THE BIONOMICS 0F
LITHOCOLLETIS BLANCARDELLA
(Lepidoptera: Gracillariidae) IN MICHIGAN

Thesis for the Degree of M. S.
MICHIGAN STATE UNIVERSITY
JAMES DWIGHT BUTCHER
1975

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ABSTRACT
The spoTTed TenTiform leafminer of apple, LiTho-

colleTis blancardella Fabricius, has Three discreTe

 

generaTions per season in souThwesTern Michigan apple
orchards. Five hymenopTerous parasiToids were idenTified
as naTural enemies of The larval sTages of This leafminer.
A chrysopid larva was observed as a naTural predaTor of
The adulT Ieafminer. In an unTreaTed ploT of JonaThan

apple Trees, Malus pymila Mill., The ToTal effecTive leaf

 

area was reduced by 32% by The leafmining larvae during

The I974 season. Many broad specTrum and sysTemic insecT-
icides were effecTive in conTrolIlng This leafminer. CerTain
carbamaTe and organophosphaTe insecTicides caused a signifi-

canT reducTion in parasiTism of The larvae.

THE BIONOMICS OF LITHOCOLLETIS BLANCARDELLA

 

( LepidopTera: Gracillariidae I IN MICHIGAN

By

James DwighT DuTcher

A THESIS

SubmiTTed To
Michigan STaTe UniversiTy

in parTial fulfillmenT of The requiremenTs

for The degree of

MASTER OF SCIENCE

DeparTmenT of EnTomology

I975

ACKNOWLEDGEMENTS

The auThor wishes To express his sincere appreciaTion
To Dr. Angus J. HowiTT for his guidance and assisTance during
This sTudy. The auThor is graTeful To The DeparTmenT of
EnTomology for granTing financial assisTance during This
period and To Drs. James E. BaTh, Dean L. Haynes, STanIey
K. Ries and Frederick W. STehr for Their service on The grad-
uaTe commiTTee.

Special Thanks To Mr. John Newman and Mr. PeTer MarTinaT
for Their aide in The idenTificaTion of collecTed maTeriaI,
Mr. Larry Olsen and Mr. James NugenT for Their aide in The
disTribuTion sTudy and Mr. Alfred Pshea for his assisTance

in familiarizing The auThor wiTh orchard pracTices.

TABLE OF CONTENTS

LIST OF TABLES

LIST OF FIGURES

INTRODUCTION

LITERATURE REVIEW

EXPERIMENTAL METHODS AND MATERIALS

RESULTS AND DISCUSSION

A.

B.

C.

D.

E.

NaTuraI Enemies

Seasonal DevelopmenT

EffecT of Mining on The HosT
Chemical ConTrol

Miscellaneous STudies on The AduIT Leafminer

LITERATURE CITED

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42

LIST OF TABLES

Table I. - CounTs of The morTaliTy facTors of
L, blancardella from a lOO mine sample Taken aT
The end of each generaTion of The leafminer,
Richland, Michigan, I974.

 

Table 2a. - CounTs of spring generaTion adulTs
from 4 adhesive Traps disTribuTed on Top of The
leaf liTTer around a single Tree, Richland, I974.

Table 2b. - The developmenT of each generaTion of

L, blancardella Through Time, recorded as The number
of individuals in each life sTage per I00 mine sample,
Richland and Hickory Corners, Michigan, I973 and I974.

 

Table 3. - EsTimaTes of The leaf area damaged by each
generaTion of L, blancardella larvae, Hickory Corners,
I974.

 

Table 4. - Field evaluaTions of indicaTed insecTicides
applied as foliar TreaTmenTs To conTrol L. blancardella

 

on apple, Fennville and Douglas, Michigan} I974.

Table 5a. - EffecT of a single applicaTion of The
indicaTed insecTicide on The sap-feeder larvae of
.L. blancardella, Hickory Corners, I974.

 

Table 5b. - EffecT of a single applicaTion of The
indicaTed insecTicide on The Tissue-feeder larvae
of L, blancardella, Richland, I974.

 

Table 6. - EffecT of indicaTed InsecTicide on The
parasiTic HymenopTera which parasiTize The immaTure
sTages of L, blancardella, Douglas, I974.

 

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LIST OF FIGURES

Figure l. - CollecTing siTes of L, blancardella
in Michigan, I973 - I974.

 

Figures 2a, 2b and 2c. - Seasonal developmenT of

L, blancardella, Richland and Hickory Corners, I974.

 

Figures 3 Through 8. — The developmenTal sTages of
L, blancardella.

 

Figures 9 Through l2. - Some naTuraI enemies of
L, blancardella.

 

Figures l3 Through l5. - The effecT of mining on
The hosT planT.

Figure l6. - The relaTive densiTy of The leafmines
of L, blancardella in a l5 Tree ploT of JonaThon
apples aT Richland, I974.

 

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37

38

39

4O

INTRODUCTION
In recenT years The spoTTed TenTiform leafminer,

LiThocolleTis blancardella Fabricius, has infesTed many

 

commercial apple orchards in Michigan despiTe exTensive
insecTicide spray schedules. This sTudy was conducTed
To deTermine The pesT sTaTus of The leafminer and iTs
bionomics in Michigan.

Personnel of The CooperaTive Michigan Apple PesT
ManagemenT ProjecT, Michigan STaTe UniversiTy, found low

levels of L. blancardella in commercial and abandoned

 

orchards in Benzie, Berrien, Ionia, KenT, ManisTee, Mason,
Newaygo and Oceana counTies. In addiTion infesTaTions

were found in Allegan, Barry, Charlevoix, EmmeT, lngham,
Iosco, Kalamazoo and MecosTa counTies. All collecTing siTes

were in apple, Malus pumila Mill., orchards. This leafminer

 

appears To have a sTaTewide disTribuTion E Figure I J.

The descripTion of L, blancardella given by PoTTinger

 

and LeRoux ( I97l ) was used by Newman* To verify The idenTiTy
of one aduIT female and one adulT male reared from pupae
collecTed aT Fennville, Michigan. To increase The cerTainTy
of The species deTerminaTion, measuremenTs of The geniTalia

of 6 male and 2 female aduITs were compared wiTh The measure-
menTs noTed by PoTTinger and LeRoux. IT was deTermined ThaT

The insecT causing spoTTed TenTiform leafmines in Michigan

 

* Mr. John Newman is an insecT idenTificaTion specialisT for
The Michigan STaTe UniversiTy CooperaTive ExTension Service.

apple orchards is L, blancardella.

