Anim. Behav., 1971, 19, 119-124

T H E E F F E C T O F L E A F G E O M E T R Y O N T H E F E E D I N G B E H A V I O U R

O F T H E C A T E R P I L L A R O F M A N D U C A S E X T A ( S P H I N G I D A E )

BY BERND HEINRICH* Department of Zoology, University of California, Los Angeles, California 90024

Abstract. The fifth instar larvae of Manduca sexta, while remaining near the petiole, usually bent large ovoid leaves and then ate them fully. Long narrow leaves were not chewed off, but after some initial feeding near the base, were also bent and eaten from the tip to the petiole. The pattern in which vari- ously shaped leaves were eaten was consistent for a given leaf shape and size. However, it could be altered by changing the flexibility and taper of the midrib.

Sight appeared to be unimportant for feeding, but ablation of the antennae and maxillae (which normally moved in unison with the mandibles) caused the caterpillars to take less uniformly sized bites from the leaf and to have a slower rate of weight gain.

Apparently the seemingly purposive behaviour of leaf bending which results in the economical harvesting of naturally hanging leaves arises from: (1) physical parameters of the leaf which restrict the larvae, (2) preferences of the larvae for immediately available leaf-edge, (3) coordination of the mouth-parts in relation to the leaf-edge, and (4) feeding forward in consecutive strips and sections.

The behaviour therefore appeared to be non-specific and equally adapted to all leaf shapes.

Many phytophagous insects have sharply deline- ated feeding preferences (Thorsteinson 1960). In some cases the preferences are known to be due to specific gustatory stimulants and deter- rents (Dethier 1954). Since the various host plants of insects also offer a broad spectrum of leaf shapes and sizes, geometrical and mechan- ical considerations may also be pertinent to feeding behaviour.

Manduca sexta feeds almost continuously during the last larval instar. During this stage over 1900 cm 2 of tobacco leaf may be eaten (Madden & Chamberlin 1945). Yet up to fifty eggs of M. sexta can occasionally be found on isolated jimson weed (Datura stramonium) plants on which the foliage is perhaps sufficient for only four or five larvae to complete their development. An efficient feeding behaviour would be advantageous. This behaviour should not be specific to one leaf shape only, since the larvae of M. sexta feed on solanaceous plants (Yamamoto & Fraenkel 1960) with a great variety of leaf shapes. Some of these plants such as Lycium halimifolium have lanceolate leaves; others such as Datura stramonium have ovate to round and roughly toothed leaves. Solanum spp. and Lycopersicon esculentum have variously shaped compound leaves, and Nico- tiana spp. have large ovoid to small lanceolate leaves. *Division of Entomology, University of California, Berkley, California 94720, U.S.A.

Leaf geometry may influence feeding be- haviour of a caterpillar in a number of ways. For example, it may: (1) affect feeding rate, (2) limit the possibility of access to only the basal areas of the leaf with resultant wastage of the tips, or (3) provide the possibility of the caterpillars' using the leaf not only as food but also as protection from predators, parasites and solar radiation (Waterhouse 1961).

This paper is concerned with the question of whether or not the caterpillars of M. sexta can manipulate differently shaped leaves so that they get the most food from each, and the factors determining the patterns in which leaves are eaten.

Methods The observations, unless specified otherwise, were restricted to the fifth (last) larval instar. Caterpillars were reared from eggs originally collected on jimson weed in the Mojave desert during the months of June, July and August 1968.

To record feeding pattern on a leaf, the leaf outline was drawn and the specific areas con- sumed were then sketched into this outline while the caterpillar fed.

Observations of the feeding behaviour were made on unaltered tobacco leaves (glasshouse grown) and leaves which were altered in shape by being trimmed with scissors. Jimson weed leaves were used for the lobate and compound shapes because these leaves were thick enough

119

120 A N I M A L B E H A V I O U R , 19, 1

to be fashioned into any desired shape without collapsing.

The maxillary palpi and antennae of some caterpillars were pinched off with forceps at least 24 hr before feeding rates were measured. The stubs were treated with aureomycin and streptomycin.

