factors governing the induction of …...factors governing the induction of diapause in the oriental...

FACTORS GOVERNING THE INDUCTION OFDIAPAUSE IN THE ORIENTAL FRUIT MOTH1

R. C. DICKSON2

University of California Citrus Experiment Station,Riverside, California

Diapause is a physiological state of arrested development whichenables an organism to survive more easily a period of unfavorableconditions. Once an organism has entered diapause it usually has toremain in that state for a certain period, regardless of the conditionsof the environment. In some species diapause is broken by exposureto particular conditions, notably cold. A few species may remainin diapause more than one year.

The term "diapause" was first used by Wheeler (1893) to specifya stage in the embryonic development of Conacephalms. Henneguy(1904) extended the term by applying it to the state of arrested develop-ment occurring in the eggs of Bombyx and in the larvae of Liparis.It has since been further extended to cover similar phenomena occurringat any stage of the life cycle of an organism.

Insects in diapause are characterized by a low metabolic rate,greatly diminished activity, practical cessation of development, and anincreased ability to survive unfavorable environmental conditions.

Many theories have been advanced to account for the initiationof diapause, since is obviously is not always induced directly by theonset of the unfavorable conditions themselves. In many cases diapausethat will serve to carry an organism through the winter starts longbefore that season begins.

This paper deals chiefly with the factors controlling the inductionof diapause in the oriental fruit moth, Grapholitha molesta (Busck).These factors are temperature and photoperiod, which operate duringthe larval feeding period. Some data on the induction of diapause inthe codling moth, Carpocapsa pomonella (L.), the greenbottle fly,Ludlia sericata Meig., and the vegetable weevil, Listroderes obliquusKlug, are also presented.

REVIEW OF LITERATURE

Published work on diapause and related phenomena in insects isextensive. This writer does not intend to review all the work, butattempts, rather, to organize and classify the results reported, par-ticularly on the basis of the factors reported as inducing diapause.Reference will be made to various publications illustrating the pointsmade. For more complete bibliographies the reader is referred toUvarov (1931), Wigglesworth (1939), Prebble (1941), and Bonnemaison(1945).

1 Paper No. 610, University of California Citrus Experiment Station, Riverside,California.

2Assistant Entomologist in the Experiment Station.

511

512 Annals Entomological Society of America [Vol. XLII,

Developmental Fatigue.—The first investigator to advance the theorythat diapause might be caused by a developmental fatigue broughtabout by the accumulation of waste products in the body appears tohave been Sajo (1896), who was working with the chrysomelid Ento-moscelis adonidis Fall. This idea was developed by Robaud (1922),who worked with various species of flies, particularly with Ludliasericata Meig. He postulated that this developmental fatigue is anautointoxication caused by the accumulation of metabolic wastes whichbuild up faster than they are eliminated during active growth, so thata period of rest (diapause) is needed to allow elimination to catch up.He also believed that this developmental fatigue is inherited andcontinues to build up during the several summer generations. Thiswork has been rather well discredited by Cousin (1932), who showedthat hibernation in Ludlia is caused by environmental factors.

Diapause Factor or Hormone.—Bodine (1932) studied diapause inthe eggs of Melanoplus diferentialis (Thos.) and advanced the theorythat there is a diapause factor (X factor) present in the diapause-typeeggs of that species at the time that they are laid. If these eggs areheld at comparatively high temperatures, the amount or potencyof the diapause factor increases until it passes a threshold at the "three-weeks" stage and stops embryonic development. The diapause factoris gradually dissipated after this point and eventually allows develop-ment to resume. Exposure to low temperature at any time, eitherbefore or after the "three-weeks" stage, rapidly destroys the diapausefactor, and development resumes as soon as the temperature is raised.

Andrewartha (1943), working with the eggs of another grasshopper,Austroicetes cruciata Sauss., offered another explanation. He believedthat the arrest of embryonic development is caused by an unfavorablecondition of the yolk, which is corrected by exposure to cold.

Salt (1947), working with Cephus cinctus Nort., has further developedBodine's theory. He postulates that diapause in this species is con-trolled not only by an X factor similar to that envisioned by Bodine,but also by a Y factor, which breaks down more slowly than does theX factor but at a constant rate, regardless of temperature. He wasable to reinstate diapause by exposure to very high temperatures atany time before the Y factor was eliminated. One might suggest thatthe Y factor could be the material from which the X factor is formed.

The evidence indicates that a hormone or diapause factor is oftenpresent to control diapause, but, as we shall see below, many thingsmay induce its formation.

Inheritance of Behavior Patterns in Diapause.—The development andbehavior patterns in regard to diapause are inherited as are all othersimilar patterns. There are many insect species which have but onegeneration per year, with a considerable part of each year spent indiapause. In these species it may well be that each individual mustenter diapause, the adjustment to the seasons occurring at the time theinsect resumes development rather than at the time it enters diapause.An example of this is found in Porthetria dispar (L.), which has but onegeneration per year, remaining in the egg stage from July until thefollowing spring. Goldschmidt (1933) stated that the length of thediapause is determined genetically and is different in the various races

1949] Dickson: Diapause in Oriental Fruit Moth 513

of this species. Those races that live where the winters are mild requiremany more hour-degrees of heat to cause the eggs to hatch than dothose that experience severe winters. Andrewartha (1943) found thatthe eggs of the one-generation grasshopper Austroicetes cruciata Sauss.always enter diapause, the embryo developing very slowly through thehot season so that when cold weather appears the egg is in such acondition that low temperature soon breaks the diapause.

A few insect species are known in which there are both single-generation strains (univoltine or monovoltine) and multiple-generationstrains (multivoltine or polyvoltine). One of these is the silkworm,Bombyx mori L., in which the diapause occurs in the egg. The univoltinestrains of the silkworm have but one generation annually, and thediapause occurs in every generation. Multivoltine strains have two toseveral generations annually: eggs laid in the summer hatch in a shorttime; those laid in the fall enter diapause. The inheritance of vol-tinism in the silkworm is somewhat complex, there being some evidencefor somatic inheritance from the mother. It is reported by Uyema(1926) that if the ovaries from an individual of one race are trans-planted to an individual of another race during the larval stage the eggsproduced show the voltinism of the moth in which they are grownrather than that of their true ancestors. The likelihood that a givenbatch of eggs will enter diapause is also influenced by the temperatureat which the eggs and larvae of the preceding generation were held.

In the case of Pyrausta nubilalis (Hbn.), a species which entersdiapause as full-fed larvae, it is well known that some areas are occupiedby one-generation strains and others by two-generation strains. Bab-cock (1924) reported that when specimens of the one-generation strainwere transferred to an area occupied by the two-generation strain, andvice versa, they persisted in retaining the same seasonal histories thatthey had shown in their original environments. Arbuthnot (1944)found that in Connecticut the population is homozygous for multiplegenerations, while in Ohio it is mixed, containing factors for bothsingle and multiple generations. He was able to isolate a homozygoussingle-generation strain from Ohio population, and found that thegenetic factors responsible for the single generation are recessive.O'Kane and Lowry (1927), working with this insect in New Hampshire,showed that although the population was homozygous for multiplegenerations, only a part of them actually went through two generationsper year, the rest having but one. All the larvae from the first eggs ofthe season pupated that same summer and produced a second gen-eration, while larvae from eggs that hatched after a certain date, usuallyabout July 20 to 25, entered diapause and so had only one annualgeneration. Apparently, environmental factors are involved in theinduction of diapause in this species, at least in the multiple-generationstrain.

