comparison of community composition of parasitoids

7232019 Comparison of Community Composition of Parasitoids

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POPULATION ECOLOGY

Comparison of Community Composition of Parasitoids that

Attack Leaf-Mining Moths (Lepidoptera Gracillariidae)

HIROAKI SATO

Biological Laboratory Nara University of Education Takabatake Nara 630 Japan

Environ Entomol 24(4) 879-888 (1995)

ABSTRACT Parasitoid assemblages associated with Phyllonorycter leaf miners (Lepidop-tera Gracillariidae) were examined on the 2 deciduous oaks Quercus dentata and () mon-

golica in Hokkaido northern Japan and those on 2 others Q acutissima and Q variabilisin Nara central Japan To address to what extent interspecific competition is important inorganizing parasitoid communities I compared species richness species composition and lev-

els of parasitism by guilds at different host immature stages among the parasitoid assemblagesParasitoids were separated into 5 guilds according to parasitism modes (idiobiosis and koino-

biosis) and host immature stages attacked and killed Pooled data showed that the number of

parasitoid species per host leafminer species in Japan (31) was similar to that in the United Kingdom (41) and that idiobionts (potential generalists) exceeded koinobionts (specialists) inspecies number (625) A koinobiont guild and 2 idiobiont guilds had an inverse relationship

in level of parasitism between 2 assemblages at each study area These results may suggest

that interspecific competition is important in organizing parasitoid communities Neverthelessdominant species and guilds varied among the assemblages resulting in different patterns of

percentage of parasitism by guilds in relation to host stage among the assemblages This implies

underuse of hosts at some stages by parasitoids and interspecific competition is unlikely to be severe Interspecific competition therefore seems to partially contribute to parasitoid com-

munity organiZlt1tion

KEY WORDS Phyllonorycter competition parasitoid community

WHETHER INTERSPECIFIC COMPETITION is an im-

portant force in structuring a community is a fun-damental question in ecology Conventional com-

petition theory predicts that if interspecific com-

petition is strong communities on similar resource

sets or habitats in different geographic regions willexhibit similar species richness and guild struc-

hIres resulting in constancy in community struc-

hIre (see Cody and Diamond 1975 Giller 1984

Begon et al 1990)

On the basis of the comparison of community

structure ecologists agree that competition is not

a strong force in herbivorous insect communities(Strong et al 1984 Begon et al 1990) In contrast

such an agreement has not been found in the study

of parasitoid communities The dispute between

Dean and Ricklefs (1979 1980) and Force (1980)

and Bouton et al (1980) is a classic example Dean

and Ricklefs (1979) tested a prediction that if in-

terspecific competition is the primary structuring

force in a parasitoid community the abundance of

a parasitoid species should be inversely related to

the number of other parasitoid species exploiting

the same host Using a large set of data on the

larval parasitoids of Lepidoptera collected by theCanadian Forest Insect Survey in southern Ontar-

io they analyzed the partial correlation between

parasitoid abundance and the species number or

abundance of other parasitoids on the same hostThe results were not in accord with their predic-tion They concluded that parasitoids probably did

not compete for hosts Their conclusion however

was fiercely attacked by Force (1980) and Bouton

et al (1980) Force argued against it by referring

to several population studies that proved compe-

tition among parasitoids and Bouton et al pointed

out the unsuitability of the data for the analysis of

Dean and Ricklefs (1979)

Recently the number of parasitoid species per

host species (that is parasitoid assemblage size)

has been used frequently to analyze the structureof parasitoid communities (Hawkins 1988 1990

Hawkins and Gagne 1989 Hawkins et al 1990

1992 Sheehan 1991 Hawkins and Compton

1992) Hawkins (1990) compared parasitoid assem-

blage sizes on ecologically similar hosts across dif-

ferent geographic regions and under a wide range

of environments He found that assemblage size

varied greatly on exophytic hosts but was relatively

constant on endophytic hosts He concluded that

competition should be widespread in the parasitoid

communities associated with endophytic hosts

(borers miners and gallers) whereas competitionwas probably unimportant in communities on ex-

ophytic hosts Furthermore using the idiobiont

(kills or consumes the host at tlle time of attack)-

0046-225X950879-0888$02000 copy 1995 Entomological Society of America



880 ENVIRONMENTAL ENTOMOLOGY Vol 24 no 4

koinobiont (pennits continued host development)criterion as an indicator of generalist and specialisthost ranges in parasitoids Hawkins et al (1990)compared not only assemblage sizes but also ratios between idiobiont and koinobiont species against

host-larval feeding site and food plant type in the parasitoid complexes of British phytophagous in-

sects They revealed that assemblage size increased with host food plant size For endophytic hoststhis was becase of an increase in idiobionts (which

should tend to be generalists [Askew and Shaw1986]) on hosts on large plants but for exophytichosts it was the number of koinobionts (potentialspecialists) that increased with foodplant size This

could be explained by Askews competition hypothesis (Askew 1980) He predicted that under severe interspecific competition species richness

of generalists (or idiobionts) will increase on hostson large food plants because a richer herbivorefauna provides a broad niche dimension that can

be partitioned by generalists whereas species rich-

ness of specialists will not Thereby Hawkins et al(1990) reached the same conclusion as Hawkins(1990) that is competition is important in orga-

nizing parasitoid communities associated with en-

dophytic hosts However Sheehan (1991) found

that the proportion of idiobiont species was higher

on trees than on herbs and shrubs in the parasitoid

complexes of exophytic Lepidoptera from the

northeastern United States He also suggested that

competition should be a determinant of the speciesrichness in parasitoid communities of exophytic

hosts

Mills (1993) however argued against the con-

clusions of Hawkins (1990) Hawkins et aI (1990)