 

Several hymenopTerous parasiToids and a chrysopid
predaTor were observed aTTacking The various life sTages
of This leafminer in an unTreaTed orchard aT Hickory Corners,
Barry 00., Michigan. The degree of parasiTism and predaTion
in The leafminer populaTion was measured aT The end of each
of The leafminer's 3 discreTe generaTions.

The seasonal developmenT of This leafminer was moni-
Tored during I973 and I974 aT 2 unTreaTed apple orchards aT
Richland, Kalamazoo Co., and Hickory Corners, Michigan.
Larval and adulT behavior were also observed aT These siTes.

CerTain broad specTrum insecTicides were applied on a
biweekly schedule aT 2 apple orchards in Allegan 00., Michigan,
To deTermine The effecT of These compounds on The leafminer
populaTion densiTy. Three sysTemic insecTicides were applied
as single applicaTions To measure The efficacy of These
compounds againsT The larval sTages of The leafminer.

The observaTion ThaT male moThs are preferenTially
aTTracTed To caged virgin female moThs indicaTes ThaT maTing
may be iniTiaTed by a chemical sTimqus or pheromone which

is released by The female moTh.

FIGURE

- CollecTing siTes of L, blancardella

 

in Michigan, I973 - I974.

 

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00M

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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.'~ v'.""."r'.

 

 

 

 

 

 

 

 

 

 

 

 

LITERATURE REVIEW

L, blancardella was originally described by Fabricius

 

in l78l and was redescribed by Bankes in l899 ( PoTTinger
and LeRoux, l97l ). This insecT was firsT recorded on apple
in The UniTed STaTes by Slingerland and Crosby ( I9l4 ).
HuTson ( I938 ) was The firsT To record This leafminer on
apples in Michigan.

The parasiToid naTural enemies of L, blancardella in

 

Europe are lisTed by Fulmek ( I962 ). The predaTory and
parasiToid naTural enemies of This leafminer in Quebec are
lisTed and caTagorized as To which life sTage of The leafminer
is aTTacked by PoTTinger and LeRoux ( l97l ). Miller ( I970 )
has wriTTen a key To The neararcTic species of Pnigalio and
Sympiesis. His sTudies on The hosT range of These eulophid

ecToparasiToids reveal many To be parasiToids of LiThocolleTis

 

spp. Hering ( l95l ) has observed predaTory chrysopid larvae
aTTacking leafmining insecTs wiThin The mines. PoTTinger and
LeRoux ( I97l ) sTaTe ThaT predaTors and weaTher are The key

morTaliTy facTors regulaTing The populaTions of L, blancardella

 

in Quebec.

L, blancardella has a mulTivoITine life cycle. The number

 

of generaTions per year varies wiTh IocaTion. Three generaTions
were compleTed in SwiTzerland ( Baggliolini, I960 ), Belgium
( Soenen and AerTs, I953 ) and Quebec ( PoTTinger and LeRoux,

l97| ). Four and occasionally 5 generaTions were compleTed

in norThern ITaIy ( Kremer, I963 ). In Quebec The 3 gener-
aTions were discreTe. In warmer climaTes The IasT generaTions,
i.e. second and Third in Virginia ( Beckham, eT al, I950 )

and second, Third and fourTh in norThern lTaly ( Kremer, I963 ),
were noT separaTe. The Terminology proposed by Schurr and

Rings ( I964 ) is used in This sTudy To disTinguish The following

sTages of The life hisTory of L, blancardella:

 

OverwinTering pupae

Spring generaTion adulTs

FirsT generaTion eggs, larvae and pupae

Second generaTion eggs, larvae and pupae

Third generaTion eggs and larvae.

The life hisTory and habiTs of This leafminer have been
observed in deTaiI by PoTTinger and LeRoux ( l97l ) and Hering
I l95l ). Their observaTions are noTed here briefly. The
spring generaTion adulTs emerge from Their overwinTering siTes
on The orchard floor during The firsT warm days of spring.

The eggs are disTribuTed randomly on The lower surface of
The apple leaves. They E Figure 3 J are dome shaped wiTh
The flaT surface affixed To The leaf, average 0.4 mm in
diameTer and have a reTiculaTe surface.

The larval sTage consisTs of 5 insTars and 2 disTincT
morphological forms. lnsTars I, II, and III are dorso—
venTrally compressed, apodous and plasmophagous and are sap-

feeders E Figure 4 ]. lnsTars IV and V are eruciform and are

Tissue-feeders C Figure 5 j. The mining habiTs of The

larvae vary wiTh each insTar. The firsT insTar larva

breaks Through The egg chorion, enTers The leaf direchy

and begins mining The area around The poinT of enTry.

The second insTar larva mines away from This poinT and

forms a linear mine or ophionome ( Hering, l95| ) beTween

The lower epidermis and The spongy mesophyll of The leaf.

The Third insTar larva exTends The laTeral margins of The

mine To form an oval bloTch mine or sTigmaTonome I Hering, I95l
The fourTh insTar larva connecTs The IaTeraI margins of The
mine TogeTher wiTh moisT silken Threads. As These Threads
dehydraTe They shorTen, bringing The IaTeral margins of The
mine TogeTher and creaTing Ionngudinal folds in The lower
epidermis of The leaf in The mined area C Figure 7 3. AT This
poinT The mine is given greaTer depTh To compensaTe for The
larva's cylindrical shape and is called a TenTiform mine or
pTychonome I Hering, l95l ). The fifTh InsTar larva increases
The depTh of The mine by spinning more silk beTween The laTeral
margins of The mine.

The firsT Three insTars feed enTirely on The proToplasm
of The spongy mesophyll cells ( plasmophagous ) which are
sheared Open wiTh The larva's specialized mouThparTs. The
mouThparTs of The lasT Two insTars are modified To faciliTaTe

Their Tissue-feeding ( hisTophagous ) habiT. Grandi ( I959 )

).

explains This dualiTy of form in deTail. FourTh insTar
larvae feed primarily on The spongy mesophyll Tissue and
rarely feed Through To The upper epidermis of The leaf.
The fifTh insTar larvae feed on boTh spongy and columnar
mesophyll Tissue and selecTively ignore The vascular Tissue
of The leaf. This insTar ofTen feeds up To buT never
Through The upper epidermis of The leaf. The maTure mine
when viewed from The Top has a spoTTed appearance due
To The irregular feeding siTes of The larva.

