Table Of ContentZOOLOGICAL SCIENCE 11: 883-887 (1994) 1994ZoologicalSocietyofJapan
Control of Seasonal Development by Photoperiod and Temperature
in the Linden Bug, Pyrrhocoris apterus in Belgorod, Russia
Aida H. Saulich1 Tatyana A. Volkovich1 and Hideharu Numata2*
,
1Laboratory ofEntomology, BiologicalResearch Institute, St. Petersburg
University, St. Petersburg 198904, Russia 2Department of
Biology, Faculty ofScience, Osaka City University,
Sumiyoshi, Osaka 558, Japan
—
ABSTRACT The life cycle of the Belgorod population of the linden bug, Pyrrhocoris apterus (L.) (Heteroptera,
Pyrrhocoridae) was observed in the field, and under quasi-natural rearing conditions. There were univoltine and
bivoltinepathwaysinthelifecycle. Theemergenceofdiapauseadultsunderquasi-naturalconditionswasconsistentwith
the parameters of photoperiodic response obtained by experiments at constant photoperiod and temperatures. The
temperaturedependenceofthephotoperiodicinductionofdiapauseplaysasignificantroleinlifecycleadaptationinthis
species.
INTRODUCTION In the present study, we first observed the life cycle of
the Belgorod population of P. apterus, and then reared the
It is accepted that photoperiodic responses play a major insects under quasi-natural conditions. We discuss a likely
role in the control ofseasonal life cycles in insects [2-4, 14]. role for temperature dependency of the photoperiodic re-
However, it is often difficult to apply laboratory results sponse in the life cycle adaptation of P. apterus based on a
obtained under constant photoperiods and temperatures to comparison of the laboratory findings [9] with those under
predict seasonal development in the field. Therefore, phe- quasi-natural conditions.
nological observation in the field and experiments under
naturalconditionsarebetterwaystodiscusslifecycleadapta- MATERIALS AND METHODS
tion in an insect.
The linden bug, Pyrrhocoris apterus, has an adult di- Observations and experiments were carried out in the reserva-
apausecontrolledbyalong-dayphotoperiodicresponse [5,9, tion, "Forest on the River Vorskla" (50°N, 36°E), in Belgorod
12, 16]. In a previous paper, we showed the photoperiodic Region, Russia, on the local population of P. apterus in 1990 and
response of P. apterus in Belgorod Region, Russia, under 1991.
conditionsofconstanttemperatureandunderthermoperiodic Nymphs of P. apterus were reared from the first instar in a
meteorologicalboothplacedintheopen, bythemethodspreviously
conditions in the laboratory. Although thermoperiod had a
slight effect on the induction of diapause, the critical day- cdemschriigbhedfr[o9]m.theThgerosuhnedl.f whOenrleyitnhseecntosrtwherseidereoafrtehdewbaosotahbooupten1e3d0
length essentially depended on the mean temperature [9]. and the insects inside were protected from direct sunlight. The
However, the adaptive significance of this temperature de- temperatureintheboothwasrecorded. Afteradultemergence,the
pendence remained unclear. insects were reared as male and female pairs in Petri dishes (9cm
In all populations of P. apterus examined until the diameter). Ovipositionwasrecordeddaily, andifafemale didnot
present, the diapause is facultative [5, 9, 12, 16], and there- layeggsfor30daysfromemergencewejudgedittobeindiapause.
fore they all have the possibility to produce two or more Fifth- (final-) instar nymphs were collected from the field and
generations a year. However, a univoltine life cycle has raised to adults in cages (45cm diameter, 80cm height) on the soil
been observedin the populationin Paris, France [10], and in surface. The cage was made of a wire-frame with a gauze net
thatincentral Bohemia [5, 6]. In Kazakhstan andUkraine, coveringthetopandsides,andtheframewasburiedintothesoilata
depth of 10cm. Thick branches andpieces ofbark were placed in
the possibility of a partially bivoltine life cycle was reported
the cage to protect the insects from rain and direct sunlight. The
[1, 15]. Until recently, however, no reliable evidence has temperature on the soil surface in the cage was recorded. The
been shown ofthe voltinism in P. apterus, because adults of incidence ofdiapausewas examined asfor the insects in the booth.
this species have a long life-span and oviposition period and Some insectswere reared from the first instar in the laboratory
therefore it is difficult to discriminate the generation of under 18L-6D at 25+TC, and transferred to 16L-8D or 12L-12D
adults. Recently, Socha and Sula [13] showed the occurr- duringthefifthinstar. Theirdiapausestatuswasexaminedasstated
ence oftwo generations ofP. apterusin oneyearinsouthern above.