and Sheehan (1991) He examined the parasitoid

complexes of tortricoid moths (Lepidoptera Tor-

tricoidea) with diverse larval feeding habits His

results showed no support for Askewscompetition

hypothesis either for exophytic hosts or for endo-

phytic hosts Hawkins and Compton (1992) were

also unable to present evidence for interspecific

competition in a parasitoid community associated

with endophytic African fig wasps They examined

patterns of species richness patterns to detennine

if the community was saturated with species Sat-

uration was tested by regressing local parasitoid as-

semblage size against the regional species richness

for each host (see Cornell and Lawton 1992) They

found no evidence that the community was satu-

rated with species which suggested that competi-

tion was not important in structuring the parasitoid

assemblages

When we compare community structure to clar-

ify interspecific competition in communities we

should consider to what degree available resourcesare exploited because by definition competition

occurs for resources limited in availability How-

ever the above investigations paid little attention

to level of parasitism In this article I examined

parasitoid assemblages associated with Phyllono~

ryeter leafminers on 4 species of deciduous oakS

(Fagaceae Quercus) in Hokkaido and Nara JapanI compared levels of parasitism by guilds at differ-ent host immature stages as well as species rich-ness and species composition among the assem-

blages I thereby addressed to what extent inter-specific competition is important in organizing par-asitoid communities

Phyllonoryeter leafminers are the most abun-

dant Quercus mining moths in Japan (see 5ato1991) Larvae of Phyllonoryeter have 5 instalSand

change their feeding habit from sap feeding to tis-sue feeding at the transition from the 3rd to 4thinstal (see Hering 1951) During the former stagelarvae feed on spongy parenchymatous tissue and form expanding blotch mines whereas during thelatter stage larvae consume palisade parenchy-matous tissue within the mine to make a tentiform

shape They pupate within the mine

Materials and Methods

This study was conducted in 2 oak forests One

is located at the Ishikari Coast 20 km north of Sapporo Hokkaido northern Japan (5 TIl in ele-

vation 430 13 N 141023 E) This forest is 500-

600 m in width running parallel with the shore

line The oceanic side of the forest 200-300 m

wide is predominately the deciduous oak Quercus

dentata Thunberg whereas the landward side is

mainly Q mongoliea Fisher The 2 oak species

break bud in late May to early June and the leavestum color in early October The other forest is lo-

cated at the Yata Hills 6 km west of Nara Honshu

central Japan (270 m in elevation 34040 N 1350

43 E) This forest is dominated by the 3 deciduous

oaks Q serrata Murray Q acutissima Carruthers

and Q variabilis Blume These oak species break

bud in mid- to late April and the leaves tum color

in late October

One thousand leaves were sampled randomly

from each of Q dentata and Q mongolica within

the forest at the Ishikari Coast usually at intervals

of 10 d from late June to early October in 1985

and 1986 At the Yata Hills 500 leaves were sam-

pled randomly from each of Q acutissima and Q

variabilis also at 10-d intervals from mid-May to

late October in 1991 and 1992 All mines of Phyl-

lonorycter on sampled leaves were divided into 5

stages according to size and external character SI

(sap-feeding mine of length 2 mm) 52 (2-4

mm) 53 (gt4 mm) Tl (tissue-feeding mine

amount of consumed palisade parenchymatous tis-

sue 20 of the area of the mine) and T2 (gt20

consumed) Preliminary studies in 1984 and 1989

revealed that these categories closely correspond

to the 5 instalST2 also included the pupal stage because of difficulty in externally distinguishing

the pupal stage mines from the 5th-instal mines

Mines of 51 52 and 53 stages from Q dentata

and Q mongolica were carefully dissected to as-

certain whether larvae were alive or parasitized

When eggs larvae or pupae of parasitoids were



August 1995 SATO COMPARISON OF PARASITOID ASSEMBLAGES 881

Table l Oltcurrence of hosl PhyUonorycter species

on Q dentata (D) Q rrwngolica (M) Q acutissima (A)

and Q variabilis (V)

Ishikari Coast Yata HilisPhyloonJrllr spbullbullcies

0 M A V

P ipponicdllt (Isshiki) + + +P orulissmae (Klimata) + + +P similL Kumata +I kalllijo (Kumata) +1 entala (Kumata) +1 lIcoconma (Kumata) +P Isllldolaulela (Klimata) +1 pygmaea (Klimata) +1 mOllgolirae (Klimata) +P msirislilOsa (Klimata) + +1 malSlldai (Klimata) +

Tutalllu species 2 7 4 3

Cited as P simlis in Sato (1991)

observed within the mine they were reared in

plastic cases under room conditions in summer and autumn or in an incubator at 5degC in winter Minesof T1 and T2 stages from Q dentata and Q rrwn-

golica and all mines from Q acutissima and Qvariabilis were reared under those conditions Spe-citS of Icafminers and parasitoids were identified

by adults emerging from these rearings Leaf-min-ing Phyllononjcter larvae were not identified tospecies because of close external resemblance

A dominant parasitoid species was defined using

95 CL of its relative abundance (Sakuma 1964)I f

nj N - 2YnlN - IIj)N3 gtnN + 2Yn(N - n )N3

where nj is the number of individuals of species i

N is the total number of individuals and n is the

mean number of individuals per species (=Ntotal

number of species) then species iwas regarded as

dominant species

Levels of parasitism were expressed by percent parasitism at different host immature stages Be-cause not all parasitoids were identified to species

mainly because of larval or pupal death from un-known Clnsesduring rearing (identification rate63 on Q dcntata 64 on Q mongolica 79 on

