THE POPULATION BIOLOGY OF THE , EUPHYDRYAS EDITHA. VIII. OVIPOSITION AND ITS RELATION TO PATTERNS OF OVIPOSITION IN OTHER BUTTERFLIESl

PATRICIA A. LABINE Biomedical Data Processing Training Program, School of Public Health, The University of Michigan, Ann Arbor, Michigan

Received December 15, 1967

This paper is one of a continuing series Similar data obtained from the literature investigating the population biology of and from personal communications for three Euphydryas editha (: Nym­ other , oetus, phalinae). The life history and general eurytheme, and Heliconius erato, are pre­ biology of this butterfly have been de­ sented in Figures 1b, Ic, and Id, The size scribed in preceding papers that have dealt of each butterfly and the size of its egg are with aspects of its ecology, phenetics, and illustrated in the figures. reproductive biology (Labine, 1964; Ehr­ An estimate of the total number of eggs lich, 1965; Ehrlich and Mason, 1966; expected per female under laboratory con­ Labine, 1966a; Mason, Ehrlich, and Em­ ditions was calculated as the sum of the mel, 1967, 1968; Johnson, Keith, and Ehr­ average number of eggs produced by fe­ lich, 1968). males of age x, weighted by the proportion The present paper is concerned with ovi­ of adult females surviving to age x. This position and its ecological consequences. measure is somewhat analogous to the net "Oviposition" is used here in a broad sense reproductive rate, R o, usually calculated and is meant to include oviposition behav­ from life table data, however, in our case ior, egg number, egg size, rate of oviposi­ only adult mortality is considered, and we tion, etc. Attempts to interpret the ovi­ are concerned with the total number of position pattern of Euphydryas editha led eggs, not just female eggs. These estimates to comparisons with what is known of ovi­ are also noted in the figures. The value for position patterns in other butterflies. Heliconius was not calculated, but taken directly from Crane (1955). OVIPOSITION IN THE LABORATORY Methods used in maintaining oviposit­ OVIPOSITION IN NATURAL POPULATIONS ing Euphydryas editha females in the lab­ Eleven complete oviposition sequences of oratory have been described elsewhere wild Euphydryas editha females were ob­ (Labine, 1966a). The butterflies used in served in the Woodside population. One this study were collected as late instar lar­ behavior pattern was consistently seen. vae from the population in Woodside, Cali­ The female would land in the ground cover, fornia. Survival and fecundity values com­ which in most parts of the colony was less piled from 53 females are presented in than 6 inches high and consisted predomi­ Table 1. nantly of the larval foodplant Plantago erecta. She would then "search" for a 1 This work was supported in part by USPHS variable period of time, crawling through Training Grants No. 5T1 GM 892-06, and 5T01 the ground cover, her wings slowly clapping GM 00365-05, and Grants GM-1430 and GB-5645 together. Oviposition would begin once the from the National Science Foundation. Present address: Dept. Biology, Williams College, Wil­ female settled quietly and folded her wings. liamstown, Mass. The sequence was always terminated by

EVOLUTION 22: 799-805. December, 1968 799 800 PATRICIA A. LABINE

the female flying off abruptly. Mean dura­ a. Euphydryas editha (No53") tion (±S.E.) of oviposition, starting from III the time the female initially landed on the 8-(98 ...... LL . Il g ground, was 29.7 ± 2.8 min. o " ... Eggs were laid in clusters. In five in­ ~ \. ca stances the eggs were not placed on the L: \ .. foodplant, but on unidentified seedlings ~:iS . o Ig w \ near Plantago plants. The mean size of ~ eight clusters that were counted was 45.2 a:: \... ~ ± 6.1 eggs (range: 75 to 21 eggs). This . value is likely to be an underestimation of °0 10 20 30 DAYS the true mean cluster size of Euphydryas editha. Females in the laboratory laid the b. (N::40U') 9 largest clusters on the first few days of ~ S I~ 8 oviposition. The above field observations, with one exception, occurred late in the ~ . adult flight season which lasts approxi­ ~ <, mately one month, and probably did not g include the first large clutches of females. Oviposition sequences were observed on the 111 \-\2~ EGGS following days, counting as day 1 the date i PER FEMALE of the first appearance of adults in the ..... colony for that year: day 3, 20, 21, 21, 20 DAYS 24, 28, 28, 28. c. DISCUSSION (N=34rj~) (98III ...... The data presented above suggest that 8 - , .. there are at least five components of varia­ lL. •••.. \ o ... tion in oviposition patterns of butterflies.

