Periodicity of Aradus cinnamomeus (Heteroptera, Aradidae)in northern Europe

KARI HELIOVAARA & RAUNO VAISANEN

HeliOvaara,K.&Viiisdnen,R:PeriodicityofAroduscinnamomeuslHeleroPtell,Aradidae)in n*tttirn'grrop". IPeriodicitet hos t allba rkstinkflyet, .4 radus c-innamomeus (H-et€roPtera'

a*JiJ'"Lii*tt"'euiopa.'l- Ent. Tidskr. l09: 53_58. Ume6, Sweden 1988 ISSN 0013-886x'

General characteristics of the life-cycle rhythms of Aradus cinnamomeus are described in

S.-Oin"ulu on,t "ompared

to previous studies from Finland. The species normally has a two-

vear life-cvcle in mosioarts ot its range, but at higher lalitudes and altitudes the life'cycle takes

inri. i.",:t tn the Aland archipelag6 and possibly on Cotland the life-cycle take.s three years

Reoroduction takes Dlace in even icars in most parts of the two-year area' while in western

iiri."J "ra

i" *..teh Swe6en therc arc wide areas where the bugs reproduce almost exclu-

sively in odd years.Nirmallv one of the alternate-year cohorts almost exclusively predominates, the shifis in

"r""""J"iin""i.ine relativelv shim. The lhree-year cohorts usually coexist in subequal num-

Liil in ouire "n

irtes,"ular fashi6n. lt is suggested t hat one of the alternate'year cohons prevents

the incriase rn denslty of the other generation by inducing dcfensive chemical chang€s ln tne

"ir.. ir-it

" arca of three-year I ife-iycle the eridus-induied chcmical changes are suggested

i;;;;;;;;;i,;ihe traisl climatic conditons' thus permitting thc coexistence of allochronrc

bug cohorts.

K- Helidvaarq, Finnish Forest Reseorch lnstitute, Pl 18, SF-l1301 Vantaa, Finlond'

i. iiiii"ii, irrtrsical Museum, ()niversity of Helsinki, P Routatiek' 13, 5F40100 Helsinki'

Finland.

Introduction

The pine bark bu g Aradus cinnamomeus (Panzer)

is a periodical species with more or less distinct re-

productively isolated allochronic populations or

cohorls. These cohorts are either sympatric orparapatric, depending on the life-cycle rhythm

conccrned and the geographical scale used in the

analysis. Examples of similar periodical pheno-

mena among insects are numerous (Bulmer 1977):

the alternate-year flight of certain Lepidoptera(e.g. Valle 1933, Suomalainen 1937, Mikkola1976, Imby & Patmqvist 1978, Douwes 1981), the

periodical apPearance of the North American 13

and l7-year cicadas (Lloyd & Dybas 1966a' b'Simon et al. 1981, Lloyd et al. 1983), and the

European cockchafers (Hurpin 1962, Niklas1974). These species show unusual biogeographi-cal patterns which are not only exciting curiosities

of nature, but of wider interest to ecologists and

entomologists.Documentation of the pattern is a prerequisity

for further discussion on the alternative hypo-

theses proposed to explain these phenomena.

Hcre, we describe the general characteristics ofthe distribution and life-cycle rh)'thms of A/aduscinnamomeus inscandinavia, as compared to pre-

vious investigations from Finland (Helitivaara &Viiisiinen 1984a. b, 1986, 1987, Heli6vaara et al.,in press). This areal extension of the study pro-

vidis further evidence for determining which of

the various explanations of the pattern is most

feasible. The pine bark bug was studied in Sweden

by Brammanis (1975) especially, whose biogeo-

graphical findings are discussed and re-evaluated.The pine bark bug is a hemimetabolous sap-

sucker living on young Scots pines (Pinus sylves-

rris) and preferring dry sunny forests and pinc

bogs. lt has caused serious damage on pine stands

in many parts of Eurasia, including esker ridges ofsouthern Finland. The life-cycle of the bug nor-matly takes two years. The bugs overwinter first as

fourth instar nymphs and, after maturation in Au-

54 Kari Helitivaara & Rauno Viiisiinen

gust-September of their second summer, again asadults. The adults mate and reproduce normallyduring the following spring. In the north the life-cycle is prolonged to three years (Brammanis197s).