Bohemia.
ReceivedJune24, 1994
AcceptedNovember 14, 1994
Towhom all correspondence should be addressed.
884 A. H. Saulich, T. A. Volkovich and H. Numata
RESULTS although we did not record the date of their earliest emerg-
ence. In 1991, new adults emerged from mid-June.
Phenological observation
Adults after overwintering appeared on the ground in Rearingfrom thefirst instar
late April both in 1990 and in 1991. On warm sunny days Todefinethenumberofgenerationsinayear,wereared
from early May, we observed mating and oviposition. P. apterus from the first instar in a meteorological booth
Thereafter we found both nymphs and adults until late under quasi-natural conditions in 1990 and 1991. We used
autumn. Because adults lived and continued to lay eggs for eggs laid by adults after overwintering. In 1990, we placed
a long period, it was difficult to divide generations only by first-instar nymphs just after hatching in the booth on 3, 13
field observations. We could only determine the beginning and 20 June. In this year, it was cool in June; the mean
of emergence of new adults, because they had a richer red temperature for ten days was 13.6-15.5°C. Therefore, the
color andsofterintegument thanolderadults. Thesediffer- nymphsdevelopedslowlyandnewadultsfirstemergedaslate
ences disappeared a few days after adult emergence. In as7August. Alladultsentereddiapauseexceptforonlyone
1990, we observed new adults at the beginning of July, that emerged on 10 August (Fig. 1).
-18
17
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16
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20 15
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May June July August
Fig. 1. Induction of adult diapause in Pyrrhocoris apterus under quasi-natural conditions in 1990 and 1991. Each horizontal line shows an
experimental series. The outset corresponds to the hatching ofthe nymphs. Date ofadult emergence in females is shown at the end of
line as histograms. Black, diapause; white, reproductive. Circles show the mean temperatures for ten days in the meteorological booth
used fortheexperimentsin 1990(closed) and in 1991 (open). Solidline, naturaldaylength includingciviltwilightat50°N(afterBeck [2]).
Dotted line, critical temperature for the induction ofdiapause in P. apterus (after Numata etal. [9]) (see Fig. 2).
Seasonal Development of the Linden Bug 885
In 1991, weplacedfirst-instarnymphsintheboothon23 Table2. Effect of photoperiodic transfer from long-day to
and 27 May, 6, 13 and 25 June. In this year, the mean short-dayconditionsbefore adultemergenceontheinduction
temperature for ten days in June was 16.5-22.9°C, and of adult diapause in Pyrrhocoris apterus at 25°C
thereforenymphsdevelopedmuchfasterthanin 1990. New Photoperiodic
adultsfirst emergedon2July. Allfemales emergingbefore Photoperiodic t—rdanasyfser,before No. of Dairs % diapause
10Julylaideggs. From 12to21 July, bothreproductiveand conditions adult used
emergence
diapause female adults emerged, and all females emerging
after 22 July entered diapause (Fig. 1). 18L-6D—16L-8D 12 25 100
9 26 100
Rearing ofthefield-collected nymphs 8 20 80
Thus, we knew when diapause adults emerged in the 4 24 50
booth under quasi-natural conditions. However, the 25 8
temperature in the booth used in this experiment differed 18L-6D—12L-12D 9-11 26 100
from that on the soil surface where the insects develop in 4 17 35
nature. Furthermore,thenymphsofthisspeciesbehavioral- 26
ly select microhabitat [8]. Therefore, to determine the
actual time of emergence of diapause adults, we collected ence were enough to induce adult diapause in all individuals,
fifth-instar nymphs from the field and kept them in cages on and four cycles were critical, irrespective of the short-day
the soil surface in 1991. After adult emergence, we ex- conditions used (Table2).
amined their diapause status (Table 1). From the samples
collected on 7 June, adults emerged on 9-14 June, which
DISCUSSION
corresponded to the first emergence ofnew adults in nature.