(fl wcr.f1 ...... c 1) Number of eggs laid} ~ II . ~ - Reproductive ~:iS h~ 1')$ \ z Gl 2) Egg size effort ~ 704 \ Distribution cr EGGS ". ~ • PER FEMALE . 3) Onset of oviposition of reproduc- 4) Rate of oviposition - tive effort 5) Cluster size ) over space DAYS and time .d. Heliconius erato ~ (Curves approximate)

~S I~ 8 FIG. 1. Survivorship and fecundity curves for laboratory populations. Dotted line = survivor­ b "ifl ship; solid line = fecundity. The scale of the drawings is indicated, and is the same for all fig­ ures. (a) Butterfly figure from Wright (1905); egg size, personal observation. (b) Data and egg ,~~ O',~'-"-". size from Thomas Emmel (pers. comm.); butter­ !. "i fly figure from Seitz (1924). (c) Data from Stern ~ PER FEMALE and Smith (1960) and Ray F. Smith (pers. comm.); butterfly figure from Wright (1905); egg size from Edwards (1884) and Comstock (1927). (d) Data from Crane (1955); egg size from Beebe et aI. (1960); butterfly figure is an approxima­ tion. OVIPOSITION PATTERNS OF EUPHYDRYAS EDITHA 801

TABLE 1. Survival and fecundity data compiled Callas philodice, making the taxonomic from 53 adult Euphydyras editha under laboratory status of some individuals uncertain. In conditions. Survival value at day x is the propor- tion of adult females surviving to age x. Fecundity the cooler areas of California, the source of value at day x is the average number of eggs pro- the butterflies used for the oviposition duced by a female of age x. data, the winter is passed by a dormant larval phase. In warmer areas Colias Day Survival Fecundity Day Survival Fecundity eurytheme has continuous generations. 1 1.00 71.8 17 0.55 13.4 Cercyonis oetus (Nymphalidae: Satyr­ 2 1.00 108.6 18 0.55 7.2 inae) is part of a large, highly variable 3 0.96 73.6 19 0.51 4.4 group of butterflies with uncertain taxo­ 4 0.96 101.4 20 0.45 3.8 5 0.94 62.0 21 0.30 6.9 nomic delineations. Cercyonis oetus ranges 6 0.94 63.3 22 0.25 2.2 from the Pacific coast to the eastern edge 7 0.91 53.0 23 0.17 2.7 of the Rockies. In Colorado, where the 8 0.91 38.7 24 0.15 2.1 material used for the oviposition data was 9 0.91 46.1 25 0.11 0 10 0.91 30.9 26 0.09 0 collected, it is a common butterfly of dry 11 0.91 30.6 27 0.09 0 open grasslands (Brown, Eff, and Rotger, 12 0.87 18.6 28 0.06 2.0 1957). It is univoltine; the larvae begin 13 0.83 26.3 29 0.04 0 winter diapause immediately upon hatch­ 14 0.72 16.1 30 0.02 0 15 0.68 14.3 31 0.02 0 ing. The larval foodplants are grasses. 16 0.64 9.5 32 0 0 Number of Eggs Laid Euphydryas editha lays the largest num­ Each component will be discussed in ber of eggs (731 per female) of the four turn, with attempts to demarcate the range butterflies compared in the figures, although of variation within the butterfly group, to females of Colias eurytheme are within the locate the position of Euphydryas editha same range with an expected number of within this range, and, where such discus­ 704. Some E. editha females lay as many sion may be profitable, to establish pos­ as 1200 eggs. This is the largest number sible life history and ecological correlates reported for any butterfly. One of the low­ of each component. est reproductive rates among butterflies is A brief description of the three other that of the tropical Heliconius erato, Fig­ represented in the figures will be ure 1d, which lays only about 24 eggs per helpful in comparisons of oviposition pat­ female. terns. A reproductive rate as large as that of Heliconius erato (Nymphalidae: Nym­ E. editha allows an impressive power of phalinae) is a neotropical butterfly show­ increase. A few calculations quickly dem­ ing great geographic variation (Emsley, onstrate this. Assume that 90% larval 1964). The data used in this paper relate mortality is to be expected in natural pop­ to the Trinidad form. H. erato is conspic­ ulations, that there is a 1 : 1 sex ratio, and uously colored and has been shown to be further assume that a single mated female unpalatable to predators (Brower, Brower, founds a colony in a suitable area. In just and Collins, 1963). It is restrictive in its the second season after this single found­ choice of larval foodplants, being associated ing event the population would have an only with species of Passijlora. expected size of over 2600 adults (2' Colias eurytheme ( : ), [(731/2) . 0.10]2 = 2672). the butterfly, is now common over A high rate of increase is an important most of North America, although it was part of a good strategy for colonization; once restricted to the western portion. It so is a strong cohesiveness of the popula­ has become an economic in some areas. tion (MacArthur and Wilson, 1967). Re­ It hybridizes over most of its range with markable inter-colony cohesion has been 802 PATRICIA A. LABINE

