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Augmentative releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to suppress a mediterranean fruit fly (Diptera: Tephritidae) population in Kula, Maui, Hawaii
BIOLOGICAL
CONTROL
1,
2-7
(1991)
Augmentative Releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to Suppress a Mediterranean Fruit Fly (Diptera: Tephritidae) Population in Kula, Maui, Hawaii TIM T. Y. WONG, Tropical
Fruit
and
Vegetable
M. M. RAMADAN, Research
Laboratory, Received
D. 0. MCINNIS, Agricultural May
N. MOCHIZUKI,
Research 21,199O;
accepted
The Mediterranean fruit fly, Ceratitis cupituta (Wiedemann), and the oriental fruit fly, Dacus dorsalis Hendel, are serious pests of fruits and vegetables in Hawaii. C. capitata was introduced into Hawaii from Australia in 1910 (Back and Pemberton, 1918) and D. dorsalis was introduced from the Pacific Islands about 1945 (Van Zwaluwenberg, 1947; Bess and Haramoto, 1961). Both species became widespread immediately after their establishment. However, within 5 years of the arrival of D. dorsalis, the distribution patterns of C. capitata changed. Associated with competition with D. dorsalis and a high rate of parasitism, C. cupituta became scarce at low elevation but remained abundant in upland areas (Bess, 1953). At present, C. capitata is isolated in
$3.00
0 1991 by Academic Press, Inc. of reproduction in any form reserved.
October
Department
of Agriculture,
Honolulu,
Hawaii
96804
2,199O
MATERIALS
AND
METHODS
Larvae of C. capitata were reared by the methods of Tanaka et al. (1969) and were used as host larvae for rearing D. tryoni. Our laboratory colony of D. tryoni was established in 1981 with adults emerged from parasitized C. capitata pupae from infested peaches that had been collected in Kula, Maui. Adult D. tryoni cohorts were kept in screened cages (26 cm3) at a capacity of 400 2
1049.9644/91
U.S.
AND J. C. HERR
patches throughout the major Hawaiian Islands, with its largest populations found in Kula, Maui, and Kona, Hawaii (Haramoto and Bess, 1970, Nishida et al., 1985). Wong et al. (1984) and Wong and Ramadan (1987) found that nearly all peach fruits in Kula were infested with fruit flies; approximately 50% of adult insects that emerged were C. capitata, 25% were D. dorsalis, and the remaining 25% were parasitoids of both fruit fly species. Biosteres arisanus Fullaway, an egg-larval parasitoid, was the dominant species and accounted for 374% and the two larval parasitoids, Diachasmimorpha longicaudata (= Biosteres longicaudatus) (Ashmead) and Diachasmimorpha tryoni (= Biosteres tryoni) (Cameron), accounted for 15 and lo%, respectively, of the parasitoids recovered (Wong and Ramadan, 1987). The rationale for augmentative releases of parasitoids has been considered and discussed by Knipling (1979). However, the utility of this method of insect suppression in the field has not been fully demonstrated with fruit flies. The present paper reports on the suppression of a C. capitata population by augmentative releases of D. tryoni in the Kula area from March to June 1988. D. tryoni is selected over other braconids because it is amenable to mass rearing in the laboratory. Also, in Hawaii, D. tryoni is relatively host specific. It successfully develops in C. capitata larvae and in the larvae of two stem gall-forming tephritids, the lantana gall fly, Eutreta xanthochaeta Aldrich, and Procecidochares utilis Stone, but it is unable to develop on D. dorsalis (Haramoto and Bess, 1970).
