Round Defence Cycloalexy

Some vertebrates are known to take to round defence, when a predator is around. Males form a circle, with their heads outward and with females and weaker adults within the circle. This behaviour is shown, for example by penguins, musk oxen of Canada, Canadian deer, etc.

Humans also sometimes resort to the round defence strategy. When Europeans were moving westward in the North American continent in the early days of white settlement, they often faced Red Indian resistance and attack. They then arranged themselves with their horse drawn coaches in a circle, with ladies and infants in the centre.

Curiously enough, the round defence strategy is seen among insects also. Andrade (1981), a Brazilian botanist, was the first to observe this phenomenon among Coelomera larvae on Cecropia leaves. One of the present authors (PJ), along with a Brazilian colleague (Vasconcellos-Neto and Jolivet, 1988) and with a Brazilian and an Australian one (Jolivet et al, 1990) gave this defence strategy among insects the name cycloalexy, and gave the first definite account of this defensive behaviour. In all cases this behaviour is shown by gregarious larvae, when they are at rest, day or night, that is when not feeding or moving. Generally, the larval individuals in a colony disperse to feed upon foliage by night (or by day when they rest during the night), one behind the other, to reaggregate in a cycloalexic arrangement before dawn.

Among beetles (Coleoptera), cycloalexy is known in some leaf beetles (Chrysomelidae), belonging to the subfamilies Criocerinae, Chrysomeli-

nae, Galerucinae and Cassidinae. A member of the family of weevils (Curculionidae) is also known to take to cycloalexy. Examples of round defence have been recorded mostly from the Neotropical (i.e. South America), the Holarctic (i.e. Europe and Asia, north of the Himalayas) and the Australian regions. One of us (Verma, 1996) and Heron (1992) have reported cycloalexy in some tortoise beetles (Subfamily Cassidinae) of India and South Africa, respectively. In Phelypera, the processionary neotropical weevil (Jolivet and Maes, 1996; Costa et al, 2004; Fitzgerald, 2004; Fitzgerald et al, 2004), the larvae travel in a loose procession along a branch of their host tree, Gua%uma ulmifolia, a Sterculiaceae. When larvae loose tactile contact with the larva immediately ahead of them, they rely on a trail pheromone. The larva secretes the pheromone from the ventral surface of the posterior abdomen. The cycloalexic formations maximize the amount of body contact in the aggregate and allow tactile signals to rapidly radiate through the group. In Tam Dao, North Vietnamese mountains, one of us (PJ) saw larvae of some Noctuidae, grouped together on Melastomataceae leaves, standing up all immediately and agitating their heads when anyone approached the plants. They are visually stimulated and are also linked through pheromone production. Among insects, processioning is known only among gregarious caterpillars (Lepidoptera) and in the weevil Phelypera. The larvae of Phelypera, when resting, arrange themselves in circular formations. As for other cycloalexic insects, this formation functions as an antipredator devise. The cycloalexic chrysomelid larvae and the larvae of Phelypera readily bite and regurgitate, when disturbed by potential predators. The entire resting assemblage can be simultaneously alerted by smallest tactile disturbances. The cycloalexic larvae of galerucines or other chrysomelid beetles suddenly raise their heads or tails seemingly for defense. Pergidae larvae, among the sawflies react the same way, and use tapping with the uropod on the leaves to communicate, by means of low frequency vibrations, in the need to reunite a dispersed colony (Carne, 1962). Tapping is also used by larvae of Paropsini, Australian chrysomelines, to reunite the dispersed colony (Meyer-Rochow, 1972). All these larvae of cycloalexic beetles or tenthredinid hymenopterans (Weinstein, 1988) show coordinated movements, threatening attitudes, regurgitation, and biting to repel predators or parasitoids. Some cycloalexic beetles, like Platyphora in Brazil, are viviparous and, when the female lays small larvae, the larvae congregate immediately making quickly a circle. Potential predators are pentatomid bugs and ants. Weinstein (1989) has observed an altruistic suicide of a larva of a pergid (Hymenoptera, Tenthredinidae) by biting the ovipositor of a parasitoid wasp.