TABLE 2. Egg sizes and total egg-mass produced. fibrous food plant may require that the mandibles of the larvae be of a certain size Egg size Eggs per Total egg (mms) female mass (mms) and strength, or a newly hatched larvae may have to be of a certain size to survive Euphydryas editha 0.17 731.0 124.3 Cercyonis oetus 0.52 111.4 57.9 winter diapause. More information is Colias eurytheme 0.04 704.0 28.2 needed to discuss the conditions determin­ Heliconius erato 0.80 ,.., 24 19.2 ing egg sizes in butterflies. An investiga­ tion is in progress surveying variability of egg sizes and their distribution over food­ demonstrated for E. editha (Ehrlich, 1961). plant and life history types. Both this characteristic, and its high rate One also needs more information to dis­ of increase could relate to the fact that E. cuss determinants of reproductive effort. editha's habitat in the San Francisco Bay This area is one of active controversy (e.g., area is essentially insular, consisting of Skutch, 1967); however, there are certain widely spread "islands" of serpentine out­ simplifications in butterflies that should croppings. make the problem easier to attack. Since Egg Size adults function mainly on reserves from Egg sizes (volumes) of the four species feeding in the larval phase, the determin­ compared were calculated by geometric ap­ ing factors are best sought in the larval proximations. These values are presented biology. The amount of time allotted to in Table 2. Among the values of the four larval feeding (by life history pattern, by species, the egg of E. editha occupies the environmental conditions, etc.), the effi­ second smallest position. The total range ciency of larval feeding, and the availabil­ of variation among the eggs of these but­ ity of the foodplant must be significant terflies which have approximately the same determinants of the amount of energy ex­ body size is very large; a factor of 20 sepa­ pended on reproduction. rates the largest from the smallest egg. The product of egg size and egg number Time of Initiatitm and Rate of Oviposition gives the volume of the egg mass expected Females of Euphydryas editha emerge as per female, and this can be taken as an heavy-bodied adults (they weigh about estimate of reproductive effort. This is a twice as much as newly emerged males) reasonable approximation with butterflies, with large numbers of eggs already ma­ although for showing parental care, ture in their oviducts. The mean number the size of the egg mass must bear little re­ (±S.E.) of eggs present in one oviduct­ lation to the total cost of reproduction. there are eight oviducts in all-in 58 newly One advantage of a small egg is obvious emerged females was 140.9 ± 18.5. Of by comparison of the values of reproduc­ these, 25.1 ± 1.4 were fully mature eggs, tive efforts in Table 2. Because of the size judging by size and appearance. In other of its egg, Colias eurytheme attains a high words, an average of 200 eggs out of a po­ reproductive rate (704 eggs per female) tential complement of approximately 1100 with a very small reproductive effort (28.2 eggs are mature and ready for fertilization mm"). A similar reproductive rate in and oviposition when the female emerges. Euphydryas editha is produced with an ef­ A necessary correlate of this pattern of egg fort of 124.3 mm", maturation is an oviposition curve in which Continual selection of genotypes leaving the greatest reproductive emphasis is placed the greatest number of offspring should re­ upon the first few days of a female's life. duce egg size to some point where the ad­ Colias eurytheme, over its adult life span, vantage of a high reproductive rate is bal­ lays a total number of eggs similar to anced by the disadvantages of a small egg Euphydryas editha, but it emerges with all and small hatching larvae. For example, a its eggs still immature, and several days OVIPOSITION PATTERNS OF EUPHYDRYAS EDITHA 803 must pass before oviposition can begin oviposition