Diachasmimorpha tryoni (Cameron), a larval parasitoid, was mass-reared in the laboratory and was used to suppress a wild Mediterranean fruit fly, Ceratitis capitata (Wiedemann), population in a nonisolated area (13 km’) of Kula, Maui, Hawaii. Weekly releases of D. tryoni, averaging 272,000 parasitoids per release, were made from March 10 to June 22, 1988. Trap catches of male C. capitata adults began to decline 8 weeks after the first release, and catches remained low throughout the summer months. However, in the control area of Keokea, adult catches began to increase in April and reached a peak in early July that was similar to that of previous years. The percentage of parasitism of C. capitata by D. tryoni was significantly higher for the six weekly collections of infested peaches in Kula than in the control area of Keokea: an average of 47.0% parasitism in Kula compared with 14.2% in Keokea. Of the total parasitoids, a significantly higher percentage of D. tryoni was recovered in fruit samples from Kula than in those from Keokea. Moreover, the number of C. capitata per fruit was significantly lower in the treated area than in the control area. 0 1991 Academic Press, Inc. KEY WORDS: Insecta; Ceratitis capitata; Diachasmimorpha tryoni; parasitoid releases.
Copyright All rights
Service,
J. I. NISHIMOTO,
SUPPRESSION
OF
C. cupitata
males and 400 females per cage. Honey, streaked on the top screen, was the source of food and water for adult wasps. The oviposition unit was a modified petri dish (9 cm in diameter and ~0.5 cm deep). Tight-fitting lids with organdy covers were used to hold C. capitata larvae inside the dishes. Third-instar hosts (about 800) mixed in artificial rearing media were packed into each oviposition unit and were exposed to parasitoids for 3 to 4 h. Parasitoid females readily oviposited through the organdy into the larvae. To allow introduction and removal of oviposition units from the outside without causing injury or loss of parasitoids, a screened opening to accommodate oviposition units was made in the bottom of the cage. After exposure to parasitoids, host larvae were removed from the oviposition units and consolidated along with additional rearing media in plastic trays (30 X 48 X 2.5 cm) which were then kept in wooden holding cabinets (91 X 183 X 61 cm). When mature, host larvae vacated the larval diet; they popped out and fell into plastic containers (30 X 48 X 14 cm) of vermiculite for pupation. Seven days later, puparia were sifted from vermiculite and held on screened trays (53 X 67 X 2 cm) in screened emergence cabinets (76 X 155 X 63 cm). Flies emerged from unparasitized pupae about 10 to 13 days after pupation and died within 2 days of adult life because no food was provided; the remainder of the puparia contained immature parasitoids. These parasitized puparia were collected and distributed in small paper bags to be placed in cohort cages to maintain the colony or were placed in plastic containers hanging from branches of fruit trees for field release. Male D. tryoni emerged 16 to 18 days after oviposition and females followed 2 days later at 26 + 1°C and 60 f 10% RH. Biological data and mass-rearing procedures for D. tryoni have been reported by Ramadan et al. (1989a,b) and Wong et al. (1990). The study area [1.8 X 7.3 km (13 km2)] on the slopes of Mount Haleakala (summit elevation, 3056 m) in Kula, Maui, with elevations ranging from 700 to 1200 m, was selected because prior study had shown it to be an area where fruits were heavily infested with C. capitata (Wong et al., 1983). Although the Kula area is not isolated, it is bordered on all sides by moderately dry rangeland that is currently used for livestock grazing. Fruit trees occurred along roadsides, in yards of residences, and in gulches. The Keokea area of 2.6 km2 (about 1.1 km south of Kula) was used as a control site because fruit-fly host trees, climatic conditions, and elevation were similar to those in the Kula area. Keokea served as a control for a test using sterile fly releases to suppress a C. capitata population in Kula in 1981-1982. Infestation patterns and parasitoids of C. capitata from loquat and peach fruits as well as adult fly trap catch data from Keokea were similar to those from the Kula area (Wong et al., 1986). White plastic containers (3.8 liters, 14 cm deep X 20 cm diameter) were
WITH
D. tryoni
3