In addition to some Coleoptera and some Hymenoptera, some Diptera also have cycloalexic larvae, which are known to show this larval defence against predators (ants and bugs) and parasitoids (wasps and flies). Among the flies, pupae and larvae of certain ceratopogonids show perfect cycloalexy in cacao plantations in Central America (Saunders, 1924). More research on ceratopogonids is needed.

All the insects, which take to cycloalexy, are subsocial or gregarious in their larval life. This is not necessarily associated with maternal care. Altruism is obvious among the cycloalexic larvae, as some larvae remain within the circle. In the ring formations, the larvae within the annular arrangement seem younger. Thus, the altruism in this case is with reciprocity, as the larvae, within the circle, will change their position, when they are older. If generally younger larvae are protected inside the circle, this situation should be referred to as reciprocal altruism. But the concept of reciprocal altruism has been recently challenged by Weinstein and Maelzer (1997) for the Australian sawflies in the genus Perga (Perga dorsalis Leach). The authors labelled individuals with oil paints and recorded their positions on consecutive nights. A subgroup of 20% of the larvae preferentially occupied the outer positions in the resting colony, and also appeared leading the foraging expeditions. Leaders were quick to regain outer positions, if removed and placed in the center of the group. So there seem to be individual differences in the dispersal aggregation behavior of the larvae in time and space, at least for Pergidae; some seem more altruistic than others.

It seems that small colonies of larvae show less viability than big ones among Pergidae. However, in the chrysomelid Coelomera on Cecropia leaves, a large cycloalexic group divides into two or three subgroups, as the larvae grow in size, and the resulting groups seem as efficient as the original big one, in repelling predators (Jolivet, in Capinera, 2004).

Ring defence is taken to by larvae, when they are more vulnerable, that is at rest or when moulting. In a cycloalexic arrangement the periphery of the ring may be formed either by heads of the larvae (e.g. in the chrysomeline Platyphora) (Jolivet et al, 1990), or by their caudal ends (e.g. in the galerucine Coehmera). Commonly, when there is an approaching danger, the larvae make coordinated and synchronous threatening movements. Larvae of the Oriental cassidine Aspidomorpha miliaris carry a chain of the cast skins or exuviae of the previous moults at the end of their abdomen. The exuviae carrying caudal ends form the periphery. When a cycloalexic congregation of this species is disturbed, the hind ends of the larvae curve upward, raising with them the trains of exuviae. The cycloalexy as such seems to be only partly effective in defence. Perhaps that is why it is supplemented or reinforced by other methods of defence, which include maternal protection (in case of New World forms), emission of glandular or digestive fluid through mouth or anus, reflex bleeding, biting movements of jaws, taking up a menacing posture, camouflage with the leaf surface, etc.

Larvae of some Platyphora, an American chrysomeline leaf beetle, form a cycloalexic arrangement on under surface of leaves of the host plant Solanum. They have a unique habit of removing hairs from the leaves and attaching them to their own body for camouflage. Other cases of using plant hairs among chrysomelids are seen among Chlamisinae. When those Platyphora larvae are disturbed, they raise their heads and an anterior part of the body in a menacing way. A fluid, which is a gastric secretion and seems to be toxic, is ejected from their mouths. If the disturbance continues, they attempt biting.

As has been pointed out earlier, cycloalexic insects are subsocial or gregarious in their larval life. It is believed that the larvae are held together through a pheromone. The chrysomeline Paropsini and the hymenopter-an Pergidae, feeding on eucalyptus in Australia, have taken to an interesting way for mutual communication. The larvae of these groups tap on leaves, and the signals, thus produced, are perceived through their special tympanic organs.

The annular arrangement of larvae is generally formed by cycloalexic insect species on leaves of the food plant, on upper or undersurface of the leaves. But, if leaves are narrow, a congregation, with some features of a ring-like arrangement, is formed on a twig, for example those cycloalex-ic forms which live on narrow leaves of a eucalyptus species. Some instances of polyspecific or even polygeneric ring formation are also known among leaf beetles and sawflies.

