LEAF-MINING INSECTS LEAF-MINING INSECTS By JAMES G. NEEDHAM STUART W. FROST BEATRICE H. TOTHILL "There's never a leaf nor blade too mean To be some happy creature's palace." J. R. Lowell, Vision of Sib Lattnfal,. BALTIMORE THE WILLIAMS & WILKINS COMPANY 1928 Copyright 1928 The Williams & Wilkins Company Made in United States of America Published May, 1928 Composed and Printed at the WAVERLY PRESS FOR The Williams & Wilkins Company Baltimore, Md., U. S. A. PREFATORY NOTE BY THE SENIOR AUTHOR Something should be said in explanation of the part that has been taken by each of the authors in the preparation of this book. It was begun under my direction by Miss Hughes, now Mrs. John D. Tothill, when she was a graduate student in my laboratory at Cornell University. It was continued by her subsequently in Illinois, Wisconsin, British Columbia, and especially at Frederickton, New Brunswick. Meanwhile, Dr. Frost had begun the study of leaf-miners at Cornell University under the direction of Dr. R. Matheson. When Mrs. Tothill was preparing to go with her husband on an important scientific mission to the Fiji Islands (where she has been during the final putting together of this book) she appealed to me to find some means of completing it. I, naturally, turned to Dr. Frost, and we agreed to complete it together. My own part has been chiefly that of editing and writing introductions, though I have contributed some notes and illustrative material from my own rearings in each of the four orders of leaf-miners. Dr. Frost has written the chapter on Dipterous miners and has compiled the bibliog- raphy and the tables of species and food plants for all four orders. We have worked together on most of it. At the end of it we are all under obligation for help to more people than we can now name. We are all indebted first of all for generous and oft-repeated aid with the Lepi- doptera to Dr. W. T. M. Forbes; likewise, with other orders, to Dr. R. Matheson. Mrs. H. E. Seemann has been very helpful in arranging the illustrations. I have been aided in the collecting and preparation of materials by Miss Anne Snitow and Miss Helen Albro. Mrs. Tothill has had the aid of her husband, Dr. John D. Tothill, and of Mr. W. VI PREFATORY NOTE Downes and Mr. Treherne of the Canadian Dominion Ento- mological Service. Dr. Frost wishes to acknowledge help in the determination of specimens from Dr. J. M. Aldrich, Dr. Adam Boeving and Mr. S. A. Rohwer, all of the U. S. National Museum. I, as senior author, wish to assume responsibility for the omission of the name of the describer of the species after each scientific name. Our undertaking has been threefold. We have endeav- ored to provide (1) an un technical introduction to the study of leaf-mining insects, intelligible to the general reader; (2) an account of their natural history sufficiently detailed to be useful to the working ecologist; and (3) lists of the leaf-miners, of their food plants, and of technical papers concerning them adequate for the needs of the specialist. Thus we have undertaken to make more avail- able to students, the rich but hitherto widely scattered results of many excellent investigations in this interesting eco- logical field. Here there is much that should be of interest to the general biologist. The mandibulate leaf-mining larvae show a convergence in form that is almost without a parallel elsewhere. They also present an unique example of hyper- metamorphosis that hitherto has been almost or quite ignored by all the text books in their discussions of that subject. Leaf -mining moth larvae are not ordinary cater- pillars; at least, the sap-feeders are not. The mouthparts they have developed for shearing and sap drinking and the form of head associated therewith are quite their own. Any one with a taste for natural history will find interest in observing how these tiny creatures get their living, find their shelter, keep their dwelling places clean and sanitary, provide for all the shifts of stage and station, and manage the ordinary business of their lives. Their ways are quite unique in the animal world. James G. Need ham. Ithaca, April 20, 1926. CONTENTS CHAPTER I A General Acquaintance with Leaf-Mining Insects 1 The leaf as a dwelling place 3 The insects 6 Life histories 9 The mines 12 Mining operations 16 Frass 20 Tenancy 21 Origin of the leaf -mining habit 22 Integradations with other habits 23 Enemies 29 Collecting and rearing leaf -miners 31 CHAPTER II Extent of the Leaf-Mining Habit 35 Economic species 35 Host plants 37 Table of orders of leaf mining larvae 39 CHAPTER III Order Lepidoptera 41 CHAPTER IV Suborder Jugatae 71 Family Eriocraniidae 72 CHAPTER V Suborder Frenatae, Superfamily Incurvarioidea 79 Incurvariidae 79 CHAPTER VI Superfamily Nepticuloidea 85 Nepticulidae 85 CHAPTER VII Superfamily Tineoidea 92 Tischeriidae 92 Lyonetidae 95 Gracilariidae 115 Coleophoridae 141 vii Vlll CONTENTS CHAPTER VIII SUPERFAMILY CYNODIOIDEA 151 Cycnodiidae 151 Douglasiidae 152 Heliozelidae 152 CHAPTER IX SUPERFAMILY GELECHOIDEA 158 Gelechiidae 158 Lavernidae 167 CHAPTER X SUPERFAMILY YPONOMEUTOIDEA 171 Yponomeutidae 171 Glyphipterygidae 173 Heliodinidae 173 CHAPTER XI SUPERFAMILIES TORTRICOIDEA, PYRALIDOIDEA, AND NOCTUOIDEA 175 Tortricidae 175 Pyralidae 175 Noctuidae 176 CHAPTER XII Order Coleoptera 181 Family Buprestidae 188 Family Chrysomelidae 195 Family Curculionidae 205 CHAPTER XIII Order Hymenoptera 210 CHAPTER XIV Order Diptera 231 CHAPTER XV List of Leaf-Mining Insects 279 CHAPTER XVI Host Plants of Leaf-Mining Insects 302 Bibliography 324 Index 341 CHAPTER I A General Acquaintance with Leaf-mining Insects Green leaves are the world's dependence for food produc- tion. Day by day, as the sun shines on them they build up the organic substances by which all men and all animals live. Directly or indirectly they feed both great and small. Their consumers range in size from the great elephants of the tropical jungle down to the little tenants of single leaves that are the subject of this volume. Leaf-miners are among the smallest of plant-eating animals. Most of them find both sustenance and shelter within the confines of a single leaf— often within a small portion of a leaf, between its upper and its nether epidermis. Their food is the thin stratum of green tissue that lies, like coal in a mine, outspread in a seam between two worth- less adjacent strata, and the insects get it and dig it out for use. That is why we call them miners. Leaf-miners are everywhere. In any lane or fence-row they may be found by one who will take the trouble to look for them. Their signatures, written in the leaves, are plainly outspread to view. The foliage of almost any oak tree or hornbeam or clump of goldenrod will show in autumn the characteristic marks of several kinds of them. Some of them make winding galleries like that of the little fly in the aster leaf shown in figure 1, and when grown leave the leaf through a slit in the epidermis and enter the soil to undergo their