Table Of Content©EntomologicaFennica.16June2006
Identification of adult males and females of Hoplothrips species
(Thysanoptera: Tubulifera) known from Norway,
and some deductions on their life history
SverreKobro&TrondRafoss
Kobro, S. & Rafoss, T. 2006: Identification of adult males and females of
Hoplothripsspecies(Thysanoptera:Tubulifera)knownfromNorway,andsome
deductionsontheirlifehistory.—Entomol.Fennica17:184–192.
The presence of multiple phenological forms has previously made adults of
Hoplothrips species difficult to identify. Wepresent aset ofdiagnosticmetric
characters by which the 8 species recorded from Norway can be recognised.
Somebiologicalinterpretationsarealsogiven.
Sverre Kobro and Trond Rafoss, Bioforsk Plant Health and Plant Protection
Division,Høgskoleveien7,Ås,N-1432Norway;correspondentauthor’se-mail:
[email protected]
Received25November2005,accepted24January2006
1.Introduction
breeding structure. Adults of both sexes of the
fungivorous thrips can be wingless for several
Deadtreesinfectedwithwood-rottingfungicom- generationsandwilldevelopwingsonlyinprep-
pose habitats for a rich fauna of specialised in- arationfordispersal.Thripsspeciesonfungusin-
sects(Hamilton1978).Manythripsspecies,half fected dead trees tend to live gregariously and
of the suborder Tubulifera, are associated with matewithinthehabitat,andsomeofthemhave
deadtrees,theirbark,deadbranchesorleaflitter developedsubsocialbehaviourandstrongsexual
(Palmer&Mound1978,Ananthakrishnan1984). dimorphism (Mound 1974, 1976, Hamilton
These thrips feed on fungal spores, hyphae or 1978,Palmer&Mound1978).Theappearanceof
breakdownproductsfromearlystagesoffungal oedymerous(major)andgynaecoid(minor)male
decay(Mound&Palmer1983,Ananthakrishnan forms reflects reproductive roles of the males
1984)andHoplothripsspeciesmaybecharacter- (Hamilton 1978, Crespi 1986). Mound (1974,
istic for some of the habitats (Ananthakrishnan 1976,2005)andHamilton(1978)suggestedthat
1984). Schliephake and Klimt (1979) noted 11 theproductionofdifferentmorphswascontrolled
speciesfromEuropeofwhichtwohavebeensyn- bytheamountorqualityofthefoodingestedby
onymised (Vierbergen 2004), while some 130 the larvae. The suggestion was confirmed by
species are known for the genus world wide Crespi(1988)intheNearcticspeciesHoplothrips
(Mound&Walker1986). karnyi(Hood).Okajima(1987)ontheotherhand
Afungusinfecteddeadlogprovidessupport related growth patterns to the colony size, and
for numerous generations of Hoplothrips, but Hood(1940)wasabletoproduceeithermacro-
over evolutionary time changes in suitability of pterousormicropterousspecimensatwillbyma-
thehabitathaveprobablyselectedfordifferently nipulating environmental conditions. Wingless-
sized individuals and specialised patterns of ness, polymorphism and gregariousness are
ENTOMOL.FENNICAVol.17 (cid:127) IdentificationofNorwegianHoplothrips 185
adaptionstoincreasethefecundityforfungusfor- Thrips were recorded from bark infested with
aging thrips on dead wood (Ananthakrishnan Hymenochaetetabacina(Kobro2003),Pseudo-
1984,Crespi1986),andatoptimalconditionsal- spiropes longipilus (Kobro & Solheim 2002),
most all individuals are micropterous (Hood Stereum spp. (Kobro 2003), Trichaptum abi-
1940). etinum (Kobro 2001) and T. fuscoviolaceus
The extreme polymorphism of Hoplothrips (Kobro2003).Approximately0.2–0.3m²ofbark
adults (Okajima 1987) is probably the reason containingbasidiocarpswascollectedanddepos-
why identification literature (Priesner 1928, itedinBerlesefunnelsforaboutaweek.Thrips
1964, Morison 1949, Stannard 1957, Mound et were stored in AGA(70% ethanol + glycerol +
al.1976,Dyadechko1977,Schliephake&Klimt aceticacid=10+1+1).Afterstoragethespeci-
1979,Mound&Walker1986,Kirk1996,Mound mensweremaceratedinhotlacticacidorpotas-
&Marullo1996)givesnosinglekeycharacterto siumhydroxide, cleared with clove oil and em-
identifyadultsinthegenus.Moreover,thekeys bedded in Canada balsam on glass slides. Most
areoftenbasedoncolourshadesorgeneralbody measurementsweremadeat500×magnification,
characterssuchasformofthehead,bodypart“a andonlyfullyextendedspecimensorbodyparts
littlelongerthan”etc.andtoalesserextentonex- weremeasured.
