The first report of gall induction in the sawfly subfamily Allantinae (Hymenoptera: Tenthredinidae)

2007·0.62 MB·

by  Andrew Liston

©EntomologicaFennica.5December2007
The first report of gall induction in the sawfly subfamily
Allantinae (Hymenoptera: Tenthredinidae)
AndrewD.Liston,TommiNyman&AlexandraKehl
Liston,A.D.,Nyman,T.&Kehl,A.2007:Thefirstreportofgallinductioninthe
sawflysubfamilyAllantinae(Hymenoptera:Tenthredinidae).—Entomol.Fen-
nica18:199–205.
GreatBurnet,SanguisorbaofficinalisL.(Rosaceae),isthepreviouslyunknown
larval host plant of the sawfly Empria testaceipes (Konow, 1896) (Tenthre-
dinidae:Allantinae).Wereportherethatyoung,endophagouslarvaeinhabitgalls
intheleaves,whilelaterinstarsareexternalfeedersonleaves.Thisisthefirstre-
port of a gall-inducing habit in the subfamily Allantinae. The galls of E.
testaceipesonS.officinalisandthelarvaearedescribedandillustrated,andthe
distributionofthisrarelyrecordedsawflyissummarised.
A.D.Liston,DeutschesEntomologischesInstitut,Leibniz-ZentrumfürAgrar-
landschaftsforschung(ZALFe.V.),EberswalderStrasse84,D-15374Münche-
berg,Germany;E-mail:[email protected]
T.Nyman,FacultyofBiosciences,UniversityofJoensuu,P.O.Box111,FI-80101
Joensuu,Finland;E-mail:[email protected]
A.Kehl,AbteilungMykologie,LehrstuhlfürPflanzensystematik,Universitäts-
strasse30–NWI,D-95440Bayreuth,Germany;E-mail:Alexandra.Kehl@uni-
bayreuth.de
Received15November2006,accepted16February2007
1.Introduction plants (Roininen et al. 2005), a gall-inducing
habit has not previously been reported for any
LarvaeofthesawflysubfamilyAllantinae(Hy- speciesoftheAllantinae.Herewepresentdetails
menoptera:Tenthredinidae)typicallyfeedexter- oftheseobservations,describetheappearanceof
nally on the leaves of a wide variety of herba- thegallsandlarvae,andsummarisethedistribu-
ceous and woody plants in ten families of tionofEmpriatestaceipes.
dicotyledonous angiosperms (Smith 1979, La-
court1999).ThehostplantandlarvaofEmpria
testaceipes (Konow, 1896) were hitherto un- 2.Material
known. During the 9th International Symphyta
WorkshopheldinJune2005intheLowerTatras, In Slovakia, Lower Tatras, Liptovsk(cid:1) Hrádok
SlovakRepublic,A.Kehlfoundyounglarvaeof ESE 9 km, Svarín W 2 km, Svarínske lúky,
what later proved to be this species inhabiting 47°00.71N19°49.38E,690ma.s.l.,about50lar-
gallsontheleavesofGreatBurnet(Sanguisorba vaewerecollectedfromSanguisorbaofficinalis,
officinalisL.,Rosaceae).Althoughmanytenthre- 19.VI.2005.Onefemaleandthreemalesemerged
dinid sawfly groups induce various galls on April2006inheatedroom,leg.A.D.Listonand
200 Listonetal. (cid:127) ENTOMOL.FENNICAVol.18
S. M. Blank, coll. Deutsches Entomologisches 3.2.Behaviouroflarva
Institut (DEI), Müncheberg, Germany. Numer-
ous larvae are also preserved in collections of Onelarvainhabitsonlyasinglegall.Faecesre-
DEI,A.Kehl,andT.Nyman. maininsidethegall.Thefirstinstarlarvaremains
Thecollectinglocalityisanextensivelyman- entirely withinthegallchamber,butthesecond
aged meadow, on the floor of the Demänovská instarmakesaholeinthewall,usuallyontheun-
ValleybesidetheDemänovskáRiver.Vegetation derside(Fig.1d),andprobablyleavesthegallto
is herb rich grassland, interspersed with bushes skeletonisesmallareasoftheleaf.Itwasnotob-
andyoungtreesofSalixspp.andBetulasp.Con- served whether this instar re-enters the gall be-
siderablelocaldifferencesinthefloraofthesite tweenperiodsofexternalfeeding,norwasitclear
seemedtoberelatedmostlytothedistributionof at what exact stage of development of the larva
slightly raised deposits of freely draining allu- the gall is permanently vacated. From the third
vium.ThepatchesofS.officinaliscontainedsev- instar onwards, feeding is entirely exophagous.