Malerial and methods

Only scattered records of the life-cycle of the pinebark bug in Scandinavia are available (Brammanis1975, Helidvaara & Viiisiinen 1987). In the pre-sent study new data were gathered from variousparts of the area, mainly during two longer excur-sions in July 1986 and August 1987. Altogetherabout 60 sample localities were examined. A ques-tionnaire was also sent lo forest zoologists, and afew well-known specialists were consulted.

The bug samples were collected from pine sap-lings growing along roadsides. Bark was removedfrom several pine trunks until at least 10 bugs hadbeen found. The developmental stage of the bugswas determined on every plot.

Results

The distribution of the pine bark bugs with differ-ent life-cycle rhythms in northern Europe is map-ped in Fig. l. The picture that emerges from thisinvestigation in Scandinavia is very similar to thatof the Finnish one. In the southern and centralparts of the study arca the life-cycle of the bugtakes two years, while in the north the bugs have athree-year development. Generally, the even-year cohort almost exclusively dominates wherethe bugs are biennial, i.e. in eastern and centralFinland, eastern and central Sweden, and south-eastern Norway. However, in large areas in bothwestern Finland and western Sweden, as well as insome areas in Norway, the odd-year bugs almostexclusively predominate. There appears to beonly a narrow transition zone between the allo-chronic cohorts in Swcden, as in Finland wherethe pattern is espccially sharp (parapatry). Insouthern Sweden and Norway the pine bark bugappears to be less abundant than in southern Fin-tand. This is probably simply due to the lack ofsuitable habitats, dry sandy heath forest and pinebogs with pine saplings. In Estonia, the even-yearcohort apparently prcdominates (20 even-yearbugs from Poltraaga, 'l odd-year bug from Tartu).

In northern Fennoscandia the life-cycle of thebug takes three years. However, the three-year

area extends much further to the south on theSwedish than on the Finnish Bothnian coast, al-though the exact location of the transition zonebetween a two and three-year development periodwas not clarified. There are difficulties in inter-preting the samples collected near Sundsvall incentral Sweden and at Hamar in southern Nor-way. They may represent normal three-year bugs,or two-year bugs reproducing in the odd years, ora mixture of these two groups. In Finland there isa narrow belt of odd-year bugs between evcn andthree-year bugs in the area N of Jy.vaskylii, whilein the area E of Kokkola this seems to be missing.The transition zone between the two and three-year bugs seems in any case to be wider and morecomplex than that between even and odd-yearbugs. In the Scandinavian mountains and at manvlocalities in central Norway, the bug seems to berare or absent in spitc of the availability of suitableyoung pines.

In Sweden, the arca between Kristianstad andKarlskrona is somewhat cnigmatic in our own ma-terial. It may either represent a transition zone be-tween the even and odd-year bugs or a narrowcoastal area of three-year bugs. The samples con-tained adults and nymphs of more than one instar.This may bc partially due to the collecting timesince individual differences are usually conspicu-ous but decreasc towards the autumn. Further-more, the unusually cold and rainy summer in1987 makes interpretation difficult in certain cases(two-year bugs: unusually small nymphs due tothe weather conditions; or three-year bugs: nor-mal cohort of young nymphs). Also the situationin Denmark deserves further studies.

Discussion

The results on the periodicity of the pine bark bugagree with previous investigations from Finland(Heliovaara & VAisiinen 1987) and, in fact, themost interesting result may be that the Scandina-vian pattern is so conspicuously similar to that inFinland. Brammanis ( 1975) had already obscrvedthat in Sweden the odd-year bugs predominate inDalekarlien (Siljanfors) and in southern Halland(Laholm, Tyldsand, Falkenberg). The odd-yeararea now appeared to be extensive in southwest-ern Sweden. The predominance of odd-ycar bugsin both western Finland and western Swcdenwould appear fascinating. What could explainsuch similar blocks of "wrong"-year bugs? Our in-

SWED EN

Periodicity of Aradus cinnamomeus 55

FINLAND

3-y r area

3-yr are a

NORWAY

{-r)N

DENMARK ( 1oo km

I

v a\Fig. 1. The distrihution of -4 rd dus cinnamomeus with different life-cycle rhythms in-nonhern.Europe. Dark grcy-evin-year area. light grey----odd-year area. The proportions of the cohorts in August 1987 are given in the sample Picsas foliows: blacklad-ulti, white-small larvae (insiars I-lII). white with arrows -nedium-sized larvae (instar lV).Additional museum samples examined and data based on literature references are indicated by squares coloured re-spectively. All samples fiom southernmost Sweden havc bccn intcrpreted to represent two-year.bugs.. The Finnishdistribution is based on Heli<ivaara & Vaisanen (198?), the rccords lrom Gotland on Brammanis (1975) and fromsoutheastern Norway pafiially on Pettersen (1975).