The larva prepares iTself for pupaTion by voiding
iTself of solid wasTe and spinning a slighT cocoon aT
one end of The mine. PupaTion C Figure 6 J Occurs wiThin
The mine. AT The Time of emergence The pupa pushes Through
The lower epidermis of The leaf E Figure 7 J and The adulT
E Figure 8 J emerges. AdulTs are weak flyers and flighT
acTiviTy is confined To a shorT period aT dusk when maTing
occurs. During The day They resT on The leaves and Trunk
of apple Trees only flying when disTurbed.

A heavy infesTaTion of L, blancardella can cause

 

sTunTing of fruiT growTh, reduced Terminal growTh, early

leaf fall and reduced fruiT seT The following season ( Kremer,
I963 ). The leafmining larvae decrease The yield of apple
Trees by lowering The phoTosynTheTic area of The leaves,
leading To premaTure ripening and drop of The fruiT ( PoTTin—

ger and LeRoux, l97l ). As leafminers affecT yield indirechy,

iT is exTremely difficulT To prove cause and effecT in
field sTudies. The preceding auThors do noT give any
daTa To supporT Their sTaTemenTs.

Kremer ( I963 I TesTed many insecTicides againsT

 

L, blancardella and found The Tissue-feeding larvae To

be more resisTanT To The ToxicanTs Than The sap—feeding
larvae. Beckham, eT al ( I950 ) found ThaT regular
applicaTion of DDT for codling moTh, Carpocapsa pomonella

Linn., conTrol also conTrolled L. blancardella.

 

ATTenTion has been drawn To The precisely Timed

flighT period of L, blancardella which occurs during a

 

2-hr. period aT dusk. The moThs are fairly inacTive
during The day and afTer The flighT period ( PoTTinger

and LeRoux, I97l ). PoTTinger and LeRoux believe This
behavior is due To a response To The reducTion in sunlighT

aT dusk.

EXPERIMENTAL METHODS AND MATERIALS

A. NaTural Enemies
Pupae of various hymenopTerous parasiToids were exTracTed

from mines of L, blancardella and reared in plasTic peTri

 

dishes ( 4" dia. ). MoisTened Tissue paper was placed in The
peTri dishes To prevenT dessicaTion of The pupae. Emerged
adulTs were preserved in 90% eThanol soluTion and senT To
MarTinaT* for idenTificaTion E Figures 9 and l0 ].

PredaTory chrysopid larvae were collecTed in The field

and reared on larvae and pupae of L. blancardella which were

 

exTracTed from The mines. The feeding raTe of The chrysopid
larvae was measured as The number of leafminer larvae consumed
per hour E Figure l2 3.

A "muscadine" ( STeinhaus, I967 ) fungus E Figure II 3
which was prevalenT in field ploTs was broughT inTo The
IaboraTory. Leafminer Tissue-feeding larvae which were
infecTed wiTh This fungus were inTroduced inTo The mines
of healThy Tissue—feeding larvae on a one—To—one basis.

Five such mines were placed in a plasTic peTri dish ( 4" dia. )
and Then placed in a conTrolled environmenT chamber. The
experimenT was replicaTed 3 Times wiTh 3 conTrol peTri dishes
conTaining 5 unadulTeraTed mines each.

In a block of 20 MclnTosh apples aT Richland, The degree

 

* Mr. PeTer MarTinaT is a graduaTe sTudenT in The DeparTmenT of
EnTomology aT Michigan STaTe UniversiTy who specializes in
Taxonomy.

of morTaliTy caused by each of The disTinguishable
morTaliTy facTors was measured aT The end of each

generaTion of The leafminer. A IOO mine sample was
dissecTed by peeling away The lower leaf epidermis
and The conTenTs of each mine were recorded on each

sample daTe E Table l ].

B. Seasonal DevelopmenT

The developmenT of each generaTion of L, blancardella

 

was moniTored in 2 unTreaTed apple orchards aT Richland
and Hickory Corners, Michigan. Samples were Taken aT
Richland from July l8, I973 unTil July l6, I974. The
degree of parasiTism increased To a high level during
The l974 season so ThaT accuraTe moniToring of The deve-
lopmenT of The leafminer was noT possible. AT This Time
The sampling siTe was changed To The Hickory Corners
orchard which is abouT 7 miles norTheasT of Richland.
JonaThan varieTy apples were sampled aT each siTe.

A l00 mine sample was Taken aT Richland from a 20
Tree ploT on each sample daTe. The sample was examined
The same day and The number of leafminers In each of The
following sTages of developmenT was counTed:

l. Sap-feeders

2. Tissue-feeders

3. Pupae - includes all non-feeding sTages beTween
insTar V and The adulT.

4. Emerged adulTs - includes The number of empTy
pupal cases found proTruding from The
mines of The currenT generaTion E Figure 7 J.
The number of leafminers which were parasiTized by any of
The disTinguishable naTural enemies also was recorded on
each sample daTe. Sampling conTinued unTil November 4, I973.
Spring generaTion adulT emergence was moniTored in l974
using 4 cardboard Traps which were given a lighT coaTing of
TanglefooT* adhesive. The l2" square boards were placed on
Top of The leaf liTTer, adhesive side down, around The base
of a single Tree which was heavily infesTed The previous
year. The boards were puT ouT on April l6, l974 and were
checked for adulTs on each sampling daTe unTil June l2
E Table 2a 3.
Leaf sampling sTarTed again on May l3 and conTinued
unTil all Third generaTion larvae eiTher pupaTed or sTopped
feeding on November 5, I974. A IOO mine sample from 20

Trees was Taken on each sample daTe from Hickory Corners

E Table 2b 3.

C. EffecT of Mining on The HosT
A 500 leaf sample was picked aT random from a ploT of

l2 JonaThan Trees aT The Hickory Corners orchard aT The end

 

* ManufacTured by The TanglefooT 00., Grand Rapids, Michigan.
AcTive ingredienTs: PolybuTenes and hydrogenaTed casTor oil.

of each generaTion during I974. The number of mines per
sample was recorded and The average number of mines per
leaf was calculaTed. A sample of 30+ mines was selecTed
aT random from The former sample and The lower epidermis
of The mined area was dissecTed away. Care was Taken To
dissecT away only mines of The currenT generaTion. The
lower surfaces of The mined leaves were phoTocopied and
The leaf copies were cuT ouT and weighed. -The mined areas
of The leaf copies were Then cuT ouT and weighed. The raTio
of The mine weighTs ( of The paper phoTocopies ) and The
whole leaf weighTs was mulTiplied by The average number of
mines per leaf and considered as an esTimaTe of The leaf
area damaged by each generaTion of The leafminer E Table 3 J.
The reacTion of The leaf To The inTrusion of The
leafminer was observed under a compound microscope. A l-cm
laTlTudinal secTion was cuT from a fresh leafmine and placed
in a l0% soluTion of saffranln dye. The secTion was placed
in a microTome made from an 8-mm bolT and nuT. Paraffin
was poured over The specimen and a Thin secTion was cuT
across The mine. The secTion was Then placed in xylol To
dissolve The paraffin and was Then mounTed on a glass micro-
scope slide. The secTion was scanned under The microscope

E Figures I4 and l5 3.