transformations. Others excavate broader chambers within the leaf, and remain inside them to transform. The mothlet whose mine is shown in figure 2 is of the latter habit. It makes a broad mine in a lobe of a leaf of the white oak. It disposes of its waste in a corner l n$ LEAF-MINING INSECTS of the mine, stowed away behind a screen of white silk. When grown it spins a filmy cocoon of silk, moored to the walls with radiating stay lines of the same material, and Fig. 1. Leaf of the white aster, Aster paniculatus, with a mine of the fly Phytomyza albiceps. Fig. 2. The white oak leaf-miner Lithocolletis hamadryadella. R, a leaf of white oak bearing a ruptured mine; Sf the mine enlarged showing the empty chrysalis protruding; T, the adult moth. (Drawn by C. H. Kennedy.) within this it transforms to a pupa. The pupa has a sharp hornlike process on its head with which, when ready for the final transformation, it can penetrate the walls. When GENERAL 6 part way out of the leaf the pupal shell (chrysalis) breaks open on the back, and from it emerges a resplendent little moth, clad in scales of gold and ermine and jet, a veritable atom of Lepidopterous loveliness. There is hardly anything in nature more beautiful than are some of the moths that have leaf-mining larvae. THE LEAF AS A DWELLING PLACE The leaf is a peculiar place in which to live. As every one knows, it is merely an expansion of the plant body con- taining green cells thinly outspread for advantageous ex- posure to the light. A leaf consists essentially of this layer of assimilatory cells, covered by and enclosed in a trans- parent epidermis, and supported by a framework of veins. It is generally, but not always flat, and it varies enormously in details of form, size, structure and content, each species of plant producing leaves after its own kind. We must have the common characteristics of leaves in mind if we would understand the operations of the insects that dwell in them. The epidermis is primarily a protective outside layer. It protects the soft semiliquid protoplasmic cells of the par- enchyma from evaporation, and to some extent also from destruction by foraging animals. It consists generally of a single layer of rather thick walled transparent cells, covering the entire leaf and continuous with the epidermis of the stem. It is perforated by pores or stomates that facilitate the intake of carbon dioxide from the air and the outgo of watery vapor. Each stomate is bordered by two guard cells, that automatically regulate transpiration, by opening when moisture is abundant and closing when it is scanty. The guard cells, unlike most other epidermal cells, contain green chlorophyl bodies. Often the cells of this epidermal layer secrete on the outside a common cuticle, that is highly protective and waxy, or varnish-like exuda- 4 LEAF-MINING INSECTS tions are sometimes added upon its surface. Plant hairs are commonly developed from single cells of the epidermis, more abundantly, as a rule, upon the lower surface of the leaf. Midrib and veins have a twofold function in the leaf. They contain hard parts that make them supporting struc- tures, and they contain the vessels that are the channels of circulation within the plant, bringing up water with its content of mineral salts from the ground, and taking to other parts of the plant the sugars and other products of assimilation that are manufactured in the leaves. In so far as the veins contain cells having hard walls, they offer an impediment to the work of the leaf-miners. The part of the leaf for which all other parts exist and on whose products all other parts of the plant subsist, is the soft living, protoplasmic, chlorophyl-containing parenchyma. This is variously disposed in different types of leaves, but in general it tends to be differentiated into two layers: a palisade layer of one or more rows of closely placed, usually columnar cells next the epidermis, and a spongy layer of irregularly placed and openly spaced cells beneath or within. The stomates of the epidermis open into the interspaces between the cells of the spongy layer. It is a part of the fitness of things that the close packed palisade cells, with their rich content of chlorophyl should be placed directly in contact with the transparent upper epidermis of the leaf where they are reached by effective light; and that stomates should be relegated mostly to the lower epidermis where they control the admission of air to the moist chamber of the spongy parenchyma, maintaining proper conditions there for the exchange of gases in me- tabolism. The palisade layer is the chief seat of food pro- duction. It is the part of the leaf that is sought out by the more specialized leaf -miners: the lower, more easily pene- trable, spongy layer is the first sought by the unspecialized. 6 LEAF-MINING INSECTS In so far as the work of these insects is concerned, we may regard the tissues in the leaf of two sorts, one of which is eaten and one is not. The latter is the epidermis with its cuticle.1 The other, whether parenchyma or vein, or both, we may for practical purposes designate as mesophyll. THE INSECTS Leaf-miners are all larvae. No adult insects have been able to establish themselves in such a habitat. It is only the worm-like, quick-growing young of those groups of insects which have complete metamorphosis with both larval and pupal stages in their life cycle, those that feed extensively on plants, and are very small in size, that have become leaf-miners. They are the larvae of four great groups, which, named in the order of their importance are: 1. Caterpillars or moth larvae; order Lepidoptera 2. Grubs or beetle larvae; order Coleoptera 3. Maggots and other two-winged fly larvae; order Diptera 4. Sawfly larvae; order Hymenoptera. These are the same four orders that everywhere are the world's keenest competitors for food, and that make up the bulk of the animal population. The pressure for room and for sustenance has been very great and all kinds of shifts for a living have been tried; and these little fellows have shifted into the interior of leaves where the mesophyll provides abundant food, and the epidermis is their shelter. The adults of these four orders are very unlike; moths and beetles and true flies, and sawflies. No one would imagine that they could come from larvae that seem so nearly alike. Every one who has studied leaf-miners is at once struck by this similarity of larvae. It is a remarkably good illustra- tion of the moulding power of environment. Within the leaf the conditions are alike for all, and all have been moulded 1 Tn descriptions sometimes mentioned by either name. GENERAL 7 to a common form. While all larvae are more or less worm- like, the free-living ones are easily referable to their orders but it is often difficult for a good entomologist to tell whether the creature he has found mining a leaf is the larva of a moth, a beetle, or a sawfly. This is true of the more specialized forms only. In each order there