Results General Feeding Behaviour

The caterpillars suspended themselves f rom the petiole and the ventrally protruding midrib near the base of the leaf. They then reached to either side of the leaf and began feeding from the edge (Plate III , Fig. 2) in rapid bites. Strips

(2 m m wide) were consumed in lateral arcs of about 0.5 cm. Many of these strips taken con- secutively in the same direction constituted a 'section' (see section 1 in Fig. 1A). The width of this section was the same as the length of the strips, and its length varied depending upon the number of consecutive strips taken. The rate of feeding was the same regardless of the shape of the leaf since strips and sections are eaten in immediate succession.

Manipulation of Differently Shaped Leaves Large ovoid leaves. The caterpillars moved out

part way onto the midrib and extended them- selves toward the edge of the leaf which they

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Fig. 1. (A) The numbers indicate more specifically how the general areas depicted in (C) are consumed. (B) The pattern in which the first and second instar larvae feed on tobacco. C. Numbers indicate the arbitrary sequence of leaf areas consumed by a fifth instar caterpillar on unaltered tobacco leaf

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HEINRICH: FEEDING BEHAVIOUR AND LEAF GEOMETRY 121

grasped with thoracic legs and pulled down by contracting themselves. With abdominal legs (prolegs and clasper) remaining at the same place on the petiole and stem, they first ate the blade from one side, then from the tip and then from the other side of the leaf (Plate III, Fig. 2d and e, and Fig. 1A).

The caterpillars rarely chewed directly into the surface of the leaf or into the ventrally protruding ribules, except on very large leaves where the edge could not be reached from the midrib. Normally the thoracic legs guide the leaf edge to the mandibles and, while feeding, the caterpillars gradually 'walked' forward on the edge of the leaf with thoracic legs, while the abdominal ones remained in place on the petiole or midrib. Leaves were bent toward the caterpillar as a result, and eaten in a pattern which was characteristic for a particular leaf shape and size (Fig. 1A and C).

Laneeolate leaves. When most of the blade from a leaf 15 to 20 em in length had been cut off,

leaving only a strip on each side of the midrib, the larvae ate the leaf in long sections toward the tip on one side of the mibrid (Fig. 3C). When the caterpillars could reach no farther by stretching, the midrib had usually bent under their weight. I f the leaf did not bend passively, the larvae either pulled it down, or failing in pulling the leaf in, chewed into the midrib (Plate 111, Fig. 2a, b and c), thereby causing the leaf to bend. With abdominal legs still in the same position as at the beginning of feeding, the larvae 'walked' forward with thoracic legs only, and again fed toward the tip of the leaf in a series of long sections. From the tip of the leaf back toward the petiole, however, they fed in successive short sections at right angles to the midrib (Fig. 3C).

Lobate leaves. A large leaf of jimson weed, which I cut into the lobate shape shown in Fig. 3A, was eaten similarly to other large leaves except that each lobe was pulled down and eaten separately. The caterpillars at first consumed

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Fig. 3. The pattern in which jimson weed leaf, altered to the lobate shape, is consumed. The larva did not move from the position shown. (B) Small jimson weed leaf and representative feeding pattern. (C) The feeding pat- tern on an artificially pinnate jimson weed leaf.

122 A N I M A L B E H A V I O U R , 19, 1

long sections of the leaf parallel to the midrib. However, after they had fed to the tip of the leaf and began eating on the other side of the midrib, successive short sections were eaten perpendicular to the midrib.

Other Leaf Alterations

The feeding behaviour cannot be character- ized by describing the responses to different leaf shapes alone. The following leaf alterations were therefore made to determine the behaviour when access to various portions of the leaf were altered.

Cut leaves. Leaves that were cut from the plant and placed on a flat surface were eaten in entirely different patterns. There was little con- sistency in these patterns with regard to leaf shape. Usually the more accessible edges of the leaf were eaten first. The caterpillar s did not continue feeding from one point, but shifted positions and initiated feeding at several places on the leaf. Portions were often left.

The midrib. A leaf was cut off, turned over, and tied onto the petiole stub (which remained on the plant) so that the midrib was no longer available to the caterpillar when it approached the leaf ventrally f rom the petiole. The larva then began to feed near the base of the leaf and crawled out gradually on the subsequently exposed midrib.

