Arthur M. Shapiro.
Non-diapause overwintering by Pieris rapae (Lepidoptera: Pieridae) and Papilio zelicaon (Lepidoptera: Papilionidae) in California: adaptiveness of type III diapause-induction curves.
Psyche 91:161-170, 1984.

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NON-DIAPAUSE OVERWINTERING BY PIERIS RAPAE (LEPIDOPTERA: PIERIDAE) AND PAPILIO ZELICAON (LEPIDOPTERA: PAPILIONIDAE) IN CALIFORNIA: ADAPTIVENESS OF TYPE I11 DIAPAUSE-INDUCTION CURVES*
Department of Zoology,
University of California,
Davis, California 956 16
Diapause is generally regarded as a physiological adaptation which increases the probability of surviving the adverse season, and thus of reproducing after it is over. Many insect species show geographic differences in the environmental regimes which induce or inhibit diapause (e.g., critical photoperiod) and in the strength of the diapause induced. Such interpopulational differences are com- monly viewed as "fine tuning" to local climates, accomplished by natural selection and reflecting a genetic basis (e.g., Istock, 1981). Intrapopulational differences in photoperiodic sensitivity and dia- pause strength (e.g., chilling requirement) also occur, and have been interpreted as polymorphisms which "spread the risk" of environ- mental uncertainty over the population (cf. Bradshaw 1973, Shapiro 1979, 1980a). In multivoltine insects in seasonal climates, offspring produced by the last seasonal generation of adults are commonly induced to enter diapause by specific combinations of environ- mental factors; in mid-latitudes these are likely to be decreasing photophase/increasing scotophase and decreasing or consistently low night temperatures. Warmer nights tend to shorten the critical photoperiod for a given population, or may effectively inhibit diapause altogether under field conditions. Beck (1980) characterized diapause induction as falling into four response types. Type I is the common long-day response, in which long days inhibit diapause and there is a single threshold beyond which diapause occurs. Type 11, the short-day response, is the reciprocal of Type I. Type I11 has two well-defined critical day- lengths, such that diapause is induced between, say, 8 and 14 hours *Manuscript received by the editor April 15, 1984.



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Psyche
[Vol. 91
light, and inhibited when either less than 8 or more than 14 hr of light occur. Type IV is its reciprocal, in which diapause is inhibited over a relatively narrow range and induced both above and below. Of the four types, Type I is by far the commonest in temperate- latitude insects and Type IV the rarest. Low-latitude insects have rarely been examined for photoperiodic responses, though the different patterns of seasonality in low latitudes might be expected to produce a rather different picture than that seen in temperate zones.
Type I11 curves are known from a variety of insects. Among Lepidopterans, two important species that show them are the European Corn Borer, Ostrinia nubilalis (Hbn.) (Beck, 1962) and the Large White, Pieris brassicae L. (Danilevskii, 1961). The adaptive significance of the short-day threshold is unclear. Nor- mally the entire population would have been induced by day-length- temperature interaction to enter diapause before the inhibition threshold was reached. Thus, the photosensitive stages would never be exposed to such short photoperiods in nature, and the existence of a short-day threshold would seem nonadaptive. This paper reports a situation in which Type 111 curves were demonstrably adaptive for two multivoltine Lepidopterans in nature. Papilio zelicaon Lucas and Pieris rapae L. are very common, widespread multivoltine butterflies in lowland California. Both have been monitored phenologically for up to 13 yr along a transect parallel to Interstate Highway 80 from sea level at the Suisun Marsh, Solano County, to treeline in the Sierra Nevada. We are concerned here with the phenology of populations at low elevations between the San Francisco Bay area and Sacramento. The flight seasons for both species may reach ten months (Table I), with four (P. zelicaon) to about six (P. rapae) generations per year. Both species have facultative pupal diapause under conventional photo- period-temperature control (Sims, 1980; Shapiro, unpublished data); both have Type 111 diapause-induction curves. Diapause is ir- reversibly determined no later than the fourth instar. P. zelicaon is the stronger diapauser and is unrecorded at any of our sampling sites between 1 December and 18 February. In some years the period with no rapae flying may, however, be as short as four weeks.