actmetriccharacters.Someoftheolderdescrip- Whenpossible,10adultsofeachsexofboth
tions are based upon only one out of several macropterousandmicropterousspecimenswere
forms,andlargeandsmallmaleformsofthesame selected fromdifferent populations and studied.
species have been placed into separate genera Additionally, if available, a larger number of
(Hood1955). specimens fromsingle populations of each spe-
Eight species of Hoplothrips are recorded cieswereexamined.Allspecimenssampledfrom
from Norway (Kobro 2001): Hoplothrips car- the same trunk (usually one sample) were re-
pathicusPelikán,1961,Hoplothripscorticis(De gardedasbelongingtothesamepopulation.Most
Geer, 1773), Hoplothrips fungi (Zetter- specimens examined were collected in Norway.
stedt,1828), Hoplothrips pedicularius (Haliday, H.fungi,H.semicaecusandH.ulmiweresupple-
1836), Hoplothrips polysticti (Morison, 1949), mentedwith38specimens(mainlymacropterous
Hoplothrips semicaecus (Uzel, 1895), Hoplo- males,whicharerare)borrowedfromThePlant
thrips ulmi (Fabricius, 1781) and Hoplothrips Protection Service, Wageningen, The Nether-
unicolor (Vuillet, 1914). Only H. semicaecus lands and The Natural History Museum, Sen-
seemstoberareinNorway(Kobro2003,Olsen ckenberg,Germany.
&Solem1982). Selectionofsignificantidentificationcharac-
Second stage larvae of H. carpathicus, H. ters were based on sample means and standard
pedicularius,H.polystictiandH.ulmicanbedis- confidence intervals (95%) calculated for all
criminatedbymeansofmetriccharacters(Kobro measuredcharacters.
&Rafoss2001).Theinitialobjectiveofthisstudy
wastofindmetricdiagnosticcharactersbywhich
3.Results
adult specimens of Norwegian species assigned
tothegenusHoplothripscouldberecognised.We
presentanddiscussanumberofsuchcharacters We have measured or evaluated 53 commonly
tofindthemostappropriatetouseinanidentifi- usedcharactersonatotalof366adultsrepresent-
cationkey.Wealsodiscusstheirlifehistoryasin- ing8speciesofHoplothrips.
dicatedbyourstudy. Theselectionofidentificationcharacterswas
basedoncomparisonofconfidenceintervalscal-
culatedfromthemeasurementsofthecharacters
2.Materialandmethods
measured(Fig.1).
Thirteencharacterswerechosenaccordingto
Barkfromtrunksorbranchesofdeadtreeswith theirutility,asindicatedinfigure1,andusedinan
visibleinfestationofwood-rottingfungiwerein- identification key for adults of Norwegian
vestigatedforthepresenceoftubuliferousthrips. Hoplothripsspecies.
186 Kobro&Rafoss (cid:127) ENTOMOL.FENNICAVol.17
Fig.1.Illustrationoftheprocedurefor
selectingofdiscriminatingcharactersof
adultsofHoplothripsspeciesbasedon
samplemeansandconfidenceintervals
(95%):length(µm)ofmediolaterale
setaonpronotum.