are leaf-miners that are not perfectly adapted to the habit, that differ but little from their externally feeding relatives. Fig. 4. The four leaf -mining orders and their larva. M, a beetle (Cole- optera) ; JV, a moth (Lepidoptera) ; 0, a fly (Diptera) ; and P, a sawfly (Hymenoptera). Speaking broadly it may be said that there are but two kinds of larvae found in leaf mines; the Diptera and the others. The Dipterous larvae are very soft and cylindric maggots, very plastic and of no permanent shape, and able to accom- modate themselves to narrow spaces by great changes of form. They readily undergo compression within the shal- low mine. They mostly lie on their sides when mining, and hence this pressure is lateral. Freed from compression 8 LEAF-MINING INSECTS the body becomes cylindric, and when fully extended it tapers forward to the mouth hooks. The mouth hooks are swung with an oscillating motion and shear unopposed like a scythe across a swath. The body rolls; and setulae and fleshy protuberances when present are developed in circles and are effective in any position. The larvae of the other three orders differ from this in almost every particular. The body is flat and of a relatively permanent form. It is generally most flattened on the ventral side — the side next the epidermis of the leaf. It is Fig. 5. Two sawfly larvae (after Yuasa) . B, an external feeder, Hylotoma spJ A, a leaf -miner, Metallus rubi; most widened and most strongly chitinized at the anterior end, where flat horny plates both dorsal and ventral cover the prothorax and take the heavy friction against the walls of the mine. Paired jaws are present and they are opposed in action. They work like pincers or shears. The lateral margins of the body become more or less serrate in outline, due to bulging prominences of the middle segments; and ambulatory processes and ambulatory setae are developed in symmetrical bilateral pairs. Details of these adaptations will abundantly appear in the following chapters which treat of the several orders. GENERAL 9 In the evolution of a form of body so well adapted to leaf- mining the main tendencies have been toward the loss of legs, loss of color, the flattening down of the body and head, the tapering of the head to a wedge, sloping forward, with the thin mouth parts at its front, the recession of the rear of the head into the wide prothorax with development of strong muscles for moving it forward and backward, in and out, and the development of heavily chitinized dorsal and ventral plates on the prothorax. LIFE HISTORIES All leaf-miners hatch from eggs and in the course of their development pass through larval, pupal and adult stages. The eggs are either deposited upon the surface of a leaf or inserted into it. In the latter case the mother insect makes a puncture to receive it, either by means of her jaws as in the case of certain beetles, or with her ovipositor as in the case of all the sawflies, most of the two-winged flies and a few of the more primitive moths. In Yponomeuta the eggs are laid in masses on the branches of the host and the young worms must wander a considerable distance to find food. The time and place of oviposition vary with the species. The larvae of some of them on hatching from the egg may come out upon the surface of the leaf, but in all the more specialized miners they pass directly into the leaf through the epidermis that the egg covers, and do not appear outside. The larva is the real leaf-miner. All the work of excava- tion falls to its share. All increase in size occurs during the larval period. The larva may develop chewing mouthparts capable of devouring cells bodily, or it may develop cell- shearing apparatus and sap-feeding habits. In any case it grows, and passes through a series of larval stages or instars, each of which is terminated by a moult. At the end of each instar it casts off its hard, inflexible, chitinous skin, that has become too close-fitting, and grows a new one. 10 LEAF-MINING INSECTS The number of larval instars, and of corresponding moults varies from three to seven (possibly more in the sawfly larvae), three being the usual number in leaf -mining maggots and beetle grubs, and five in moth larvae. There are some- times changes of habits with each succeeding moult and these may in some cases be read in the appearance of the completed mine. The Strigifin miner on chestnut (see fig. 40 on p. 123) changes its habit with four out of five of its successive moults. 1PH5 -■ j j j1 * <^; Fig. 6. Two moth larvae. A, an ordinary caterpillar that feeds down- ward; B, a leaf -mining caterpillar that feeds forward. Besides the sudden increase in size that follows upon moulting, there are changes of form that are sometimes very considerable, even before the final change to the pupa. The head capsule is widened with such regular steps that it is possible to read the story of the moultings from a good series of the cast capsules by comparing them as to size. The widths of head capsule will fall into as many groups as there are instars. The earlier instars are the more plastic, and are more specialized than the later ones. They are more precisely adapted to the operations of leaf -mining. The form in the later instars tends to revert to that of ordinary non-mining GENERAL 11 larvae of the several groups. Sometimes there are two distinct forms of larvae and the change from one to the other is so great as to constitute a true hypermetamorphosis. This occurs in the order Lepidoptera and will be discussed and illustrated under that order in Chapter VII (see p. 136). The ordinary larva, as every one knows, has a cylindric worm-like body with a head capping its front end, and mouth parts directed downward. It is, of course, an insect with three main body divisions, head, thorax and abdomen; but the last two are very similar in external appearance, the three rings of the thorax being distinguished from the more numerous rings of the abdomen by the possession of minute jointed legs on each: even this distinction fails when these legs disappear. The ordinary larva feeds downward from the surface to which it clings. The leaf -miner, on the contrary, must feed forward. The ordinary larva creeps freely about, but the leaf -miner is confined within its narrow gallery. To understand the modifications of form that go with the leaf -mining habit we must bear in mind the condi- tions imposed by the habitat. The principal needs of the miner in accordance with which all its peculiarities of form have been evolved, are for thin, flat forward-reaching mouth parts, and for holding apparatus to keep them up against the mesophyll for their work. Hence the mouth turns forward, and the head takes on the form of a flat wedge. Walking legs tend to disappear and a variety of stay-apparatus tends to be developed — spacing humps, and tubercles and bristles and bands of setulae, and sometimes an anal sucker. The miners that live in the more solid leaves have the prothorax greatly enlarged, filled