When I 'stiffened' leaves by fastening the tips to a support, the larvae did not crawl out farther onto these leaves than onto leaves that were hanging freely. The tips of the leaves which did not bend were left uneaten.

Two leaves were cut and joined so that effectively a large leaf with a non-tapering mid- rib was constructed. The larvae continued to feed forward on such a leaf until they had eaten all of the blade on one side of the midrib. I t

appeared therefore that the size of the midrib or the firmness with which the caterpillars were attached to it, were of influence in gauging how far they would crawl out onto the leaf. Wax was applied to the claspers, rendering them in- operable. With waxed claspers, the caterpillars were presumably less firmly attached to the leaf. However, they crawled under the leaf as far as before. With normal claspers the larvae started feeding when the posterior end of the body was on the average 1.2 (0 to 2.4) cm (N=6) from the stem of the plant. With the clasper made useless as a grasping organ, feeding began when the larvae had advanced 1.6 (0 to 3.2) cm (N=6) . This difference was not sig- nificant (P>0.05).

Sensory Role in Leaf Manipulation

Stemmata. In the nearly complete darkness of a temperature control cabinet the larvae continued feeding and gained weight at the same, or at a slightly greater rate than in the light (Table I). Judging from partially eaten leaves, it seemed probable that the caterpillars did not feed in patterns noticeably different from those observed in the light. Sight was therefore probably of negligible importance during feeding.

Antennae and maxillae. Normally both the maxillary palpi and the antennae are moved sychronously with the mandibles and appear to touch the sides of the leaf edge with each bite. Without either the antennae or the palpi the biting rate on the leaf is not significantly differ- ent from normal animals (Table I). However, after ablation of both antennae and palpi some of the 'bites', although taken at about the same rate, missed the leaf entirely. The weight increase is reduced by 11 to 14 per cent after amputation of either antennae or palpi. Without both, the reduction to about 19 per cent is significant (P<O.05) and the patterns eaten from whole

Table I. Feeding Performance and Weight Increase of Fifth Instar Caterpillars in Darkness, in Light and with or Without Antennae and Maxillary Palpi (The Numbers Refer to Means, Sample Size and the 95 per cent Confidence Intervals)

Whole animals Operated animals

In light In dark Without Without Without antennae M. palpi both

Bites/s 2.79 - - 2.80 2.47 2.66 ~0"058(8) • • =t=0.063(10)

Weight increase O. 112 O. 116 0.099 0.095 0.091 (g]hr) =t=0.005(8) • ~0.006(7) ~0-006(6) -4-0.003(12)

HEINRICH: FEEDING BEHAVIOUR AND LEAF GEOMETRY 123

leaves were more variable than those observed when the antennae and maxillae were intact.

Discussion An animal is obviously circumscribed in be- haviour by sensory limitations. Therefore it is useful to know its sensory capabilities in order to understand the coordination of a particular behaviour pattern.

Caterpillars are presumably able to distinguish coarse mosaic of light intensities (Dethier 1943) and can distinguish shapes and sizes (Hundert- mark 1937). The present study suggests, how- ever, that sight is not essential during feeding in M . sexta.

The antennae and maxillae bear chemo- receptors (Dethier 1941) which are used to distinguish the proper food plants (Waldbauer 1962). The antennae also have temperature and humidity receptors believed to provide inform- ation to the caterpillar about the turgidity of the leaf (Detheir & Schoonhoven 1968). In addition the antennae have hairs receptive to tactile stimuli (Detheir 1941). It appears that the an- tennae and maxillae, presumably because of the tactile information which they provide, aid M . sex ta in feeding. The thoracic legs are used to pull the leaf within reach of the mandibles and thereby make possible leaf-bending and feeding in the observed patterns.