Other examples of the measurements are Distancebetween themedioposteromarginal
shownintables1–4.Amoredetailedanalysisof setae on tergite IX shorter than the width of
thevariationinthelengthofsensecones(multi- tubus. Anteroangular setae at the margin of
porous olfactory chemoreceptors) on antennal pronotum 3
segment III and the length of mediopostero- 3. Almost always two large sense cones on
marginalsetaeontergiteIXareshowninFigure antennalsegmentIV 4
2. Posterior prolongation of the fore femora of Almostalwaysmorethantwosenseconeson
oedymerous males (Fig. 3), the apices of antennalsegmentIV 5
medioposteromarginalsetaeontergiteVIII(Fig. 4. Distancebetweenbasesofantennalsegments
4),andglandularareasonsterniteVIIIofmaleH. Ilargerthan18µm.Apicalwidthofantennal
carpathicus(Fig.5)areshown. segment I larger than 40 µm. Medio-
posteromarginal setae on tergite IX longer
IdentificationkeytotheHoplothripsspeciesre- than140µm.AntennalsegmentVIIIlonger
cordedinNorway: than75µm Hoplothripscarpathicus
Distancebetweenbasesofantennalsegments
1. Mediolateralsetaeonpronotumshorterthan I less than 18 µm. Apical width of antennal
110µm 2 segment I less than 40 µm. Mediopostero-
Mediolateral setae on pronotum longer than marginalsetaeontergiteIXshorterthan125
110µm 6 µm. Antennal segment VIII shorter than 75
2. Distancebetween themedioposteromarginal µm Hoplothripssemicaecus
setaeontergiteIXthesameasorlargerthan 5. Distancebetweenbasesofantennalsegments
thewidthoftubus.Anteroangularsetaeonthe I larger than 16 µm. Width of antennal seg-
marginofpronotum Hoplothripsunicolor mentIlargerthan36µm.Antennalsegment
ENTOMOL.FENNICAVol.17 (cid:127) IdentificationofNorwegianHoplothrips 187
Fig.2.CombineduseofthelengthofsenseconesonantennalsegmentIIIandthelengthofmediopostero-
marginalesetaonabdominaltergiteIXfordiscriminatingofadultsofHoplothripsfungifromthoseofHoplothrips
ulmiandHoplothripscorticis.H.fungifemalemacropterous((cid:1)),H.fungifemalemicropterous((cid:1)),H.fungimale
macropterous((cid:2)),H.fungimalemicropterous((cid:2))H.ulmifemalemacropterous((cid:3)),H.ulmifemale
micropterous((cid:3)),H.ulmimalemacropterous((cid:4)),H.ulmimalemicropterous((cid:4)).
4.Discussion
IVlongerthan68µm.Medioposteromarginal
setaeontergiteVIIIendinginaveryfinetip
oropenlikeasuctionstraw(Fig.4) We present estimates and appraisals for metric
Hoplothripspedicularius charactersforadultsof8speciesofHoplothrips
Distancebetweenbasesofantennalsegments fromNorway,andinsertthesecharactersintoan
Ilessthan16µm.WidthofantennalsegmentI identificationkey.
shorter than 36 µm. Antennal segment IV ThesizeofHoplothripsadultsvariesbothbe-
shorter than 68 µm. Medioposteromarginal tweenandwithinthespecies.
setaeontergiteVIIIevenlytapering Females are larger than the males (Table 1)
Hoplothripspolysticti and the micropterous specimens are larger than
6. Long sense cones (longer than 25 µm) on the macropterous. Micropterous males vary in
antennal segment III and short medio- sizeandcanbeofthelargeoedymerousformor
posteromarginal setae on abdominal tergite thesmallergynaecoidform(Hood1940).Thus,
IX(lessthan190µm) Hoplothripsfungi thesmallmalesofH.polystictiinourstudywere
Short sense cones (shorter than 35 µm) on abouthalfthesizeofthelargestfemalesofH.car-
antennal segment III and long medio- pathicus (Table 1). Morison (1949) considered
posteromarginal setae on abdominal tergite identification to rely mainly on the females, as
IX(longerthan170µm) 7 theyarethevaryless.Thus,foranentomologist
7. Headbroaderthanlong Hoplothripscorticis withasingleoedymerousmalespecimen,accu-
Headlongerthanbroad Hoplothripsulmi rateidentificationisdifficult.
Thecharacterswestudiedcanbeseparatedin
188 Kobro&Rafoss (cid:127) ENTOMOL.FENNICAVol.17
Table1.Averagetotalbodylength(mm)ofmale(m)andfemale(f)micropterae.
Singlepopulation Severalpopulations
n µm S.D. n µm S.D.
H.carpathicusf 11 3.4 0.1 7 3.4 0.3
H.carpathicusm 32 2.7 0.2 4 2.7 0.1
H.pediculariusf 10 3.2 0.2 9 3.0 0.2
H.pediculariusm 32 2.6 0.2 9 2.4 0.2
H.polystictif 21 2.8 0.1 10 2.7 0.1
H.polystictim 17 2.0 0.2 10 1.9 0.1
Table2.Averagelength(µm)ofmediolateralesetaonpronotumofmale(m)
andfemale(f).
Singlepopulation Severalpopulations
n µm S.D. n µm S.D.
