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Vibrational Communication and the Ecology of Group-Living, Herbivorous Insects1

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Vibrational Communication and the Ecology of Group-Living, Herbivorous Insects1 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 conspeci®cs; locating food resources; and avoiding predation. Studies of groups of immature treehop- pers, saw¯ies and butter¯ies 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 cause there often are considerable bene®ts The ecological importance of eusocial in- to individuals of living in groups, one chal- sects such as bees, ants and termites is due lenge is to locate and remain with other in- in part to their remarkable ability to monitor dividuals. Second, because the location of changing resources in their environment high-quality feeding sites will vary over (HoÈlldobler and Wilson, 1990; Seeley, time within a host plant, another challenge 1995; Shellman-Reeve, 1997). The ability is to locate currently pro®table feeding of an insect colony to ef®ciently exploit un- sites. Finally, herbivorous insects must predictable resources is, in turn, based on avoid predation. I will suggest that, in many elaborate systems of communication among species, vibrational communication among colony members. Accordingly, one of the group members is important for solving hallmarks of the eusocial insects is that col- each of these challenges. ony members communicate in relation to important features of their environment BENEFITS OF GROUP LIVING (Seeley, 1995). The eusocial insects, how- Although there are inherent disadvantag- ever, represent only one end of a broad es to group living, such as increased com- spectrum of insect sociality. Analogous petition and risk of disease (Alexander, communication systems can exist in very 1974), plant-feeding insects may bene®t in different forms of insect society, as shown, various ways from being in a group. Pro- for example, by studies of trail-marking tection against predators has been proposed pheromones in group-living lepidopteran to be one of the most general factors se- and saw¯y larvae (Fitzgerald, 1995; Costa lecting for group living (Hamilton, 1971; and Louque, 2001). Here I will suggest that Alexander, 1974; Vulinec, 1990; Mooring for some (and perhaps many) group-living and Hart, 1992). In insects, this might oc- insects that feed on plants, substrate-borne cur, for example, through dilution effects vibrational communication is an important (Foster and Treherne, 1981) or through en- component of their ability to exploit host hancement of chemical defenses (e.g., Ad- plant resources. rich and Blum, 1978). For some herbivo- I focus on three challenges faced by rous insects, feeding ef®ciency is increased group-living, herbivorous insects. First, be- by the presence of conspeci®cs (Ghent, 1960; Kalin and Knerer, 1977; Lawrence, 1 From the Symposium Vibration as a Communi- 1990), resulting in faster growth rates and/ cation Channel presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3±7 or greater survivorship. Other bene®ts of January 2001, at Chicago, Illinois. grouping can include increased water up- 2 E-mail: [email protected] take (Lockwood and Story, 1986), slower 1215 1216 REGINALD B. COCROFT water loss (Friedlander, 1965), and en- Australian saw¯y Perga dorsalis, larvae hanced thermoregulation (Seymour, 1974). (sometimes called ``spit®res'') form groups Indeed, Costa and Pierce (1997) suggest that move not only within a single tree, but that there may often be suf®cient direct also from one tree to another. According to bene®ts of group living that grouping is fa- Carne (1962), individual P. dorsalis larvae vored whether or not the individuals are ge- in migrating groups continually assess the netically related. One line of evidence sup- presence of nearby individuals by ``tap- porting this view is that, in many species, ping'' with a hardened sclerite at the end of groups that encounter each other merge into their abdomen: ``If an individual strays a larger group composed of individuals from the moving column and fails to make from different family groups, species, or contact with another larva, it manifests dis- genera (Carne, 1962; Wood, 1984, 1993). turbance by an abrupt increase in its rate of tapping. The larvae in the main body of the LOCATING AND REMAINING IN A GROUP colony respond immediately by uncoordi- In some cases, the individuals on the nated tapping for a period of 10±15 sec. same plant may be in groups from the start, There is usually an ``answering'' signal if they hatch from eggs laid in a cluster. from the stray, then further tapping on the However, in other cases, groups are com- part of the colony. It seems certain that this posed of