Prebble (1941) found that some strains of the European sprucesawfly, Diprion hercyniae (Htg.) entered diapause more readily thanother strains.

Effect of Temperature on the Induction of Diapause.—Most insectsliving in temperate or frigid climate undergo an arrest of developmentduring the winter. If this is caused directly by the low temperature


and is brought to an end whenever the temperature again rises, it iscalled "quiescence" and is not diapause. Some instances have beenreported, however, in which low temperature induces diapause.

Dawson (1931) was able to induce pupal diapause in Telea poly-phemus (Cramer) by subjecting the last larval stadium to decliningtemperatures. Ditman, Weiland, and Guill (1940) reported thatdiapause during the pupal period of the corn earworm, Heliothis armigera(Hbn.), is induced by low temperature during the larval feeding period.Prebble (1941) found that diapause in emergent (polyvoltine) stocksof Diprion hercyniae (Htg.) is determined environmentally, and showedthat, at least under certain conditions, larval feeding at low tem-peratures favors entry into diapause as full-fed larvae.

Food and Water.—Food and water are closely related in insecteconomy since most of the water taken by insects is taken in the food.Strelnikov (1936) reported that when Loxostege sticticalis (L.) was fedon plants having a high moisture content no diapause was induced,but when the moisture content of the plants was low the insects entereddiapause. He stated that in this species diapause is induced undernatural conditions by insufficiently moist food, by low temperature,and by food having increased nutritive value.

Squire (1940) reported that diapause of the full-fed larvae of thepink bollworm, Pectinophora gossypiella (Saund.), is independent ofthe season and depends on the moisture content of the seeds in whichthey feed. If the seeds are comparatively mature, the larvae enterdiapause, but if the seeds are immature and moist, they do not. Dia-pause in this species is closely related to changes in the host plant, andonly indirectly to climatic changes.

Van der Goot (1925) reported that the white rice-borer, Scirpophagainnotata Wlk., enters diapause when the larvae feed in maturing riceplants. Once in diapause they remain for at least four and one-halfmonths, and resume development in response to the first showers of therainy season.

Photoperiod.—The earlier reports of the effect of the length of thephotoperiod on diapause in insects concern aphids, in which the situationis complex. Aphids reproduce parthenogenetically throughout thesummer, only females being produced. In the fall oviparous femalesand males are produced, also by parthenogenesis; they mate, and thefemales produce the eggs, which enter diapause and thus enable thespecies to pass the winter. Marcovitch (1924) found that Aphisforbesi Weed and three other species of aphids produced males andoviparous females when the days were artificially shortened to 73^ hours.Davidson (1929) reported similar results. Wadley (1931) foundthat, in the production of sexuals in Toxoptera graminum (Rond.),the temperature has some influence, but that the principal factor isthe photoperiod, which acts either on the mother or on the individualbefore birth.

Baker (1935) found that he could break the diapause in young larvaeof the treehole mosquitoes Orthopodomyia signifera Coq. and Anophelesbarberi Coq. by using six hours of artificial light to prolong winter days.Dickson and Sanders (1945) reported that they could control theinduction of diapause in Grapholitha molesta (Busck) by regulatingtemperature and photoperiod during the larval feeding period.


MATERIALS AND METHODS

All experiments were conducted in insulated cabinets in whichconstant temperatures and humidities were maintained. The illumina-tion used was entirely artificial, and its intensity was controlled.

Larvae of the oriental fruit moth and of the codling moth weregrown in small, immature apples, which were held in cold storage untilneeded. The full-fed larvae were collected each morning as theyemerged and allowed to spin in strips of a celluloid device made inimitation of corrugated paper.

Larvae of the greenbottle fly, Lucilia sericata, were grown in fishheads or rabbit heads, and the full-fed larvae were allowed to crawl intodamp sand. Larvae and puparia were sieved from the sand forobservation.

Vegetable-weevil larvae were grown on wild mustard in battery jars.The adults were allowed to gather under trash in the bottom of thesesame containers.

The constant-temperature cabinets held the temperature reasonablywell, the maximum variation amounting to about one degree Centigrade.The temperature recorded in this paper as 24° C. represents a tem-perature which varied from 24° C. to 25° C, but which was usuallynear 24°. The intensity of illumination used in most of the experimentsis recorded as 26 f. c. (foot-candles). This represents a mean of theintensity of illumination, which varied above and below 26 f. c, depend-ing on the age of the bulb, the cleanliness of the glass window, and thelocation of the growing insects in the cabinets. A tungsten-filamentlamp was used in all experiments except those in which the use ofanother light source is noted. Illumination was measured by a GeneralElectric photometer, a barrier-layer type, DW-47. The light intensityrecorded represents the light intensity reaching the top surface of thefruit in which the larvae were feeding.

Certain data are presented in more than one table in order tofacilitate comparisons.

EXPERIMENTAL RESULTS

The oriental fruit mothBehavior under Natural Conditions.—The oriental fruit moth,

Grapholiiha molesta (Busck), feeds in the twigs and fruit of severalrosaceous plants, its favorite host being the peach. There are fromtwo to seven generations annually, the number depending on thelocality. The insect passes through the several spring and summergenerations without entering diapause. Beginning in the late summeror early fall, an increasing proportion of the emerged, full-fed larvaeenter diapause and do not pupate until spring. It has been advan-tageous to this species to develop the habit of entering diapause whilethe weather is still warm, for if the insects remained active until theonset of cold weather the population would be greatly reduced by thescarcity of suitable food. As will be shown in this paper, the propertiming has been achieved by the use of the shortened length of day inthe late summer as a stimulus to enter diapause.

516 Annals Entomological Society oj America [Vol. XLII,

A typical record of the onset of diapause in the fall is shown inTable I and figure 1. All larvae that emerged earlier than those shown

26 OCT.6

E M E R G E N C E

FIG. 1. Relation between the average date of emergence of full-fed larvaeof the oriental fruit moth grown under outside conditions at Riverside, California,and the percentage of larvae that entered diapause.

TABLE IRECORD OF BATCHES OF ORIENTAL FRUIT MOTH LARVAE GROWN UNDER OUTSIDE

CONDITIONS AT RIVERSIDE, CALIFORNIA, SHOWING RELATION BETWEEN DATEOF EMERGENCE AS FULL-FED LARVAE AND ENTRANCE INTO DIAPAUSE

DATEEGGS

HATCHED(1944)

Aug. 1Aug. 4Aug. 4Aug. 8Aug. 11Aug. 15Aug. 16Aug. 18Aug. 18Aug. 22Aug. 25Aug. 25Aug. 25Aug. 29Sept. 1Sept. 5Sept. 9Sept. 12

LARVAL FOOD

Green applesRipe peachesGreen applesGreen applesGreen applesGreen applesGreen applesRipe peachesGreen applesGreen applesGreen peachesRipe peachesGreen applesGreen applesGreen applesGreen applesGreen applesRipe peaches

FULL-FED LARVAE

AverageDate of

Emergence(1944)

Aug. 17Aug. 16Aug. 19Aug. 26Aug. 27Sept. 3Sept. 6Sept. 1Sept. 7Sept. 11Sept. 10Sept. 10Sept. 14Sept. 19Sept. 21Sept. 25Sept. 29Oct. 2

TotalNumber

4791799873

20558

11411391

14312153

110101113126173

Per CentEnteringDiapause

0.00.01.37.19.6

25.427.636.047.887.076.969.490.697.694.199.1

100.0100.0


in this table pupated a few days after emergence; all those that emergedlater, entered diapause. The temperature when diapause first appearedwas almost as warm as that of midsummer. The type of food onwhich the larvae were fed appears to have had no effect on their entryinto diapause.