H.corticisf 8 203 12 10 204 24
H.corticism 6 197 8 10 194 13
H.carpathicusf 11 60 12 10 69 16
H.carpathicusm 31 56 7 10 52 8
H.pediculariusf 10 90 8 10 92 14
H.pediculariusm 32 89 10 10 92 11
H.polystictif 21 71 10 10 62 11
H.polystictim 17 55 8 10 49 8
severalgroups.Mostofthecharactersexamined length and width, fore femur length and width
are positively correlated with body length in a and the most striking external male character
general allometric pattern regardless of sex and whichistheposteriorprolongationoftheforefe-
morph.Somecharactershowever,arenotcorre- mur(Fig.3).Variationinlengthofthisprolonga-
lated to the body length. Despite males being tioninforefemurofthreeofthespeciesisshown
smallerthanfemales,anumberofcharactersare in table 3. These characters vary considerably
larger in males. Such characters include the within some species, as indicated by the high
length of the pronotum, the fore tarsal tooth standarddeviationsandmaybeparticularlyim-
portantfordefenceoftheovipositionsiteandfe-
males and is expressed most in oedymerous
males of H. pedicularius (Crespi 1986). If ac-
ceptedasanindicatorofbehaviour,variationin
sizeofthesecharacterswithinourmaterialindi-
cates that the males of H. corticis, H. fungi, H.
semicaecus and H. ulmi have an aggressive be-
havioursimilartothatofH.pedicularius,i.e.they
defend resources such as oviposition sites and
mated females. By the same argument, the spe-
cies H. polysticti and H. unicolor, are more
“peaceful” as their males are not equipped for
Fig.3.Posteriorprolongationofforefemurindicated
withathinbar.Thickbar100µm. fighting,whilemalesofH.carpathicusareinter-
ENTOMOL.FENNICAVol.17 (cid:127) IdentificationofNorwegianHoplothrips 189
Table3.Averagelength(µm)ofposteriorprolongationofforefemurofmicropteraemale(m)andfemale(f).
Singlepopulation Severalpopulations
n µm S.D. n µm S.D.
H.carpathicusf 10 26 7 10 34 15
H.carpathicusm 31 35 14 10 44 16
H.pediculariusf 10 33 8 10 41 6
H.pediculariusm 32 74 25 10 91 28
H.polystictif 22 20 3 10 20 5
H.polystictim 17 18 5 10 21 8
mediate in this respect. However, experimental Table4.RelativelengthoftheheadofH.corticisand
evidence for the association between body size H.ulmi(p<0.0001).
anddefenceislackingforthesespecies(Mound
n Mean S.D.
2005).
Theconspicuouscharacteristicsoftheoedy-
Hoplothripscorticis 19 0.94 0.03
merous micropterous males make identification
Hoplothripsulmi 13 1.07 0.04
difficultandthesecharactersareavoidedinour
identification key. The characters we have se-
lected are typical for adult Hoplothrips species
regardlessofsexormorph. thripsspeciesintotwodistinctgroups(Fig.1).In
Thenumberofsenseconesonantennalseg- onegroupthethreespeciesH.corticis,H.fungi
mentIIIandIViscommonlyusedforidentifica- and H. ulmi are closely related (Mound et al.
tionoftubuliferans(Schliephake&Klimt1979, 1976). The combined use of the length of the
Mound & Walker 1986). In our material of sense cones on antennal segment III and the
Hoplothrips this character is constant only in lengthofmedioposteromarginalsetaeonabdom-
H.carpathicusandH.semicaecus.Thenumber inaltergiteIXtodistinguishH.ulmiandH.fungi
ofsenseconesisparticularlyvariableinH.poly- (Mound et al. 1976) is verified by us (Fig. 2).
sticti where antennal segment III can have 2–3 Basedonthischaracter,H.corticisisinthesame
(rarely1)andantennalsegmentIV3–4(rarely2) groupasH.ulmi,butthesetwospeciescanbedis-
sensecones.Relyingtoomuchonthenumberof tinguishedbytheproportionsoftheirheads:the
sense cones therefore makes identification inef- headofH.corticisisbroaderthanlong,whilethat
fective.Thenumberofsenseconesvarieswithin ofH.ulmiislongerthanbroad(Table4).
Hoplothrips species in other parts of the world
andalsoinspeciesofDeplorothripsandPsilado-
thrips(Mound&Walker1986).
Moundetal.(1976)andKirk(1996)consid-
ered rounded apices of medioposteromarginal
setaeontergiteVIIIascharacteristicforH.pedi-
cularius. This character was ambiguous for our
material, as these setae can be very sharply
pointed;whereathintipcanbreakandmakethe
apex look rounded or more often open like a
drinkingstraw(Fig.4)butneverexpandedasin
H.semiceacus(Moundetal.1976).