patterns similar to Euphydryas (Stern and Smith, 1960). Its oviposition editha, with the emerged females heavy curve is very different from that of Euphy­ with eggs and restricted in mobility; but dryas editha (d. Figs. la and lc). Follow­ their efficient assembling devices eliminate ing the preoviposition period, the oviposi­ any concomitant dependency upon high tion rate rapidly builds to a maximum and population densities for mate discovery. is maintained at this level for over a week. It is still difficult to explain why some The oviposition curve of Cercyonis oetus butterflies, e.g., Heliconius erato, wait more (Fig. Ib), although reduced in magnitude, than just a few days before beginning ovi­ is similar to that of Colias eurytheme, and position. An interesting hypothesis is that presumably reflects a similar pattern of for these species, feeding by the adult may egg maturation. be necessary to furnish energy for egg pro­ There is little additional information in duction. Unlike the situation in Euphy­ the literature on the timing of oviposition dryas editha and similar species, larval in butterflies. Magnus (1953) reports that feeding in these butterflies may not pro­ for Argynnis paphia, an Old World fritil­ vide the full cost of reproduction. This lary, 8 to 10 days are required for a female may relate to a limited supply of suitable to mature before she will mate. Oviposition larval foodplant, or to a foodplant of lim­ then begins a day or so later (Magnus, ited nutritional value. It may be the re­ 1950). The white admiral, Limenitis ca­ sult of a short larval period, shortened in milla, mates soon after emergence, but ovi­ response to heavy larval mortality by forces position is delayed 3 days (Lederer, 1960). to which other phases of the life history Immediate oviposition after emergence are immune. does have important advantages, although Cluster Size it is obviously not universally used by but­ terflies. There are certain ancillary condi­ Euphydryas editha lays its eggs in large tions to the oviposition pattern of Euphy­ clusters. Three other Euphydryas species, dryas editha which may suggest why more E. phaeton (Clark, 1928), E. aurinia (Ford, butterflies do not exploit these advantages. 1962), and E. chalcedona (personal obser­ The newly emerged Euphydryas editha fe­ vation) also lay eggs in clusters of 50 or male is heavy with eggs, and hence her par­ more. ticipation in any search for mates is re­ Most butterflies, however, deposit their stricted. Yet the female must mate soon eggs singly. This is true for Colias eury­ after emergence if there is to be any ad­ theme (Stern and Smith, 1960), Heliconius vantage gained by the early maturation of erato (Beebe et al., 1960), and probably large numbers of eggs. Most matings in also true for Cercyonis oetus. Of all the Euphydryas editha are initiated by males British butterflies (about 60 species ex­ that sight females as they rest in the cluding skippers), Ford (1962) reports that ground cover (Labine, 1966b). This means only nine oviposit eggs in large clusters. of mate discovery suffices only because E. Seven of these are Nymphalids: Melitaea editha maintains localized populations of cinxia, M. athalia, Euphydryas aurina, high density in which the probability of Nymphalis antiopa, N. io, N. polychloros, any female being discovered is quite high. and Aglais urticae. Two are Pierids: Pieris For butterflies not restricted to dense lo­ brassicae and Aporia crataegi. Two other calized colonies, a more active role by the British species lay eggs in clusters of 5 to female must be required to bring about 15: one Lycaenid, Hamearis lucina, and mate encounters, and this probably pro­ one Pierid, Pieris rapae. Clark and Dick­ hibits a heavy female laden with already son (1952) have described the life histories mature eggs. of 38 South African species and report that It is interesting that many moths have of these only two oviposit in clusters: 804 PATRICIA A. LABINE