Livscykelrytmcr h()s Aradus cinnamomeas i olika delar av Nordeuropa, Tvi-irig livscykel finns blde med vuxna un-der jiimna'(miirkgritr) resp udda (ljusgritt) ir. I ringar och kvadrater anges propotionerna av vuxna (svart), sma

nymter (viti), resf mcdelsiora nymfer (vitt med pil) fbr augusti 1987. Ringarna,baseras pa egna insamlingar, medan

kiadraterna'red&isar proportioner beiaknade utifrin littciaturuppgifter resp djur i museisamlingar. Alla prov frensydligaste Sverige har ansetts representera tvi-6riga stinkflyn.

56 Kari Helitivaara & Rauno Viiisiinen

terpretation is, however, quite trivial. We believethat rhe similarity is primarily due to chance. Theodd-year bug blocks lying in the middle of areaspredominated by even-year bugs may havc bconcaused by a weather catastrophe (cf. Vallc 1933)

that has destroyed the original preponderancc re-Iationships by decreasing thc population dcnsitiesto such a low levcl that the odd-year bugs can con-quer "empty arcas".

Dispcrsal could provide anothcr explanation.In thc arcas wherc the three-vear life-cycle is pre-dominant. all thc thrcc cohorts usually'coexist insubcqual numbers. A three-vear area close to a

two-year area could function as a "random domi-nance generator" and change the two-year cyclefrom an even to an odd year one. This is possiblein Finland if the bugs have penetrated via thcAland archipelago or northern areas, while inScandinavia this may have taken placc via thcnorthern arcas, the mountains or possibly south-ern Swcdcn (if three-year bugs exist there).Elscwhcrc in Europe. the even-year bugs are saidto predominatc, but small odd-year cohorts havebecn observed in the Kiev region (Tropin 1949)and in Czechoslovakia (Turtek 1964). In Polandthe pine bark bug has been reported to reproducemainly in odd years (Strawinski 1925).

As mentioned above. the life-cycle of the bugtakes three years in the Aland archipelago in Fin-land (Heliovaara & Viiisiinen 1987). Samplcs cx-amincd from Oland clearly represent thc even-ycar cohort observed by Brammanis (1975). How-ever, he tound that the bugs commonly repro-duced in all years in Mastermyr on Gotland, whileat other sites on the island (Klintehamn, Roma)the bugs reproduced mainly in even years. Theseconfusing records from Gotland may, in fact,suggest that the bug also has a three-year life-cycleon Cotland, at least occasionally. It is also possi-ble that even and odd-year cohorls prcdominatcIocally, and that samples from Mdstermyr wercfrom a transition zone.

Thc predominance ofeven and odd-year bugs indifferent areas, in a parapatric pattern, requiresan explanation. The reason why the odd-yearcohort cannot invade successfully the area whcreeven-year bugs abound (and vice vcrsa), seems tobe duc to thc rclationships between the cohortsthcmsclvcs. One cohort appears to prevent thedispersal and increase in density of the other one.We have suggested that the mechanism might beintraspecific interference compelition, reinforced

by the impact of parasitoids (Heliovaara & Viiis[-nen 1984b). The interference may be mediatedchemically by the pine.

It has been reported that the polyphenol con-tent of Pinus sylvestris changes after attack byNeodiprion sertifer (Thielges 1968). Mechanicaldamage to Pinus ponderosa can cause changes inphenols, procyanins and protein in the foliage(Wagner & Evans 1985). Recently, Leather et al.(1987) reported that insect-induced chemicalchanges caused bv previous defoliation in youngPinus contorta have a negative effect on theoviposition. growth and survival of Panolis flam-msa. Furthermore. adult fcmalcs wcrc able to dis-tinguish between host plants with and without prc-vious defoliation, and lay their eggs so as to takeadvantage of these differences. We thus suggestthat the Aradus female can distinguish betweenpines which have and which have not been at-tacked by another Aradus cohort. Studies on thechemical changes causedby Aradus attack in pinesare in progress. We have observed in field experi-ments that the presence of one cohort has a nega-tive effect on the othcr one, suggesting heavy in-traspecific competilion that may bc pinc mcdiated(Helirivaara & Viiisdncn 1986). Studics do notsupport the idea that predators or discascs wouldhavc a central role in maintaining thc status quo inthc present biogeographical pattern (Helirivaara& Viiisiinen 1984b, Hokkanen et al. 1987).