Effect of Hours of Light per Day at Medium Temperatures.—Experi-mental data show that at medium temperatures the proportion of larvaeentering diapause is determined by the number of hours of light perday to which they are exposed during the larval feeding period.(Table II). In figure 2 some of the data from Table II are shown ingraphic form.

3 6

H O U R S

9 1 2

L I G H T

15

P E R

18 21

D A Y

FIG. 2. Effect of exposure to various daily photoperiods, during larval feedingperiod, on the percentage of oriental fruit moth larvae entering diapause. Larvaegrown at a medium temperature of 24° C ; prepupal period, 24° C ; illumination,26 f. c.

When grown in total darkness or total light, very few of the larvaeenter diapause. This indicates that basically the larvae tend to pupatewithout entering into a state of diapause. The fact that a few of thelarvae do enter diapause when grown without any photoperiod indicatesthat there is also present an inherent tendency to enter diapause. Asthe daily photoperiod is increased, the proportion of the larvae enteringdiapause increases until the hours of light per day number about 12.As the photoperiod is increased to more than 13 hours of light per day,the percentage of larvae entering diapause drops very sharply to prac-tically zero, and this almost total absence of diapause is maintained


as the photoperiod is increased beyond 14 hours per day. This responseto the number of hours of light per day explains the behavior in thefield very well, particularly when the studies on the minimum effectiveintensity of illumination (see p. 523) are considered.

TABLE II

EFFECT OF THE NUMBER OF HOURS OF LIGHT PER DAY DURING LARVAL FEEDINGPERIOD, AT VARIOUS MEDIUM TEMPERATURES, ON THE PERCENTAGE OF

ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

HOURS PER DAY OF

Light Darkness

TOTALLARVAE

LARVAE ENTERING DIAPAUSE

Number Per Cent

Tempera tore, 21 °C.

069

12151824

24181512960

997291

101728949

15689199247

15.294.4

100.098.02.84.5

14.3

Temperature, 24°C.

0369

11121314151824

2421181513121110960

423293864302118745380230147137340

83295

203110735367

9011

1.910.911.067.294.298.796.63.90.00.70.3

Temperature, 26°C.

0XAXA

l369

12151824

2423M231^2321181512960

2478694

13410978

1311089680

182

2877

3649

106100

502

0.89.37.45.2

33.062.880.992.65.20.01.1

*Larvae held at given temperatures throughout growth and prepupal period;illumination, 26 f. c.


Effect of Hours of Light per Day at High and Low Temperatures.—The influence of the photoperiod on entrance into diapause is dominantat medium temperatures, but when the larvae are grown at high orlow temperatures it loses most of its effect (Table III). Almost 100per cent of the larvae grown at medium temperatures (21°, 24°, and26° C), with 12 hours illumination per day, entered diapause; butneither those grown at 12° C. nor those grown at 30° C, exposed to thesame photoperiod, entered diapause in appreciable numbers.

TABLE III

EFFECT OF VARIOUS EXTREME TEMPERATURES, DURING LARVAL FEEDING PERIOD, ONTHE PERCENTAGE OF ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

TEMPERATURE,DEGREES C.

TOTALLARVAE


Number Per CentUnweighted

Mean Per Cent

121221242426303030

Light: 12 Hours—Darkness

49341013643811083793199

1199364371100032

: 12 Hours

2.0\2.9/98.0100.0\97.4/92.60.013.2[i.oj

2.4

98.098.7

92.6

1.4

Light: 15 Hours—Darkness: 9 Hours

1212212424263030

3951726384965046

10200500

2.610.0/2.80.010.0/5.20.010.0/

1.3

2.80.0

5.20.0

*Photoperiods during larval feeding period, as given; illumination, 26 f. c.Temperature during prepupal period, 24°C. (21 °C. for larvae grown at 21 °C.or26°C).

The absence of diapause in oriental fruit moth larvae grown at lowtemperatures may be an advantage to the species, since belated indi-viduals feeding during the cold of winter do not enter diapause andthus are not unduly delayed in their spring emergence. Larvae grownat low temperatures show a sensitivity to low temperatures in inducinga delay in pupation (see section on '' Temperature During the PrepupalPeriod")-


The lack of sensitivity to photoperiod at high temperatures maybe a disadvantage to the species in certain localities, since it may unduly

TABLE IVEFFECT OF LOW "NIGHT" TEMPERATURE (2°C), DURING LARVAL FEEDING PERIOD,

ON THE PERCENTAGE OF ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

HOURS PER DAY OF

Light(at 26°C.)

69

1518

Darkness(at2°C.)

181596

TOTALLARVAE

981198257


At VaryingTemperatures

of 26<rand 2°C.

Number

981196030

Per Cent

100.0100.073.252.6

At a ConstantTemperature of26°C. (SamePhotoperiods)f

Per Cent

80.992.65.20.0

*Feeding larvae held at 26° C. during hours of light and at 2° C. during hoursof darkness; prepupal period, 21° C ; illumination, 26 f. c.

fData from Table II, for comparison.

TABLE V

EFFECT OF INCREASING, DECREASING, AND CONSTANT PHOTOPERIODS ON PERCENTAGEOF ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

PHOTOPERIOD t

Constant...Increased 5Decreased 5

Constant...Increased 5Decreased 5

Temperature During

minutes each day... .minutes each day...

Temperature During

minutes each day—minutes each day...

TOTALLARVAE

LARVAE ]

Larval Feeding

101108101

Larval Feeding

108106141

ENTERING

Number

Period,

9910899

Period,

10094

130

21°C.

26°C.

DIAPAUSE

Per Cent

9810098

9?8892

000

672

*Temperature during prepupal period, 21 °C.fAverage photoperiod, 12 hours per day; illumination, 26 f. c.

delay the onset of diapause in climates where very high temperaturespersist into the fall. On the other hand, it may allow continuousdevelopment in tropical areas.


In natural surroundings the oriental fruit moth is seldom exposedto constant temperatures, the temperature being considerably lower atnight than during the day. It was not possible to make a series oftests under such conditions, but in one test a night temperature wellbelow the threshold of development was used. The results of thistest are shown in Table IV. Evidently, the low temperature duringthe period of darkness tended to induce diapause, even though it waslow enough to stop all development.

Increasing, Decreasing, and Constant Photoperiods.—Experimentswere conducted to determine the effect of small increases or decreases inthe photoperiod each day, in comparison with a constant photoperiod,on the percentages of larvae entering diapause. The results (Table V)showed that it is the actual length of the photoperiod rather than itsincrease or decrease that affects the larvae.

