Florida F,', -. ..., .: 87(2)
FIELD OBSERVATIONS QUANTIFYING ATTRACTION OF THE PARASITIC
WASP, DIACHASMA ALLOEUM (HYMENOPTERA: BRACONIDAE) TO
BLUEBERRY FRUIT INFESTED BY THE BLUEBERRY MAGGOT FLY,
RHAGOLETIS MENDAX (DIPTERA: TEPHRITIDAE)
L. L. STELINSKI', K. S. PELZ' AND O. E. LIBURD2
'Department of Entomology, Michigan State U.... -,: East Lansing, MI 48824
S..: ... I & Nematology Department, University of Florida, Gainesville, FL 32611
The host foraging behavior of the larval parasitoid Diachasma alloeum (Muesebeck) (Hy-
menoptera: Braconidae) from natural populations was directly observed in a highbush blue-
berry, Vaccinium corymbosum L., plantation. More D. alloeum were observed alighting on
blueberry fruit clusters infested with Rhagoletis mendax Curran larvae than were observed
alighting on uninfested blueberry fruit clusters 80 cm away. Approximately equal numbers
of D. alloeum alighted on uninfested blueberries that were mechanically damaged versus
undamaged. The majority of D. alloeum females were attracted to host-infested blueberries
15 to 21 days after R. mendax females had ;. -;: .1 into fruit. Female D. alloeum spent
more time alighting on R. mendax-infested blueberry fruit clusters than on uninfested blue-
berry clusters 80 cm away. There was no difference in the duration of time spent by D. al-
loeum on mechanically damaged versus undamaged uninfested blueberries. The data herein
are an initial step toward elucidating the cues mediating microhabitat selection by D. al-
loeum in blueberries.
Key Words: Conservation biological control, alighting behavior, Diachasma alloeum, Rhago-
El comportamiento del ., ..- .1. larval Diachasma alloeum (Muesebeck) (Hymenoptera:
Braconidae) por la busqueda del hospedero para alimentarse en poblaciones naturales fue
observado directamente en plantaciones de mora azul, Vaccinium corymbosum L. Se obser-
varon un mayor numero de D. alloeum posando sobre los racimos de la fruta de la mora azul
infestados con larvas de Rhagoletis mendax Curran de los que fueron observados posando so-
bre los racimos de fruta de mora azul no infestados separados por 80 cm de distancia. Aproxi-
madamente numerous iguales de D. alloeum posaron sobre las moras azules no infestadas
que fueron danadas por la maquinaria agricola versus las no danadas. La mayoria de las
hembras de D. alloeum fueron atraidas a las moras azules infestadas con el hospedero 15 a
21 dias despues que las hembras de R. mendax ovipositaron en la fruta. Las hembras de D.
alloeum pasaron mas tiempo posando sobre racimos de fruta de la mora azul infestados con
R. mendax que en los racimos de la mora azul no infestadas separados por 80 cm de distan-
cia. No habia una diferencia en la duraci6n del tiempo que paso el D. alloeum sobre las moras
azules daAadas por la maquinaria agricola versus las moras azules no daAadas y no infesta-
das. Los datos presentados aqui son un paso inicial hacia el aclaramento de las seniales me-
diadoras para la selecci6n del microhabitat hecho por el D. alloeum en la mora azul.
Hosts of insect parasitoids are often character-
ized by complex and patchy distributions making
successful host location a major challenge for in-
sect natural enemies (II:..I .- I1 i & Gienapp
1999). Exploitation of chemical or visual cues as-
sociated with plants utilized by herbivorous hosts
is known to increase host-searching efficiency of
insect parasitoids (Vet & Dicke 1992; Godfray
1994; Vet et al. 1995). In ..I.i, .!. parasitoids are
often attracted to damaged plants with cases of
heightened attraction to plant damage created
specifically by the herbivore host I T,, .... et al.
1991; McAuslane et al. 1991, Henneman et al.
2002). The chemical cues released by herbivore-
damaged plants and exploited by parasitoids in-
clude systemically released ;.I ...t ...I I' com-
pounds (I ,, I et al. 1993; Rose et al. 1996).
