining an association with ants (deVries, 1991; Travassos and Pierce, 2000). Travassos and Pierce (2000) also tested the hypothesis that signals were in- volved in the formation of groups; however, their results did not suggest a direct role of the signals in attracting conspecifics. As in these lepidopterans, signaling to attract mu- tualistic ants might also be expected in membracids. Whether membracids signal to attract ants is unknown, although observa- tions suggest that this may be the case for nymphs of one ant-attended Neotropical species (Tomogonia vittatipennis; R.B.C., unpublished data). GENERAL DISCUSSION One common feature of many of the communication systems described here (es- pecially in sawfly larvae, membracids, and chrysomelid beetle larvae) is the simulta- neous production of signals by multiple in- dividuals. This process also occurs in the chemical signals produced during recruit- ment communication in some eusocial in- sects and in tent caterpillars (Costa and Pierce, 1997; Holldobler and Wilson, 1990). This coordination of signaling may provide a means by which individuals with COMMUNICATION IN HERBIVOROUS INSECTS 1219 a common interest can enhance the signals of other colony or group members (see Cos- ta and Pierce, 1997). However, although group members will often have an overlap of reproductive interests, this will not al- ways be true. Although there may be ben- efits of group living, these benefits will of- ten be unequally shared among group mem- bers (reviewed in Krause, 1994). The nymphal aggregations of U. crassicornis treehoppers provide an illustration. Al- though maternal defense is important in re- ducing predation, the distribution of pre- dation risk in offspring aggregations is far from uniform. Individuals on the edges of aggregations, and those farther from the fe- male at the time they are contacted by a predator, are substantially more likely to be preyed on than individuals in the center of the aggregation and/or closer to the female (Cocroft, 2002). While there is a clear ele- ment of cooperation in offspring signaling, then, the finding that predation risk is un- equally distributed suggests that coopera- tion may have its limits. This would be es- pecially true if offspring are able to influ- ence the female's position during an attack. Although it is currently not known whether competition for access to maternal defense is even possible in this species, it is clear that there is at least the potential for conflict among group members. A divergence of in- terests may also occur in other groups, such as those of migrating sawfly larvae. For ex- ample, if edge individuals are more vulner- able to predators or parasitoids, individuals in that position may be more likely to signal to attract 'strays' than individuals in the center. Indeed, if strays will become edge individuals, shielding those currently on the edges, it is conceivable that edge individu- als could compete among each other to at- tract strays to their location. Came (1962) reports that after strays had rejoined a mi- grating group, the only individuals that still signaled were those on the edges of the group. In other cases, such as in the food re- cruitment signals of nymphs of the treehop- per Calloconophora pinguis, it may be in the interests of all of the individuals re- cruited to a food source to recruit the re- maining individuals in the group. If so, then the joint signaling of these nymphs may in- deed represent a case of signal enhance- ment. Further examination of the costs and benefits of group living, and of the dynam- ics of signaling, will be needed to resolve the issue. In general, resolving the interplay of cooperation and conflict in the signaling interactions of group members will proba- bly require a case-by-case examination. In many insect groups, chemical com- munication plays a role similar to that of the vibrational communication systems de- scribed here. In some group-living insect herbivores, chemical cues attract individu- als to groups of conspecifics (Aldrich and Blum, 1978). In group-living lepidopteran and sawfly larvae, a complex system of chemical trail-marking underlies their for- aging behavior (Fitzgerald, 1995; Costa and Louque, 2001). Chemical cues are often im- portant in anti-predator defense in group- living species, in which alarm pheromones and/or cues associated with injury alert oth- er group members to the presence of a pred- ator (Nault and Phelan, 1984). In some in- sects with parental care (e.g., the treehopper Umbonia crassicornis), both chemical cues (Wood, 1976) and vibrational signals (Co- croft, 1999a) can elicit parental defense of offspring, and there is likely to be an inter- action between the two kinds of signals in their effect on parental responses to preda- tors. Although evidence for the role of vibra- tional communication is anecdotal or lack- ing for many group-living herbivorous in- sects, studies of membracids, sawflies, and lepidopteran larvae suggest that this form of communication may represent an impor- tant set of adaptations to herbivory. Anal- ogous communication systems may be pre- sent in other groups, many of which are known to use vibrational signals in com- munication in at least some contexts. Par- ent-offspring communication in response to predators might be especially likely in so- cial Hemiptera, chrysomelid beetles, and sawflies with maternal care (Dias, 1975, 1976; Windsor, 1987; Kudo, 1990; Kudo et al, 1995; Tallamy and Schaeffer, 1997). Vi- brational communication among group members might also be expected in taxa such as many lepidopterans (Costa and 1220 REGINALD B. COCROFT Pierce, 1997), some aphids (Williams, 1922; Eastop, 1954), Neuroptera (Henry, 1972), tingid bugs (Faeth, 1989), and ant- attended cicadellids (Dietrich and Mc- Kamey, 1990) and fulgoroids (Bourgoin, 1997). Only further study of communica- tion in these fascinating insect societies will reveal the extent to which vibrational com- munication is a widespread adaptation to the challenges of herbivory in group-living insects. ACKNOWLEDGMENTS I thank Peggy Hill for the opportunity to participate in this symposium. The manu- script benefited from the comments of J. 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