with powerful muscles for moving head and jaws, and covered above and below with flat plates of chitin, to take the brunt of the pressure against the walls of the mine. The rear of the head capsule has become more widely opened, and the hind margins have been produced backward within 12 LEAF-MINING INSECTS the prothorax for the attachment of the powerful muscles there. It is the mid-dorsal margin of the head capsule that is prolonged backward in sawfly larvae, the side margins, in mining grubs and caterpillars. The pupa is, as always, the stage of making over from the worm-like larva into the winged aerial adult insect. It is a quiescent period of variable duration. It is passed in seclusion either in the mine or in some shelter outside, or in the ground. Cocoons are spun by the larvae of weevil miners, sawfly miners, and by most mining caterpillars. Each species has its own way of meeting its own needs. The adult insects of the four orders are in habits very similar to the other members of their respective groups. On reaching maturity their chief business is mating and egg- laying. The females must seek out proper food plants and deposit eggs in a fit manner to produce another generation. In the annual cycle there is always one brood per season, and there may be several. The single-brooded forms may be early, requiring soft, young leaves for their operations (see Eriocrania, p. 76), or they may be late in season, waiting until the leaf -tissues are full sized before entering them (see Brachys, p. 190). The repeaters may have a definite number of broods per season, two, three, four, or even more, or the broods may so overlap in time as to be indistinguishable. As with insects of other habits, the number of broods may depend on climate and length of season, there being more of them per year in southern latitudes. THE MINES The dwelling places that these small miners excavate for themselves within the leaves differ greatly in details, but they may for convenience be grouped in a few categories. 1. As to spread in the leaf, they are of two principal kinds — linear and blotch. GENERAL 13 Linear mines are formed when the larva tunnels straight ahead through the parenchyma. If the course taken be winding they are called serpentine mines. Fig. 7. Mine types, a and b, upperside blotch mines of Lithocolletia; c, full depth blotch mine of Brachys; d, a serpentine mine of Nepticula; all on a leaf of white oak. Blotch mines are formed when the larva excavates a broad patch. The blotch may take on various shapes, circular, oblong, lobed, etc. When a number of slender lobes radiate from its margin, it is called a digitate mine. 14 LEAF-MINING INSECTS Between typical linear and blotch mines there are all sorts of intergradations. Often a linear mine expands suddenly and broadly; then it is called linear-blotch. Some- times a mine starts in linear form and widens gradually to flaring margins; then, on account of its outline, it is called a trumpet mine. Many mines start in linear form and become blotched through winding, and intercrossings and cutting out of all the mesophyll between passage ways that were at first separate; but blotches are regularly formed by systematic peripheral excavation, which may be made irregularly or all around or in one general direction only or alternately at opposite ends, or by back and forth "swath cutting' ' across one end. The boundaries of both linear and blotch mines are generally determined in part by the impeding larger veins of the leaf. 2. As to depth, mines may extend from upper to lower epidermis, full depth mines, or they may occupy only the uppermost or the lowermost layers of the mesophyll, in which case they are called upper surface and lower surface mines, respectively. Only the full depth mines are equally visible from both sides of the leaf. A few linear mines run irregularly through the mesophyll, some of them, while small, appearing first on one surface of the leaf, and then on the other. Most mines become deeper as the size of the larva increases. The terms used in descriptions, unless otherwise stated, apply to completed mines. The very common miners of the genus Lithocolletis make a very shallow surface mine during the first three larval instars, completed as to area by that time, and then excavate the remaining mesophyll during the next two larval instars, leaving when completed a full depth mine. 3. As to finish, mines may be open or closed. The larvae of moths of the genus Cosmopteryx, Lyonetia and other genera maintain as an open door a hole in the epidermis GENERAL 15 through which they thrust out all their frass, keeping the interior clean and white. Most mines are closed. Those of the Buprestid beetles have the hole through which the larva enters capped with the empty egg shell glued down so securely that it remains in place through the season. Those unspecialized leaf -mining larvae that wander from leaf to leaf making new mines as they choose, must needs make an opening when they enter; but it is often no more than a slit through the epidermis, and the edges of the slit L0W2R SUBFACELi MINE Fig. 8. Diagrams of cross sections of three leaf mines that differ as to depth. close behind them. The common mode of entrance for all the better leaf -miners is through the attached surface of the egg, leaving no hole for unwelcome bacteria and spores to enter. 4. As to distribution, mines often take a definite position or course on the leaf surface, along the margin or along the midrib, originating at the edge and proceeding inward or following between parallel veins (see fig. 11). They may be greatly elaborated, they may take a more or less regular appearance and become star-like or linear mines may curve upon themselves in concentric arcs (see fig. 18). Their 16 LEAF-MINING INSECTS operations may be confined to a small territory or may cover the entire leaf. Leaf-mining caterpillars spin less silk than do most other moth larvae, but even within the mines silk may serve a variety of uses, such as lining the mine (Tischeria), tying up frass pellets out of the way, and making cocoons. Some highly specialized leaf-miners, notably species of Litho- colletis, increase the space within the mine by spinning silken threads across the loosened epidermis. These threads on drying contract and the mine is thrown into wrinkles or into a single roof -like fold. It is then called a tentiform mine. Many details of spinning habits will be found in the chapter on Lepidoptera under the several species, each of which spins in its own way. Mines may further differ in size, in smoothness and color of surface, in transparency, and in manner of frass disposal. This last will often give a clue to the relationships of the larva within the mine. Sap-feeding larvae of the Lepidoptera have little solid matter in their food and hence there is not much frass deposited in their mines, and that little is rarely in the form of distinct pellets. Tissue-feeders, on the contrary, consume