D. Chemical ConTrol

CerTain carbamaTe and organOphosphaTe insecTicides
were TesTed during The l974 season To deTermine The effecT
of These compounds on The populaTion densiTy of L, IELEET
cardella. The insecTicides were applied in 4 differenT
ploTs which differed in apple varieTy. Specifics of each

ploT are as follows:

PloT l - Apple varieTy: Red Delicious
LocaTion: Fennville, Michigan
Spray schedule: A*

PloT 2 - Apple varieTy: MclnTosh
LocaTion: Fennville
Spray schedule: A*

PloT 3 - Apple varieTy: JonaThan
LocaTion: Fennville
Spray schedule: A*

PloT 4 - Apple varieTy: JonaThan

LocaTion: Douglas, Michigan
Spray schedule: 8*

There were 3 replicaTions for each TreaTmenT in each ploT.
A 50 leaf clusTer sample was Taken from each replicaTe of
each TreaTmenT. The number of mines per sample was considered

as an esTimaTe of The populaTion densiTy of L, blancardella

 

in each Tree. Each replicaTe consisTed of a single TreaTed
Tree E Table 4 J.
The following experimenTal and regisTered broad specTrum

insecTicides were applied wiTh a John Bean air blasT sprayer:

 

* For spray schedule 'A' applicaTion daTes were: 5/24, 6/7,
6/20, 7/3, 7/l7, 7/3l, 8/28, 9/ll. For spray schedule '8'
applicaTion daTes were: 6/3, 6/l7, 7/l, 7/l5, 7/29, 8/l2,
8/26, 9/9.

San I97 - organophosphaTe, Sandez Wander, Inc.

San 20l - organophosphaTe, Sandez Wander, lnc.

OS l5647 — carbamaTe, Diamond Shamrock Chemical Co.

CGA l8809 - organophosphaTe, Ciba - Geigy Corp.

CA 6900 - E. M. LaboraTories, Inc.

CME 74020 - E. M. LaboraTories, Inc.

Mobil 9087 - Mobil Oil Co.

Lorsban - chlorpyrifos, organophosphaTe, Dow Chemical Co.

LannaTe - meThomyl, carbamaTe, DuPonT Chemical Co.

ParaThion - Thlophos, organophosphaTe, MonsanTo Chemical Co.

GuThion — azinphos meThyl, organophosphaTe, Chemagro Corp.
To deTermine The effecT of sysTemic insecTicides on

The larval sTages of L, blancardella The following compounds

 

were applied in a randomized compleTe block design wiTh a
hand held spray gun:
SysTox - demeTon, organophosphaTe, Chemagro Corp.
MeTa—sysTox R - oxydemeTon meThyl, organophosphaTe, Chemagro Corp.
Cygon - dimeThoaTe, organophosphaTe, American Cyanamid Co.
Each replicaTe consisTs of one side of a single Tree. There
were 3 replicaTes per TreaTmenT and azinphos meThyl was used
as a sTandard for comparison.

TreaTmenT blocks were designed To reduce variance due
To populaTion densiTy measured in The pre-spray counTs E Fig-

ure l6 3. Leafminer densiTy was deTermined In The pre—spray

counTs by recording The number of leafmines in a sample of
IO leaf clusTers E Figure l6 3. The effecT of These sysTemic
insecTicides was measured in Two separaTe Trials on The sap-
feeders and The Tissue-feeders. JonaThan apple varieTy was
used in each Trial. AT Hickory Corners, The sprays were
applied while The larvae were in The sap-feeder sTage on
AugusT 20, I974. Six days afTer TreaTmenT a l5 mine sample
was collecTed from each replicaTe and The percenT morTaliTy
was deTermined by dissecTing The mines in The IaboraTory.
AT Richland, The sprays were applied while The larvae were
in The Tissue-feeder sTage on June 27, I974. SixTeen days
afTer TreaTmenT a 25 mine sample was Taken from each replicaTe
and The percenT morTaliTy was deTermined by dissecTing The
mines in The IaboraTory. To reduce The variance due To naTural
morTaliTy of The leafminer and To gain a beTTer esTimaTe of
The effecT of The insecTicides, The efficacy of each maTerial
was deTermined using The formula proposed by AbboTT ( I925 )
as presenTed by UnTersTenhofer ( I963 ).

no. living leafminers no. living leafminers

in The conTrol ' in The TreaTmenT

Efficacy : living leafminers in The conTrol

X IOO

The percenT morTaliTy and efficacy daTa for These Trials is
given in Tables 5a and 5b.

The effecT of cerTain broad specTrum sprays on The degree
of parasiTism in The leafminer populaTion was deTermined aT

The Douglas orchard ( ploT 4 ). The degree of parasiTism by

ApanTeles ornigis and eulophid parasiToids was measured

 

in TreaTmenT replicaTes which had a sufficienT number of
mines for sampling. For This deTerminaTion a sample of

leafmines was collecTed from each replicaTe and examined
in The IaboraTory. The sample size varied from 20 To 50

mines depending on The availabiliTy of maTerial E Table 6 j.

