VOLUME 28, NUMBEH 3 269

PIERIS BRASSICAE L. ESTABLISHED IN CHILE; ANOTHER PALEARCTIC PEST CROSSES THE ATLANTIC ()

BHlAN O. C. GAHDINEH A.R.C. Unit of Invertebrate Chemistry & Physiology, Department of Zoology, Downing Street, Cambridge, England

In about 1860 rapae L. (the imported worm) was recorded from Canada (Seitz, 1924). It spread rapidly and already by 1870 was causing great damage to cruciferous truck crops from Montreal to New York and within a surprisingly short time had spread throughout the Union (Chittenden, 1905). In 1972 I received for identification some white from the region of Santiago, Chile. They are undoubtedly L., the large cabbage white , to give it its English vernacular name. The specimens were forwarded to me by fellow member J. H. Robert who had received them from Sf. Luis E. Pena who reports that they are now (1972) "flying around gardens in the vicinity of Santiago" which means the species is clearly established and was doubtless introduced some years ago. In view of the enormously rapid rate of spread of which Pieris species are so clearly capable it would seem desirable to give some details of it so that it can be immediately recognised and dealt with, if that be possible. Already grave concern is being expressed about an Mrican honeybee, Apis mellifera adansonii, which is sixteen years has spread virtually throughout the whole of South America and is heading fast toward the U.S. (Orsak, 1973). It would seem quite possible for P. brassicae to follow the same course, it is a noted migrant and just as fond of Cruciferae as is P. rapae; indeed its larvae will feed on plants of any family containing mustard oil glucosides. However, in the Canary Islands it is not a pest, the larvae feeding only on Tropaeoleum (Fernandez, 1955). The probability that it will now spread through South America appears to be a very real one, as Sf. Pena informed me in June 1973 that it is already widespread in all the Province of Valparaiso and adults are already flying in other provinces and the Cruciferae are being destroyed. It would seem desirable therefore to take the opportunity to give some account of the species, so that it can be looked out for; and at the same time to correct certain errors concerning it in the literature and put on record some new observations. P. brassicae differs 270 JOURNAL OF THE LEPIDOPTERISTS' SOCIETY

Fig. l. Typical eggbatch of P. hrassicae. quite markedly from other European members of the . There are some quite good reasons for considering that it should be separated off into another genus, and it is only the great confusion that this would cause that seems to have prevented this step from being irrevocably taken. Egg. Fig. 1 shows a batch of eggs and Fig. 2 eggs in situ on cabbage. They are laid in more or less regularly arranged batches which vary in size from a few eggs to a hundred or more, the number varying according to the age of the butterfly, with an average around 40-50. When first laid the eggs are a very pale straw color; within twenty four hours this has darkened to yellow and in at least one subspecies (P. h. cheiranthi Hueb) they are bright orange. Eggs from butterflies whose larvae have been reared on semi-synthetic diets not containing cabbage leaf powder, remain a very pale straw color, indeed may be almost white. A female is capable of producing 750 eggs during a full lifespan (David & Gardiner, 1962) but it is doubtful if the full number is ever produced under feral conditions. In very warm weather the eggs will hatch in 4-6 days but may well take 2-3 weeks in cold weather. A few hours before hatching the eggs turn black and the form of the can be seen through the shell. The first larvae to hatch turn round and often commence to eat the tops of the shells of the other VOLUME 28, NUMBER 3 271 larvae. In this fashion the hatch of a batch of eggs will take place over about 30 minutes. The young larvae consume the eggshells and then, en mass, spin a silken pad on which they rest when not feeding. Larva. Fullgrown larvae are shown in Fig. 3A. The larvae are gregarious throughout their life, unlike P. rapae and other "small white species" which are not only solitary, but cannabalistic, both to smaller brethren and, in particular, to their own eggs, which they eat and kill (unlike brassicae which merely eat the top of the shell and release the contained larva). They invariably have five and, depending on the temperature, the larval stage lasts from two to eight weeks. It has been erroneously stated by both Klots (1958) and more recently again by Wigglesworth (1972) that five ins tars only occur under cold conditions and that the number of ins tars falls to four and finally only three as the temperature of rearing increases. These statements are based on an observation of Klein (1932). Frohawk (1934), a careful recorder, who had the experience of rearing every species of British butterfly, considered only five instars, and David & Gardiner ( 1962a) proved conclusively that the number of instars is constant at five over the very wide range of environmental conditions at which rearing is possible, and further extensive rearing by the present author with various stocks and races of brassicae has subsequently confirmed this. The color of the larvae is virtually the same in all instars; blue­ grey or yellowish ground color, a yellow dorsal stripe and irregular and intricate black markings which are more intense the lower the temperature of development. The yellowish ground color is recessive to the blue-grey (David & Gardiner, 1962a) but appears to be so common in the wild that there must be some advantage in it. The larvae prefer to feed openly on the outside of the leaves. Fig. 3B shows an aggregate of mainly fourth larvae and Fig. 4 the remains of a garden cabbage plot. Chrysalis. These are formed in a similar fashion to those of P. rapae, that is to say suspended by a cremaster and a silken girdle. Also as in P. rapae similar situations are sought by the larvae in which to pupate. The color of the chrysalis is either a pale straw or a shade of green, with variable black markings, and in general the color is lighter or darker according to the background. It has been stated (Babers & Pratt, 1952) that the color is influenced by the illumination of the larva before pupation. As a result of numerous experiments and the rearing of more than one million larvae I have never found any evidence of this. I have, however, found conclusive evidence that diapausing chrysalids are much more inclined to be green in color than summer 272 JOURNAL OF THE LEPIDOPTERISTS' SOCIETY