eralhundredplants,butthesepatcheswereappar- Theselargerlarvaearefoundmostlyontheleaf
ently restricted to a rather small, comparatively undersides, adopting a coiled posture when not
wet part of the area. Galls caused by Empria feeding.
testaceipes were abundant, indicating the pres- Larvaewererearedindoorsinalaboratoryat
enceofatleast200larvae. theDEIby thefirstauthor. GalledSanguisorba
leaves were put in narrow-necked flasks filled
withwater,andtheflasksplacedinalarge,venti-
lated,glasschamber.Largerlarvaewerefedwith
3.Results
Creeping Cinquefoil (Potentilla reptans L.,
Rosaceae)asasubstituteforSanguisorbaoffici-
3.1.Descriptionofgall nalis under rearing conditions, because S. offi-
cinaliscouldnotbeobtainedlocally.Theyfedon
Galls occurred on the lower, rosette leaves of P.reptansfor1–2weeksandsuccessfully com-
Sanguisorbaofficinalis.Flowerstemshadnotyet pleted larval development. M. Kraus (pers.
beenproducedatthetimeofcollectionofthelar- comm.)reportsthatSanguisorbaofficinaliswas
vae. The closed galls are irregular in shape, notpresentatthelocality wherehecaptured an
strongly domed above the upper side of the adultspecimenofE.testaceipesinBavaria.The
leaves, but flush with the lower leaf surface. possibility that E. testaceipes also uses other
Whilstthewallsoftheuppersurfacearecompar- Rosaceaespeciesaslarvalhostsshouldtherefore
atively thick, apparently because of abnormal beconsidered.
growth of the mesophyll layer, the underside Larvaecompletedfeedingduringthefirsttwo
seemsnottobesoaffected.Asthelarvadevelops, weeksofJuly.Itwaspresumedthatthisspeciesof
thefloorofthegallisreducedtolittlemorethan Empria,likeallknowncongeners(Smith1979),
thethicknessoftheepidermis(Fig.1a).Exterior is univoltine. They were therefore given sphag-
ofthegallmayremaingreen,butuppersurfaces nummoss,cutstemsofRubusandSambucus,and
ofmanyolderoneswerecolouredred.Thegallis some 3–4 cm diameter corks (natural cork, not
positionedononesideofthemidribofaleaflet. made of glued fragments) to overwinter in. Ex-
Lengthoftheaxisofthegallparalleltothemidrib amination of these materials showed that the
varieswidelyfromapproximately5mmuptoc. corkshadbeenstrongly favouredasthesitefor
20mm(Figs.1b,c).Thelongergallsthusoccupy diapause. The containers were kept outside, but
almost the whole length of the leaflet (Fig. 1b). under cover, during the winter and periodically
Ovipositionscarscouldnotbeidentified.How- moistened.Emergencewasunnaturallyearly,af-
ever,thelargergallsappeartoconsistofachainof terthecontainerswerebroughtindoorsinMarch
confluentchambers,possiblyresultingfrommul- toaheatedroom.Noparasitoidswerereared.
tipleinsertionsoftheovipositor(asinNematinae
speciesofthePontaniadolichuraspeciesgroup,
orPhyllocolpaspp.).