Q acutissima and 92 on Q variabilis) the per-centage of parasitism for a given parasitoid species

or group (P I) was estimated as follows

Pp = Ngs(l + NNid)(N ac + N id + Nm) X 100

where Ngs is the number of leafminers killed by

the parasitoid species or group at the time of cen-sus N un is the number of leafminers killed by un-

identified parasitoids at the time of census Nid isthe number of leafminers killed by identified par-asitoids at the time of census and Nac is the num-

ber of active leafminers (that is those actually

feeding within the mine at the time of census)Leafminers that were alive but being parasitized

by koinobionts at the time of census were regarded not as parasitized but as active leafminers and hy-

perparasitized leafminers were treated as thosekilled not by primary parasitoids but by hyperpar-asitoids Leaf-mining larvae were sometimes ab-

sent from mines or dead because of predation and unknown causes or an exuvia of a parasitoid was

sometimes observed within the mine These mineswere excluded from the analysis

Results

Host Species Composition Ilnd AbWldllnceOccurrence and densities of Phyllonorycter specieson Q dentata Q rrwngolica Q acutissima and Q variabilis are shown in Tables 1 and 2 Speciesrichness was highest on Q rrwngolica (7 species)followed by Q acutissima (4) Q variabilis (3) and

Q dentata (2) Leafminer density was significantly

higher on Q dentata tllan on Q rrwngolica in theIshikari Coast in both years In the Yata Hills the

density was higher on Q acutissima than Q var-iabilis in 1991 and 1992 although not significantly

so in the latter yearSpecies Richness and Composition of Parasit-

oid Assemblages In total 29 parasitoid species

were recorded from Phyllonorycter leafminers on

the 4 oaks (Figs 1 and 2 see also Appendix 1)Species richness was similar among Q dentata (18

species) Q rrwngolica (19) and Q acutissima

(17) but was rather Iowan Q vmiabilis (13) Mostof the parasitoid genera were common to 3 or 4

oaks Each parasitoid assemblage contained only1-3 parasitoid species that were recorded exclu-sively from a single oakmiddotand these parasitoids were

low in abundance The assemblage size (number of parasitoid species per host species) varied be-

tween 27 (on Q rrwngolica) and 90 (on Q den-

Table 2 Densities of total Phyllonorycter leafminers (active plus parasitized) on Q dentata (D) Q rrwngolica(M) Q acutissUna (A) and Q variabilis (V)

No (bullbullaves Ishikari

Study ytar collected Coast Yata Hills gt df p

per sample D M A V

1985 1000 625 300 1142 P lt 0001

1986 1000 348 222 2785 P lt 0001

1991 500 155 85 204 P lt 0001

1992 500 102 88 0968 03 lt P lt 04

The density is represented by the maximum value among samples collected at lO-d intervals in the year




Guild Parasitold

species oI

Q dentata

20

I

400I I

Q mongolea

20

I

40I

Ichneumonld

spp ()

Phoetesor

spA

Chrysocharls Lujiyei U

Aehrysoeharoides LspA 0

Aehrysocharoldes 1bull bull bull bull bull bull - -spB _

A

8

c

HoeothoraxspA

Pteromaus

spA

Eupemus

urozonus

Cirrospilus

dialus

Crrospilus

Iyncus

Dimmokia

brevieorns

Pngallo

spA

Tetrastiehus

spA

Chrysoeharis

aomedon

Chrysoehars

spC

Chrysonotomya

spD

Costeroeerus

trfaseatus

o

~~--I

~--

D

o

bull

o

D Eaehertus

b ~fenestratus

Sympess

~ I ~aevfrons

Sympiesis

~ ~sereeicornis

E Peurotroppopsis

japonea 0 bullTotal number of host leafmlners killed by Identified parasitoid species

1985 422 1631986 239 156

Total no species 18 19

Assemblage size 90 27

Fig 1 Relative abundances of parasitoids on Q dentata and Q lIwngolica at the Ishikari Coast Hokkaido

northern Japan Percentage represents the proportion of leafminers killed by a given parasitoid species A to E indicate

parasitoid guilds (compare Fig 3) Solid bar 1985 open bar 1986




Guild Parasltold

species oI

O scutisslms

20 40I I

oII

O vsrisbllls

20 40I I

60I

A HolcothorsxspA o o

B Phoetesor

~spB

Ollgoneurus IInoplnstus

Psrahormfus

slblpes 0Chrysochsrls

uJiyel 0 Achrysocharoides

spA

0

C Clrrospilus

0dlslus

Clrrospilus

IIyncus

Clrrospilus

rlngonels8

Chrysochsris

~spC

Tetrastlchus

IspA

Mlschotetrastichus

spA

Chrysonotomyla

~spB

Teeopterus

spA

D

D

bull~

-D Elachertus 0

fenestatus

~ ~Sympiesls

laevifrons

~Sympiesis

sericecornis

E Pleurotroppopsis _

japonca LJ Apleurotropls

spA 0

Total number of host leafmlners killed by Identified parasitoid species

1991 118 38

1992 145 63



Fig 2 Relative abundances of parasitoids on Q acutissima and Q variabilis at the Yata Hills Nara central Japan

Percentage represents the proportion of leafminers killed by a given parasitoid species A to E indicate parasitoid guilds (compare Fig 3) Solid bar 1991 open bar 1992



884 ENVIRONMENTAL ENTOMOLOGY VoL 24 no 4

Table 3 Abundance of the congeneric species of Cir-

rospilus and Sympiesis on Q dentata (D) and Q mon-goliea (M)

Study year

Guild

Hosllealmlner stage

Egg Larva Pupa

1st 2nd 3rd 4th 5thI I I I I I

S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn

24) and was 30 whendata were pooled Thus although the parasitoid

assemblages exhibited taxonomically similar spe-

cies composition they varied in size

Dominant parasitoid species also varied among

the assemblages Aehrysoeharoides sp B Cirros-

pilus lyncus and Pnigalio sp A on Q dentata C

diallus and Sympiesis laevifrons on Q mongolieaTetrastichus sp A and C lyncus on Q acutissima

and Pholetesor sp B on Q variabilis The domi-nant species did not differ between the 2 yr in Q

mongolica Q acutissima and Q variabilis but

somewhat differed in Q dentata where C lyncus

and Pnigalio sp A were dominant species in 1985 but not in 1986

Notable differences in abundances of congener-

ic species between host oaks may attract attention

(Table 3) The abundance of Sympiesis serieeicor-

nis was significantly higher on Q dentata than on

Q mongolica in both years By contrast the other

congener S laevifrons showed significantly higher abundance on Q mongolica than on Q dentata