Theywereallnondiapauseadultsandbegantolayeggsinlate Interaction betweenphotoperiodand temperature
June. On 21 July, the first diapause adults emerged, and In the Belgorod population of P. apterus, the photo-
thereafterdiapauseadultsprevailedinthesamples. Insome periodicinductionofadultdiapausedependsontemperature,
periodstherewasonlyalittledifferencebetweenthetemper- andthe critical daylength is longeratlowertemperatures [9],
atureonthesoilsurfaceandthatinthemeteorologicalbooth, as in many other insects with long-day photoperiodic re-
although in other periods the former was much higher than sponses [2-4, 14]. Moreover, the critical daylength under
thelatter. Forexample, inlateAprilthemeantemperature thermoperiodic conditions is close to that at the constant
of the soil surface was 23.3°C and that in the booth was temperature equivalent to the mean temperature of the
10.3°C, while in mid- and late July, the difference was 3.6- thermoperiod [9]. This species is slightly sensitive to a
3.8°C. gradual increase of the photophase only in the threshold
range [17]. Therefore, we examined whether we could
Table1. Incidence of adult diapause in Pyrrhocoris apterus applythe photoperiodicresponse obtained experimentally at
collected as fifth-instar nymphs from the field in 1991 constantphotoperiodsandtemperaturestothenaturalinduc-
Date of No. of Date of No. of % tion ofdiapause. First, we determined the critical tempera-
collection cnoylmlpechtsed eadmuelrtgence paadiurlst diapause ture for a given daylength, as we had ascertained the critical
daylengths at each temperature (Fig. 2). Then, we showed
7 June 46 9-14 June 20
2 July 35 4-6 July 22 30
12 July 32 14-18 July 18
21 July 6 33
22 July 70 30July-2 August 19 84 P Reproduction
6 August 15 75
Photoperiodicsensitivity 2 25
InP. apterus,thephotoperiodicsensitivitycommencesin CQD.
the fourth or fifth instar and continues throughout the adult E Diapause
life[5]. Fiveorsixshort-daycyclesexperiencedbeforeadult
emergencewereenoughtoinducediapauseinthepopulation
from central Bohemia [7]. We examined the photoperiodic
sensitivity in the Belgorod population at 25°C. We used 20
18L-6D as long-day conditions, and 16L-8D or 12L-12D as 16 17
short-dayconditions,becausethecriticaldaylengthwasabout Photophase (hr/day)
17hrat25°C[9].
Fig. 2. Effect ofphotoperiod and temperature on the induction of
Nine short-day cycles experienced before adult emerg- adult diapause in Pyrrhocorisapterus (afterNumataetal. [9])
886 A. H. Saulich, T. A. Volkovich and H. Numata
the critical temperature for the natural daylength as a dotted surfacewhereP. apteruslivesinnature, becausethetempera-
line in Figure 1. During periods when the environmental ture on the soil surfacewas sometimes much higherthanthat
temperature is lower than this value, diapause might be in the meteorological booth. Furthermore, we observed in
induced. spring that nymphs and adults aggregated in warm places on
the soil surface where the temperature was muchhigherthan
Voltinism ofthe Belgorodpopulation inthe meteorologicalboothbecauseofradiantheat. There-
IntheBelgorodpopulation ofP. apterus, thereweretwo fore the behavioral regulation ofbody temperature may also
alternative pathways in the life cycle, i.e., univoltine and contribute the difference between the quasi-natural and the
bivoltine. In 1990 (coolweather), newadults emergedfrom real natural conditions. However, we cannot predict the
earlyAugust, andmostofthese entereddiapause. The mean seasonal development ofP. apterus with the temperature on
temperaturefortendaysneverexceededthecriticalvaluefor thesoilsurface,becauseduringthewarmseasonsthenymphs
the induction ofdiapause. Low temperature contributed to of P. apterus select microhabitat where the temperature is
theinductionofdiapauseintwoways: First, itlengthenedthe much cooler than on the soil surface [8].