placed in nearly all of the 480 peach trees located in Kula (Wong et al., 1983). Paper bags holding parasitized pupae were slit across the top and placed into the containers at weekly intervals when fruits were in season. Male parasitoids usually began emerging on the day of release and females about 2 days later. Emerging parasitoids escaped by flying out of eight l-cm-diameter holes near the tops of the containers. Seasonal distribution and abundance of adult male C. capitata were determined with 250 plastic traps baited with trimedlure in the Kula area from 1978 to 1981 (Wong et al., 1985). In the present study, we reduced the number to 100 traps, or approximately every other trap site of the original distribution, and placed 25 traps in the Keokea area to detect and monitor the adult population. Trapped flies (>99% males) were removed weekly by the methods of Nakagawa et al. (1971). The trap catches of 1988 in Kula were used to compare with those of a high catch year of 1978 and a moderate catch year of 1979, as well as with those in Keokea during 1982,1983, and 1988. Traps were in place for only these years. No yearly collection data were omitted from analysis. Weekly from June to early July 1988, we collected windfallen peaches on the ground. These fruit samples were brought back to the laboratory, counted, weighed, and placed in screen-sided fiberglass containers (30 X 50 X 15 cm), at 26 k 2°C and 60 t 10% RH. Four to five days later, each fruit was examined, discarded if not infested, or held for 2 or more weeks if infested. Mature tephritid larvae were collected, counted, and placed in plastic cups containing moistened fine white sand and were covered with screened lids (144 mesh/cm2). About 6-8 days after pupation, all puparia were examined under a stereomicroscope, and C. capitata and D. dorsalis were separated using differences in the anterior puparial characters as described by Yamada et al. (1962). Puparia of each tephritid species were then held in separate plastic cups with screened lids for emergence. Numbers of adults were recorded, and parasitoids were identified to species using published keys (Beardsley, 1961; Wharton and Gilstrap, 1983). The total percentage parasitism was determined by dividing the total number of parasitoids by the total of C. capitata and parasitoids eclosed. In Kula, eight sites (15 X 15 m per site) with lantana bushes, Lantana camara L., were selected for monitoring the potential impact of the parasitoid releases on the lantana gall fly, Eutreta xanthochaeta Aldrich, at monthly intervals from January to November 1988. In Keokea, four sites were selected. At each site, galls on freshly grown shoots were counted; then about 3 to 5% of the galls were cut from shoots randomly and were brought back to the laboratory, weighed, and held individually in plastic cups with screen lids. All insects that emerged from the galls were recorded. Plans to monitor the population of the other nontarget species P. utilis
4
WONG
TABLE
ET
1
sitism and percentage D. tryoni of total parasitoids in Kula and Keokea were compared with a-paired t test. data were transformed using the arscine procedure before analysis (Snedecor and Cochran, 1967).
Number of Diachasmimorpha tryoni Released and Number of Release Sites on Peach Trees in Kula, Maui, Hawaii, in 1LY”” OPP
Month
NO. weekly releases
March April May June
4 4 4 3
No. parasitoids Total
released
Average/week
l&X2,350 1,194,120 1,313,361 510,648
265,587 298,530 328,340 170,216
NO. release sites
Average No. parasitoids/ site/week
144 191 169 67
1844 1563 1943 2540
RESULTS
,
,
,
,
/
l
I
I
IIIIIIIIIIl
,
,
,
,
,
,
,
AND
DISCUSSION
From March 9 to June 22, 1988, 4.1 million laboratory-reared D. tryoni, an average of 272,000 parasitoids per week, with a range of 170,000 to 328,000 parasitoids per week, were released into the Kula area of Maui to suppress larvae of C. capitata infesting peach fruits (Table 1). The number of release sites varied from week to week because of fruit development and maturation rates at different altitudes. However, in most instances, parasitoids were released wherever fruits were present on each peach tree or adjacent tree. During the peak of peach production in April and May, the average number of parasitoids released per site per week ranged from 1563 to 1943. Emerging D. tryoni males were observed to hover near the containers and mated with females as the latter emerged. Copulation occurred for about 10 to
had been made, but this was not done because few or none of its host plant, Ageratina adenophoria (Spreng), were found in Kula or Keokea. The x2 procedure was used to compare differences in the proportion of each parasitoid species for each fruit collection date and the total fruits collected from Kula and Keokea. Student’s t test was used to compare differences in C. capitata adults obtained from windfallen peaches from both Kula and Keokea. Percentage para-
6,
AL.
,
,
,
,
,
,
,
,
,
/
,
,
,
,
4-
2G n l!z”. a
12
IIIIIIIIIIII
% E
KULA IO-
\ \ 2
2 9
w”
8-
nI -
‘a
\
/
a----m -
1978
o-----o
1988
1979
\
:
I
6-
4-
2-
o-
1/1,,,1(1,,,,,,,,,,,/,,,(1 5 19 2 16 JAN FEE
FIG. 1. Comparison period between arrows
of male represents
C.