In the genus Cirrospilus C diallus had higher

abundance on Q dentata than on Q mongolica

whereas for C lyncus the reverse was true al-

though not significantly so in 1986

Levels of Parasitism by Guilds in Parasitoid

Assemblages Parasitoid species were classified

into 5 guilds according to parasitism modes (ko-

inobiosis and idiobiosis [Askew and Shaw 1986])

and host immature stages attacked and killed (Figs

1-3) Koinobiont species belong to guilds A and B

Guild A included only the polyembryonic Holeo-

thorax sp A that oviposits into eggs of hosts and

emerges at stage T2 whereas guild B comprised 8

species that oviposit into host larvae and emerge

mostly at stage T2 In contrast idiobiont species

belong to guilds C (15 species) D (3) and E (2)

Guild C and guild D attack mainly larvae of stages52 to T1 and those of stages T2 respectively Idio-

bionts exceeded koinobionts in species number in

each parasitoid assemblage (61-66 in the total

number of species) (Figs 1 and 2)

Figure 4 shows percentage of parasitism by the

5 parasitoid guilds at different host stages in the

16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont

Is interspecific competition an important forcein structuring the parasitoid assemblages I cannot

give a definite answer because the results present

both support and denial of interspecific competi-

tion In addition there is an ambiguity that inter-

specific competition cannot necessarily explain the

influence of host species richness and abundance

Fig 3 Definition of 5 parasitoid guilds (A-E) by themode of parasitism (idiobiosis or koinobiosis) and hostimmature stages attacked and killed Thickness of arrowsroughly indicates the relative intensity of parasitism

Kolnoblont

Discussion

assemblages Each assemblage possessed its own

characteristic guild as well as dominant speciesLeafminers on Q dentata were killed mainly at

middle and late stages by guild C and guild B

respectively whereas those on Q mongolica were

attacked largely at late stages by guild D On Q acutissima guild C contributed to high levels of

parasitism at early to middle stages and guild B

and E increased levels at stage T2 On Q varia-

bilis percent para~itism at stage T2 by guild B was

distinctly high As a consequence on Q dentata

Q mongolica and Q variabilis the lessened abun-

dance of guild C resulted in the lower parasitism

at stage S2 while on Q variabilis a decrease of

guild D depressed parasitism at stage TlKoinobiont guild Band idiobiont guilds D and

E exhibited an inverse relationship in percent par-

asitism at stage T2 (Fig 5) as Fig 4 shows on Q

dentata and Q variabilis the level of parasitism by

guild B was obviously higher than that by guilds D

and E whereas on Q mongoliea and Q acutissima

the latter was as high as or somewhat higher than

the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus



Au~ust 1995 SATO COMPARISON OF PARASITOID ASSEMBLAGES 885

o dentata O mongolca O acutssima O varabllis

1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2

Immature stage at which host leafminers are killed

Fi~ 4 Percentage of parasitism along host immature stage by the 5 parasitoid guilds on the 4 oak species Solid

column 1985 for Q dl~ntata and Q mongolica and 1991 for Q acutissima and Q variahilis open column 1986 for Q dentata and Q mongolica and 1992 for Q acutissima and Q variahilis

on parasitoid species richness in local assemblagesI discuss them in order below

Support of Interspecific Competition Con-ventional competition theory predicts that if inter-

specific competition plays an important role in or-

~ani7ingparasitoid communities the size of para-

sitoid assemblages on ecologically similar hosts

should be constant over geographic and climatic

gradients In addition Askew (1980) predicts that

if so the richness of generalist species should in-

crease in parasitoid assemblages on large plantswhereas the richness of specialist species should

not (see introduction) In fact Hawkins (1990) and

Hawkins et al (1990) found that parasitoid assem-

blages associated with endophytic hosts show not

only similar assemblage size in all geographic



886 ENVIRONMENTAL ENTOMOLOCY Vol 24 no 4

Fig 5 The inverserelationshipin the percentageof parasitismat stage T2 between koinobiontguild Band idiobiontsguildsD and E

regions but also an increase in species richness

with increasing host foodplant size caused by theaccumulation of idiobiont species (potential gen-eralists [Askewand Shaw 1986]) However neither holds true for parasitoid assemblages on exophytichosts (external feeders) Hence they concluded

that competition might be widespread in parasitoid

communities on endophytic hosts whereas competition is probably unimportant in those on exo-

phytic hostsThe current study recorded 29 parasitoid species

from 11 Phyllonorycter species (Table 1 see also Appendix 1) Preliminary studies of 1984 and 1989

(H S unpublished data) add 5 more species Pe -

diobius saulius (Walker) Elachertus inunctus(Nees) Elachertus sp C (nr longipetiolus) Cir-

rospilus vittatus Walker and Achrysocharoides sp

C Hence the assemblage size of the parasitoid

community associated with Phyllonorycter leaf-

miners on deciduous Quercus oaks in Japan be-

comes at least 31 (34 parasitoid species per 11host species on 4 Quercus species) Compared with

the results of Hawkins (1990) this figure is notgreatly different from 41 for the equivalent para-sitoid community in the United Kingdom (37 par-

asitoid species per 9 host Phyllonorycter species on

2 Quercus species) (Askew and Shaw 1986) In

both regions idiobionts exceed koinobionts in spe-cies number (2032 = 625 in Japan [2 specieswhose mode of parasitism are unknown are omit-

ted] W37 = 648 in the United Kingdom) Onthe basis of the predictions from conventional

competition theory and Askew (1980) this geo-

graphic comparison suggests that interspecificcompetition has an important role in structuring

parasitoid communities associated with Phyllono-

rycter leafminers on Quercus oaks

Moreover the present assemblages exhibit a pat-

tern for which interspecific competition provides

the most plausible explanation That is an inverse

relationship in the percentage of parasitism be-

tween koinobiont guild Band idiobiont guilds D

and E on 2 oaks at each of the study sites (Fig 4)