ENTOMOL.FENNICAVol.18 (cid:127) GallinductioninAllantinae 201
Fig.1.Gallsandlar-
vaeofEmpriatesta-
ceipes(Konow)on
Sanguisorbaoffici-
nalisL.,Slovakia,
LowerTatra.–a.
Undersideofgall,
openedtoshowa
youngendophagous
larva.–b,c.Upper-
sideoflargeand
smallgalls.–d.Un-
dersideofgall.–e.
Matureexophagous
larva.Figs.1a–dby
T.Nyman,Fig.1eby
C.Kutzscher.
3.3.Descriptionoflarva pale brown apart from black stemmatum. Body
uniformly pale green. The first markings to de-
LarvalmaterialhasbeensenttoM.ProusandM. veloparearowofblackspotsjustaboveeachspi-
Heidemaa (Tartu University, Estonia), who are racle.
preparingakeytothelarvaeofEuropeanEmpria Mature larva (Fig. 1e) (length 11–14 mm):
species.Becauseadetailedmorphologicalchar- headpalebrownwithtriangularmarkingrunning
acterisationwillappeartherein,only abriefde- alongcoronalsuture,itsanteriorpointendingex-
scriptionisgivenhere. actly wherecoronalsuturemeetsthefrontalsu-
Younglarva(Fig.1a)(length3–5mm):head ture.Thoraciclegsbrown.Bodypalegreenwitha
202 Listonetal. (cid:127) ENTOMOL.FENNICAVol.18
rathercomplexpatternofdarkergreenmarkings, some such deformed plants 4–6 irregular, pale
comprising a medial dorsal stripe and on each green “procecidia” are simultaneously found
body side a supraspiracular stripe (in which the scattered over the compound leaf, projecting
blackishsupraspiracularflecksaresituated)anda mainlyfromtheleafunderside.Itcouldnotbees-
slightlynarrowerstripebetweenthese.Anarrow tablished whether these are caused by the same
interrupted stripe also runs along the ventral wasp”. The size of these structures is not indi-
edgesofthesurpedallobe. cated.ItseemsunlikelythatE.testaceipesisre-
Thepreciseextentofthesegreenpigmented sponsibleforeitherofthesetypesofdeformation,
areasisvisibleinalcoholmaterial,butintheliv- becausetheappearanceofthecompoundleaves
inglarvaisobscuredbytheunderlyingcolourof and their ribs was not otherwise noticeably af-
haemolymphandgut.Thelivinglarvaappearsto fectedbythepresenceofE.testaceipesgalls,and
the naked eye mottled dark green dorsally, pale theswellingsdescribedbyBuhrprotrudedmore
green ventrally, with conspicuous white (wax from the undersides of the leaflets (in E. testa-
covered) glandubae on dorsum of thorax and ceipesonlyfromtheuppersides).
annulets 2 and 4 of abdominal segments. There are no other galls known on Sangui-
Supraspiracular fleck occupies approximately sorba,orrelatedgenera,inEuropewhichresem-
fulllengthofannulet2. blethoseofE.testaceipes.Forthisplantgenus,
Colourationofmaturelarvaisverysimilarto Buhr(1965)keysthegallsofsixarthropodspe-
E. pumila (Konow, 1896) (Heidemaa & Prous cies, comprising the mite Aceria sanguisorbae
2006),whichisattachedtoFilipendulaulmaria (Canestrini,1891)(Acarina),thegallmidgeDa-
(L.)Maxim.MaturelarvaeofE.testaceipesare sineurasanguisorbae(Rübsaamen,1890)(Dip-
smallerthanthoseofE.pumila,whichare13–17 tera:Cecidomyiidae),andfourapparentlypoly-
mm long according to Heidemaa and Prous phagous aphids and coccids (Homoptera). No
(2006).Thisdifferenceistobeexpected,because gallwasps(Hymenoptera:Cynipidae)areknown
the length of E. testaceipes imagines (4–5 mm from Sanguisorba, although a few species are
based on our reared specimens and two males, stem gallers on the related genus Potentilla
caughtasadults,intheDEIcollection)islessthan (Ronquist & Liljeblad 2001). E. testaceipes is
thatofanyotherEmpriaspecies,exceptperhaps therefore,accordingtopresentknowledge,oneof
forthesmallestindividualsofE.alpinaBenson, atmosttwohymenopteranswhichcausegallson
1938 and E. gussakovskii Dovnar-Zapolskij, Sanguisorba.