Of the allometric characters examined, the
length of mediolateral setae on the pronotum is Fig.4.Medioposteromarginalsetaonabdominalter-
the most useful in separating adults of Hoplo- giteVIIIwithpointedoropenapex.Bar100µm.
190 Kobro&Rafoss (cid:127) ENTOMOL.FENNICAVol.17
Adultsofthe5speciesintheothergroupcan
bediscriminatedbysinglecharacters.Morethan
onecharacterisgivenatseveralstepsinthekey
even if one is conclusive, in case they will be
neededifmorespeciesareaddedtothekeyinthe
future.
Lewis(1973)usedthetermbrachypterousfor
specimenswithwingsofreducedsize.Thesmall
wings of the Hoplothrips species are so minute
thattheyareeasilyoverlooked,andmicropterous
(Hood 1940, Mound 2005, Mound & Marullo
1996,Mound&Walker1986)isamoreappropri-
Fig.5.SterniteVIIIonHoplothripscarpathicus.Bar
ate term. In two species, H. semicaecus and H.
100µm.
unicolor, the wings are rudimentary (only 1–2
micrometers long), while in H. carpathicus we
foundacontinuoustransitionbetweenrudimen- & Walker (1986), except for H. carpathicus
tary wingsandsmallwingpads.Werefertoall whichisfiguredhere(Fig.5).
theseasmicropterous. DespitethefactthatHoplothripsspecieshav-
Winglessness increases fecundity (Crespi ing been regarded as difficult to identify due to
1986),asproducingwingsonlywhennecessary theirmorphologicalvariation,severaloftheNor-
saves energy. In macropterous forms of Hoplo- wegian species are easily distinguishable by
thripshowever,wingsareproducedbutareoften “macroscopic”charactersvisiblewithoutprepa-
broken off at a characteristic position. Flimsy ration, given some experience and that they are
wing structures appear to be functional adapta- collectedondeadwood.H.corticis,H.fungiand
tionstotheleaflitterhabitats(Ananthakrishnan H. ulmi superficially resemble Phlaeothrips
1984),arecalledcaducousandaretypicalforthe annulipesO.M.Reuter,1880andaremorediffi-
habitat(Hamilton1978).Wehaveobservedbro- culttoidentify,evenifH.corticiscanberecog-
kenwingsandabreakagezonedistallytothesub- nised by its cheeks appearing moreswollen be-
basalsetaeinwingsofmacroptersofallspecies hindtheeyesandtheirtibiaeareusuallyyellow.
studiedhere,mostfrequentlyinH.carpathicus, The5otherspeciesofHoplothripsaredifferent
H.pediculariusandH.polysticti.Moritz(2002) and relatively easy to recognise. Adults of H.
suggestedthewingbreakagetoresultfromcopu- carpathicusarelarge(Table1)andone-coloured
lation and to preventfurther matingswith other greyish-brown, and are rarely recorded unless
males. Dominant males defend a number of fe- bark is removed with an axe from large dead
malesatanovipositionsite(Crespi1986),andthe birches(Kobro&Solheim2002).ThoseofH.pe-
wingbreakagemightbeanotherwaytokeepthe diculariusarealsolargeandmainlydarkbrown
femaleswithintheharem. with a light yellow gore posterior on the abdo-
Itisvery difficulttoidentify adultfemaleat men, while micropterous specimens also have
genuslevelbyusingtraditionalcriteria(Mound bright yellow forelegs and head. Adults of H.
et al. 1976, Palmer & Mound 1978, Anan- polystictihaveaboutthesamecolourasH.car-
thakrishnan 1984). Allmacropterousspecimens pathicus,butaremuchsmaller(Table3),withthe
ofHoplothripsinourmaterialhavetwosub-basal head often square. H. semicaecus adults have
setae on the fore-wings in contrast to those of antennal segments VII and VIII broadly fused.
mostothergeneraofPhlaeothripinae.Thechar- Theantennalsegmentsareofcontrastingcolour:
acterisoflimitedvalue,however,asthemicro- segments I–III are yellow, while the other seg-
pterousform,inwhichthesub-basalsetaecanbe ments are darker than the rest of the body. H.
absent or difficult to see, predominates. Males unicolor adults are small, light brown and with
canberecognisedatthegenuslevelbytheform darkerbrowncrossbandsontheabdominalseg-
oftheglandularareaonsterniteVIII.Goodfig- ments,whichfadeduringpreparation.
uresaregiveninMoundetal.(1976)andMound NorwegianHoplothripsspeciesliveonfungi
ENTOMOL.FENNICAVol.17 (cid:127) IdentificationofNorwegianHoplothrips 191
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