Figs. 2-4. P. brassicae: 2, eggs in situ on cabbage leaf; 3A, fullgrown larvae on same plant; 3B, gregarious cluster of mainly fourth ins tar larvae; 4, devastated crop of in a garden plot. brood ones (Gardiner, in prep.). This was strikingly born out by the chrysalids I received from Chile, the straw-colored ones eclosed a few days after receipt; the green-colored ones are still unchanged after several weeks and therefore clearly in diapause. The pupal stage of summer brood specimens lasts 10 days in warm weather, but may be as long as 60 days if the weather is cold. If the has entered diapause then this stage will last for 6-8 months. Adult. In general appearance the adults of P. brassicae are similar to those of the imported P. rapae, but are quite distinctive and sexually dimorphic. In particular the black markings have a sharp cut-off from the white instead of the gradual fade-out from one to the other as in P. rapae and P. napi. Both sexes are white with a black apical spot. The female only, has two black distal spots and a black discal streak along the inner margin. Both sexes have two black dis cal spots on the underside. The underside of the hind wing tends to be very variable and may be yellow to orange (race cheiranthi); or pale straw, greenish, and at times almost black. Greenish and blackish forms are an over-all effect VOL UME 28, NUMBER 3 273 produced by a light to heavy sprinkling of black scales. Unlike other Pieris species the veins of the wings in brassicae are never heavily marked to give a rayed or chequered effect. In size brassicae is larger than all other United States Pieris with a wingspan of from 55-65 mm in certain bred examples (David & Gardiner, 1961), up to 63-76 mm in wild caught specimens (Frohawk, 1934). All other United States Pieris have a wingspan of under 50 mm (Chang, 1963). P. rapae crucivora from Japan are exceptionally large. Esaki & Yokoyama (1955) give the wingspan as 55 mm and I have bred specimens up to 60 mm. Fig. 5 shows one such bred specimen for comparison with brassicae. Since Esaki & Yokoyama use a different basis for their wingspan measurement than Chang (which gives a lesser figure), the actual size of P. r. crucivora comes out as the mean of the P. brassicae bred by David & Gardiner (1961). As in other Pieris the black coloring of the spring brood is much paler than in the summer broods. The Chilean examples have the typical upperside facies, but the hindwing underside is of the dark green form. This form certainly occurs in British, Spanish, German, and Maltese race wollastoni, and in East European brassicae, but an examination of my collection and of the extensive series in the room of the Cambridge University Museum of Zoology reveal that it is uncommon, the lighter forms being by far the more numerous. It does not therefore seem possible to pin down the exact origin of the Chilean P. brassicae. It has been suggested by Sr. Pena that they may have come from Eastern , there now being considerable trade between there and Chile. What is more certain is that the specimens are not of one of the numerous races of P. brassicae, which has distinct forms in certain parts of its range where it also appears to be non-migratory. Details of the distribution are given in Fig. 13. Three of the Chilean specimens are shown in Figs. 6,7,8. For com­ parison, a typical English pair (Figs. 9,10), the male English underside (Fig. 11), and the dark green form of a Spanish example (Fig. 12) are shown. The dark green color on the hindwing underside of the Chilean examples is interesting. This may well be due to adaptation to certain environmental factors which confers some advantage in a particular area. It has already been shown by Gardiner (1973) that the facies of brassicae can be changed by careful selective breeding, and the dark green and the yellow form of the hindwing underside are amongst the characters which can be so selected. The Cambridge stock of brassicae, as was maintained for so many years by David & Gardiner, 274 JOURNAL OF THE LEPIDOPTERISTS' SOCIETY