Askew and Shaw (1986) mention that koinobionts

of Phyllonorycter leafminers are under severe

pressure from facultatively hyperparasitic idio-

w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50

Percent perasltlsm by guild B

60

bionts and are poor competitors of idiobionts be-

cause unlike exophytic hosts leafminers parasit-ized by koinobionts cannot move away from the

vulnerable larval feeding site Thus parasitoids of guild B seem to enter the competitor (or enemy)

poor space of Q dentata and Q variabilis from

the competitor rich space of Q rrwngolica and Qacutissima respectively

Lack of Interspecific Competition If a com-munity is dominated by interspecific competitionthe rate of resource use by competitors will reacha limit This may be expected from the definitionthat competition occurs for limited resources

(Keddy 1989) This being so communities depen-dent on ecologically similar resources should ap- proach similar limited rates of resource use The

parasitoid assemblages on each host oak exhibit

different patterns of percentage of parasitism byguilds in relation to host stage This suggests thatthe rate of host use remains below the limit incertain assemblages For instance host larvae of

stage S2 are parasitized at obviously lower rates onQ dentata Q mongolica and Q variabilis than

on Q acutissima and tllOse of stage T1 on Q var-iabilis were less exploited than those on other oaks

Thus interspecific competition for hosts among

parasitoids does not seem to be severe in the par-

asitoid assemblagesAmbiguity Although the geographic assem-

blage size is similar between Japan and the United

Kingdom as mentioned before the local assemblages on each oak are highly variable in size (27-

90) The local variability might be attributable to

differences in host abundance and host species

richness If component species in a community

partition resources under severe competition the

species richness of the community will increasewith the variety and amount of available resources

(Begon et al 1990) On the Ishikari Coast the par-

asitoid assemblage on Q dentata which supportslower species richness of host leafminers has a

similar species richness to that on Q rrwngolica

which supports higher species richness of hosts Q

dentata harbors more hosts than Q rrwngolica OnQ dentata the lower species richness of hosts

seems to be compensated by the higher abundanceof hosts In the Yata Hills low species richness and

abundance of hosts result in low species richness

of parasitoids on Q variabilis compared with Q

acutissima It may be concluded that the host

abundance and host species richness complemen-

tarily affect the species richness of parasitoid as-

semblages on each oak

This conclusion nevertheless does not auto-

matically imply that each assemblage is dominated

by interspecific competition Mills and Kenis

(1991) and Mills and Schaberg (1988) report that

the species richness of parasitoid assemblages as-

sociated with the fir budworm Choristoneura mu-

rinana Hiibner and the coniferous Zeiraphera spe-

cies increase with host abundance Mills (1993)

mentions that such correlations of parasitoid spe-




cies richness with host abundance could be ex-

plained by host apparency (Askew and Shaw 1986)rather than interspecific competition However

Hawkins and Compton (1992) refer to their un-

published data that the number of parasitoid spe-

cies per fig species is highly correlated with species

richness of fig wasps in southern Africa Their care-

ful analyses of regression between local and re-

gional species richness (see Cornell and Lawton

1992) provide no evidence that the parasitoid com-

munity is saturated with species thus suggesting

that it is not dominated by interspecific competi-

tion

The differences in abundances of the 2 species

of each Cirrospilus and Sympiesis between Q den-tata and Q mongolica does not directly imply in-

terspecific competition between the congeners ei-

ther (Table 3) Askew and Shaw (1986) also find

such relationships in several parasitoid genera on

oak and birch at one locality They suggest that not

interspecific competition but some physical and

chemical properties of a host tree species have a

strong influence on the extent to which parasitoids

search for hosts on it There is another possibility

tllat the congeneric species may show preference

for the attack of particular host leafminer species

on the 2 different oaks and thus the congeneric

differences in abundances may be caused by such

preferences rather than direct competition This

possibility is however questionable As Boueek

and Askew (1968) show each species of the con-geners has a very wide range of host leafminer spe-

cies other tllan Phyllonorycter Thus it is unlikely

tllat each of the parasitoid species has developed

particular preference for certain species of Phyl-lononjcter

Conclusion

In conclusion geographic comparison of tl1e as-

semblage size and the ratio of generalists and spe-cialists between Japan and the United Kingdom

suggests that interspecific competition is important

in the organization of parasitoid communities as-sociated with Phyllonorycter leafminers Although

the local comparison of tl1e percentage of parasit-

ism by guilds at different host immature stages be-

tween the assemblages suggests interspecific com-

petition between a koinobiont guild and 2 idio-

biont guilds the comparison simultaneously im-

plies underuse of hosts of some stages by

parasitoids Neither tl1e influence of host species

richness and abundance on species richness of tl1e

parasitoid assemblages nor tl1e differences in abun-

dances of tl1e congeneric species between host

oaks is tenuous evidence for interspecific compe-

tition Therefore as Begon et al (1990) point out

it is concluded that interspecific competition may

affect only a small proportion of tl1e species inter-

actions and that despite significant competition be-

tween parasitoid guilds that is not strong enough

to be able to have an important influence upon the

species richness or structure of the parasitoid as-

semblages

Acknowledgments

I thank K Kamijo and K Maeto for identifYing a hugenumber of parasitoid specimens I am also grateful to M

T Kimura for his critical readings of the manuscript and

to S Higashi for his encouragement throughout the CUT-

rent study This study was supported in part by a Grant-

in-Aid for Encouragement of Young Scientists from the

Japan Ministry of Education Science and Culture in1992 (No 04740359)

References Cited

Askew R R 1980 The diversity of insect communi-ties in leaf-mines and plant galls J Anim Ecol 49