Several braconid species from the subfamily
Opiinae are known to parasitize larval stages of
Tephritidae (Wharton & March 1978).Diachasma
alloeum li ir,, .. ) occurs on hawthorn, Cratae-
gus mollis, and apple, Malus domestic
Borkhausen, in the northeastern U.S.A. and bor-
dering regions of Canada and was thought to spe-
cifically attack the apple maggot fly, '; .
pomonella (Walsh) (Glas & Vet 1983). Recently, D.
",t 1;, 1 i et al: D. alloeum Attracted to Host Infested Blueberries
alloeum has also been reported attacking another
member of the Rhagoletis sibling species complex,
the blueberry maggot fly, Rhagoletis mendax Cur-
ran (Liburd & Finn 2003). Parasitization percent-
ages of R. mendax larvae by D. alloeum collected
from abandoned blueberry plantings in Michigan
were extremely high, ranging from 30-50%. These
rates of parasitization are higher than those
known for R. pomonella, which range from 0.1 to
20.1% (Rivard 1967; Cameron & Morrison 1977;
Only three detailed studies have been pub-
lished on the behavior ofD. alloeum attacking R.
pomonella in hawthorns or apples. Boush & Baer-
wald (1967) reported on the courtship behavior
and suggested the presence of a female-produced
sex pheromone. Prokopy & Webster (1978) and
later Glas & Vet (1983) analyzed the oviposition
behavior of D. alloeum with specific interest in
elucidating the stimuli involved in host-searching
behavior. Visual orientation was found to play an
important role for location of picked hawthorn
fruit in laboratory assays and no difference in at-
tractiveness was found between uninfested and
R. .. ", -., I, I hawthorn fruit (Glas & Vet
1983). However, ovipositor probing activity and
duration of stay were strongly influenced by the
presence and movement of R. pomonella larvae
- .. 1.i, inside hawthorn fruit. The authors con-
cluded that host movement within hawthorns
was the prime stimulus for the location of host-in-
fested fruit by D. alloeum (Glas & Vet 1983).
Recent studies with Diachasmimorpha juglan-
dis i i(.. i. .. i i have shown that females can dis-
tinguish between host-infested and uninfested
walnut fruits before alighting (Henneman 1996,
1998). As they approach fruit, females hover close
to the fruit surface for up to 1 sec before they
alight or fly away, possibly assessing volatiles in
order to decide whether to land (Henneman et al.
2002). Presence of fruit damage, however, rather
than presence of larval infestation by R. juglan-
dis larvae appears to produce the necessary cues
for fruit choice by D. juglandis females (Henne-
man et al. 2002). Furthermore, both olfactory and
visual cues are used by D. juglandis females to
distinguish between infested and uninfested wal-
nuts (Henneman et al. 2002).
To our knowledge, nothing has been published
about the biology of D. alloeum in blueberry
plantings. The current communication describes
observations of the behavioral interactions of
D. alloeum females with uninfested, mechani-
cally damaged, and R. mendax-infested blueber-
ries in an abandoned blueberry plantation. The
specific objectives were to 1) determine whether
blueberries infested with R. mendax larvae are
more attractive to D. alloeum females than unin-
fested fruit, 2) determine whether mechanically
damaged and uninfested blueberries are more at-
tractive to D. alloeum females than undamaged
and uninfested fruit, 3) document duration of vis-
its and associated behaviors of D. alloeum on R.
mendax-infested and uninfested blueberries in
MATERIALS AND METHODS
Observational studies were conducted in the
summer of 2001 in an abandoned plantation of
highbush blueberry, Vaccinium corymbosum L. in
Fennville, MI. The abandoned plantation was
highly infested by R. mendax with approximately
45% of picked berries containing developing lar-
vae in 1999 and 2000. In addition, this plantation
was known to harbor a substantial population of
D. alloeum. Parasitization rates ofR. mendax col-
lected from this plantation were above 50% in
1999 and 2000.
S .. i mendax were reared from larvae
collected from fruit of unsprayed blueberries (var.
Jersey) from the plantation described above and
from an organically managed plantation 3.2 km
away. Flies were reared according to the protocol
outlined in Liburd et al. (2003). Prior to testing,
flies were maintained in aluminum screen-Plexi-
glas cages (30 x 30 x 30 cm) (BioQuip, Gardenia,
CA) and supplied with water and food (enzymatic
yeast hydrolysate and sucrose) (ICN Biomedicals,
Inc., Costa Mesa, CA). Adults were kept at 24C,
55-60% RH, under a 16:8 (L:D) photocycle.