individuals hatching from eggs de- is a form of communication for it invariably posited in different locations (e.g., the tree- results in the individual rejoining its colo- hopper Vanduzea arquata; [Fritz, 1982]). ny.'' Once the individual rejoins the colony, Furthermore, groups may move from one tapping activity subsides. Carne (1962) fur- location to another (e.g., Carne, 1962). ther suggests larvae respond not to the air- Consequently, individuals will often be borne sound, but to the vibration produced faced with the challenge of locating or re- by tapping. Evans (1934) suggested that joining a group. Several lines of evidence tapping occurs in a similar context during suggest that this task can be accomplished group movements in other species in the ge- by means of vibrational communication. nus Perga. First, is it possible for a small insect to A strikingly similar pattern has been ob- detect the location of a vibration source? In served in the chrysomelid beetle Polychal- many cases, the answer is yes. There is ex- ma multicava (D. Windsor, personal com- tensive evidence that insects can locate a munication). In this species, groups of lar- vibration source to one of two stems at a vae migrate from resting positions at the branching point (Latimer and Schatral, base of small plants to feeding areas at the 1983; Steidl and Kalmring, 1989; Ota and tips. When individuals become separated at Cokl, 1991; Roces et al., 1993; Pfannenstiel a branching point, the two groups re-aggre- et al., 1995). This ability is not surprising, gate after back-and-forth bouts of substrate given the large number of taxa in which tapping. males localize receptive females by means Vibrational signaling during group of plant-borne vibrations (Michelsen et al., movements may occur in the tingid bug 1982; Markl, 1983; Claridge, 1985; Gogala, Corythucha hewitti, in which groups of 1985; Henry, 1994; Stewart, 1997). There nymphs are attended by a female. Faeth is also indirect evidence that some insects (1989) observed that disturbance of the leaf can determine whether a vibration source is containing an aggregation of C. hewitii in front them or behind them on a single, caused a nymph to stop feeding and move unbranched stem (Cokl et al., 1999; see dis- away, ``occasionally stopping and vibrating cussion in Cocroft et al., 2000). its abdomen in the vertical plane. Other What evidence is there that insects use nymphs in the brood followed.'' Because plant-borne vibrational cues to locate a such abdominal vibrations are involved in group of conspeci®cs? Observations sug- signal production in other insects (e.g., gest that group-living saw¯y larvae use vi- Henry, 1994), and because such movements brational signals to rejoin a moving group will unavoidably produce a vibration in the from which they become separated. In the substrate, these observations suggest the COMMUNICATION IN HERBIVOROUS INSECTS 1217 FIG. 1. Audiospectrograms of plant-borne vibrational signals. (A) A signal produced by a nymph of the tree- hopper Calloconophora pinguis after having located a FIG. 2. An aggregation of nymphs of the treehopper high-quality feeding site; (B) A coordinated, group sig- Umbonia crassicornis on a host plant stem. 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 appears to allow sibling groups to take ad- by an (unidenti®ed) ant-attended lycaenid caterpillar. vantage of changing nutritional resources on the plant. It also shows that locating a feeding site can, in some circumstances, be production of vibrational signals in the con- essentially the same task as locating a text of group movement. group. The only additional requirement for food recruitment is that group-location sig- LOCATING A FOOD RESOURCE nals are produced at an appropriate feeding In the membracid treehoppers Callocon- site. ophora caliginosa and C. pinguis, nymphs Hograefe (1984) reported that larvae of develop to adulthood in tight aggregations, the saw¯y Hemichroa crocea, which live in accompanied at least in the early nymphal groups on birch and alder, communicate stages by their mother (Wood, 1978 [as Gu- while feeding. A signal is produced as the ayaquila compressa]; R.B.C., unpublished end of the abdomen is repeatedly scraped data). These treehopper groups have a no- against the leaf surface in a characteristic madic foraging pattern, in which the entire rhythmic pattern. Signaling is more fre- group moves from one feeding site to an- quent when larvae are on new, undamaged other. In C. pinguis, aggregated nymphs on leaves, which represent high-quality feed- a stem whose nutritional quality is declin- ing sites, and less frequent when larvae are ing (such as a maturing stem or a cut stem) on already heavily damaged leaves.
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