quantities of indigestible cellulose cell walls, and reject the cellulose generally in distinct pellets, that are often very considerable in amount and may even seem almost to fill the mine. The manner of bestowal of the frass — whether in central or peripheral midden-heaps or lines, or irregularly, is often characteristic of particular species. It is a very small flat that leaf-miners occupy, and their housekeeping problems are serious. All of the more specialized among them have ways of maintaining free working space and of keeping their food clean. MINING OPERATIONS The feeding operations of many leaf-mining larvae may be readily observed with a good lens, holding their leaf up GENERAL 17 to the light and watching them at work by looking through the transparent epidermis. However dark colored the body of the mine, the outer margin when freshly excavated is apt to be clear enough to permit the movement of the larvae to be seen. By one means or another — legs, prolegs, ambulatory processes or setae, anal sucker: any or all of these — the body is held rigid while the jaws are moved up against fresh mesophyll. But there is a great difference in jaws and consequently in manner of attacking the mesophyll. If one watch the larva of a beetle like Zeugophora or of a sawfly like Fenusa, the head will be seen to be thrust for- ward and drawn backward, in and out of the prothorax at every bite. The opened mandibles are driven forward into the new tissue, closed and withdrawn with each movement of the whole head forward and backward. The prolonga- tions of the chitinous shell of the head to rearward have muscles attached that control this in and out movement. If one watch a highly specialized sap-feeding Lepidopter- ous larva in its mine the thin, flat, saw-edged, wall-shearing mandibles will be seen to be moved steadily along, oscillat- ing as they go, cutting a thin slit through one cell-layer only, while the freed cell contents as steadily flow into the mouth of the caterpillar. Generally in these mandibulate larvae the ventral side of the body lies flat against the epidermis. In contrast with this, the Dipterous maggot lies on its side in the mine, as already stated, and swings its mouth hooks vertically; i.e., in the median plane of its body, parallel to the leaf surface. The body remains stationary except at the anterior end, which swings in the arc of a circle as the shearing of the mouth hooks proceeds. On certain plants, like the windflower, Anemone pennsylvanica, the shorn cellulose walls lie in the mine in swaths, like leaning stubble cut with a dull scythe, and show exactly the course the larva has taken from side to side within the interspaces that are bounded by the stronger veins. The 18 LEAF-MINING INSECTS larva cuts the swath across the end of the blotch mine, doing all its cutting in one direction, scythe-like, across the field, and at the end of its reach swings back idly to the Fig. 9. Diagrams of the mines and mining operations of a Dipterous leaf -miner on Anemone. A, a leaf with three mines; B, a portion of a mine enlarged; C, a smaller portion of the same, more enlarged;/), the "swing" of the larva as it cuts successive "swaths." starting point, hitches up closer, and makes another cut. And when the swath has reached the edge of the vein- bordered field that is being harvested, the larva rolls over GENERAL 19 (thus reversing his sickle), turns about and cuts another swath back across the same field. The cross strokes of the swath are always concave to rearward, as swinging in an arc, necessitates. It follows that going and return swaths have opposed concavities. A rather beautiful herringbone pattern results from this, made in a single line of progression, back and forth, redoubled, wavering at vein barriers and becoming regular again when new leaf areas are entered but continuous from the beginning to the end of the mine; and in it one may read the complete record of the miner's travels. Fig. 10. A leaf of ragweed, collapsed where mined by the moth, Tischeria ambrosifoliella. The effect of the mining-operations on the plant varies with the character of the leaf, as well as with the extent and nature of the injury to the tissues. Thus the firm leaves of the oaks stand up well under the attacks of a great variety of miners, while the soft leaves of garden herbs, often col- lapse rather quickly after even moderate injury. The structural strength of the parts surrounding the mine deter- mines this as is well seen by comparing the mines of two species of Lithocollitis, — belonging to the group that, in the late larval instars, normally makes tentiform mines. The 20 LEAF-MINING INSECTS mine of L. lucetiella is located on the underside of a linden leaf between strong veins, and it remains quite flat to the end. But the mine of L. morissella on the underside of the thin and weakly braced leaf of the hog-peanut, becomes completely folded together in a single ridge: collapsed- tentiform, so to speak. (See fig. 41.) Certain portions of the leaf are preferred by different leaf-miners, some, like Brachys, choosing the vicinity of Fig. 11. Leaf-maps of mine distribution. A, 50 mines of Bracks sp.? on Basswood (note their scarcity within the central circle); B, 50 mines of Antispila viticordifoliella on wild grape (general); C, 100 mines of Litho- colletis ostryarella on hop hornbean (note avoidance of the leaf margin). the stronger veins, and others avoiding these as much as possible. FRASS As an African hunter follows his big game by taking note of its spoor, and as an ornithologist learns something of the habits of owls from the examination of their pellets, so the student of leaf -mining insects may gather much information concerning their identity and their behavior from an ex- amination of their frass.2 This varies with their food, 1 Frass is the rejectamenta of their food (as the name implies) left in the mine after feeding, and of their feeding operations: fecula, chips, etc., collectively. GENERAL 21 according to the nature of the leaves in which they mine, and with their size, in amount, color, consistency and dis- position. A few leaf -miners eject all their frass through a hole in the epidermis of the leaf. The dainty little herb-mining larvae of the genus Cosmopteryx thus keep their mines clean and white. At the opposite extreme are some of the cy- lindric Lepidopterous larvae and the sawflies, whose mines are almost rilled with frass pellets ; also some of the Dipter- ous larvae whose smeared-up mine-walls have a very messy appearance. The arrangement of the frass in the mines of certain species is very characteristic. In the mine of the maggot of Phytomyza nigritella on peach and cherry the frass is arranged in a distinct line of spots, that is at once distinctive. So, also is the crossbanded arrangement of it in the winding part of the mine of the trumpet miner of the apple (see figs. 2 and 3 of pi. 2). The digitate leaf-miner of the locust, Parecopta robiniella maintains a sort of