Figs. 5-12. Various imagoes for comparison: 5, P. rapae crucivora C( ex Japan; 6-12 P. brassicae: 6, 5 underside ex Chili; 7, C( upperside ex Chile; 8, 5 under­ side ex Chili; 9, C( upperside ex David & Gardiner's "Cambridge" stock; 10, 5 upperside ex "Cambridge" stock; 11, 5 underside ex "Cambridge" stuck; 12, 5 underside ex Spain. VOLUME 28, NUMBER 3 275

Fig. 13. Palearctic distribution of P. brassicae (within heavy line), and area in South America from which now recorded. has rather a light straw-colored underside and I have similar specimens in my collection from most areas of Europe and also from the North African litoral and near East. It will be interesting to hear in due course if all Chilean examples are of this dark green form or if the lighter colored ones are also to be found. The question of this underside coloration presents a good opportunity for some field research. Eastern European and Asiatic material is not so readily available but I have seen all types of underside from those areas. P. brassicae is a well known migrant. Although, due to destruction of former breeding areas, very vast swarms no longer occur, regular migration usually in a southerly and westerly direction still takes place. Return flight does not occur. The migrate within a day or two of emergence, the females often mated, but not yet with mature eggs, and are capable of traversing up to 250 miles, without food, in a few days. (For further details, see Johnson, 1969.) It can therefore readily be appreciated that, once a nucleus colony is established, a very rapid spread of the butterfly can take place. Diapause. P. brassicae has a facultative diapause controlled by the daylength on the larva (Way, Smith & Hopkins, 1949; David & Gardiner, 1962a). Consequently as long as the daylength is sixteen hours or longer, dawn to dusk, and the temperature averages above 100 C, there will be a continuous succession of broods, at least one every six weeks in very warm tropical weather. As soon as the daylength falls the pupae will enter diapause. All summer brood stages can withstand frost for 276 JOURNAL OF THE LEPIDOPTERISTS' SOCIETY

short periods and diapausing pupae can withstand severe and prolonged winter conditions. There is no doubt that the species must be considered very hardy. Parasites, predators and diseases. P. brassicae larvae are parasitized by a number of Apanteles species, in particular A. glomeratus L., which is known to attack P. rapae in the United States (Blunck, 1957). The pupa is also parasitised by Pteromalus puparum L., which is believed to have been imported into the States at the same time as P. rapae which it also attacks (Chittenden, 1905). Both larvae and adults are also predated by social . The only avian predator which has been observed eating the very distasteful larvae is the European thrush, Turdus musicus L. Flying adults are sometimes attacked but appear to be rarely eaten by birds, although mice (Mus musculus L.) will eat the bodies. The pupae, however, are eaten in considerable numbers (Moss, 1933). Eggs do not seem to be attacked by any parasite or predator and even larvae of its own kind have been observed by me to eat carefully round eggbatches without doing them any damage. Various potential parasites already present in the Nearctic region, notably A. rubecula, which helps to control P. rapae and could also attack P. brassicae, have recently been surveyed by Blunck (1957) and Wilkinson ( 1966). Various species of ant have been observed in England to carry off and consume the young larvae. Microsporidian parasites are recorded from Europe (but not England), but Blunck (1957) could not find these in the United States. P. brassicae is certainly susceptible to many of the usual commercial insecticides and also to Bacillus thuringiensis. From time to time the larvae and pupae succumb to an undescribed bacteria, but it is my experience that they are far less susceptible in this respect than many other species of . However, they are very susceptible indeed to a granulosis virus disease. Although the virus might be the better method of control, it is not yet commercially available, although B. thuringiensis is. (For data on these two possible control agents, see Burges & Hussey, 1971.) Although certainly susceptible to many in­ secticides, brassicae is difficult to eradicate and its present-day cessation as a major pest in large parts of the palearctic region is due in my view not so much to control measures as such, but to changed agricultural practices and, above all, to the bringing into other uses of enormous areas of its former wild breeding areas with consequent wholesale destruction of its foodplants in these areas. The enormous migrations recorded fifty and more years ago no longer occur. VOLUME 28, NUMBER 3 277