TABLE VIRESULTS OF EXPERIMENTS TO DETERMINE EFFECT OF DIAPAUSE-INDUCING AND

DIAPAUSE-PREVENTING PHOTOPERIODS, DURING VARIOUS PARTS OF THELARVAL FEEDING PERIOD, ON THE PERCENTAGE OF ORIENTAL FRUIT

MOTH LARVAE ENTERING DIAPAUSE*

DURATION OF PHOTOPERIODICCONDITIONS

D iapause- Inducing(12 hours light

per day )

Last 0-5 daysLast 4-9 daysLast 8-13 daysFirst 12 daysFirst 8 daysFirst 4 days

Diapause-Preventing(15 hours light

per day)

First 12 daysFirst 8 daysFirst 4 daysLast 0-6 daysLast 4-10 daysLast 8-13 days

TOTALLARVAE

15611885

18555

178

LARVAE ENTERINGDIAPAUSE

Number

024

179383

Per Cent

0.01.74.7

96.869.11.7

""Temperature during larval feeding period and prepupal period, 24° C ,illumination, 26 f. c.

Cumulative Effect of the Photoperiod.—An experiment was con-ducted to determine whether the photoperiod is operative during allor only part of the larval feeding period. Results (Table VI) showedthat practically no diapause was induced unless the larvae were exposedto a diapause-inducing photoperiod in the early part of their feedingperiod, but that such a photoperiod had some effect if applied anytime during the feeding period. Although there does not appear tobe an actually critical point, the early part of the period is more criticalthan any other part.

The Color of the Light.—Experiments were conducted to determinewhich wavelengths of light are most capable of affecting the inductionof diapause in this species. Oriental fruit moth larvae were exposed,during their feeding period, to 12 hours' illumination per day with lightwhich had been filtered through various glass filters. The source of

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illumination was a 200-watt, gas-filled tungsten filament lamp, exceptin the experiments with ultraviolet light, in which a mercury vaporlamp was used, and with infrared light, in which a heater cone wasused. Results of these experiments are shown in Table VII.

Neither the ultraviolet light nor the infrared was effective in inducingdiapause. Of the visible light, the shorter wavelengths were moreeffective than the longer. The "lantern red" filter, which cut off alllight having wavelengths shorter than 6,000 A, in the yellow orange,induced diapause in only about one-fifth of the larvae, and even thelight passed through the "traffic-shade yellow" filter was less effective ininducing diapause than was light containing the blue end of the spectrum.

Intensity of Illumination.—It was considered important to discoverthe lower limit of intensity at which illumination is effective in inducingdiapause, so that the length of the photo-periodically effective twilight

TABLE VIIIEFFECT OF VARIOUS INTENSITIES OF ILLUMINATION, 12 HOURS PER DAY DURING

LARVAL FEEDING PERIOD, ON THE PERCENTAGE OF ORIENTALFRUIT MOTH LARVAE ENTERING DIAPAUSE*

INTENSITY OFILLUMINATION,

IN F.C.

2626

3331100

TOTALLARVAE

364381207308250124146179245


Number

364371186286207

1253

Per Cent

100.097.489.992.982.80.81.42.81.2

UnweightedMean Per Cent

98.7

88.5

1.1

2.0

""Temperature during larval feeding period and prepupal period, 24°C.

might be estimated. As pointed out by Greulach (1942), the totalphotoperiodically effective daylight is longer than the time betweensunrise and sunset. He found that, in Ohio in the summer, the total(morning and evening) photoperiodically effective twilight ranges from20 minutes to one hour, the variation depending on the amount ofcloudiness. He used 1 f. c. as a base, since light is effective on plantsdown to about 1 f. c.

The results of experiments to determine the minimum effectiveintensity of illumination on larvae of the oriental fruit moth are shownin Table VIII. Illumination having an intensity of 3 f. c. was effectivein controlling the onset of diapause, but that of 1 f. c. was not. Thismeans that, for the oriental fruit moth, the photoperiodically effectivelength of the day is almost as long as that found by Greulach for plants.On a clear summer evening in southern California it takes only abouttwo minutes for the intensity of illumination to sink from 3 f. c. to 1 f. c.


The inclusion of the morning and evening twilight periods in thelength of the day makes the experimentally demonstrated effect of thephotopenod correspond very well with the response of the oriental fruitmoth to natural illumination throughout the season.

Mode of Action of the Photoperiod.—Series of experiments wereconducted in an attempt to discover how the photoperiod operates ingoverning the induction of diapause. When a day length of 24 hoursis used, periods of illumination of approximately 12 hours per day inducea high percentage of diapause. With these photoperiods the ratio oflight to darkness is at or near one to one. Experiments were therefore

TABLE IXEFFECT OF VARIOUS " D A Y " LENGTHS, HAVING RATIO OF HOURS LIGHT TO HOURS

DARKNESS ALWAYS 1:1 DURING LARVAL FEEDING PERIOD, ON THE PERCENTAGEOF ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

HOURSLIGHT

15151414131312121111101099663

HOURSDARKNESS

151514

. 14131312121111101099663

TOTAL" D A Y "

LENGTH,IN HOURS

303028282626242422222020181812126

TOTALLARVAE

18514317119510077

3643811291072431411012068982

149


Number

41

29327364

3643711271061559444523

Per Cent

2.20.7

17.016.473.083.1

100.097.498.499.163.866.74.01.95.62.42.0


1.4

16.7

78.0

98.7

98.7

65.2

2.9

4.02.0

•Temperature during larval feeding period and prepupal period, 24°C;illumination, 26 f. c.

conducted using various "day" lengths in which the ratio of hours oflight to hours of darkness was kept at one to one. Results are shownin Table IX.

It is apparent from these results that the ratio of hours of lightto hours of darkness is not enough to explain the method of operationof the photoperiod. Although the ratio was kept at one to one, diapausewas induced in half or more of the larvae only in a comparativelynarrow range of "day" lengths, namely, 20 to 26 hours. The absolutelengths of the periods of light and of darkness are both of importance.As is shown in Table X, the use of 15 hours of light per "day" tends toprevent diapause, but by reducing the dark period from 15 hours to


11 or 12 hours, it is possible to induce some diapause. The same tableshows the results of experiments using 12-hour periods of light or ofdarkness. It is apparent that neither, by itself, is able to inducediapause; each must be combined with the appropriate period of lightor darkness, as the case may be. Table X also gives the results ofexperiments using 9-hour periods of light or of darkness. It will be notedthat whenever a period of darkness of only 9 hours was used, little or nodiapause was induced. Apparently, diapause is induced only if a period

TABLE XEFFECT OF VARIOUS COMBINATIONS OF LIGHT AND DARKNESS PER " D A Y , " DURING

THE LARVAL FEEDING PERIOD, ON THE PERCENTAGE OFLARVAE ENTERING DIAPAUSE*

HOURS PER

Light

1515151515151515151212121212129999999

" D A Y " OF

Darkness

1515121212111199

1515121299

151512121299

TOTALLARVAE

185143425321274216220

6384

201192364381128177127175180292156101206

LARVAE ENTERING

Number

41

5113487556000

156128364371

20

76127178290156

44

Per Cent

2.20.7

12.041.731.725.527.30.00.0

77.666.7

100.097.4

1.60.0

59.872.698.999.3

100.04.01.9

DIAPAUSE


1.4

28.5

26.4

0.0

72.1

98.7

0.8

66.2

99.4

2.9

""Temperature, during larval feeding period and prepupal period, 24°C;illumination, 26 f. c.

of at least 11 hours of darkness per "day" is used. The only exceptionto this is the experiment using 10 hours light and 10 hours darkness(Table IX).