Acraea horta (Nymphalidae) and Belenois SUMMARY aurota (Pieridae). The oviposition pattern of Euphydryas A preliminary survey of the literature editha is described and compared with the has found reference to 10 other butterflies oviposition patterns of Cercyonis oetus, which oviposit in clusters of several eggs or Colias eurytheme, and Heliconius erato. more. Eight are Nymphalids: Chlosyne Five components of variation in the ovi­ (Melitaea) harrisii (Dethier, 1959), C. position patterns of butterflies are dis­ hoffmanni (Newcomer, 1967), Asterocampa cussed: (1) Number of eggs laid, (2) Egg celtis (Scudder, 1889), , Heli­ size, (3) Onset of oviposition, (4) Rate of conius doris, H. wallacei, H. sara, H. ricini oviposition, (5) Cluster size. Ecological (Beebe et aI., 1960). Two are Lycaenids: and life history correlates of these com­ Eumaeus debora, E. minyas (Ross, 1964). ponents are suggested. Is there any pattern in the tendency to cluster eggs at one oviposition site? There LITERATURE CITED seems to be at least a taxonomic regularity. BEEBE, W., J. CRANE, AND H. FLEMING. 1960. A The subfamily Nymphalinae is dispropor­ comparison of eggs, larvae, and pupae in four­ tionately represented among butterflies that teen species of Heliconiine butterflies from cluster their eggs. Of the 26 species listed Trinidad, W. I. Zoologica 45:111-154. above, 18 are members of this subfamily. BROWER, L. P., J. VZ. BROWER, AND C. T. COL­ LINS. 1963. Experimental studies of mimicry. Most instances of egg clustering seem to 7. Relative palatability and Mullerian mim­ be associated with the type of larval de­ icry among neotropical butterflies of the sub­ fenses against predators that can be inten­ family . Zoologica 48:65-84. sified by aggregations of larvae. These in­ BROWN, F. M., D. En, AND B. ROTGER. 1957. clude spinning a sheltering web, emitting Colorado butterflies. Denver Museum of Natural History, Denver, Colo. offensive odors, showing warning patterns, CLARK, A. H. 1928. Notes on the melitaeid but­ etc. (see Ford, 1962:89). terfly, Euphydryas phaeton with a description The Euphydryas species E. editha, E. of a new and a new variety. U. S. aurinia, and E. phaeton, spin communal Nat. Hist. Mus. Proc. 71 (Article 11). CLARK, G. C., AND C. G. C. DICKSON. 1952. Some larval webs. The webs of the early instars South African butterflies. Longmans Green of E. editha are much more evident in and Co., Cape Town. laboratory broods than in the field; how­ COMSTOCK, J. A. 1927. Butterflies of California. ever, the latter two species build very struc­ Published by the author, Los Angeles, Califor­ tured webs in nature. In addition, the lar­ nia. CRANE, J. 1955. Imaginal behavior of a Trini­ vae of all three species show a synchronized dad butterfly, Heliconius erato hydara Hewit­ behavior pattern when disturbed. They son, with special reference to the social use of will stop and together snap their heads up color. Zoologica 40:167-196. several times in succession. Edwards (Vol. CROW, J. F., AND N. E. Morton. 1955. Measure­ II, 1884) has observed this behavior elic­ ments of gene frequency in small populations. Evolution 9:202-214. ited in E. phaeton by an ichneumon para­ DETHIER, V. G. 1959. Food-plant distribution site. In populations of E. editha, braconid and density and larval dispersal as factors af­ parasites can cause heavy larval mortality fecting populations. Canadian Entomol­ (Ehrlich, 1965). ogist 91:581-596. EDWARDS, W. H. 1884. The butterflies of North It is interesting to note that clustering America. Houghton, Mifflin and Co., Boston. of eggs will result in a tendency for the EHRLICH, P. R. 1961. Intrinsic barriers to dis­ young to die or survive together as a brood. persal in checkerspot butterfly. Science 134: This will increase the variance of the num­ 108-109. ber of surviving offspring per female and --. 1965. Population biology of the butterfly, Euphydryas editha. II. Structure of the Jasper this in turn can considerably reduce N 6, the Ridge Colony. Evolution 19:327-336. effective population size (Crow and Mor­ EHRLICH, P. R., AND L. G. MASON. 1966. Popu­ ton, 1955). lation biology of the butterfly, Euphydryas OVIPOSITION PATTERNS OF EUPHYDRYAS EDITHA 805