Another important question concerns the factthat three cohorts of ulradus usually coexist in thethree-year life-cycle area, while in the two-yeararea one of the cohorts almost exclusivcly prc-dominates. If the parasitoids were thc kcy factorcontrolling the pattern, then thc limit between twoand three-year areas would bc thc limit of therange of the parasitoid species. lf intraspecificcompctition was the key factor, the pattern couldbe explained by adopting the stress hypothesis(White 1984). In the north pines may grow undersuch severe climatic conditions that their chemicaldefence mechanisms against insect herbivoreshave deteriorated, and the intraspccific competi-tion mediated by the pine would thus be small.Furthermore, in the thrce competitive cohort sys-tem the rate of disappearance of a smaller cohortor cohorts may be substantially lower than that inthe system consisting of two competitive cohorts,although the intensity of competition would be thesame (Helirivaara & Viiisiinen 1987).

Some evidence supporting the latter pine-

mediated competition hypothesis was obtainedfrom a study on Retinia resinella (L.) (Lepidop-tera, Tortricidae) in northern Europe (Heli<ivaara& Viiis2inen, manuscript). In both these speciesthe limit between the two and three-year life-cycleareas runs almost in the same way (except in theAland archipelago). According to the parasitoidhypothesis, we must assume that both the specificparasitoids of Aratlus and the specific parasitoidsof Retin la (these species have no common parasit-oids) would havc the same distribution limits inthe north. In thc case of thc pine-mediated com-petition hypothesis we only have to assume thatthe stress caused by climate breaks down thechemical defence mechanisms of the pine. Thusthe same assumption could be adopted for bothAradus and Retinia.

Ackmrwledgements. we are vcry grateful to E. Annilaand A. N. Nilsson for t heir comments on lhe manuscriptand to L. Greve Jensqn (Bergen). A. Lindeldw (Upp-sala). F. Midtgaard (As;. E. Olofsson (UPpsala). H. P.

Ravn (Lyngby), K. Skipnes (Stavanger), J. O. Solem(Trondheim), G. E. E. Soti (Tromso) and J. Viidalepp(Tartu) for information about the pine bark bug in Scan-dinavia. The namcs of the authors appear in alphabeticalordcr.

References

Brammanis. L. 1975. Die Kiefernrindenwanze, Araduscinnamomeus Panz. (Hemiptera-Heteroptera). EinBeitrag zur Kenntnis der Lebensweise und derforstlichen Bedeutung. - Stud. Forest. Suecica 123:t-It1.

Bulmer. lvl. C. 1977. Periodical insects. Amer. Nat.111;1099 1117.

Douwes, P. 1981. Periodical appearance of species ofthe butterfly genera Oeneis and Erebia in Fenno-scandia. Ent. Gener. 6 (1980): 151-157.

Heliiivaara. K. & Viiisdnen, R. 1984a. Parapatry of thealtcrnate-year populations of Aradus cinnamomeus(Hctcroptera, Aradidae) in Finland. - Ann. Ent.Fennici 50: 65-68.

- 1984b. The biogeographical m-vster,y of the alternate-year populations ol Aradus cinnamomeus(Heteroptera, Aradidae). - J. Biogeogr. ll: 491-499.

- 1986. Bugs in bags: intraspccific competition affectsthe biogeography of the alternate-year poPulationsof Aradus cinnamomeus (Hctcroptera, Aradidae).

- Oikos 47: 327-33.1.

- 1987. Geographic variatior in the lifc-history ofAradus cinnamomeus and a hreakdown mechanismof the reproductive isolati()n of allochronic bugs(Hcteroptera, Aradidae). - Ann. Zool. Fennici 24:1-17 .

- Manuscript. Poriodicity of Retinia resinella(Lcpidoptera, Tortricidae) in northern Europe.

Heli(ivaara. K. , Vrisenen. R.. Hantula, J. , Lokki, J. &Saura, A.. in press. Genetic differentiation in sym-

Periodicity of Aradus cinnamomeus 5'7

patric but temporally isolated pine bark bugs,Aradus cinnamomeus (Hcteroptera). - Hereditas.

Hokkanen, T.. Helidvaara. K. & VAisiinen. R. 1987.

Cootrol of Aradus cinnamomeus (Heteroptera,Aradidae) with special reference to pine stand condi-tion. - Commun. lnst. Forest. Fenniae 142: 1-27.