Three weeks after removal of R. mendax pu-
paria from 4C (diapause), D. alloeum began
emerging from more than 50 and 2% of puparia
collected from the abandoned and ... .. ".
managed sites, respectively. The parasitoids were
identified by R. A. Wharton (Texas A&M Univer-
sity) and voucher specimens were deposited at
Michigan State University (A. J. Cook Arthropod
Forty pairs of blueberry fruit clusters were se-
lected for observation on 12 June before R.
mendax emergence. Each pair of clusters was ap-
proximately 80 cm apart and each individual
cluster contained 20-35 blueberries. All clusters
were approximately 15-cm from the uppermost
bush; this location within the blueberry bush can-
opy has been found to be the most effective posi-
tion for trapping blueberry maggot (Liburd et al.
2000). At this stage of the season, blueberry fruit
was still green and unripe. Experimental bushes
were l :,. .- and selected clusters were individu-
ally enveloped with 1 L translucent plastic bags
that had been punctured with a pin multiple
Florida F,' .-.'..7., .: 87(2)
times. Bags were positioned around blueberry
fruit clusters such that berries did not directly
contact the bag surface. The purpose of this bag-
ging was to prevent native R. mendax from ovi-
positing into the selected berry clusters. On 19
June, we captured the first R. mendax on moni-
toring traps in the abandoned plantation. Twenty
of the 40 bagged berry clusters were monitored
from 25 June until 15 July to determine whether
this bagging method interfered with normal berry
development and to determine whether this tech-
nique -*..,.:: -- :.. i i prevented R. mendax from ovi-
positing into berries. On each day, a single bagged
cluster was randomly chosen for inspection. All
fruit within that cluster were dissected and in-
spected for R. mendax larvae. In addition, on each
day, two randomly selected clusters (15-20 ber-
ries) that had not been previously enveloped with
a plastic bag were dissected for R. mendax larvae.
No R. mendax larvae were found in berries that
were enveloped by our plastic bags. In addition,
berry size and color did not differ between bagged
and unbagged berries. Among the unbagged clus-
ters that were dissected, R. mendax infestation
was first detected on 14 July.
The remaining 20 pairs of bagged clusters
were used for the observational study. On 16 July,
10 of the 20 pairs of bagged blueberry clusters
were randomly chosen for R. mendax infestation.
Ten laboratory-reared and mated R. mendax fe-
males (10-15 days old) were introduced into one of
the bagged blueberry clusters from each pair at
1200 hours. IntroducedR. mendax were left in the
bags for 24 h and then removed. Four of the 10
bags containing introduced R. mendax were ob-
served for 1 h to confirm that flies were oviposit-
ing into berries.
The other 10 pairs of bagged blueberry clusters
were chosen for mechanical damage. The blueber-
ries on one cluster of each bagged pair were me-
chanically damaged by making three .-, ,.
spaced punctures in the skin of the berries with a
0-size insect pin. These manipulations resulted in
10 replicates of two paired treatments: 1) unin-
fested and undamaged berries versus R. mendax-
infested berries, and 2) uninfested and undam-
aged berries versus uninfested and mechanically
damaged berries. All other blueberries within a
1.5 m radius of each experimental pair were re-
moved from bushes. The paired treatment clus-
ters were 80 cm apart in a two-by-two design with
the two treatments placed in alternate positions;
each pair of treatment clusters was separated by
at least 4 m.
Direct visual observations began 24 h after ini-
tial treatment manipulations were made and con-
tinued thereafter on every second day.
Observations were conducted between 1230 and
1530 h. Two or more observers rotated among the
ten replicates of each treatment pair conducting
approximately 20-min observational bouts per lo-
cation. Observations were terminated 31 days af-
ter the treatment manipulations were conducted.
During each period of observation, the plastic
bags enveloping blueberry fruit clusters were re-
moved and replaced immediately after observa-
tions were terminated. Also, native R. mendax
were prevented from alighting on experimental
clusters during observations. Observed events
were spoken into a hand-held microcassette audio
recorder by an investigator sitting or standing
0.75 m from the paired treatment clusters. Data
recorded were: 1) landing by D. alloeum on berry
clusters, 2) duration of visits on berry clusters, 3)
oviposition into berries by D. alloeum. We at-
tempted to collect observedD. alloeum with an as-
pirator after they oviposited and before they left
experimental berry clusters. We estimate to have
captured 70% of all visitors. The captured D. al-
loeum were taken to the laboratory and their
identity was confirmed.