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Shapiro - Pieris rapae




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Psyche [vo~. 91
In contrast, the Pierid Colias eurytheme Bdv., which overwinters as a quiescent (non-diapausing) larva, flew continuously during the drought years of 1975-76 and 1976-77 and nearly so in 1983-84. Collections of mature larvae of both P. zelicaon and P. rapae made in late October and November over 12 yr have consistently given from 85-100% diapause pupae. Larvae of P. zelicaon are normally absent from all sites by the third week of November. Rapae larvae are occasionally found on garden cabbages and weedy Crucifers into early January. A fifth-instar larva was collected on a weed on 29 January 1979.
The winter of 1982-83 produced 200% or more of normal rainfall over most of northern and central California. Nearly 20 cm of rain fell in March 1983 at our study sites, and the weather remained showery and unsettled into May. The spring flights of most butter- flies were late and poor; for many species the densities observed were the lowest in 12 yr. Both P. rapae and P. zelicaon were severely depressed at most sites; P. rapae was actually rare in spring, and the Willow Slough population of P. zelicaon, north of Davis, went extinct overwinter. The summer was unusually cool, cloudy, and moist. By autumn the populations of both species were near normal levels and at the Suisun Marsh P. zelicaon was commoner than usual at the end of the season. The latest flight recorded at Suisun for this species is 18 November (1973), a "false brood." Although the species shut down nearly a month earlier in 1983, the autumn brood oviposited three to four weeks later than average. Similarly, at Davis, the last flight date of P. rapae was unexceptional but the population densities at the end of the flight were unusually high. For both species, these circumstances translated into an unprecedented number of larvae through mid-winter.
In the Suisun Marsh, fourth- and fifth-instar larvae of P. zelicaon were common on Sweet Fennel, Foeniculum vulgare Mill. (Umbelli- ferae) on levees; collections were made on 28 December (4 L5, 1 LA, 1 L3) and 16 January (2 L5). In addition, one L3 was found on the same plant at Gates Canyon in the Vaca Hills, Inner Coast Range,. near Vacaville, Solano County, 1 January. In the Davis area, a total of 67 larvae of P. rapae were collected from cultivated and weedy Cruciferae and Tropaeolum between 29 December and 15 January. Although Li-L3 were still numerous early in the period, only larger larvae (LA-L5) were taken. Numbers were so high that Cruciferous vegetables were seriously damaged in many gardens at this time.




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19841 Shapiro - Pieris rapae 165
All larvae were placed in outdoor mesh cages over fresh cuttings of their hosts, and allowed to complete development under ambient conditions. The cages were less than 0.3 km from the U.C. Davis campus meteorological station. The first pupa of P. zelicaon was formed 13 January and the last 24 February. 50 of the 67 rapae larvae were parasitized by Apanteles (Cotesia) glorneratus (L.) (Hymenoptera: Braconidae) and failed to pupate; 5 died of un- known causes; 12 pupated between 9 January and 28 February. Of the nine winter zelicaon, 1 prepupa died of unknown causes; 5 eclosed without diapause; and 3 apparently entered diapause. Eclosions occurred on 21 and 24 February and 1, 5, and 12 March 1984. As can be seen from Table 1, these dates coincide with the flight of P. zelicaon in the field. (At Gates Canyon, Vaca Hills, one zeiicaon was found as early as 19 February 1984, the earliest flight ever recorded in the region.) All the butterflies which emerged were female, as was one of the 3 diapausers.
Of the 12 healthy rapae pupae, all eclosed between 9 February and 24 March (seven males, five females). The flight began some- what earlier afield but continued throughout this period. The Apanteles wasps emerged without diapause in synchronized batches, each from its own host, between 24 January and 11
March-again, well-timed to parasitize first-instar larvae from eggs laid by first-brood rapae females. Diapause in this species is known to be under direct photoperiodic control (rather than mediated through the host, hormonally) in the U.S.S.R., but has not been studied in the introduced North American populations (Danilevskii, 196 1).
The phenotypes of emerging adults of both butterflies were compared with long series of field-collected specimens from Suisun and Davis from 1984 and prior years, including many individuals which must have come from diapaused pupae, and with reared ex- diapause individuals. No phenotypic differences which might permit the detection of non-diapaused adults in the spring populations were recognized. This result confirms experimental results which indicated that the post-diapause adult phenotype is not physio- logically coupled to the prior developmental arrest, but is rather a function of ambient conditions after reactivation (Shapiro, 1975a, 1978), superimposed on irreversible short-day prediapause deter- mination.