Hurpin, B. 1962. Superfamilie des Scarabaeoidea. ln:Balachowsky, A. S. (ed.). Entomologie appliqude a

l'agriculturc. Vol. I . Part 1:24-204. Massin. ParisImby, L. & Palmqvist, G. 1978. De svenska Anomo-

gyna-arternas utseende. biologi och utbredning(Lep.. Noctuidea). (Abstract: The biology and oc-currence of the Swedish Anomogyna species (Lep.,Noctuidae)). - Ent. f idskr. 99: 97 107.

Leather, S. R.. Watt, A. D. & Forrest, G. l. 1987. ln-sect-induced chemical changes in young lodgepolepine (Pinus contorta): the effect of previous defolia-tion on oviposition, growth and survival of the pinebeauty moth, Panolis flammea. - Ecol. Ent. l2:2'.7 518t.

Lloyd, M. & Dybas, H. S. 1966a. The periodical cicaiaproblem. l. Population ecology. - Evolution 20:

l33 149.Lloyd, M. & Dybas, H. S. t966b. The periodical cicada

problem. II. Evolution. - Evolution 20; 44G505.t-lord, M., Kritsky, G. & Simon, C. 1983. A simple

Mendelian model for l3- and [7-ycar life-cycles ofperiodical cicadas, with historical cvidence of hy-bridization between them. - Evolution 3'7: l162-1 180.

Mikkola. K. 1976. Alternate-year flight of northern Xes-tia species (Lep., Noctuidae) and its adaptive signifi-cance. - Ann. Entomol. Fennici 42: l9l-199.

Niklas. O. F. 1974. Familie nreihe Lamcllicornia. Blatt-hornkiifcr. - ln: Schwenke. W. (ed.), DicForstschidlinge Europas. Zweiter Band. pp. 85- 129.

Hamburg. Berlin.Pettersen. H. 1975. Furubarktegen. Aradus cinna-

momeus Panz. (Hemiptera. Heteroptera) - et litekjent skadeinsekt pe skog i Nor8e. (Summary: Thepine flatbug, Aradus cinnamomeus Panz. (Herni-ptera, Hcteroptera) - a little known pest in Nor-wegian forcstry).

-Tidsskr. Skogbr. 2: 259-269.

Simon, C.. Karban, R. & Lloyd, M. 1981. Patchiness,density, and aggregativc behaviour in symparic al-lochronic populations of l7-year cicadas. Ecology62: 1-525-1535.

Strawinski. K. 1925. Historja naturalna korowca sos-nowego. Aradus cinnamomeus Pnz. (Hemiptera-Heteroptera). (Summary: Natural history of Araduscinnamomcus Pnz.). - Rep. Inst. Forcst Prot. Ent.2 ( 1): 1-51.

Suomalaincn, E. 1937. Uhcr das periodische Auftretcnvon Erebia ligea L. (Lcp.. Satyridae) in Finnland. -Ann. Ent. Fennici 3: 78-83.

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58 Kari Helidvaara & Rauno Viiisiinen

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Sammanfaltning

Tallbarkstinkflyet, Aradus cinnamomeus, h^rnormalt en tvir-irig livscykcl. men i norra Skandi-navien och norra Finland dr dcn tre-irig. Diir livs-cykeln er trc-arig sA civerlappar de tre generatio-nerna helt och vuxna djur forekommer varje ar.

Sd iir inte fallet diir livscykeln ir tvi-drig. och vux-na djur forekommer har endast vartannat ir. Den-na periodicitet hos tallbarkstinkflyet iir miirkligsetillvida att regionalt forekommer de vuxna ochreproducerar sig antingen pa udda eller jiimna Ar.Bide i Sverigc och Finland si frirckommer vuxnadjur pl udda dr i tlcn sydviistra dclen, samt i ettsmalt blilte lings griinsen mot det tre-ariga omre-det. Att generationcrna ar Atskilda niir livscykelniir tvi-6rig kan I'orklaras av att den ena kohortenhindrar den andras tillvdxt genom att stimuleratallens kemiska fcirsvar. I mer nordliga omreden,ddr livscvkeln dr treirig, iir tallens kemiska frirsvarej lika efiektivt, och de tre generationerna kansamexistera.

Rccension

Vdgtle, F. & Schuss, W. 19U5. Spiegelstcreoskop.VCIH Vc rlagsgesellsch aft, Weinheim, Vasttysk-land. Pris: zlti:- DM (Besrell-Nr. 1010097).

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Ulf Carlberg