Results of all dual-choice tests were analyzed
by paired t tests (SAS Institute 2000). In all cases,
significance level was P < 0.05. All values are
Significantly more D. alloeum alighted per day
on blueberry clusters that were infested with R.
mendax larvae than on blueberry clusters that
were uninfested (2.6 + 0.5 and 0.3 + 0.09, respec-
tively). There was no significant difference be-
tween the number ofD. alloeum alighting per day
on blueberry clusters containing mechanically
damaged and uninfested fruit compared with the
number alighting on clusters containing undanm-
aged and uninfested fruit (0.5 0.8 and 0.5 0.9,
respectively). Blueberries that were infested with
R. mendax larvae attracted the majority (64%) of
D. alloeum females between 15 and 21 days after
R. mendax females had oviposited into fruit (Fig.
1). There was no noticeable difference in attrac-
tiveness of mechanically damaged and undam-
aged fruit over time.
Female D. alloeum spent significantly more
time alighting on R. mendax-infested blueberry
clusters than on uninfested blueberry clusters
(10.0 t 1.1 min and 2.3 1.2 min, respectively).
There was no significant difference in the dura-
tion of time spent by D. alloeum on mechanically
damaged and uninfested blueberries compared
with undamaged and uninfested blueberries (1.1
0.1 min and 0.9 + 0.2 min, respectively). Of the
41 D. alloeum observed alighting on R. mendax-
infested blueberry clusters, 34 were observed
making a single ovipositional probe into blueber-
ries. All of the D. alloeum that were observed ovi-
positing into berries performed :, I... "
-r. 1;, 1 i et al: D. alloeum Attracted to Host Infested Blueberries
R. mendax-infested versus uninfested berries
S n i i II .
1 3 5 7 9 11 13 15 17
19 21 23 25 27 29 31
Day after blueberry manipulation
Fig. 1. Numbers of D. alloeumn observed alighting on R. ntendax-infested and uninfested blueberries spaced 80
cm apart every other day after R. mendax oviposition.
behavior directly thereafter as previously de-
scribed by Glas & Vet (1983). Specifically, after
ovipositing, these females walked on the blue-
berry dragging and dabbing their ovipositors on
the fruit surface and excreting a clear fluid. None
of the D. alloeum observed alighting on unin-
fested fruit attempted to oviposit.
More host-infested blueberry fruit were visited
by female D. alloeum than uninfested fruit sug-
gesting that females have the capability of distin-
guishing R. mendax-infested berries prior to
alighting. D. juglandis have also been shown to
distinguish host-infested from uninfested fruits
prior to alighting (Henneman 1996, 1998), relying
on both visual and olfactory cues to make their
decision (Henneman et al. 2002).D. juglandis dis-
tinguish host-infested fruit in the early stages of
infestation (3-4 d after fly oviposition) as eggs are
beginning to hatch (Henneman et al. 2002). In
contrast to our results, previous laboratory stud-
ies comparing the attractiveness ofR. pomonella-
infested hawthorn fruit with uninfested fruit,
showed that D. alloeum did not exhibit a prefer-
ence and landed equally on both types of fruit
(Glas & Vet 1',- :. However, the hawthorn fruit
used in that study were field collected and in-
fested by R. pomonella under laboratory condi-
tions following a period of cold storage (Glas & Vet
1983). Thus, it is possible that the volatile ....i .'
released by such picked and stored fruits may
have differed from those of unpicked and R.
pomonella-infested hawthorn fruit. It will be in-
formative to determine whether D. alloeum dis-
tinguishes between R. pomonella-infested and
uninfested hawthorn fruit under field conditions
using unpicked fruit as was done in this study.