A series of experiments was conducted using 11 hours of darknessper "day" with various periods of illumination. Results (Table XI)show that as the number of hours of light per day is increased to morethan 13 the proportion of diapause is progressively decreased.

From the results shown in Tables IX to XI, it is apparent that forthe induction of an appreciable percentage of diapause, the larvae must

526 Annals Entomological Society of America [Vol. X L I I ,

be exposed during the feeding period to not less than 10 (usually 11) not more than 15 hours of darkness per day, and to not less than 8 nor more than 15 hours of light per day. The results of all experiments on photoperiod during the larval feeding period, at 24° C , are presented in figure 3. This figure shows the rather sharp dividing line at about 11 hours of darkness per day; it also shows that practically complete diapause is induced only under a rather narrow range of conditions. These data indicate that diapause in the oriental fruit moth larva is induced by a hormone or hormone-like substance that is produced by the larva during the larval feeding period. They further indicate that this hormone is produced by a two-phase reaction, which requires

T A B L E X I

EFFECT OF 11 H O U R S D A R K N E S S AND VARIOUS PERIODS OF LIGHT PER " D A Y , " DURING LARVAL FEEDING PERIOD, ON THE PERCENTAGE OF ORIENTAL

F R U I T M O T H L A R V A E ENTERING D I A P A U S E *

H O U R S PER " D A Y " OF

Darkness

TOTAL L A R V A E

L A R V A E ENTERING DIAPAUSE

Number Per Cent Unweighted

Mean Per Cent

129 136 216 220

98 124 247

63 64

129 107 143 206 103 107

1 6

55 60 48 66

238 61 62

127 106 142 203

11 12

0.8) 4 .4/

25.51 27.31 49.01 53.2( 96.41 96. 96.91 98.41 99.11 99.31 98.5J 10.71 11.2/

*Temperature during larval feeding period and prepupal period, 24°C. illumination, 26 f. c.

darkness for one phase and light for the other, as does photosynthesis. The darkness-induced phase is extremely sensitive to the length of the period of darkness and does not reach its effective point unless there are at least 11 hours of darkness per "day."

It is apparent that in the field in the late summer the onset of diapause is caused both by the decrease in the hours of light and by the corresponding increase in the hours of darkness, but that the rather rapid increase in percentage of diapause is caused mainly by the fact that the number of hours of darkness passes the critical minimum point for the induction of diapause at this time.

Interruption of the Photoperiod.—In the experiments reported so far, the periods of light and of darkness used were uninterrupted. Two


-J 0>

4 -

3 - - - 26-29 1 -

s i - i7 ! 96 j 78

99 72 99 ; 94 !

"65 ; i

99 66 99 ; \

99 99 j

11 - - ! • - - - - 99

JL

- 11

3 6

H O U R S

9 12

D A R K N E S S

15 18

P E R

21 2 4

"D A Y"

F I G . 3. Mean percentages of oriental fruit moth larvae entering diapause when exposed to various combinations of light and darkness per " d a y " during the larval feeding period. Temperature during larval feeding period and pre-pupal period, 24° C ; illumination, 26 f. c.

show a mistake: by reducing the main period of darkness to 10 hours, the induction of diapause was prevented. It was therefore necessary to repeat this experiment with the period of darkness increased to 11 hours. When this was done, it was shown that the effect of interrupting the period of light by 2 hours was to reduce the larval diapause by about one-third.

Results of the experiments on the interruption of the period of darkness (Table XIII) are similar to those obtained by interrupting

series of experiments were conducted to determine the effect of interrupting the period of light or of darkness. The results obtained by-interrupting the period of light are shown in Table XII . Some decrease in the incidence of diapause was obtained by the use of 1 hour of darkness to interrupt the period of light. The first experiment in which the light period was interrupted by 2 hours of darkness is included only to

528 Annals Entomological Society of America [Vol. X L I I ,

T A B L E X I I

EFFECT OF INTERRUPTING THE PERIOD OF LIGHT E A C H " D A Y " DURING THE L A R V A L FEEDING PERIOD ON THE PERCENTAGE OF ORIENTAL F R U I T M O T H

L A R V A E ENTERING D I A P A U S E *

H O U R S PER ' D A Y "

TOTAL L A R V A E

Light Dark Light Dark Tota l ness ness

12 12 24 364 12 12 24 381 6 1 6 11 24 202 6 1 6 11 24 204 6 2 6 10 24 73 6 2 6 10 24 129 6 2 6 11 25 271 6 2 6 11 25 206 6 3 6 11 26 91 6 3 6 11 26 80 6 6 6 6 24 89 6 6 6 6 24 82

L A R V A E ENTERING DIAPAUSE


Mean Per Cent

364 371 188 189

1 1

176 123

2 3 5 2

100.0 97.4 93.1 92.6

1.4 0.8

64.9 59.7

2.2 3.7 5.6 2.4

98.7

92.8

1.1

62 3

3.0

4.0

Tempera ture during larval feeding period and prepupal period, 2 4 ° C ; illumination, 26 f. c.

T A B L E X I I I

EFFECT OF INTERRUPTING THE PERIOD OF D A R K N E S S E A C H D A Y DURING THE LARVAL FEEDING PERIOD ON THE PERCENTAGE OF ORIENTAL F R U I T M O T H

E N T E R I N G D I A P A U S E *

H O U R S PER D A Y

Light Darkness Light Darkness

TOTAL L A R V A E

L A R V A E ENTERING D I A P A U S E


Mean Per Cent

12 12 UH n% 11 11 10 10 9 9 6 6

12 12 6 6 6 6 6 6 6 6 6 6

364 381

38 90

204 232 107 86

145 110 89 82

364 371

38 90

169 184 51 54

1 0 5 2

98.7

100.0

81.0

55.2

0.3

4.0

•Temperature during larval feeding period and prepupal period, 2 4 ° C ; illumination, 26 f. c .

the period of illumination, except that the effect was slightly more pronounced. Oriental fruit moth larvae are much less sensitive to interruption of the dark period than are certain plants. Parker et al.


(1946) showed that in soybean and cocklebur the production of the flower primordia could be prevented by interrupting the period of darkness by only a few seconds at the proper illumination. With larvae of the oriental fruit moth, an interruption of two hours was required to reduce the incidence of diapause by one half.

T A B L E X I V

EFFECT OF VARIOUS TEMPERATURES DURING THE PREPUPAL PERIOD ON THE PERCENTAGE OF ORIENTAL F R U I T M O T H L A R V A E ENTERING

DIAPAUSE OR QUIESCENCE

PHOTOPERIOD

D U R I N G LARVAL

FEEDING* TEMPERA

TURE D U R I N G

PREPUPAL PERIOD,

D E G R E E S C.

TOTAL

L A R V A E

L A R V A E ENTERING D I A P A U S E

OR QUIESCENCE

Hours Light

Per Day

Hours Darkness Per Day

TEMPERATURE

D U R I N G PREPUPAL

PERIOD, D E G R E E S C.