817-829Askew R R and M R Shaw 1986 Parasitoid com-

munities their size structure and development pp

225-264 In J Waage and D Greathead [eds] Insect parasitoids Academic London

Begon M J L Harper and C R Townsend 1990

Ecology individuals populations and communities

2nd ed Blackwell Oxford

Boueek Z and R R Askew 1968 Index of Palearc-

tic Eulophidae Le Fran~is ParisBouton C E B A McPheron and A E Weill

1980 Parasitoids and competition Am Nat 116

876-881Cody M L and J M Diamond 1975 Introduction

pp 1-12 In M L Cody and J M Diamond [eds]Ecology and evolution of communities Harvard Uni-versity Press Cambridge MA

Cornell H V and J H Lawton 1992 Species in-

teractions local and regional processes and limits tothe richness of ecological communities a theoretical

perspective J Anim Ecol 61 1-12Dean J M and R E Ricklefs 1979 Do parasites

of Lepidoptera larvae compete for hosts No Am

Nat 113 302-3061980 Do parasites of Lepidoptera larvae compete for

hosts No evidence Am Nat 116 882-884

Force D C 1980 Do parasitoids of Lepidoptera lar-

vae compete for hosts Probably Am Nat 116 873-

875Giller P S 1984 Community structure and the niche

Chapman amp Hall London

Hawkins B A 1988 Species diversity in the third and

fourth trophic levels patterns and mechanisms JAnim Ecol 57 137-162

1990 Global patterns of parasitoid assemblage size J

Anim Eco 59 57-72Hawkins B A and S G Compton 1992 African fig

wasp communities undersaturation and latitudinal

gradients in species richness J Anim Ecol 61 361-

372Hawkins B A and R J Gagne 1989 Determinants

of assemblage size for the parasitoids of Cecidomyi-

idae (Diptera) Oecologia (Bed) 81 75-88Hawkins B A R R Askew and M R Shaw 1990

Influences of host feeding-niche and foodplant type

on generalist and specialist parasitoids Ecol Ento-

mo 15 275-280

Hawkins B A M R Shaw and R R Askew 1992

Relations among assemblage size host specialization




and climatic variability in North American parasitoid communities Am Nat 139 58-79

Dering E M 1951 Biology of the leaf miners JunkGravenhage

Keddy P A 1989 Competition Chapman amp Hall

LondonMill8 N J 1993 Species richness and structure in the

parasitoid complexes of tortricoid hosts J Anim Ecol62 45-58

Mills N J and M Kenis 1991 A study of the par-asitoid complex of the European fir budworm Char-

istoneura murinana (Lepidoptera Tortricidae) and itsrelevance for biological control of related hosts BullEntomol Res 81 429-436

Mill8 N J and F Schoherg 1988 The structure md diversity of the parasitoid complexes of Zeiraphera

bud moths in relation to the dynamics of their pop-

ulations pp 159-160 In M Bouletreau and G Bon-not [eds] Parasitoid insects Les Colloques de lIN-RA Paris

Sakuma A 1964 Statistics in biology Tokyo Univer-sity Press Tokyo (in Japanese)

Sato H 1991 Differential resource utilization and co-occurrence of leaf miners on oak (Quercus dentata)Ecol Entomol 16 105-113

Sheehan W 1991 Host range patterns of hymenop-teran parasitoids of exophytic lepidopteran folivores

pp 209-248 In E Bernays [ed] Insect-plant inter-actions vol 3 CRC Boca Raton FL

Strong D R J H Lawton and R Southwood1984 Insects on plants community patterns and mechanisms Blackwell Oxford

Received for publication 26 September 1994 accepted 6 March 1995

Appendix l Taxonomy guild and occurrence of parasitoid species of PhyUonorycter leafminers 011 4 host oaksQ dentata (D) Q mongolica (M) Q acutissUna (A) and Q variabilis (V)

Family Ishikari Coast Yata Hills

Species Cuild

D M A V

Ichneurnonidae

Unknown spp B + +Braconidae

pholetesor sp A B + +Pholetesor sp B B + +Oligoneums inopinatus Tobias amp Belokoblskij B + +Parahonnills albipes (Ashmead) B + +

PteromalidaePteronuzlus sp A C +

Eupelmidae Eupelmus urownus Dalman C +

Encyrtidae Holcothorax sp A A + + + +

Eulophidae Elachertus fenestatus Nees D + + +Cirrospilus dialus Walker C + + +Cirrospilus lyncus Walker C + + + +

Cirrospilus ringonelae Kamijo C +Sympiesis laevifrons Kamijo D + + + +Sympiesis senceicorois (Nees) D + + +

Dimmocka brevicorois (Erdos) C + +Pngallo sp A C + +Tetrastichlls sp A C + + +

Mischotetrastchus sp A C + +Plmrvtroppopsis japonca (Kamijo) E + + + +

Aplmrotropis sp A E +Chrysocharis laomedoll (Walker) C + +Chrysocharis Iljyei Kamijo B + + +Chrysocharis sp C C + + + +

AchnJSocharoides sp A (nr splendens) B + + + AchnJSocharoides sp B B + +Chrysonotamyia sp B C +ChnJSonotomyia sp D C + +

Closterocems tnfasciatlls Westwood C +Teleoptems sp A C +

Total no species 29 18 19 17 13

For definition of guilds see Fig 3




koinobiont (pennits continued host development)criterion as an indicator of generalist and specialisthost ranges in parasitoids Hawkins et al (1990)compared not only assemblage sizes but also ratios between idiobiont and koinobiont species against

host-larval feeding site and food plant type in the parasitoid complexes of British phytophagous in-

sects They revealed that assemblage size increased with host food plant size For endophytic hoststhis was becase of an increase in idiobionts (which

should tend to be generalists [Askew and Shaw1986]) on hosts on large plants but for exophytichosts it was the number of koinobionts (potentialspecialists) that increased with foodplant size This

could be explained by Askews competition hypothesis (Askew 1980) He predicted that under severe interspecific competition species richness

of generalists (or idiobionts) will increase on hostson large food plants because a richer herbivorefauna provides a broad niche dimension that can