critical daylength for the induction of diapause. Second, it
delayed nymphal development, and therefore the sensitive Retardation ofnymphal development
stage was postponed to the period when the daylength was The nymphal development of P. apterus is retarded at
short enough to induce diapause. the critical daylength for the induction ofadult diapause ora
In 1991 (warm weather), however, new adults emerged little shorter [9, 12]. The combination of photoperiod and
from early July, and early emerging adults of the first temperature in early July in 1990 was in the range where
generation reproduced. Their progeny, i.e., the second nymphal development is retarded in the laboratory [9],
generation, developing in August and September should although it is unclear whether the slow development of
enter diapause. Furthermore, late emerging adults of the nymphs underquasi-natural conditions in 1990 resulted from
first generation also entered diapause. The mean tempera- retardation due to the threshold range or only from the
tures for mid- and late June and early July were higher than normal effect of temperature. The combination of photo-
the critical value for the induction of diapause. All adults period and temperature in both mid-June and early July in
emerging on and after 22 July entered diapause. When 1991 was also in the range where nymphal development is
insects were transferred from long-day to short-day condi- retarded in the laboratory [9]. Thus, in warmer years
tions nine days before adult emergence in the laboratory, all nymphs possibly meet with threshold conditions twice
of them entered diapause. Therefore, the emergence of throughout the season.
diapause adults under quasi-natural conditions is consistent We assume that at threshold conditions before summer
with the parameters of photoperiodic response obtained by solstice, nymphs had not reached the sensitive stage for the
the experiments at constant photoperiods and temperatures. retardation of development because no nondiapause adults
In the regions where the duration ofthe growing season had an extremely long nymphal period in the present study.
in individual years is nearly constant, photoperiod is an Under threshold conditions after the summer solstice, pro-
effective cue forthe predictionofthecoming season. Sauer longation ofthe nymphal period will delay the emergence of
etal. [11] regardedthetemperaturedependenceofthecritical diapause adults, as Saunders [12] suggested in the univoltine
daylength in Pieris brassicaeboth as an adaptationto the low lifecycleinthepopulation ofthis species in centralBohemia.
predictability of the end of the growing season, and as an In the second series in 1991 under quasi-natural conditions,
adaptationrelatedtomigration. P. apterusdoesnotmigrate some adults emerged much later than the others and entered
and therefore the temperature dependence of the photo- diapause. It has been generally accepted that the range of
periodicresponsehasadaptivesignificancewherethetemper- temperature and photoperiod for the induction of winter
ature varies much between years as in Belgorod Region. diapause is adequate to reach the diapause stage before
Although Honek and Sramkova [8] pointed out that the winter (e.g., [11]). The diapause adults developing in ear-
production of the second generation as an unfavorable mod- lierseasonshave enoughtime beforewinterandprolongation
ification of the life cycle in P. apterus in central Bohemia, ofthe nymphal period is less harmful for them than for those
there is no doubt that the Belgorod population of P. apterus developingin laterseasons. Ifthe diapause adultsemerging
partially produces two generations in warmer years. after an extended nymphal period have a larger body size,
However, it seems that even in cooler years the Belgorod higherfecundity or lower mortality in winter, the retardation
population is not homogeneously univoltine, because we of nymphal development would have adaptive significance.
found some new adults layingeggs in earlyJulyeven in 1990, Further studies are needed to clarify these.
when it was cool (unpublished). Furthermore, the propor-
tion ofdiapause adults emergingfrom the fifth-instar nymphs ACKNOWLEDGMENTS
collected from the field was lower than that in insects reared
from the first instar under quasi-natural conditions in 1991. We thank Dr. Ivo Hodek. Institute of Entomology, Czech
We attribute these differences in part to the differences in Academy ofSciences, for critical reading ofthe manuscript.
temperature between the meteorological booth and the soil
Seasonal Development of the Linden Bug 887
de development chez Pyrrhocoris apterus L. (Heteroptera,
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