TOTAL

L A R V A E


Mean Per Cent

Temperature during Larval Feeding, 12°C.

12 12 30 49 1 2.0Ì 12 12 30 43 2 4.71 O . O

12 12 24 49 1 2.0^ O A 12 12 24 34 1 2.91 12 12 12 52 51 98.11 99.0 12 12 12 65 65 100.0/ 99.0

12 12 12t 50 5 10.01 11.3 12 12 12t 63 8 12.71 11.3

15 9 24 39 1 2 . 6 \ 1 9 15 9 24 51 0 O.OY 1 .O

15 9 12 52 29 55 .8 / 59.4 15 9 12 65 41 63.1. r 59.4

15 9 12t 8 0 0.0 I 1.3 15 9 12t 38 1 2.6 f 1.3

Temperature during Larval Feeding, 24°C.

15 9 30 21 0 0.01 0.0 15 9 30 39 0 0.01 0.0

15 9 24 63 0 0.01 0.0 15 9 24 84 0 0.0! 0 .0

15 9 12 42 10 23.81 31.1 15 9 12 26 10 38.5,

31.1

15 9 12t 42 1 2.4< 1 o 15 9 12t 25 0 0 .0 ; i . ¿i

*Illumination, 26 f. c. fTemperature, 12°C. for 30 days; then 24°C.

These data again show that the production of the diapause factor or hormone is not dependent on the simple ratio of hours of light to hours of darkness, but is controlled by the absolute lengths of the periods of light and darkness.

Effect of Temperature During the Prepupal Period.—All the data previously shown (Tables II to XIII , inclusive) were from experiments

530 Annals Entomological Society of America [Vol. XLII ,

EFFECT OF VARIOUS TEMPERATURES DURING THE PREPUPAL PERIOD ON THE PERCENTAGE OF ORIENTAL F R U I T M O T H LARVAE ENTERING DIAPAUSE

OR QUIESCENCE. TEMPERATURE DURING L A R V A L FEEDING, 30°C.

PHOTOPERIOD DURING LARVAL TEMPERA L A R V A E ENTERING DIAPAUSE

FEEDING* TURE TOTAL OR QUIESCENCE

DURING LARVAE PREPUPAL

Hours Hours PERIOD, Unweighted Mean

Per Cent Light Per Day

Darkness Per Day

DEGREES C. Number Per Cent Unweighted

Mean Per Cent

9 15 30 38 0 O.O1

0.0 9 15 30 50 0 0 0 0.0 9 15 24 44 0 0.0 0.0 9 15 24 39 0 0 0 0.0 9 15 12 48 13 27.1 23.8 9 15 12 44 9 20.5. 23.8 9 15 12t 48 2 4.21 2.1 9 15 12f 44 0 O.Oi 2.1

12 12 30 38 1 2.7< 12 12 30 99 1 1.0 1.5 12 12 30 134 1 0.7 12 12 24 37 0 0.01 12 12 24 93 3 3.2 1.4 12 12 24 199 2 1.0 12 12 12 46 24 52.2^ 12 12 12 94 34 36.3 37.3 12 12 12 94 22 23.4 12 12 12f 45 2 4.4 12 12 12t 84 2 2 4 3.4 12 12 12f 88 3 3.4 15 9 30 46 0 0.01 0.0 15 9 30 31 0 0.01 0.0

15 9 24 50 0 0.01 0.0 15 9 24 46 0 0.0! 0.0

15 9 12 27 8 29.61 31.1 15 9 12 43 14 32.61 31.1 15 9 12f 27 0 0.01 0.0 15 9 12f 43 0 0.0J 0.0

*niumination, 26 f. c. fTemperature, 12°C. for 30 days; then 24°C.

It should be remembered in reading Tables XIV and X V that larvae grown at 12° and 30° C. did not exhibit true diapause even when grown under a photoperiod that induced diapause at medium temperatures. No differences are shown between the larvae held at 30° C. and those held at 24° C. When held at 12° C. during the prepupal period, pupation was greatly delayed, but about the same pupation pattern was shown as

with insects held at 24° C. during the prepupal period, except for a few held at 21° C. Certain other larvae were held at 12° and 30° C. during the prepupal period in order to determine the effect of high and low temperatures at this stage of the life cycle. Results are shown in Tables XIV and XV.

T A B L E X V


at higher temperatures, so that pupation was apparently completeafter about 30 days. If these larvae were then moved to 24° C, manyof those that had not pupated at the lower temperature did so in thecourse of the next week. This showed that many of the larvae that didnot pupate in the expected time at 12° C. were not actually in diapausebut only temporarily arrested in development.

It is well known that the full-fed larvae of the oriental fruit mothmay be stored for several months at 1° C. without pupation. Theeffect of holding the larvae at 12° C. was similar. Some of the larvaepupated, but the others were quiescent. This state of quiescence, dueto cold, resembles diapause, except that it is nonpersistent and develop-ment is resumed as soon as the insects are warmed; whereas diapause,once started, must run its course.

As is shown in Table XIV, those larvae which had been fed at 12° C.were quite prone to remain quiescent when held at the same temperatureduring the prepupal period. They showed a sensitivity to cold in the

TABLE XVIEFFECT OF VARIOUS HUMIDITIES DURING THE PREPUPAL PERIOD ON THE PERCENTAGE

OF ORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

PER CENT RELATIVEHUMIDITY

050

100

TOTAL LARVAE

5011435


Number

110

Per Cent

2.00.90.0

Temperature during larval feeding period, 30°C; daily photoperiod, 12hours; temperature during prepupal period, 24°C.

matter of the induction of quiescence when compared with larvae grownat higher temperatures. It may be that this result was obtained becauselarvae grown at 12° C. had not begun the first part of the changesleading to pupation before emergence, as may have been the case withlarvae grown at higher temperatures. Larvae completing developmentin the field during the winter may delay their emergence until springbecause of this sensitivity to the induction of quiescence by cold, eventhough they did not enter a state of true diapause. Cousin (1932)recorded a similar effect in Lucilia sericata, and stated that those larvaewhich were grown at low temperatures were more readily stored at lowtemperatures.

Effect of Humidity During the Prepupal Period.—Mainly becauseCousin (1932) reported that Lucilia larvae stored in either saturated ordesiccated air failed to pupate, an experiment was conducted to testthis on oriental fruit moth larvae. A batch of larvae grown at 30° C,with a 12-hour photoperiod, was divided into three lots. One lot washeld at 50 per cent relative humidity; the second lot was placed in atight jar over anhydrous calcium chloride, which reduced the relativehumidity to practically zero per cent; and the third lot was placed in


another tight jar over wet sand, which saturated the air. As shown inTable XVI, there were no differences between the lots. No diapauseor arrest of development was induced.

Miscellaneous Observations.—It was noticed early in the work that inany experiment in which only a part of the larvae entered diapause,those larvae which emerged from the fruit early were less likely to enterdiapause than those which emerged later. An example of this is shownin Table XVII. Apparently, those larvae which will enter diapausefeed a little longer, on the average, than those which will not.