Some larval saturniids, such as Lonomia electra,, in tropical America, aggregate in circular formations (Fitzgerald, pers. com.), and other gregarious saturni-ids, like Arsenura and related ones, rest by day on the trunk of the food plant, not in a circle, as the geometry of the tree does not allow it, but in an irregular group, and use a trail pheromone for procession formation (Costa et al, 2003). Those larvae are very smooth to touch, while other saturniid larvae are dreadfully poisonous. The former have only the group resting position as a defensive mean against predators. Aggregations of an ascalaphid neuropteran larvae (Ascaloptynxfurciger) around a branch is quite similar to cycloalexy (Henry, 1972).

Cycloalexy or the making of rosette-shaped resting formations is a relatively unexplored area, which deserves further observations and investigations. No sooner has an effective defense developed than a new attack strategy follows; trigonalyid parasitoids for example, have succeeded in producing such eggs as are swallowed by sawfly larvae, thus obviating the need to confront the defensive ring (Weinstein, 1989).

— Fig. 14.1. Third instar of Platyphora conviva Stal (Col. Chrysomelinae). Rupture of the cycloalexic ring and predation by a bug of one larva (photo J. Vasconcellos-Neto, 1986). Itataia National Park, Brazil.

— Fig. 14.3. First instar larvae of Coelomera lanio Dalman (Col. Galerucinae). Cycloalexic ring (photo P. Jolivet, 1990). Vi^osa, Brazil.

— Fig. 14.2. Eggs of Coelomera lanio Dalman (Col. Galerucinae), laid on the underside of the folioles of Cecropia adenopus (Cecropiaceae). The newly hatched larvae will aggregate (Photo P. Jolivet, 1990). Vi^osa, Brazil.

— Fig. 14.4. Second instar larvae of Coebmera lanio Dalman (Col. Galerucinae) on a leaf of Cecropia adenopus. The ring has doubled. It will increase threefold (photo P. Jolivet, 1990). Viçosa, Brazil.

— Fig. 14.5. Third instar of Coelomera lanio Dalman on a leaf of Cecropia adenopus. The cycloalexic ring is near to be broken and the larvae will go feeding (photo P. Jolivet, 1990). Vi^osa, Brazil.

— Fig. 14.6. Cycloalexic ring of Platyphora conviva Stal (Col. Chrysomelinae). First instar. The larvae have covered themselves with the hairs of the underside of the leaves of a Solanum for extra protection (photo J. Vasconcellos-Neto, 1986. Itataia National Park, RJ, Brazil).

— Fig. 14.7. Second instar larvae of Perga australis (Hym. Pergidae) in cycloalexy.

— Fig. 14.8. An ichneumonid parasitoid (Westwoodia sp.) attacking the group shown in the Fig. 14.7. Larvae of the pergid are raising their abdomen in defence.

— Fig. 14.9. A heroic larva sacrifies itself (altruism) to grip the ichneumonid ovipositor with its mandibles, rendering the parasitoid incapable of further attack. This is altruistically suicidal (photos P. Weinstein, 1989).

— Fig. 14.10. Platyphora kollari (Stal) (Chrysomelinae) on Solanum sp., Brazil.

— Fig. 14.11. Platyphora batesi (Baly) (Chrysomelinae). Iquitos, Peru. Platyphora species are only found in tropical America. Often viviparous and larvae doing cycloalexy (after Jolivet, 1997).

Cycloalexy Chrysomelidae Larvae

— Fig 14.12. Second instar larvae of Perga dorsalis (Hymenoptera: Pergidae) in cycloalexy. White tachinid eggs can be seen on the thoracic sclerites of some larvae (photo Weinstein).

— Fig. 14.13. Perga dorsalis, a cylindrical cluster of late instar larvae on an Eucalyptus twig. The cylinder appear when the larvae increase in size and the leaf becomes too narrow. In fig. 3 and Fig. 4 no mother protection is shown (photo Weinstein).

References

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Capinera, J. L. 2004. Encyclopedia of Entomology. Kluwer Academic Publishers, Dordrecht, The Netherlands.

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Weinstein, P. 1989. Cycloalexy in an Australian pergid sawfly (Hym. Pergidae). Bull. Soc. R. Belge Ent. 125: 53-60.

Weinstein, P. and Maelzer, D. A. 1997. Leadership behaviour in sawfly larvae, Perga dorsalis. Oikos 79: 45G-455.

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