storage cellar for frass down next the lower epidermis of the leaf, while it lives and mines in the palisade layer of cells close to the upper epidermis. It is said to dump its moulted skins, like castor! clothes, into the same receptacle. The makers of linear mines, as they move forward, leave their frass behind in continuous or broken, straight or zig-zag lines or in spots. The polygon miner of the basswood, Lithocolletis luciella, bestows its frass pellets in the extreme periphery of the mine while it feeds from the outside toward the center. Many other mining caterpillars store it in the center, or in one end, often webbing it in place with silk. Most of them keep their feeding areas clear of it. TENANCY The time during which a leaf mine is occupied may vary from less than a single larval instar to the entire develop- 22 LEAF-MINING INSECTS mental life of the insect. Here again, permanence of resi- dence within a single mine is a sign of better adaptation to the leaf -mining life. Some of the less specialized leaf maggots seem to slip in and out of a soft leaf at will. Encountering a vein, they cut a slit in the epidermis and slip out through it ; and, presently in a new place, cut another slit and slip into the leaf again. The locust leaf-mining beetle, Chalepas dorsalis, regularly occupies several leaflets in succession; when it has finished the mesophyll in one leaflet it rambles off in search of another one. The grass leaf -miner, Aphelosetia orestella, occupies one leaf of bottle-brush grass, Hystrix patula, in the late season and hibernates in it; but this old leaf is frozen in the winter, and in the spring the larva enters a new leaf and completes its growth there. Others of this genus have similar habits. This subject will receive special treatment in our dis- cussion of the order Lepidoptera, in which order all the grades of tenancy are best illustrated; but here it may be said that most leaf-mining larvae spend their entire larval life within a single mine, and many pupate there, either with or without a cocoon, and either attached to the wall or free. More often the pupa is formed outside, in a crevice or a fold of the leaf or in the ground. THE ORIGIN OF THE LEAF-MINING HABIT It is probable that the leaf -mining habit has been ac- quired independently many times. The Buprestid beetles may well have come to it through their wood-boring habit. Many of them live in succulent twigs and originally they may have come into the leaf blade by way of the stalk. At any rate, their earlier stages are more typically of the form of body of the wood borers and the later stages are more cylindric. The mines are often started upon the surface of a vein. GENERAL 23 Dipterous larvae, accustomed to burrowing in soft sub- stances, may have come to the mining of green leaves through the habit of boring in dead ones. At any rate, there are species that still do both these things and that are sometimes saprophytes, at other times leaf-miners, being not wholly committed to either habit. But it seems probable that leaf -mining caterpillars and sawfly larvae and leaf-beetle grubs are derived from fore- bears that fed on leaves in the ordinary way. Perhaps the earliest among them merely ate a hole in the leaf: later ones put their heads farther in and kept on eating down underneath the epidermis: finally some of them bodily followed their heads down into the hole and dwelt there. INTERGRADATION WITH OTHER HABITS Leaf -mining as a mode of life intergrades with gall-making, "^ with stem-boring and with feeding from shelter. All these shifts for a living are common enough in the insect world. Each has its host of strict adherents, but there are border- line forms that combine two or more of these ways of getting on. Gall-making insects enter the leaf while its tissues are still in a formative state, and stimulate it to overgrowth and to remarkable secretory activity. They do not need to mine the tissues, for they possess the power to stimulate the plant to produce both food and shelter. From the walls of the gall chamber they lap up the food that the tissues prepare for them and bring to them. This is a wonderful power, but not all gall-making insects possess it to the degree that is sufficient to meet all the needs of their larval life. A number of them that are true gall-makers at first, have to resort to the use of their jaws in ordinary foraging when of a larger growth. The tulip-tree blister-gall maker, Thecodiplosis liriodendri, for example, at first makes a thick- walled discoid gall within the leaf, and later eats most of it 24 LEAF-MINING INSECTS away before completing its growth. The little caterpillar, Heliozela aesella, does likewise, in the leaves of grape. By the time it has finished its tenancy the walls of the gall are almost wholly consumed. The sawfly larva that makes the familiar "apple galls" on the leaves of willows when full grown and of larger appetite has to resort to the ordinary use of its jaws, as is evidenced by the large, irregular, frass- filled cavity3 that it then excavates. Fig. 12. Leaf of tulip tree, bearing six mined-out gall of the midge Thecodiplosis liriodendri. Stem-boring and bast-mining and leaf-mining are habits closely akin. Stem-boring probably came first since the 8 The case of the leaf-mining fly of the iris Agromyza laterella as detailed by Claassen (1918) is quite different, and quite unique. This larva is a true leaf-miner. WThen grown it bores down into the undeveloped iris bud to form a pupation chamber. The presence of the pupa there when growth starts in the spring, causes a gall to develop; but its development is quite incidental: it profits the fly nothing. GENERAL 25 greater thickness of stems requires less alteration of the ordinary larval form. i' i Fig. 13. A leaf-tyer of Southern California that is also a leaf-miner (undetermined). A, a spray of Baccharis viminea, bearing a leaf -tie; B, a single leaf detached, its upper portion mined above the entrance hole; C, the silken bag containing the larva, removed from the center of the tie. The surface of a stem when it is green and covered by a smooth and transparent epidermis, is not very different from that of a leaf. Some observations made by one of us 26 LEAF-MINING INSECTS (Mrs. Tothill) in Vancouver on the madrona leaf-miner, Marmara arbuticlla, indicate how easy is the passage from stem to leaves. In some cases the mining of a single larva is confined to a single leaf ; in some cases the larva does not enter a leaf at all but tunnels up and down under the cuticle of the shoot. In many cases, however, the mines either begin in the leaves and pass by way of the leaf petioles down under the epidermis of the shoots, or, beginning under the epidermis of the shoots pass up the petioles into the leaves. In a few cases the mine begins in one leaf and passes by way of the petiole into the shoot and then up another petiole into another leaf. The surface of green apples is some- times mined by another species of