ACKNOWLEDGMENTS I am indebted to Sr. J. H. Robert of Alicante, Spain for forwarding to me the original Chilean specimens and for Spanish examples of P. brassicae; to Sr. Luis E. Pena of Santiago, Chili for subsequent live material and information from Chili; to Hr. Hermann Wilde of Darmstadt, Germany for Fig. 4 and to Mr. G. H. Runnalls and Miss Yvonne R. Carter of this Department for photographic help.

LITERATURE CITED BABERS, F. H. & J. J. PRATT. 1952. Life Processes of Insects. In, The Yearbook of Agriculture 1952. [Ed. A. Stefferud]. Washington, D.C. BLUNCK, H. 1957. (L.), its parasites and predators in Canada and the United States. J. Econ. Entomol. 50: 835-836. BURGES, H. D. & N. W. HUSSEY. 1971. Microbial Control of Insects and Mites. Academic Press, London & New York. CHANG, V. C. S. 1963. Quantitative analysis of certain wing and genitalia characters of Pieris in Western North America. J. Res. Lepid. 2: 97-125. CHITTENDEN, F. H. 1905. The imported cabbage worm. USDA. Bureau Entomol., Circular No. 60. 8 p. DAVID, W. A. L. & B. O. C. GARDINER. 1961. The mating behaviour of Pieris brassicae (L.) in a laboratory culture. Bull. Entomol. Res. 52: 263-280. --- & ---. 1962. Oviposition and the hatching of the eggs of Pieris brassicae (L.) in a laboratory culture. Bull. Entomol. Res. 53: 91-109. --- & ---. 1962a. Observations on the larvae and pupae of Pieris brassicae ( L.) in a laboratory culture. Bull. Entomol. Res. 53: 417-436. ESAKI, R. & M. YOKOYAMA. 1955. Coloured Illustrations of the Butter- of Japan. Hoikusha, Osaka. FERNANDEZ, J. M. 1955. Evolucion de la fauna Canariense. Instituto de Estudios Canarios. Teneriffe. FROHAWK, F. W. 1934. The Complete Book of British Butterflies. Ward, Lock, London. GARDINER, B. O. C. 1973. Gynandromorphism in Pieris brassicae L. J. Res. Lcpid. 11: 129-140. JOHNSON, C. G. 1969. Migration and Dispersal of Insects by Flight. Methuen, London. KLEIN, H. Z. 1932. Studien zur 6kologie und Epidemiologie der Kohlweisslinge. 1. Der Einfluss de Temperatnr und Luftfeuchtigkeit auf Entwicklung und Mortalitat von Pieris brassicae L. Z. Angew. Entol11ol. 19: 395-448. Moss, J. E. 1933. The natural control of the cabbage caterpillars, Pieris spp. J. Anim. Ecol. 2: 210-23l. ORSAK, L. 1973. A threat to the bee industry. TIEG Newsletter 7: 22-24. SEITZ, A. 1924. The Macrolepidoptera of the World. 5. Alfred Kernan Verlag, Stuttgart. WAY, M. J., B. A. HOPKINS & P. M. SMITH. 1949 Photoperiodism and diapause in insects. Nature 164: 615. WIGGLESWORTH, V. B. 1972. The Principles of Insect Physiology. Chapman & Hall, London. WILKINSON, A. T. S. 1966. Apanteles rubecttla, Marsh, and other parasites of Pieris rapae in British Columbia. J. Econ. Entomol. 59: 1012-1013.