Larvae grown under conditions that induce very little diapausepupate promptly, the pupation occurring over a comparatively shortperiod. With larvae grown under conditions that induce considerablediapause, however, the pupation period is protracted, stragglers pupatingover a rather extended period. This suggests that there is a balance

TABLE XVIIRELATION BETWEEN LENGTH OF LARVAL FEEDING PERIOD

LENGTHOF

LARVALFEEDINGPERIOD,IN DAYS

12131415161718

AND PERCENTAGE OFORIENTAL FRUIT MOTH LARVAE ENTERING DIAPAUSE*

EXPERIMENT 28

TotalLarvae

437

116151663516

Per CentDiapause

0.00.02.6

14.625.814.325.0

EXPERIMENT 29

TotalLarvae

13539164602713

Per CentDiapause

0.024.544.050.056.744.423.1

EXPERIMENT 30

TotalLarvae

10637646402217

Per CentDiapause

10.015.928.932.645.045.564.7

MEANPER CENT

LARVAEENTERINGDIAPAUSE

3.313.525.232.442.534.737.6

*Temperature during larval feeding period, 24°C; 15 hours light and 12hours darkness per "day"; illumination, 26 f. c. Temperature during prepupalperiod, 24°C.

within the insect, and that under these conditions certain individualsare "on the fence," the factors pushing them toward immediate pupationjust about equaling the factors pushing them toward diapause.

The duration of the period that oriental fruit moth larvae remain indiapause, once they have entered, is determined by the temperature atwhich they are held. The higher the temperature, the shorter theperiod of inactivity. At 26° C. they emerge from diapause in abouttwo months. Exposure to low temperature appears to have no tendencyto break the diapause, its only effect being to prolong the period thatthe larvae remain in that state.

Discussion.—Length of day plays the dominant role in determiningwhich individuals of the oriental fruit moth will enter diapause. It ispossible to grow this species indefinitely without the intervention ofdiapause by using a photoperiod either too long or too short to induce it.The potentiality of dispause always remains, however, since diapause


occurs when any larvae are exposed to the proper conditions during thelarval feeding period.

The induction of diapause appears to be caused by a hormoneproduced during the larval feeding period in response to the properphotoperiod at medium temperatures. This hormone apparentlyis produced by a two-phase reaction, one phase of which goes on in thedark, and the other in the light. The darkness-induced phase of thereaction must continue for about 11 hours each day before it is suffi-ciently complete to allow the production of the hormone; and, similarly,the light-induced phase of the reaction must continue for about 7 hours.There is also a maximum limit for each phase of the reaction, that forthe darkness-induced phase being about 16 hours and that for the light-induced phase being between 16 and 18 hours.

It seems probable that this diapause-inducing factor acts only toinduce diapause, not to control it after its induction. Once diapausehas been started, it must run its course, and the amount of the hormonewhich caused its onset does not appear to affect its normal course.

The question has been raised whether the effect of the photoperiodon the larvae may not be secondary, that is, caused by a hormoneproduced in the fruit and taken up by the larvae in feeding, ratherthan by a hormone produced in the larvae. It has not been possibleto grow either the oriental fruit moth or the codling moth on any non-living medium, which would have settled this point. Three con-siderations point to the primary nature of the effect: (1) The fruit isnot opaque; light passes through it reasonably well and so reaches theinsect feeding inside. (2) So far as is known, the production of photo-periodically induced hormones in plants is in the leaves, and allexperiments reported here were with excised fruits. (3) Plant hormonesare ordinarily rather persistent, but results obtained in this work showedno influence from the photoperiod to which the fruits had been exposedbefore their infestation.

The codling mothThe codling moth, Carpocapsa pomonella (L.), is closely related to

the oriental fruit moth and is similar to it in life history and habits.Individuals of this species also enter diapause in the late summer or falland pass the winter as full-fed larvae. The main difference betweenthe codling moth and the oriental fruit moth in regard to diapause isthat the codling moth produces hibernants in appreciable numbersduring the summer.

Only enough experiments were conducted to show that the sameprinciples hold for the codling moth as for the oriental fruit moth.Table XVIII shows the effect of the photoperiod on the percentage ofcodling moth larvae entering diapause. By comparing this table withTable II, it may be seen that the results are similar, the difference beingthat at 14 hours light and 10 hours darkness per day a considerablylarger percentage of the codling moth larvae entered diapause. Thetwo species react the same to 15 hours light per day.

Experiments were also conducted to determine the effect of growingthe codling moth larvae at 12° and 30° C. Results were similar tothose obtained with the oriental fruit moth, except that at 12 hours light


per day and 30° C. about three-fourths of the codling moth larvaeentered diapause. It appears that either a higher temperature or alonger photoperiod is required to prevent diapause in the codling moththan in the oriental fruit moth.

The greenbottle fly

A great deal of work on diapause has been done with the greenbottlefly, Lucilia sericata Meig. It was decided to investigate this species,incidentally, partly as a check on the earlier work by Robaud (1922)and Cousin (1932), and partly in hope that the species would reactto length of photoperiod and thus give us a species in which the photo-periodic effect could be shown to be definitely primary. Results obtainedshowed that, although there is a considerable amount of true diapausein this species, the photoperiod has no effect. The percentage of larvaeentering diapause was greatly increased by the use of low temperatures

TABLE XVIII

EFFECT OF NUMBER OF HOURS OF LIGHT PER DAY DURING LARVAL FEEDING PERIODON THE PERCENTAGE OF CODLING MOTH LARVAE ENTERING DIAPAUSE*

HOURS PER DAY OF

Light

12131415

Darkness

1211109

TOTALLARVAE

22636136


Number

2261460

Per Cent

100.096.875.40.0

""Temperature during larval feeding period and prepupal period, 24°C;illumination, 26 f. c.

during the larval feeding period. Low temperatures during the pre-pupal period did not induce diapause, but only arrested developmenttemporarily.

Cousin (1932) reported that the pupation of full-fed Lucilia larvaewas prevented by holding them in closed containers at either 100 percent or zero per cent relative humidity. These larvae died after a fewdays. We repeated this work with the addition of an experiment inwhich saturated fresh air was circulated through a container. Theresults obtained in the closed containers were similar to those reportedby Cousin, but the larvae held at 100 per cent relative humidity withair circulation pupated normally. The prevention of pupation in theclosed containers was apparently caused by the foulness of the confinedair, which poisoned the larvae.

The vegetable weevil

The vegetable weevil, Listroderes obliquus Klug, has only onegeneration per year. Adults pass the summer in diapause, hidingunder trash on the ground, and do not develop eggs until fall. The


larvae feed through the winter, pupate, and emerge as adults in thespring.

An experiment was conducted to determine whether or not thelength of the photoperiod affected entrance into diapause in this species.Larvae were grown under conditions of 9, 15, and 24 hours light perday. In all cases all the adults entered diapause, the length of thephotoperiod having no effect on the induction of diapause. Apparently,the vegetable weevil enters diapause each generation, regardless of theconditions under which it is raised and held. Attempts were madeto break the diapause in the adults by changing the photoperiod and bysoaking them in water. Neither method was successful.

SUMMARY

Diapause is a physiological state of arrested development whichenables an organism to survive more easily a period of unfavorableconditions.

It is possible to divide the insect species which enter diapause intothe following groups:

1. Species which enter diapause each generation. It may be thatany conditions which allow these insects to live and develop inducediapause.