E. Miscellaneous STudies on The AdulT Leafminer

a. FecundiTy — A sample of 35 leafmines was collecTed
and placed inTo a single l8" X 6" nylon mesh sleeve. The
sleeve was Then placed around a l2" branch of apple. The
leafminers in The sleeve were In The pupal sTage. Four weeks
afTer The sleeve was puT inTo The field The sleeve was removed
along wiTh The enclosed branch. The number of mines on The
leaves of The branch and The number of empTy female and male
pupal cases in The 35 mine sample were counTed.

b. ParThenogenesis - A sample of 25 female pupae was
placed inTo a peTri dish ( 4" dia. ) and were Then reared
To adulTs. In 3 weeks 20 females emerged which were placed
in a nylon sleeve similar To The one used in The fecundiTy
experimenT. The sleeve was placed around an apple Twig which
was cuT from The Tree and placed in a jar of waTer. AfTer
all The females had died ( 2 weeks I The leaves of The Twig

were examined for eggs and leafmines.

c. Pheromone sTudies - On AugusT 2, I973 virgin

female moThs of L, blancardella were placed inTo 2

 

cylindrical plasTic cages ( 6 females per cage ) measuring
I-cm deep by 2-cm in diameTer wiTh one end covered by a
fine mesh nylon screen. Each cage was placed inside of

a 3M 'SecTar' Trap which is commonly used To Trap oTher
orchard pesTs via pheromones. The 2 Traps were seT ouT

in The field along wiTh 2 empTy conTrol Traps aT The

Richland orchard.

RESULTS AND DISCUSSION

A. NaTural Enemies
The following hymenopTerous parasiToids were found

To aTTack The larval sTages of L, blancardella in Michigan:

 

Braconidae ApanTeles ornigis Weed

 

Eulophidae Sympiesis conica ( Provancher )

 

Sympiesis marylandensis GiraulT

 

Sympiesis sp.

Pnigalio flavipes ( Ashmead )

 

Predacious chrysopid larvae were observed To be naTural

predaTors of adulT L, blancardella, aTTacking Them during The

 

dayTime soon afTer They emerged. These chrysopid larvae were
able To consume an average of 7 leafminer larvae per hour in
The IaboraTory. These predaTors were only idenTified To The
family level as rearing Them To The adulT sTage was noT
accomplished.

Of The l5 mines infecTed wiTh The "muscadine" fungus,
5 healThy larvae became overgrown by The fungus. One healThy
larvae in The l5 conTrol mines became infecTed. When These
infecTed larvae where Transferred To 6 healThy sap-feeder mines
no furTher infecTions occured.

The counTs of The morTaliTy facTors of L, blancardella

 

aT The end of each generaTion E Table l ] reveal a decrease

20

Table l. - CounTs of The morTaliTy facTors of L, blancardella
from a IOO mine sample Taken aT The end of each
generaTion of The leafminer, Richland, Michigan, l974.

 

 

 

MorTaliTy Sampling daTe and generaTion
facTor July l6, lsT SepT. 3, 2nd Nov. 5, 3rd
I no. per sample )

 

 

ApanTeles ornigis 32 l4 l8
All eulophids I6 49 I7
HyperparasiToid* l2 5 0
" Muscadine" fungus l4 l6 8
Unknown causes** l6 ll l9
Emerged adulTs l0 5 38

and living pupae

 

* ATTemst To rear The pupae of This insecT failed so idenTificaTion
was noT possible. However, iTs biology is very similar To The
hyperparasiToid described by Beckham I I950 ) and PoTTinger and
LeRoux I l97l ) of The genus Horimenus.

** MorTaliTy in This caTagory may have been caused by predaTion or
dehydraTion of The larvae.

2l

in The incidence of parasiTism by A, originis and an
increase in The incidence of eulophid parasiTism afTer

The firsT generaTion. MorTaliTy was lowesT in The Third

generaTion.

8. Seasonal DevelopmenT

Tables 2a and 2b show The field daTa for The I973
and l974 seasons. Table 2b is annoTaTed wiTh significanT
field observaTions. Figures 2a, 2b and 2c are ploTs of The
developmenT of The life sTages in I974. The daTa show ThaT
The generaTions of The leafminer are discreTe in souThwesTern
Michigan. The degree of parasiTism seems To be leasT during
The sap-feeder sTage of The leafminer. Spring generaTion
adulT emergence occurs during The firsT warm ( 70+° ) days

of spring.

C. EffecT of Mining on The HosT

A ToTal leaf area reducTion of 3|.7% was realized by
The end of The Third generaTion aT Hickory Corners In I974.
The average area per mine increases wiTh each generaTion
E Table 3 ]. FirsT generaTion mines appeared on The cenTral
leaves and waTer sprouTs more frequenle Than on The ouTer
canopy. Second and Third generaTion mines were fairly
evenly disTribuTed ThroughouT The canopy.

Even Though The larvae specifically ignore The vascular

22

Table 2a. - CounTs of spring generaTion adulTs from 4 adhesive
Traps disTribuTed on Top of The leaf IiTTer around
a single apple Tree, Richland, l974.

 

 

 

 

Sample daTe No. of adulTs Trapped
April 23 O
26 264
May 2 50
I3 6|
20 57
June I 5
6 3
l0 0
Table 2b. - The developmenT of each generaTion of L. blancardella

 

Through Time, recorded as The number oT individuals
in each life sTage per l00 mine sample, Richland and
Hickory Corners, Michigan, I973 and l974.

 

 

 

 

Life sTages

Sample Sap- Tissue- Emerged ParasiTized
daTe feeders feeders Pupae adulTs leafminers
I973
July l8 5 20 2 3 70

25 7 l5 0 25 53

3i 8 24 0 I4 54
Aug. 2 3 44 20 6 27

6 O 25 l0 IS 50

9 I 20 3 l2 64

l4 0 ll 8 32 49

I6 5 l2 0 IS 68

24 22 l2 ll I7 48
SepT. 5 90 4 0 O 6

I7 60 37 0 0 3

29 23 75 l 0 l
OcT. 6 0 77 3 O 20

20 0 58 0 0 42

27 O 46 20 0 34
Nov. 4 O 26 63 0 ll

23

Table 2b. I conTinued )

 

 

 

Life sTages
Sample Sap- Tissue- Emerged ParasiTized
daTe feeders feeders Pupae adulTs leafminers
l974
May 2b 0 o o o 0
I3 68 o o 0 32a
20 46 I3 0 o 4IC
June I 38 22 o 0 4o
6 23 25 o 0 52d
IO 28 32 3 o 39
I2e I6 46 I o 33
I4 II 36 4 o 39
I8 8 62 4 o 26
2o 0 42 6 o 52
22 4 52 8 o 36
28 o 56 6 o 38
July I o 38 8 o 54
4f 0 I8 l6 l8 58
l0 0 0 I8 I4 64
I3b l0 0 l0 I4 66
I6h 28 35 0 I2 25
22 2o 38 0 I9 23
279 2I 46 7 8 I8
Aug. I 6 62 I4 4 I8
7f 0 44 3| 5 2o
I3b 33 I3 27 9 25
2o 28 3 l0 33 26
26 34 o I 36 29
SepT. 3e 49 l0 0 I2 28
IO 6| 5 0 IO 24
I8 49 l6 0 I4 2|
23 5o 20 0 l5 I5
OCT. 2 I9 73 0 4 4
8 8 79 I 3 9
I5 0 85 2 I I2
22 o 82 5 I I3
29 0 4| 5| 0 l4
Nov. 5 0 2 5l 0 479

 

Dead larvae were eiTher dehydraTed or overgrown by fungus.
Eggs in advanced sTage of developmenT firsT sighTed.