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166 Psyche [VOI. 91
As is evident from Table 2, low-temperature lethality is a rare event in this part of California. Although diapause may confer a degree of frost-tolerance, its principal benefit in P. zelicaon and P. rapae in north-central lowland California seems to be to delay the onset of adult development until the bulk of the rainy season has passed; thus, adult eclosion coincides with sunny, warm weather suitable for flight and hence for reproduction. Pupae accumulate enough chilling by roughly mid-January to come out of diapause; subsequent development is timed by the weather, which thus determines not only the date of first flight but the degree of synchronization of the spring brood (Shapiro, unpublished data). The unusual 1983-84 winter larvae pupated at about the same time as normal diapausing pupae would have resumed development; hence it is not surprising that their subsequent development was synchronized with the wild population. (On the other hand, dia- paused pupae of Pieris napi L. ssp. will develop to the pharate adult at a constant temperature of 3OC, while non-diapause ones will not; hence in that species, diapausers might be expected to eclose first; S hapiro, unpublished .)
The 3 diapausing zelicaon presumably cannot accumulate enough chilling to break diapause in spring 1984 and will thus lay over until early 1985. This would expose them to additional risks of mortality, and in terms of contribution to the rate of population increase, place them at a great selective disadvantage relative to nondiapausing members of their 1983-84 cohort (a delay of 4 generations). Multiple-year diapause occurs in most populations of P. zelicaon even under normal circumstances, although it is rare in the multi- voltine populations; it is especially common in univoltine foothill races which face unusually unpredictable and stressful climates and which would be expected to engage in "risk-spreading" (Sims, 1980). On the other hand, although pupae of P. rapae will remain viable for two years under constant refrigeration, no multiple-year dia- pause has ever been observed in that species under field conditions, and there is no indication that it has any physiological ability to diapause in summer (Shapiro 1975b, 1980b). Thus any diapause pupae produced by winter larvae of this species would presumably be doomed.
In a Mediterranean climate, then, a Type I11 diapause-induction curve permits stragglers at the end of the season to complete development and enter the reproductive pool the following spring at



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Table 2.
Climatic parameters for Sacramento (from U.S. Weather Bureau, NOAA Technical Memorandum NWS-WR-65, 1971). Temperatures are in degrees Fahrenheit. This table covers the period from the beginning of the last autumn generations of P. rapae and P. zelicaon to the end of the diapause in spring. TEMPERATURE (To 1971)
SUNRISE SUNSET daily mean mean record record DATE (PST) (PST) mean max min high low'
2
a
Sept. 15 0547 1815 72 87 56 104 47
2.
0602 1749 69 43
0
Oct. 1 8 3 54 98
Oct. 15 06 15 1728 64 77 5 1 94 3 8 1
Nov. 1 0632 1706 59 70 47 86 34
3?
Nov. 15 0648 1653 55 66 43 80 29 2
3 2
w
Dec. 1 0705 1645 50 59 40 7 1
1-1'
Dec. 15 07 16 1646 47 5 5
39 72 26 s
Jan. 1 0724 1656
46 53
39 65 24
Jan. 15 0722 1709
46 54
38 67 19
2
<t
Feb. 1 07 12 1728 48 57 39 68 28
Notes:
'Low lethal temperature for P. rapae pupae not in diapause is ca. 22O F; for P. zeiicaon ca. 19' F. Not determined for larvae, but both species can cool at least to the mid-20s overnight in protected micro-sites.