Marmara (M. pomonella, (fig. 4, pi. 2) ; and the phyllodia of prickly pears (species of Opuntia), by the larger larvae of the Phaloniid moth, Melitara prodenialis. In the chapter on Lepidoptera a number of examples will be cited4 of moth larvae that mine the blade of the leaf while very small, and the strong veins and stalk when older and larger. The natural cavities of seme leaves provide a home for certain unspecialized young larvae of Noctuidae.5 These cavities are soon outgrown. Feeding from shelter is often combined with leaf -mining, and in a variety of ways. A leaf-tyer of the southwestern United States, when it has fastened together with silk three or four leaves at the summit of the wandlike stem of Bac- charis viminea and has spun about itself a white silken bag in which to dwell, makes a hole in the upper end of the bag, where it is attached to a leaf, and eats through the epidermis of the leaf and then mines the leaf through this hole. It lives well up in the bag and deposits all its frass in a midden heap at the bottom. It reaches out of the holes at the top (one into each leaf that it mines) and feeds there without 4 See Phthorimaea operculella, p. 159; Acrocercops strigifinitella, p. 124. 5 See Arzama obliqua, p. 176. GENERAL 27 exposing itself. All the feeding is done from the holes up- ward, and full depth blotch mines are formed.6 The only alteration of such a habit that would be necessary to make a confirmed leaf-miner would be the abandonment of the bag. The leaf-sewer of the hog-peanut, Stilbosis tesquella, manages the matter a little differently. It draws one Fig. 14. Diagrams of the mining operations of the midge Chironomus braseniae. (After Leathers.) A, a leaf of watershield showing the tor- tuous mines in the upper surface; B, a bit from the forward end of one of these mines showing at c the pellets of frass held together with silk, that form the roof of the mine, lying between the elevated side strips d, of partially dissevered epidermis, and extending forward in a sort of porch upheld by a few silken stay lines, /. leaflet flat upon another and sews the two together with stitches of white silk placed about an eighth of an inch apart all about the edges where in contact. For further security it adds a few central stitches joining the stronger veins. 8 See further in this connection the accounts of Recurvaria piceaella, p. 165, and Argyresthia annetella, p. 171. 28 LEAF-MINING INSECTS Thereafter it feeds within the narrow space quite as do its leaf -mining relatives; it lies on its flattened back and feeds from the leaflet on the upper side, clearing away the mes- ophyll and leaving only the upper epidermis. (See fig. 41.) Conversely, the locust leaf-sewer, Gelechia pseudoacaciella, is said to invade the mines of other little moth larvae when young, later betaking itself to a home of its own between two leaflets sewed together. There is a little greenish-yellow midge, Chironomus braseniae, whose larva is a sort of leaf-miner. It trenches the upper surface of the floating leaves of the watershield, Brasenia schreberi, roofing over the trench with loosened epidermis and with frass, and it lives and feeds within the trench as in a mine. Apparently it does this only when well grown; for the trenches are all of about one diameter: they do not increase as do true linear mines with growth. Its earlier larval habits are still unknown. Its method differs from true leaf-minmg chiefly in that it cuts the epidermis as it goes. From the middle line of the trench it cuts this in narrow strips extending to the side margin, then it removes the thick palisade cells from beneath them. Then it elevates them at their free inner ends, like the strips of a slat roof, fills in the middle interspace with loose pellets of frass and binds all together with silk. Thus its trench is completely covered. At the end it makes a slight enlargement for a pupation chamber. When the adult midge emerges the empty pupal skin is left partly protruding. Many interesting details are given in Leathers' (1922) account of its work. There are in our Southern States little caterpillars of the genus Homaledra, that make covered trenches in the leaves of palmettos and excavate parenchyma from their trenches. There is one species for each surface of the leaf ; H. sabalella chooses the upper surface and lives gregariously in irregular runways that are sheltered under a roof of brownish frass GENERAL 29 pellets, webbed together with silk, and looking like old weather-stained sawdust. The other species, H. hep- tathalama, lives solitarily in a fold on the underside of the leaf, and makes for itself a fr ass-roofed, linear, seven-roomed house, of altogether unique character. From Busck's brief account of it we quote the following description: It begins by making a small, elongate chamber and adds, as it grows, successively larger, more or less rectangular, thick-walled, communicating rooms to its house, the entire length of which is 1 J to 2 inches, and which when finished contains 7 (or sometimes 8) chambers; hence the name of the insect. It pupates inside its case, and the moth issues through a round Fig. 15. The seven-chambered house (roofed-in mine) of Homaledra heptathalama on palmetto. (After Busck.) hole in the last chamber. This is different from the other cham- bers, being rather loosely built. The other chambers are very firm, smoothly finished outside, dark brown. The pupa is brown, very- slender, antennae and wing-cases reaching only halfway down the abdomen. Pupa skin is not protruded at issue. The genus Homaledra includes the two species of aberrant habits mentioned on page 28. Both occur on the palmetto. Both mine from shelter, but the one on the lower side of the leaf, H. heptathalama, is solitary, and the one on the upper side, H. sabalella, is gregarious. ENEMIES Like other animals, leaf -miners have both predacious and parasitic enemies, and as yet comparatively little is known 30 LEAF-MINING INSECTS about either. They are too small to be very attractive to the larger and more familiar animals, and too small to be readily observed by us when sought out and eaten, as doubt- less they are, by warblers, creepers and nuthatches. For- bush says that the beet leaf-miner is eaten by chipping sparrows. At Picton, Nova Scotia in 1908 there was a heavy infestation of birch leaves by sawfly that over winter in a circular silken hibernaculum within the leaves. Dr. Matheson found most of the hibernacula empty, with a small hole in one side, wherein, presumably, some bird had extracted the larvae. Many larvae are taken from their winter quarters by mice and shrews. When one sees a little red squirrel sitting among the fallen leaves under a red oak tree, tossing a handful of leaves and cocking his head on one side as if intently listening, it is easy to imagine that he is trying to catch the sound of a loose pupa of the beetle Brachys, tumbling about within its mine. Dr. Martin Hering in his comprehensive work on "the