FirsT eulophid larva sighTed wiThin mine E Figure 9 ].
FirsT A, ornigis cocoon sighTed wiThin mine E Figure l0 ].
No adulTs sighTed in The field.

AdulTs firsT sighTed flying in The field.

ParasiTism mainly due To A, originis.

Sampling siTe swiTched from Richland To Hickory Corners.

D'LQ-hCDQOU'OJ

24

FIGURES 2a, 2b and 2c - Seasonal developmenT of L, blancardella,

 

Richland and Hickory Corners, Michigan, l974.

Figure 2a is a ploT of The percenT of The unparasiTized
sample E Table 2b 3 in The adulT and sap-feeder

sTages versus sampling daTe. Solid line represenTs The
adulT sTage and The doTTed line represenTs The sap-feeder

sTage.

Figure 2b is a similar ploT of The Tissue-feeder and
pupa sTages. Solid line represenTs The Tissue-feeder

sTage and The doTTed line represenTs The pupa sTage.

Figure 2c is a ploT of The developmenT of each sTage of

each generaTion of The leafminer as iT relaTes To TemperaTure.
TemperaTure daTa were provided by The NaTional WeaTher Service
which moniTors daily TemperaTures aT Hickory Corners, Michigan.
Degree days were calculaTed from daily minimum and maximum
TemperaTures using a base TemperaTure of 40° F. Degree days

were accumulaTed from April I, l974 unTil November 5, I974.

percent of nonparasltlzed sample in indicated stage

Ind, (::> 25

80 Adults

7 Sap feeders ,-'

“I :
log

 

 

 

 

_L.=

Apfll May

Illllq

80 Tissue feeders

 

 

, 70
so
soq

fizzso

 

 

40 .1 Pupae

 

 

3Q_, o 5 1
2L
.- 9
I o—I 0. o: . : .
3 : 5' °.
9v” ‘in: 3.,

 

 

 

I .
April May lune July Aug. Sept.

26

 

996‘

 

 

 

2.3 32: :3 2:3.—
aaon coca

 

 

 

aca—

 

 

 

 

 

=2:

aga~

Logos. aamu_—
Lagos» gum
mum

a.==¢

was.

.32: 2.3:
Loco». new
mum

u_=u¢

«Ea;

Luau». nan“.—
.uumom a.»
any

am»

wen

“u—

at»
=a_:___.u.§w

26

2.3 :2: :3 :33
econ oaov can” econ sea—

2...:

«as;

Lagos. ¢=»»_—
Lang». an»
mum

 

 

 

u_=u<

«as;

:2: 2.3:
Logo». an”
sum

 

 

 

 

    

; . ,m we ~_=u‘
. 5.5. 5..., 3....
Lugs». °=»m_—
Luau.“ a.”
any

a

 

 

 

ugu

«a—

new
§_:___.o.§w

 

 

 

 

27

Tissue of The leaf while feeding, The separaTion of The lower
epidermis from The spongy mesophyll causes dessicaTion of The
mined area afTer The adulT emerges. In severe infesTaTions,
i.e. 5 or more mines per leaf, The leaf becomes folded To

The exTenT ThaT effecTive leaf area is reduced.

While scanning The parenchyma cells inside The mines of
new leaves under a microscope, clusTers of ca. 20 To 30
hyperTrophied parenchyma cells are ofTen observed proTruding
ouTward Toward The lower epidermis. These cells are ca. 4X
The size of normal parenchyma cells. Close examinaTion of
The parenchyma cells along The ouTer margin of The mine
reveals many areas of cell regeneraTion E Figures l4 and l5 3.
This indicaTes ThaT The leaf is able To repair iTself if The
leafmining larva dies.

ReducTion in leaf area is minimal afTer The firsT Two
generaTions E Table 3 J. The greaTesT damage occurs afTer
The Third generaTion. IT is doubeul ThaT a significanT
reducTion in yield will occur during The season of a heavy
infesTaTion since mosT of The damage occurs so laTe in The
season. Such an infesTaTion, however, will cause reduced

vigor and possibly reduced yield The following season.

D. Chemical ConTrol
All broad specTrum insecTicides aT The Fennville siTe

I ploTs l, 2 and 3 ) gave excellenT conTrol of L, blancardella

 

28

Table 3. - EsTimaTes of The leaf area damaged by each generaTion
of L. blancardella larvae, Hickory Corners, Michigan,

 

 

 

 

I 974’.
Sample Genera- Mines/ Mines Mean area/ EsTimaTed
daTe Tion 500 leaves sampled mine damage
I no. ) I no. ) I cm2 I I % leaf area )
July I lsT 75 34 0.8I 2.I
AugusT 7 2nd 284 33 0.90 5.7
OcTober l6 3rd I262 35 0.92 23.9

 

29

E Table 4 J. This can be aTTribuTed To The early and
conTinuaI coverage of The foliage. AT The Time of The
firsT applicaTion, spring generaTion adulTs were emerging
and firsT generaTion larvae were in The sap-feeder sTage.
InfesTaTions of The sprayed Trees were minimal and noT of
economic imporTance.

AT Douglas I ploT 4 ) all TreaTmenTs were significanle
lower wiTh respecT To leafminer infesTaTion Than The conTrol.
No significanT difference was found beTween The high and low
raTes of San I97, San 20l or OS l5647. The populaTion densiTy
in The DS l5647, single applicaTion, TreaTmenT was greaTer Than
in The DS l5647, regular schedule, TreaTmenT. No significanT
difference was found beTween The 2 formulaTions of meThomyl.
These daTa indicaTe ThaT conTinuous coverage of The foliage
wiTh DS l5647 gives beTTer conTrol Than a single applicaTion

of This compound. SaTisfacTory conTrol of L, blancardella

 

can be achieved using The reduced raTes of San I97, San 20l
and DS l5647.