editha. III. Selection and the phenetics of the --. 1953. Methodik und Ergebnisse einer Pop­ Jasper Ridge Colony. Evolution 20:165-173. ulationsmarkierung des Kaisermantels. Verh. EMSLEY, M. G. 1964. The geographical distri­ dtsh. Entomol. 1953:187-197. bution of the color-pattern components of MASON, L. G., P. R. EHRLICH, AND T. C. EMMEL. Heliconius erato and Heliconius melpomene 1967. The population biology of the butter­ with genetical evidence for the systematic re­ fly, Euphydryas editha. V. Character clusters lationship between the two species. Zoologica and asymmetry. Evolution 21:85-91. 49:245-286. --. 1968. The population biology of the but­ FORD, E. B. 1962. Butterflies. Collins, London. terfly, Euphydryas editha. VI. Phenetics of JOHNSON, M., A. KEITH, AND P. R. EHRLICH. the Jasper Ridge Colony, 1965-1966. Evolu­ 1968. Population biology of the butterfly tion 22:46-54. Euphydryas editha. VII. Has E. editha evolved NEWCOMER, E. J. 1967. Early stages of Chlo­ a serpentine race? Evolution 22:422-423. syne hollmanni manchada (Nymphalidae). J. LABINE, P. A. 1964. Population biology of the Lepid. Soc. 21:71-73. butterfly, Euphydryas editha. I. Barriers to Ross, G. N. 1964. Life history studies on multiple inseminations. Evolution 18:335-336. Mexican butterflies. III. Nine Rhopalocera --. 1966a. Population biology of the butter­ from Ocotal Chico, Veracruz. J. Res. Lepid. fly, Euphydryas editha. IV. Sperm prece­ 3:207-229. dence-a preliminary report. Evolution 20: SCUDDER, S. H. 1889. The butterflies of the east­ 580-586. ern United States and Canada with special --. 1966b. The reproductive biology of the reference to New England. Cambridge, Mass. checkerspot butterfly, Euphydryas editha. Ph.D. SEITZ, A. 1924. The American Rhopalocera. Al­ Thesis, Stanford University. fred Kernen, Stuttgart. LEDERER, G. 1960. Verhaltensweisen der Imag­ SKUTCH, A. F. 1967. Adaptive limitation of the ines und der Entwicklungsstadien von reproductive rate of birds. Ibis 109:579-599. Limenitis camilla camiUa L. (Lep., Nym­ STERN, V. M., AND R. F. SMITH. 1960. Factors phalidae). Zeit. fur Tierpsych. 17:521-546. affecting egg production and oviposition in MACARTHUR, R. H., AND E. O. WILSON. 1967. The theory of island biogeography. Princeton populations of eurytheme University Press, Princeton. Boisduval (: Pieridae). Hilgardia MAGNUS, D. 1950. Beobachtungen zur Balz und 29:411-454. Eiablage des Kaisermantels Argynnis paphia L. WRIGHT, W. G. 1905. Butterflies of the West (Lep., Nymphalidae). Zeit. fur Tierpsych. 7: Coast of the United States. Whitaker and Ray 435-449. Co., San Francisco.