The behavior ofD. alloeum documented in the
current study varied in some respects from that
previously reported in hawthorns. The majority of
D. alloeum visits and ovipositions into R. mendax-
infested blueberries occurred 15-21 days after fe-
male R. mendax had oviposited into the fruit. At
this stage, the majority ofR. mendax were likely in
the second instar (Lathrop & Nickels 1932; Neun-
zig & Sorensen 1976). After the t -.. ..t -:., -: day,
Florida F,' .-.-...: .: 87(2)
there was a dramatic reduction in the number ofD.
alloeum approaching and alighting on R. mendax-
infested blueberries (Fig. 1). At this point, the ma-
jority of R. mendax larvae should have reached the
third instar and were likely beginning to exit dry-
ing fruit to pupariate in the soil (Lathrop & Nick-
els 1932). In hawthorns, D. alloeum is known to
attack the third (final) instar ofR. pomonella (Glas
& Vet 1983). In addition, D. alloeum spent less to-
tal time on blueberries during oviposition conm-
pared with hawthorns. On average, D. alloeum
spent approximately 10 min on blueberries after
alighting, while they spent anywhere from 18 to
140 min on hawthorn fruit during probing and ovi-
: ... :: .... bouts (Glas & Vet 1983). Furthermore, D.
alloeum were observed making only one oviposi-
tional probe per blueberry, while 1 to 5 oviposi-
tional probes have been observed per individual R.
pomonella-infested hawthorn fruit (Glas & Vet
1983). These differences in behavior ofD. alloeum
in blueberries versus hawthorns are :.- i-- I:.1- due
to the differences in size and skin rigidity between
blueberries and hawthorns. Given the smaller size
and comparatively less rigid fruit skin of blueber-
ries, it may be easier forD. alloeum to find and ovi-
posit into a younger R. mendax larva in less time
in blueberries than a comparably sized R.
pomonella larva in hawthorns.
In the current study, more D. alloeum females
landed on R. mendax-infested blueberries com-
pared with uninfested berries, but not on me-
chanically damaged blueberries compared with
the undamaged ones. This activity peaked 15-21 d
after R. mendax had oviposited into blueberries.
In contrast, D. juglandis females chose walnuts
based on the presence of fruit damage rather than
the presence of R. juglandis larvae inside the
fruit (Henneman et al. 2002). However, in that
study, .... ... ;. ."11 damaged walnuts took on a
distinctly different appearance (darkened) com-
pared with undamaged walnuts, which was
shown to influence fruit selection by D. juglandis.
Color of host-infested walnuts is known to be an
important visual cue mediating searching behav-
ior of D. juglandis (Henneman 1-'-'. In the cur-
rent study, mechanically damaged blueberries did
not appear different from undamaged berries.
Furthermore, R. mendax-infested blueberries re-
mained morphologically indistinguishable from
uninfested berries for more than 20 days after R.
mendax oviposition. It has been documented that
certain female parasitic wasps exhibit an innate
attraction to plant-released volatiles (Geervliet et
al. 1996). Also, parasitic wasps are known to ex-
hibit attraction to the host marking pheromone of
tephritid fruit flies (Hoffmeister & Gienapp
1999). Based on the current results, we postulate
that plant volatile compounds released by R.
mendax-infested blueberries, but not mechani-
cally-damaged ..... provide an olfactory cue that
attracts female D. alloeum. However, it is also
possible that acoustic signals given. .: I chewing
and tunneling R. mendax larvae within infested
blueberries provide D. alloeum with an oviposi-
Although labor intensive, our approach of con-
ducting direct visual observations of D. alloeum
responding to R. mendax-infested blueberries un-
der authentic field conditions was indeed possi-
ble. Moreover, the data produced are an initial
step toward elucidating the cues mediating rni-
crohabitat selection by D. alloeum in blueberries.
The next step will be to determine whether R.
mendax-infested blueberries release volatile pro-
files that differ quantitatively or qualitatively
from those released by uninfested fruit. F,;,; 11I
we hope to identify the relevant volatiles that
may be involved in mediating attraction ofD. al-
loeum to R. mendax-infested blueberries as has
been done for other parasitoids 1 I. i I. .- et al.
1991). Identification of plant volatiles attractive
to D. alloeum may allow for recruitment of these
beneficial insects in blueberry plantations,
thereby improving biologically based manage-
ment tactics for R. mendax.
We thank the owners of the blueberry plantings used
in this study, who wished to remain anonymous. We
thank Dan Young and Jessie Davis for assistance in col-
lecting R. mendax-infested blueberries and with con-
ducting field observations. We also thank Gary Parsons
(Assistant curator, A.J. Cook Arthropod Research Col-
lection, MSU) for his assistance in preparation of D. al-
loeum specimens before species identification and
deposition of vouchers.
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