Differently shaped leaves are eaten in char- acteristic patterns probably because the cater- pillars begin to feed from a similar area, namely the edge of the leaf near the petiole. The physical parameters of the leaf then restrict or promote feeding in a certain sequence. For instance, long narrow leaves are eaten to the tip, instead of through near the base, because the thick mid- rib is consumed only after the leaf edge is gone. However, when the midrib is partially eaten the stiffness of the leaf is reduced and the cater- pillar continues to eat distally on the blade that it now easily pulls toward itself. On flexible leaves and lobes the larva can walk forward with its thoracic legs only, while remaining at the same position on the petiole and/or midrib. It can eat long strips of leaf in the forward direction without encountering increased tension in the leaf and without locally 'depleting' the food.

Small larvae cannot bend leaves and usually do not find a leaf edge. Instead of initiating feeding at an edge they chew holes into the surface of the leaf. Large larvae can attach themselves only to the midrib on the ventral surface of the leaf. They are thus limited in the

places where they can begin to feed. Large larvae can reach farther out to the sides, however, and begin to feed at the edge of the leaf, which bends naturally from their weight. Because of large size (up to 15 g), fifth instar larvae are restricted in their movements to the vicinity of the petiole. However, greater weight and strength make leaf- bending possible and permit feeding with a minimum of locomotion.

Distinct feeding patterns, perhaps having functional significance, have been observed in the caterpillars of the Heliconiinae (Alexander 1961). Some of the solitary caterpillars of this group chew channels into the leaf and thereby isolate the tip of the leaf from the base. Alex- ander suggested that this behaviour might be related to territoriality. The feeding behaviour of M . sex ta appears to be more meaningful in terms of maximizing rates of food consumption. The behaviour that has been described permits continuously feeding larvae to eat entire leaves regardless of shape or size. Feeding is possible in light as well as in darkness. The behaviour is structured and loss of coordination, as indicated by biting behaviour, results in a reduction in the rate of weight gain.

Acknowledgments

I thank Professor Franz Engelmann and Pro- fessor George A. Bartholomew for reading the paper and making helpful comments and critic- isms. I am also very grateful to Bill Hudson for an ample provision of tobacco plants. The work was supported in part by National Science Foundation Grant GB 5139 to Professor Bartholomew.

R E F E R E N C E S Alexander, A. J. (1961). A study of the biology of the

caterpillars, pupae and emerging butterflies of the subfamily Heliconiinae in Trinidad, West Indies. I. Some aspects of larval behavior. Zoo- logica, 46, 1-24.

Dethier, V. G. (1941). The function of the antennal receptors in lepidopterous larvae. Biol. Bull., 80, 403--414.

Dethier, V. G. (1943). The dioptric apparatus of lateral ocelli. J. cell. comp. Physiol., 22, 115-126.

Dethier, V. G. (1954). Evolution of feeding references in phytophagous insects. Evolution, 8, 33-54.

Dethier, V. G. & Schoonhoven, L. M. (1968). Evalu- ation of evaporation by cold and humidity re- ceptors in caterpillars. J. inst. Physiol., 14, 1049- 1054.

Hundertmark, A. (1937). Das Formenunterscheidungs- vermtgen der Eiraupen der Nonne (Lymantria monacha L.). Z. vergL PhysioL, 24, 563-582.

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Madden, A. H. & Chamberlin, F. S. (1945). Biology of the tobacco hornworm in the southern cigar- tobacco district. U.S. Dept. Agric. Tech. Bull., 896 pp.

Thorsteinson, A. J. (1960). Host selection in phyto- phagous insects. Ann. Rev. Entomol., 5, 193-218.

Waldbauer, G. P. (1962). The growth and reproduction of rnaxillectomized tobacco hornworms feeding on normally rejected non-solanaceous plants. Ento- moL exp. AppL, 5, 147-158.

Waterhouse, F. L. (1961). The microclimatic zones near leaves and twigs and the postural behavior of a Geornetrid larva. Verh. X1 Int. Kongr. Ent., Wien (1961), 689-693.

Yarnamoto, R. T. & Fraenkel, G. S. (1960). The specific- ity of the tobacco hornworrn Protoparce sexta (Johan.) to solanaceous plants. Ann. entomol. Soc. Am., 53, 503-507.

(Received 15 March 1970; revised 26 May 1970; MS. number: A961)