be partitioned by generalists whereas species rich-

ness of specialists will not Thereby Hawkins et al(1990) reached the same conclusion as Hawkins(1990) that is competition is important in orga-

nizing parasitoid communities associated with en-

dophytic hosts However Sheehan (1991) found

that the proportion of idiobiont species was higher

on trees than on herbs and shrubs in the parasitoid

complexes of exophytic Lepidoptera from the

northeastern United States He also suggested that

competition should be a determinant of the speciesrichness in parasitoid communities of exophytic

hosts

Mills (1993) however argued against the con-

clusions of Hawkins (1990) Hawkins et aI (1990)

and Sheehan (1991) He examined the parasitoid

complexes of tortricoid moths (Lepidoptera Tor-

tricoidea) with diverse larval feeding habits His

results showed no support for Askewscompetition

hypothesis either for exophytic hosts or for endo-

phytic hosts Hawkins and Compton (1992) were

also unable to present evidence for interspecific

competition in a parasitoid community associated

with endophytic African fig wasps They examined

patterns of species richness patterns to detennine

if the community was saturated with species Sat-

uration was tested by regressing local parasitoid as-

semblage size against the regional species richness

for each host (see Cornell and Lawton 1992) They

found no evidence that the community was satu-

rated with species which suggested that competi-

tion was not important in structuring the parasitoid

assemblages

When we compare community structure to clar-

ify interspecific competition in communities we

should consider to what degree available resourcesare exploited because by definition competition

occurs for resources limited in availability How-

ever the above investigations paid little attention

to level of parasitism In this article I examined

parasitoid assemblages associated with Phyllono~

ryeter leafminers on 4 species of deciduous oakS

(Fagaceae Quercus) in Hokkaido and Nara JapanI compared levels of parasitism by guilds at differ-ent host immature stages as well as species rich-ness and species composition among the assem-

blages I thereby addressed to what extent inter-specific competition is important in organizing par-asitoid communities

Phyllonoryeter leafminers are the most abun-

dant Quercus mining moths in Japan (see 5ato1991) Larvae of Phyllonoryeter have 5 instalSand

change their feeding habit from sap feeding to tis-sue feeding at the transition from the 3rd to 4thinstal (see Hering 1951) During the former stagelarvae feed on spongy parenchymatous tissue and form expanding blotch mines whereas during thelatter stage larvae consume palisade parenchy-matous tissue within the mine to make a tentiform

shape They pupate within the mine

Materials and Methods

This study was conducted in 2 oak forests One

is located at the Ishikari Coast 20 km north of Sapporo Hokkaido northern Japan (5 TIl in ele-

vation 430 13 N 141023 E) This forest is 500-

600 m in width running parallel with the shore

line The oceanic side of the forest 200-300 m

wide is predominately the deciduous oak Quercus

dentata Thunberg whereas the landward side is

mainly Q mongoliea Fisher The 2 oak species

break bud in late May to early June and the leavestum color in early October The other forest is lo-

cated at the Yata Hills 6 km west of Nara Honshu

central Japan (270 m in elevation 34040 N 1350

43 E) This forest is dominated by the 3 deciduous

oaks Q serrata Murray Q acutissima Carruthers

and Q variabilis Blume These oak species break

bud in mid- to late April and the leaves tum color

in late October

One thousand leaves were sampled randomly

from each of Q dentata and Q mongolica within

the forest at the Ishikari Coast usually at intervals

of 10 d from late June to early October in 1985

and 1986 At the Yata Hills 500 leaves were sam-

pled randomly from each of Q acutissima and Q

variabilis also at 10-d intervals from mid-May to

late October in 1991 and 1992 All mines of Phyl-

lonorycter on sampled leaves were divided into 5

stages according to size and external character SI

(sap-feeding mine of length 2 mm) 52 (2-4

mm) 53 (gt4 mm) Tl (tissue-feeding mine

amount of consumed palisade parenchymatous tis-

sue 20 of the area of the mine) and T2 (gt20

consumed) Preliminary studies in 1984 and 1989

revealed that these categories closely correspond

to the 5 instalST2 also included the pupal stage because of difficulty in externally distinguishing

the pupal stage mines from the 5th-instal mines

Mines of 51 52 and 53 stages from Q dentata

and Q mongolica were carefully dissected to as-

certain whether larvae were alive or parasitized

When eggs larvae or pupae of parasitoids were








0 M A V















dominant species















Results

















per sample D M A V

1985 1000 625 300 1142 P lt 0001

1986 1000 348 222 2785 P lt 0001

1991 500 155 85 204 P lt 0001

1992 500 102 88 0968 03 lt P lt 04





Guild Parasitold

species oI

Q dentata

20

I

400I I

Q mongolea

20

I

40I

Ichneumonld

spp ()

Phoetesor

spA




A

8

c

HoeothoraxspA

Pteromaus

spA

Eupemus

urozonus

Cirrospilus

dialus

Crrospilus

Iyncus

Dimmokia

brevieorns

Pngallo

spA

Tetrastiehus

spA

Chrysoeharis

aomedon

Chrysoehars

spC

Chrysonotomya

spD

Costeroeerus

trfaseatus

o

~~--I

~--

D

o

bull

o

D Eaehertus

b ~fenestratus

Sympess

~ I ~aevfrons

Sympiesis

~ ~sereeicornis

E Peurotroppopsis


1985 422 1631986 239 156









Guild Parasltold

species oI

O scutisslms

20 40I I

oII

O vsrisbllls

20 40I I

60I


B Phoetesor

~spB


Psrahormfus



spA

0

C Clrrospilus

0dlslus

Clrrospilus

IIyncus

Clrrospilus

rlngonels8

Chrysochsris

~spC

Tetrastlchus

IspA

Mlschotetrastichus

spA

Chrysonotomyla

~spB

Teeopterus

spA

D

D

bull~

-D Elachertus 0

fenestatus

~ ~Sympiesls

laevifrons

~Sympiesis

sericecornis



spA 0


1991 118 38

1992 145 63










Study year

Guild

Hosllealmlner stage

Egg Larva Pupa


S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn








































16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont








Kolnoblont

Discussion




















the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus





1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae






















0 M A V















dominant species















Results

















per sample D M A V

1985 1000 625 300 1142 P lt 0001

1986 1000 348 222 2785 P lt 0001

1991 500 155 85 204 P lt 0001

1992 500 102 88 0968 03 lt P lt 04





Guild Parasitold

species oI

Q dentata

20

I

400I I

Q mongolea

20

I

40I

Ichneumonld

spp ()