Ecology of leaf- mining Insects/ ' mentions inquilines and symbiotic dwellers namely; thrips, fungi, yeasts and bacteria, in the mines of these insects. Predaceous insects are rather more commonly observed. Webster and Parks (1913) record a species of mite (Ery- thraens sp.?) attacking the larvae, of Agromyza pusilla within the mines. One of us (Frost) has seen the bug, Nabis feras feeding on larvae of Pegomyia calyptrata, and Chrysopa rufilabris feeding on Agromyza jacunda. The Nabis has also been reported as an enemy of the beet leaf- miner. More is known concerning parasites because every one who tries to rear leaf-miners finds emerging in his cages plenty of these instead. In the beginning, the mine may have been a place of comparative security from parasites, but it is not so now. Once the parasites has learned how to effect an entrance, the miner is worse off than its free-living ancestor, having no means of escape. A very high percent- age of parasitism is the rule among leaf -miners. GENERAL 31 There is no existing list of the known parasites of leaf- miners, but one of us (Frost, '24: 131-132) has compiled a list of those known from Dipterous miners. This list of 67 species includes at least one secondary parasite. COLLECTING AND REARING LEAF-MINERS It is easy to collect leaf-mining larvae. All that is neces- sary is to gather the leaves and hull the insects out from their mines. A fine, curved-pointed pair of forceps is the most useful instrument for this, though a hook-pointed needle in a handle will do it almost as well. The larvae are best preserved in alcohol of about 80 per cent strength. Very soft larvae, like those of the Diptera, are better pre- served if first dropped for a minute in boiling water, before being put in the alcohol. Pupae that are formed in the mines, are obtained and preserved in like manner. But it is very difficult to find pupae in nature when formed outside the mines, and they are better obtained by rearing them. The best way to rear leaf-miners when they are common and near at hand is to let them rear themselves as far as possible : to keep watch on their progress and to gather the material when in the desired condition. The one rule for success in rearing any thing is to maintain natural condi- tions. Since this is rather hard to do in parched leaves, it is better to leave them on the stems whenever it is possible to watch them there until the larvae are full fed. Then they may be put in containers provided with proper con- ditions for formation of pupal cells — earth, trash, leaves or rough twigs in the bottom, according to the demands of the species; or if they pupate in the mines, then nothing at all besides the leaves containing them. The adult moths, beetles, etc., when they emerge are pinned and mounted by the methods well known to every entomol- ogist. Method of collecting Dipterous leaf-mines. For collecting 32 LEAF-MINING INSECTS Diptera, a round, seamless, tin box is used, a separate box for each host plant and for each of the different types of mine found on the same host plant. The proper records are placed in the respective boxes. As a rule, the leaves remain fresh in the boxes until the larvae have transformed. This method requires a large number of boxes, and there is a limit to the number that one can conveniently carry. There is a more compact method. The leaves containing the miners may be folded in tissue-paper triangles, much as many entomologists use for duplicate material. These small packages are then placed in a tin box. The box retains enough moisture to prevent the leaves from drying out, and leaves from many different plants may be placed in the same box without confusing the records. If the larvae transform before reaching the laboratory the pupar- ium will be found within the envelope with their records. Ordinarily the larvae are not yet mature when they reach the laboratory, and it is therefore necessary to allow them to continue to feed. Larvae that naturally leave the wilted leaves and enter the fresh ones are easy to rear, but those that do not go to the fresh leaves are more difficult. Often the leaves wither or decay before the larvae are full-grown. When the larvae transform they may be removed to small vials by means of a camel's-hair brush. The vials are then closed with cork stoppers in order to prevent evaporation during the short period of pupation. When a larva trans- forms within the leaf, the puparium is cut from the leaf and allowed to dry for a few hours before the cork stopper is placed in the vial. The pup aria are kept in these vials until the adults emerge. The adults should be kept alive for several days in order that they may attain their proper color, since teneral specimens are practically indetermin- able, especially among the Agromyzidae. Leaves bearing mines may be preserved as herbarium specimens, mounted on white cards, with the name of the family, the genus, and GENERAL 33 the species, of both the host plant and the insect mining the leaf. A thin sheet of celluloid may be placed over each of the mounts. Most of the herbarium specimens show very clearly the arrangement of the frass within the mines, the exit holes of the larvae, and other characters of interest. Photographs have the advantage of being more durable than the herbarium records, but they are far from being as accurate and as rich in minute details. Fig. 16. Diagram illustrating head form in two orders of leaf -mining larvae. A, a sawfly larva (Hymenoptera) ; B, a beetle larva (Coleoptera). How to identify leaf-miners. First collect them, and get the name of the plant on which you find them. Then look in the list on page 302 to see what insects are known as miners in the leaves of that species of plant and of others near akin to it; that is, in members of the same plant family. Among these you may find your specimens described; so note carefully the form and depth and spread of the mine, the presence and distribution or absence of holes, silk and frass, and the form and structure of the larva within it. The table on page 35 may then be used to determine the 34 LEAF-MINING INSECTS order to which the larva belongs, and among the members of this order that infest the leaves of this plant you may find your leaf -miner described. For final certainty of determina- tion it is always best to rear some adults from the larvae and have them named by a specialist in the group to which they belong. GENERAL 35 h C O H hi ft. On pro- thorax On meso- thorax On pro- thorax On pro- thorax O m 8 M Ph < K ^ o 2 ° 8 J n EH Ph Ph Ph a « c h S o n T3 T3 n ' « ° ° -i 5 M 02 03 M C rf> 03 03 03 +Z C *S s-. s-< »-i a •—> f-^ ft ft ft a * S O O > « » Q Q Q O £2 S « o o o *-> J£ > > x ft ft 03 =3 S d ^ fl t> a > « -tf C fl c fl 2 « ° O O O * » w o a a ^ STEM OF EPICRANIAL SUTURE 11 1 l| § g * ^ 2 fl ^ Ph < Ph < w to Eh Eh C £ ^1 -g-s ■§■§ | § E s s s 3 w o o ■»- *h T3 £ T3 03 o O • O a> ■- ^ S '3 ^ ^ S. ft a> *d o 7. 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