1929. Imagines of E. testaceipes are also more WhileE.testaceipesistheonlyEmpriaspe-
slenderthanotherspecies. ciessofarknowntobeattachedtoSanguisorba,
thishost-plantassociationisnotunexpected.Of
the 49 Empria species worldwide currently re-
4.Discussion gardedasvalid(Taeger&Blank2006),hostsare
recorded for 20 species. Their combined host-
Asearchofliteratureonplantgallsfailedtore- plant spectrum includes plants from the Betu-
vealpreviousrecordsofgallinductionwithinthe laceae,Salicaceae,andmultiplewoodyandher-
subfamily Allantinae, or similar galls made by baceous genera in the Rosaceae (e.g., Fili-
Tenthredinidae on Sanguisorba, apart from in- pendula,Rubus,Fragaria,PotentillaandGeum)
conclusivecommentsbyBuhr(1965)forClare- (Smith 1979, Lacourt 1999). Rosaceous plants
montia puncticeps (Konow, 1886) (as Mono- alsosupportnumerousspeciesinotherallantine
phadnoidespuncticeps)(Blennocampinae).This genera, but the presently known collective host
work tentatively attributes to C. puncticeps, rangeofthesubfamilycomprisestenplantfami-
thickeningofleavesandleaf-petiolesanddefor- lies(Smith1979,Lacourt1999).Oftheapproxi-
mation of young leaflets. Such a plant is illus- mately 210 species of Allantinae whose larvae
tratedbyDittrich(1924:plate45,Fig.61),who areknown,only asinglespecieshaspreviously
howeverstatedthatthegallinducerisaNematus beenfoundtofeedinternally:larvaeofthetaxo-
species.Asecondtypeofdamageisdescribedby nomically isolated Eopsis beaumonti Benson,
Buhr(translatedfromGerman):“Sometimeson 1959mineinsideleafstalksofCommonBistort,
ENTOMOL.FENNICAVol.18 (cid:127) GallinductioninAllantinae 203
Polygonum bistorta L. (Polygonaceae) (K. Be- to feed externally only one or two days after
ne(cid:2),pers.comm.). hatchingfromtheegg.
Because no other gall inducers are known E. testaceipes, described by Konow (1896)
fromtheAllantinae,itisverylikelythatthegall- from the holotype male collected in Moravia,
ing habit has been derived independently in E. CzechRepublic,isaveryrarelyrecordedspecies,
testaceipes. Gall-inducing sawflies are so far at least in Europe. Three other previously pub-
known from multiple, phylogenetically widely lishedEuropeanrecords,allbasedonsinglespec-
separated taxa of the Xyelidae and Tenthre- imens, are from Germany and Slovakia (Kraus
dinidae (Lorenz & Kraus 1957, Roininen et al. 1998;Roller&Luká(cid:2)1999).Furtheroccurrences
2005). Within Tenthredinidae, galling species are reported from the European parts of Russia
havebeenfoundonly inthesubfamiliesNema- (Zhelochovtsev & Zinovjev 1996), Mongolia,
tinaeandBlennocampinae(Roininenetal.2005, andtheIrkutskRegionofSiberia(Muche1968).