The sysTemic insecTicides were generally more effecTive
againsT The sap-feeders Than The Tissue-feeders E Tables 5a
and 5b J. OxydemeTon meThyl and dimeThoaTe caused higher
morTaliTy of The sap-feeders Than demeTon. No significanT
difference was found beTween The azinphos meThyl and demeTon

TreaTmenTs in The sap-feeder ploT wiTh respecT To morTaliTy.

30

Table 4. - Field evaluaTions of indicaTed insecTicides applied as
foliar TreaTmenTs To conTrol L, blancardella on apple,
Fennville and Douglas, Michigan, l974.

 

 

 

 

TreaTmenT and Mean no. leafmines/
PIoT formulaTion oz. AI/IOO gal. 50 leaf clusTers*
l ConTrol 5|.7 a
I CGA |8809, 50 WP 4 0.0 b
I CGA |8809, 50 WP 6 0.0 b
l Azinphos meThyl, 50 WP 4 0.0 b
2 ConTrol l24.3 a
2 Thiophos, 2 EC 8 2.7 b
2 Thiophos, 25 WP 8 0.7 b
2 CA 6900, 4 EC 3 0.0 b
2 CME 74020, 25 WP 3 0.0 b
2 CME 74020, 25 WP 4 0.0 b
2 Azinphos meThyl, 50 WP 4 0.0 b
3 ConTrol I00.3 a
3 Chlorpyrifos, 25 WP 3 4.0 b
3 Chlorpyrifos, 25 WP 8 4.0 b
3 Azinphos meThyl, 50 WP 4 0.0 b
4 ConTrol 40.0 a
4 DS l5647, 4 EC** I6 22.7 b
4 Mobil 9087, 2 EC*** 4 l4.0 bc
4 MeThomyl, I.8 EC 4 9.0 bc
4 DS l5647, 4 EC 8 7.3 bc
4 San I97, 4.3 EC 4 6.7 c
4 MeThomyl, 90 WP 4 4.7 c
4 San 20l, 4.3 EC 4 3.3 c
4 San I97, 4.3 EC 8 2.0 c
4 DS l5647, 4 EC l6 2.0 c
4 San 20l, 4.3 EC 8 |.7 c
4 Azinphos meThyl, 50 WP 4 0.0 c

 

Means in The same ploT which are followed by similar leTTers are
noT significanle differenT aT The I% level I Duncan's mulTiple
range TesT ).

Single applicaTion on June 3, I974.

*** Applied every fourTh week on June 3, July I, July 29, and

AugusT 26, I974.

**

3l

Table 5a. - EffecT of a single applicaTion of The indicaTed
insecTicide on The sap-feeder larvae of L, blan-
cardella, Hickory Corners, Michigan, I974.

 

 

 

TreaTmenT and MorTaliTy of

formulaTion oz. Al/IOO gal. larvae I % )* Efficacy I % )
ConTrol 20.0 a

DemeTon, 50% EC 2.25 62.3 b 87

Azinphos

meThyl, 50 WP 4.00 73.3 CD 68
DimeThoaTe,

40% EC 6.75 88.9 c 87
OxydemeTon

meThyl, 25% EC 6.00 95.6 c 95

 

Table 5b. - EffecT of a single applicaTion of The indicaTed
insecTicide on The Tissue-feeder larvae of
.L. blancardella, Richland, Michigan, l974.

 

 

 

 

 

TreaTmenT and MorTaliTy of
formulaTion oz. Al/IOO gal. larvae I % )* Efficacy I % )
ConTrol 6l.5 a

Azinphos

meThyl, 50 WP 4.00 85.3 b 62
DemeTon, 50% EC 2.25 90.7 b 76
DimeThoaTe,-

40% EC 6.75 90.7 b 76
OxydemeTon

meThyl, 25% EC 6.00 90.7 b 76
if

Means of 3 replicaTes. Means followed by similar leTTers are
noT significanle differenT aT The I% level ( Duncan's
mulTiple range TesT ).

32

However, The efficacy of azinphos meThyl was lower Than The
efficacy of any of The sysTemic insecTicides in boTh sap-
feeder and Tissue—feeder Trials. MorTaliTy in all TreaTed,
sap—feeder ploTs was significanle higher Than in The conTrol
ploT. This is also True of The morTaliTy in The TreaTed,
Tissue-feeder ploTs excepT ThaT all TreaTmenT means are
equivalenT. No significanT differences were encounTered in
The degree of parasiTism beTween any of The sysTemic insecT-
icide TreaTed ploTs and The conTrol ploTs.

Table 6 shows ThaT parasiTism by A, ornigis was
significanle reduced in ploTs TreaTed wiTh San 20l and
Mobil 9087 I ploT 4, Douglas, Michigan ). ParasiTism by
A, ornigis in ploTs TreaTed wiTh DS l5647 and meThomyl was
The same as in The conTrol. ParasiTism by all eulophid
parasiToids was significanle lower in all TreaTed ploTs

Than in The conTrol ploT.

E. Miscellaneous STudies on The AdulT Leafminer

a. FecundiTy - Of The 35 pupae placed in The nylon mesh
sleeve, 25 reached The adulT sTage I l2 males and I3 females ).
When The leaves enclosed in The sleeve were checked 4 weeks laTer,
l05 linear leafmines were presenT.

b. ParThenogenesis — AfTer all female moThs enclosed in

The sleeve died I 2 weeks afTer The sTarT of The experimenT )

33

Table 6. - EffecT of indicaTed insecTicide on The parasiTic
HymenopTera which parasiTize The immaTure sTages
of L. blancardella, Douglas, Michigan, l974.

 

 

 

TreaTmenT and 02. Al/ Mean % sample parasiTized wiTh: Mean no.

 

formulaTion IOO gal. A, ornigis* All Eulophidae* mines sampled
ConTrol l3.7 a 28.7 a 38
MeThomyl,

90 WP 4 |2.7 a l2.0 b 27
MeThomyl,

I.8 EC 4 6.3 ab I2.0 b 38
DS l5647,

4 EC 8 5.7 ab I2.0 b 30
Mobil 9087,

2 EC 4 2.3 b l5.7 b 27
San 20l,

4.3 EC 4 |.3 b 9.0 b 29

 

* Means followed by similar leTTers are noT significanle differenT
aT The I% level I Duncan's mulTiple range TesT ).

34

The leaves of The enclosed apple Twig were checked for
leafmines and leafminer eggs. No leafmines or eggs were
found.

c. Pheromone sTudies - AlThough none of The daTa was
sTaTisically significanT some replicaTes gave resulTs ThaT
could noT be ignored.