Phoetesor

spA




A

8

c

HoeothoraxspA

Pteromaus

spA

Eupemus

urozonus

Cirrospilus

dialus

Crrospilus

Iyncus

Dimmokia

brevieorns

Pngallo

spA

Tetrastiehus

spA

Chrysoeharis

aomedon

Chrysoehars

spC

Chrysonotomya

spD

Costeroeerus

trfaseatus

o

~~--I

~--

D

o

bull

o

D Eaehertus

b ~fenestratus

Sympess

~ I ~aevfrons

Sympiesis

~ ~sereeicornis

E Peurotroppopsis


1985 422 1631986 239 156









Guild Parasltold

species oI

O scutisslms

20 40I I

oII

O vsrisbllls

20 40I I

60I


B Phoetesor

~spB


Psrahormfus



spA

0

C Clrrospilus

0dlslus

Clrrospilus

IIyncus

Clrrospilus

rlngonels8

Chrysochsris

~spC

Tetrastlchus

IspA

Mlschotetrastichus

spA

Chrysonotomyla

~spB

Teeopterus

spA

D

D

bull~

-D Elachertus 0

fenestatus

~ ~Sympiesls

laevifrons

~Sympiesis

sericecornis



spA 0


1991 118 38

1992 145 63










Study year

Guild

Hosllealmlner stage

Egg Larva Pupa


S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn








































16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont








Kolnoblont

Discussion




















the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus





1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae


















Guild Parasitold

species oI

Q dentata

20

I

400I I

Q mongolea

20

I

40I

Ichneumonld

spp ()

Phoetesor

spA




A

8

c

HoeothoraxspA

Pteromaus

spA

Eupemus

urozonus

Cirrospilus

dialus

Crrospilus

Iyncus

Dimmokia

brevieorns

Pngallo

spA

Tetrastiehus

spA

Chrysoeharis

aomedon

Chrysoehars

spC

Chrysonotomya

spD

Costeroeerus

trfaseatus

o

~~--I

~--

D

o

bull

o

D Eaehertus

b ~fenestratus

Sympess

~ I ~aevfrons

Sympiesis

~ ~sereeicornis

E Peurotroppopsis


1985 422 1631986 239 156









Guild Parasltold

species oI

O scutisslms

20 40I I

oII

O vsrisbllls

20 40I I

60I


B Phoetesor

~spB


Psrahormfus



spA

0

C Clrrospilus

0dlslus

Clrrospilus

IIyncus

Clrrospilus

rlngonels8

Chrysochsris

~spC

Tetrastlchus

IspA

Mlschotetrastichus

spA

Chrysonotomyla

~spB

Teeopterus

spA

D

D

bull~

-D Elachertus 0

fenestatus

~ ~Sympiesls

laevifrons

~Sympiesis

sericecornis



spA 0


1991 118 38

1992 145 63










Study year

Guild

Hosllealmlner stage

Egg Larva Pupa


S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn








































16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont








Kolnoblont

Discussion




















the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus





1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae


















Guild Parasltold

species oI

O scutisslms

20 40I I

oII

O vsrisbllls

20 40I I

60I


B Phoetesor

~spB


Psrahormfus



spA

0

C Clrrospilus

0dlslus

Clrrospilus

IIyncus

Clrrospilus

rlngonels8

Chrysochsris

~spC

Tetrastlchus

IspA

Mlschotetrastichus

spA

Chrysonotomyla

~spB

Teeopterus

spA

D

D

bull~

-D Elachertus 0

fenestatus

~ ~Sympiesls

laevifrons

~Sympiesis

sericecornis



spA 0


1991 118 38

1992 145 63










Study year

Guild

Hosllealmlner stage

Egg Larva Pupa


S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn








































16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont








Kolnoblont

Discussion




















the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus





1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae




















Study year

Guild

Hosllealmlner stage

Egg Larva Pupa


S1 S2 S3 T1 T2

tata) (mean plusmn

5D 57 plusmn








































16 27 43

114 18 132

K - =4103 df =1P lt 0001

5 60 65

24 5 29

K - = 5297 df = 1P lt 0001

Emergence

Host alive

Oviposition

Oviposition

$Emergence

E

o

c

Idloblont








Kolnoblont

Discussion




















the former

1986

M TotalD

30 37 67

19 11 30

K - = 285 df = 1005 lt P lt 01

3 49 52

21 7 28

K - = 4154 df = 1P lt 0001

1985

M TotalD

S laevifro1S

S sericeicomis

Host oak

C dialllls

C lyncus





1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae



















1 1 A ~ II 1 ] ] 1 a l n l- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

BI I I I

50 r-

40 I-

30 r-

20 r-

E 10

II)

bull 0II)

1 150

C -11

C- bull 40cQ)

u

- 30Q)

a

20

10

0

20

10

0

20 E

10

0

81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2 81 82 83 T1 T2




















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae


















































w

30

o

~ 20 D

E

i i i 10 iiia

C1 liii 0

a

o

10 20 30 40 50


60

























































tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae





























tion





















Conclusion























semblages

Acknowledgments







References Cited


































mo 15 275-280
























Species Cuild

D M A V

Ichneurnonidae




































Species Cuild

D M A V

Ichneurnonidae















comparison of community composition of parasitoids

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