Nymanetal.2006).Swellingoftheplanttissue AsalreadypointedoutbyConde(1940),there-
around the oviposition site has, however, also peatedlymentionedpresenceofE.testaceipesin
been recorded in tribes Blennocampini and the Middle East (Enslin 1914), Asia Minor
PhymatoceriniofBlennocampinaeandgeneraof (Zhelochovtsev & Zinovjev 1988), or Iraq (La-
Nematinaewhoselarvaefeedexophytically(Lo- court1999)isaresultofmisidentificationsofE.
renz&Kraus1957,Scheibelreiter1973,Zinov- archangelskiiDovnar-Zapolskij,1929.Imagines
jev&Vikberg1998).Inthesegroupsitisnotal- ofthesespeciescanbeidentifiedusingthekeyby
ways clear whether the pustule which develops Zhelochovtsev and Zinovjev (1988). The de-
aroundtheeggiscausedbyasecretionappliedby scriptionofEmphytusimmersus(Klug,1818)in
the female during oviposition, or whether the Stephens (1835), said to have been collected in
planttissueissimplydistendedbyanincreasein theareaofLondon,matchesEmpriatestaceipes
egg size caused by absorption of fluid fromthe butnotE.immersa(Klug1818).Thisispossibly
host. Similar small swellings at the oviposition anindicationthatE.testaceipesis,orwas,more
sitealsooccurinsomeEmpriini(Allantinae)spe- widespreadinEuropethanisatpresentthought.
cies (genera Empria, Monsoma, Monostegia), Theabilitytorecognisethegallsshouldinfuture
butthesearevacatedimmediatelyafterthelarva enabletheeasierdetectionofthisraresawfly.The
hatches (Miles 1936, Kontuniemi 1951, 1955, importancealready attachedtotheconservation
Pieronek 1980, Altenhofer & Pschorn-Walcher ofSanguisorbaofficinalisasahostplantforen-
2003).Thestructureinhabitedbytheyounglarva dangeredbutterflyspecies(e.g.,Bergmannetal.
ofEmpriatestaceipesissomuchlargerthanthe 2005)mayincreasethelikelihoodthatsomepo-
larva which it encloses, and the upper walls so tentialandactualhabitatsofEmpriatestaceipes
stronglydistendedandthickened(thusindicating receive adequate protection. Finally, we would
astimulationofgrowthbythecausativeorganism liketorecommendstudyofthebehaviourofthe
not resulting from simple mechanical influence secondinstarlarvae,whichcouldnotbesatisfac-
on the host-plant’s tissues) that it must be re- torily clarified in the present study, as a subject
gardedasatruegallinthesenseofMeyer(1987) worthyoffutureexamination.
andRedfernandAskew(1992).Amongstprevi-
ously described sawfly life histories, the larval
development of the Amauronematus longiserra Acknowledgements.Dr.LadislavRoller(Bratislava,Slo-
speciesgroup(Nematinae)onSalixspecies(Sali- vakia)andDr.AndreasTaeger(Müncheberg,Germany)
organisedthe9thInternationalSymphytaWorkshopinthe
caceae)seemstomostcloselyparallelthatofE.
LowerTatras,Slovakia,duringwhichthelarvaewerecol-
testaceipes.Thegallsformedbythesenematine
lected.Dr.StephanM.Blank(Müncheberg)assistedwith
speciesaresimilartoE.testaceipesgallsinthat collectionofmaterial.Mr.ChristianKutzscher(Münche-
growth of the upper leaf tissues is accelerated, berg)photographedthematurelarva.Weareindebtedto
and the underside of the leaf is reduced to the Dr.ManfredKraus(Nürnberg,Germany)forvaluabledis-
cussionsonthecontentofthiscontribution,andwealso
thicknessoftheepidermis(Zinovjev&Vikberg
thankDr.SusanneSchulmeister,Dr.AnttiKause,andan
1998).However,unlikeE.testaceipes,thelarvae
anonymousreviewerfortheircomments,whichhelpedto
oftheA.longiserra-groupleavethegallandstart improvethemanuscript.
204 Listonetal. (cid:127) ENTOMOL.FENNICAVol.18
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