2. Species which enter diapause only in response to certain stimuli.There may be several generations between periods of diapause, or,under the proper conditions, diapause may appear in each generation.Diapause may be induced by any factor in the environment or by anycombination of factors. The factors most commonly involved are:(a) temperature, either high, medium, or low; (b) moisture, eitheratmospheric or in the food; (c) food, through its quantity, quality, ormoisture content; and (d) photoperiod.

All these behavior patterns are inherited, and there are a few speciesin which some strains differ from others in their behavior patternsor in their sensitivity to environmental stimuli.

The induction of diapause in the oriental fruit moth is controlledby temperature and daily exposure to light during the larval feedingperiod. Larvae grown in the absence of light do not enter diapause.As the period of light per day is increased to more than 3 hours, thepercentage of diapause increases, reaching 100 per cent with about12 hours of light per day. As the photoperiod is increased to morethan 13 hours per day, the percentage of diapause drops suddenly topractically zero, and remains at or near this point during furtherincreases in light.

The photoperiodic effect on the induction of diapause in the orientalfruit moth is apparently caused by a hormone which is produced by atwo-phase reaction during the larval feeding period. The light-inducedphase requires not less than 7 nor more than 15 hours per day, andthe darkness-induced phase requires not less than 11 nor more than 16hours per day, to bring the reaction to a successful conclusion.

Diapause is induced only at medium temperatures. Either highor low temperatures during larval feeding prevent its occurrence.

The codling moth, Carpocapsa pomonella (L.), enters diapause underthe same conditions as does the oriental fruit moth, except that it


requires a slightly higher temperature or a slightly longer photoperiodto prevent diapause.

The greenbottle fly, Lucilia sericata Meig., enters diapause inresponse to low temperatures during the larval feeding period. Thephotoperiod has no effect.

The vegetable weevil, Listroderes obliquus Klug, has only onegeneration each year and apparently enters diapause in each generation.

ACKNOWLEDGMENTS

The author wishes to express appreciation for advice and assistancegiven by Professor H. S. Smith, Dr. Earl Sanders, Mrs. Metta McD.Johnson, Professor Roderick Craig, Professor A. M. Boyce, Dr. S. E.Flanders, Professor W. M. Hoskins, Dr. F. M. Turrell, Dr. F. A.Gunther, Dr. Frank Summers, Mr. J. G. Shanafelt, Miss MargaretBuvens, Mrs. Louise Ratcliff, Dr. M. M. Barnes, Miss Helen Hillman,and Mr. C. A. Fleschner.

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Arbuthnot, K. D. 1944. Strains of the European corn borer in the United States.U. S. Dept. Agr. Tech. Bui. 869: 1-20.

Babcock, K. W. 1924. Environmental studies on the European corn borer(Pyrausta nubilalis Hubn.). (Abstract.) Jour. Econ. Ent. 17: 120-125.

Baker, F. C. 1935. The effect of photoperiodism on resting, treehole, mosquitolarvae. Canad. Ent. 67: 149-153.

Bodine, J. H. 1932. Hibernation and diapause in certain orthoptera. III. Dia-pause—a theory of its mechanism. Physiol. Zool. 5(4): 549-554.

Bonnemaison, L. 1945. Arrets de development et diapauses. Ann. desfipiphyties (n.s.) 11: 19-56.

Cousin, G. 1932. Etude experimental de la diapause des insects. Bui. Biol.de la France et Belg. Sup. 15: 1-341.

Davidson, J. 1929. On the occurrence of the parthenogenetic and sexual forms inAphis rumicis L., with special reference to the influence of environmentalfactors. Ann Appl. Biol. 16: 104-134.

Dawson, R. W. 1931. The problem of voltinism and dormancy in the poly-phemus moth (Telea polyphemus Cramer). Jour. Exp. Zool. 59(1): 87-131.

Dickson, R. C, and Earl Sanders. 1945. Factors inducing diapause in the orientalfruit moth. Jour. Econ. Ent. 38: 605-606.

Ditman, L. P., G. S. Weiland, and J. H. Guill, Jr. 1940. The metabolism in thecorn earthworm. III. Weight, water, and diapause. Jour. Econ. Ent. 33(2):282-295.

Goldschmidt, R. 1933. Lymantria. 186 pp. Berlin-Dahlem.Greulach, V. A. 1942. The length of the photoperiodically effective twilight

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Prebble, M. L. 1941. The diapause and related phenomena in Gilpinia polyloma(Hartig). I. Factors influencing the inception of diapause. Canad. Jour.Res., Sect. D, Zool. Sci. 19: 295-332.

Robaud, E. 1922. Etudes sur le sommiel d'hiver pr6-imaginal des muscids. Bui.Biol. de la France et Belg. 56: 455-544.


Sajo, K. 1896. Sommerschlaf eines Kafers. Illustrierte Wchnschr. f. Ent.1:87-89.

Salt, R. W. 1947. Some effects of temperature on the production and eliminationof diapause in the wheat stem sawfly, Cephus cinctus Nort. Canad. Jour.Res., Sect. D, Zool. Sci. 25(2): 66-86.

Squire, F. A. 1940. Observations on the larval diapause of the pink bollworm,Platyedra gossypiella Saund. Bull. Ent. Res. 30: 475-481.

Strelnikov, I. 1936. Wasserumsatz und diapause bei Loxostege sticticalis. Compt.Rend. Acad. Sci. U.R.S.S. (n.s.) 1(6): 267-271.

Uvarov, B. P. 1931. Insects and climate. Ent. Soc. London, Trans. 79: 1-247.Uyema, Y. 1926. Bui. Seric. Assoc. Japan 1: 1-26.Van der Goot, P. 1925. Levenswijse en bestridjing van den witten rijstboorder

op Java. Meded. Inst. Plantenziekten. No. 66. 306 pp.-Wadley, F. M. 1931. Ecology of Toxoptera graminum, especially as to factors

affecting importance in the northern United States. Ent. Soc. Amer. Ann.24:325-395.

Wheeler, W. M. 1893. A contribution to insect embryology. Jour. Morph.8: 1-160.

Wigglesworth, V. B. 1939. The principles of insect physiology. 434 pp. E. P.Dutton and Co.

WHAT BUTTERFLY IS IT?, by ANNA PISTORIUS. 25 pages. Wilcox andFollett Co., Chicago. 1949. Price, $1.25.

This is something more than an ordinary children's book (if the term "ordi-nary" can be applied to children's books of today); it has some usefulness for thebeginning leopdopterist. Fifty-three butterflies (the cover advertisement saysfifty-four) are illustrated in color, with some condensed, simply and interestinglywritten information concerning each of them. One might take exception tocertain statements in the book, for example, the implication that the monarchoccurs earlier in the season than the mourning cloak, or the answer to the question,"What butterfly worries farmers?" (Why not the cabbage butterfly, ratherthan the hop merchant?) Nevertheless, the book, with its quiz-game style,its attractive appearance, and the apparent accuracy of the natural-size illustra-tions, should, in addition to its entertainment value, inspire appreciation andcreate new interests among young nature students. Entomology needs to beadvertised favorably, and one way to do this is to place such works as this in thehands of children.—M. T. J.

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