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168 Psyche [vo~. 91
no disadvantage; it is a valuable hedge against off-season repro- duction. In such benign climates the photoperiodic threshold for diapause inhibition may be under intermittent selection at both ends of the curve. Non-diapause overwintering may be fairly frequent in some California butterflies, especially P. rapae. At the latitude of Sacramento it is definitely rare in P. zeiicaon, since midwinter larvae were not observed in the first 12 yr of this study. In coastal southern California, however, this species flies more or less all winter (Emmel and Emmel, 1973; Orsak, 1977; Shapiro, unpub- lished) and larvae may often be found during the shortest days of the year. Although diapause intensity is reduced and thresholds are moderately shifted relative to further north, even the San Diego populations retain the ability to diapause (Sims, 1980). How often they use it under field conditions may depend on the timing of autumn reproduction on a year-by-year basis. The hypothesis that both thresholds of a Type I11 curve are adaptive and under selection is testable in principle by examining latitudinal shifts in critical photoperiods.
We have had under study a culture of P. rapae from Xochimilco, D.F., Mexico, the southernmost (ca. 19ON) population of this species in the Americas; it also displays a Type I11 curve with the short-day inhibition threshold shifted upward (Shapiro, in prepara- tion).
In climates where the onset of cold is more rapid than the change in photoperiod, that is, where strong air-mass contrasts exist and thermal lethality can occur with great suddenness, it is difficult to envision the low end of a Type I11 curve as adaptive. Cold nights should assure conservatism in the critical photoperiod, so that nearly all individuals will be determined as diapausers before the inhibition threshold can be reached. Larvae of P. rapae can be found into December and rarely into January at Philadelphia and New York City as well when early winter conditions are mild, but they never seem to survive. On the other hand, the occasional very early onset of
lethal cold in such areas should select for more conservative diapause induction than the average conditions seem to warrant.
The natural selection of diapause characteristics, already compli- cated by its nature as a recurrent (cyclical) process operating every 4th and 5th generation, is further complicated by the ability of stochastic variation to override it occasionally in benign climates.



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Shapiro - Pieris rapae
This research is part of California Agricultural Experiment Station project CA-D*-AZO-3994-H, "Climatic Range Limitation of Phytophagous Lepidopterans," AMS, principal investigator. BECK, S. D.
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1975a. Papilio "gothica" and the phenotypic plasticity of P. zelicaon (Papili- onidae). J. Lepid. SOC. 29: 79-84.
1975b. The role of watercress, Nasturtium officinale, as a host of native and introduced Pierid butterflies in California. J. Res. Lepid. 14: 158-168. 1978. The evolutionary significance of redundancy and variability in pheno- typic-induction mechanisms of Pierid butterflies (Lepidoptera). Psyche 85: 275-283.
1979. The phenology of Pieris napi microstriafa (Lepidoptera: Pieridae) during and after the 1975-77 California drought, and its evolutionary significance. Psyche 86: 1-10.
1980a. Egg-load assessment and carryover diapause in Anthocharis (Pieridae). J. Lepid. SOC. 34: 307-315.
1980b. Mediterranean climate and butterfly migration: an overview of the California fauna. Atalanta 11: 18 1-188. SIMS, S. R.
1980. Diapause dynamics and host-plant suitability of Papilio zelicaon (Lep- idoptera: Papilionidae). Amer. Midi. Nat. 103: 375-384.



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