In The virgin female Traps seT ouT AugusT 2, I973,

7 male moThs were caughT in one Trap and 2 female moThs were
caughT in The oTher. No moThs were caughT in The 2 empTy
conTrol Traps. ExperimenTs conducTed by Ayers* indicaTe ThaT
male moThs are aTTracTed To cis-7-hexadecenyl aceTaTe and
cis,cis—7,ll—hexadecadecenyl aceTaTe and cis-ll-TeTradecenyl
aceTaTe.

The lack of parThenogenesis, The equal abundance of males
and females in The field and The aTTracTiveness of virgin
females and The preceding organic aceTaTes To The male moThs
indicaTe ThaT maTing is iniTiaTed by an air-borne chemical

pheromone which is released by The female moTh.

AlThough many broad specTrum insecTicides are effecTive
againsT This leafminer, resisTance To These maTerials may occur
as is The case wiTh oTher mulTivoITine fruiT pesTs, e.g. Psylla

Eygiggla_on pear and Typhlocyba pomaria on apple. The

 

 

* Dr. George S. Ayers is an insTrucTor and researcher in The
DeparTmenT of EnTomology aT Michigan STaTe UniversiTy.

35

nonspecific acTion of The broad specTrum insecTicides
also desTroys The naTural conTrol mechanisms of This
leafminer, i.e. The proTelean parasiTes and predaTors.
An inTegraTed conTrol approach is suggesTed employing
correcT Timing of low dosage insecTicide applicaTions
and The use of parasiToid-safe sysTemic insecTicides.
To increase The accuracy of spray applicaTion
Timing, more research is required To elucidaTe The

sTrucTure of The sex aTTracTanT pheromone of L, blancardella.

 

A correlaTion beTween The emergence of The leafminer and
The developmenTal sTage of The hosT apple Tree would give
us a beTTer undersTanding of The relaTionship beTween

developmenT of The insecT and The phenology of The hosT.

36

FIGURES 3 Through l5 -
Figures 3 Through 8 depicT The developmenTal

sTages of L, blancardella.

 

Figures 9 Through l2 depicT The naTural enemies

of L, blancardella.

 

Figures I3 Through I5 depicT The effecT of mining

on The hosT planT.

 

 

Figure 3. - Leafminer egg on lower Figure 4. - Sap-feeding larva on
surface of apple leaf. inner mine surface.

 

 

Figure 5. - Tissue-feeding larva on Figure 6. - Male pupa wiThin slighT
inner mine surface. , cocoon. NoTe irregular feeding
siTes I arrow ).

. e

{ids

4'"
" \

I
c
‘ r

J

 

Figure 8. - AdulT.

Figure 7. - EmpTy pupaT-casgfpro;
Truding from leafmine. NoTe folds
in The leaf epidermis ( arrow ).

37

 

 

38

 

 

0..
'\
Figure 9._- Eulophid parasiToid - Figure l0. - Cocoon of A, orni is
larva I arrow ) aTTacking Tissue- as IT is found in The leafmine.

feeding leafminer.

 

 

v ——4.__

 

 

Figure II. - FungalflgrowThon larva Figure l2. - Chrysopid larvae
I arrow ) and mine surface, commonly aTTacking exTracTed leafminer pupa.
found in The mines.

<‘.__.-—.._—L_

rd

 

39

 

 

Figure l3. - Close-up view of
3 maTure leafmines on a single
apple leaf.

r '3

' 5

   

\J

 

l

‘7‘-

Figures l4 and IS I lefT and rlghT, resp. I. - Thin cross-secTions of The
laTeral margin of The leafmine I mag. = IOOX ). The upper epidermis of The
apple leaf is To The righT and The lower epidermis which has been separaTed
from The resT of The leaf is To The lefT in each figure. RegeneraTing cells
of The spongy mesophyll Tissue of The leaf are evidenT beTween The 2 epidermal
layers I arrows ). NoTe The cellular connecTion I arrow ) beTween The lower
epidermis and The spongy mesophyll Tissue In figure l5.

40

FIGURE l6 - The relaTive densiTy of The leafmines of

L, blancardella in a l5 Tree ploT of JonaThan apple Trees

 

aT Richland, Michigan, used for The experimenT which TesTed
The effecT of cerTain sysTemic insecTicides on The morTaliTy
of The Tissue-feeder larvae. Each square represenTs a
single Tree and The encircled number is The mean densiTy

I based on 3 counTs per Tree ) of leafmines in The Tree
expressed as The number of mines per l0 leaf clusTers.

The solid lines enclose The Three blocks of The randomized
compleTe block design which was designed To remove variance
due To leafmine densiTy. Blocks l and III are plain and
block II is sTippled. The 4 arrows in The lower lefT corner
represenT The direcTion of The souThwesTerly prevailing

winds.

 

OOOOOOOOOOOO

 

 

 

 

 

 

 

 

NORTH

4i

42

LITERATURE CITED

AbboTT, W. S. I925. A meThod of compuTing The effecTiveness
of an insecTicide. J. Econ. EnTomol. l8: 265~7.

Baggliolini, M. I960. ObservaTions sur la biologie des deux
du genre LiThocolleTis: L. corylifoliella eT L, blancardella,
nuisibles aux arbes fruiTTers en Suisse romande. Bull.
Soc. EnT. Suisse. 32(4): 385-97.

 

 

Beckham, C. M., W. S. Hough and C. H. Hill I950. Biology and
conTrol of The spoTTed TenTiform leafminer on apple Trees.
Va. Agric. Exp. STa. Tech. Bull. No. I44. l9 pp.

DouTT, R. L. I964. Ecological considersTions in chemical
conTrol - lmplicaTions To non-TargeT inverTebraTes. Bull.
EnT. Soc. Am. l0: 83-8.

Fulmek, L. I962. ParasiTinsekTen der BlaTTminierer Europas.
UiTgeverij Dr. W. Junk, DeHaag, The NeTherlands 203 pp.

Grandi, G. I959. The problems of morphological adapTion in
insecTs. SmiThsonian Misc. Coll. I37: 203—30.

Hering, E. M. l95l. Biology of The Leafminers. UiTgeverij
Dr. W. Junk, 's—Gravenhage, The NeTherlands. 420 pp.

HuTson, R. I938. NicoTine sulfaTe and summer oil for conTrol
of TenTiform leafminer. J. Econ. EnTomol. 3i: 455.

Kremer, F. W. I963. Major leafminer species occuring in The
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