I
I5 MAR
29
12
26 APR
capituta trap catches parasitoid
release
IO
24 MAY
7
21 JUN
in Kula (1978-1979 during 1988.
5
I9
2
JUL and
1988)
I6 30 AUG and Keokea
13 27 SEP
II 25 OCT
(1982-1983
8
22 NOV
and 1988),
6 20 DEC Maui,
Hawaii.
The
SUPPRESSION
OF
‘2. cupitutu
20 s and then females flew off to nearby fruit trees. Females were found on the surface of leaves and fruits. Greany et al. (1977) reported that D. longicaudata was attracted to fermentation products emanating from rotting fruit, a probable site for the location of host larvae. In our study, rotting fruit was attractive, irrespective of the presence of host larvae, and attraction was attributed to microbial fermentation products rather than to kairomones from host larvae. On many occasions in the field, we observed D. longicaudata and D. tryoni sitting, probing, and ovipositing into fruits on the ground. Figure 1 shows the seasonal trends of wild male C. capitata caught by traps placed in Kula for 1978, 1979, and 1988 and in Keokea for 1982, 1983, and 1988. In Keokea, trap catches for all 3 years began to increase in April and the peaks reached in July 1988 were higher than those reached in the other 2 years. In Kula, the catch patterns for 1978 and 1979 were similar to those in Keokea, but in 1988 the population reached a peak in late April and then began to decline rapidly before increasing again to a smaller peak in early July. Wong et al. (1985) reported that the increase in population each year in April was the result of infested loquat fruits appearing in the winter months and that the peak population in the summer months was from infested peaches in the spring. They also found that adult catches were
Date
Numbers
Location
No. pupae”
of C. cupitutu in Kula No. C. capitatu and parasitoids
Pupae and and Keokea
1
Kula Control
1,191 1,030
1,129 970
621 131
June
8
Kula Control
4,646 1,089
4,511 947
2093 152
June
14
Kula Control
2,206 1,119
2,106 1,021
835 180
June
21
Kula
2,428
2,271
1384
June
28
Control Kula Control
2,805 1,402 1,712
2,483 1,314 1,617
191 425 266
July
6
Kula Control
819 578
774 527
326 154
12,105 7,565
5684 1074
Kula Control
18,399 11,305
tryoni
5
2
Their Parasitoids (Control), Maui,
Collected Hawaii, No.
Total parasitoids
June
Total
D.
significantly correlated with the number of infested fruits. In this study, we found that a similar peak in trap catches occurred 8-12 weeks after the peak in fruit infestations. This lag time provided an indication of the minimum total time required for C. capitata to complete development in fruit, to pupate, and finally to be trapped as adults. In 1988, fruit production and tephritid infestation were similar or perhaps higher than those in previous years. Therefore, we conclude that the reduction in trap catches in May and June of 1988 in Kula was the result of the augmentative releases of D. tryoni because trap catches began to decrease about 8 weeks after the beginning of the releases on March 9. The decline in trap catches in May and June indicated that the ratio of parasitoid females to C. capitata females was sufficient to cause and decline in population. In April, when the C. capitata population began to increase, the ratio of parasitoid females to C. capitata females decreased, with the lowest ratio in the week of April 26. This resulted in a peak in C. capitata numbers about 10 weeks later on July 5. Table 2 presents numbers of C. capitata and parasitoids collected from windfallen peaches on six dates in 1988 at Kula and Keokea. The percentages of parasitization based upon eclosion of adults ranged from 32.3 to 60.9% for Kula and from 7.7 to 29.2% for Keokea.
TABLE Total
WITH
B. arisanus
(4.8:;* 63 169 (174.06)*** 196 131 (29.96)*** 2,537 733 (201.72)***
Peaches
D. tryoni
Other@
1
260
35
(O.Pl)‘NS 51
(36.7;;** 1,172
(3.9$ 44
t9.2:** 16
(104.4:*** 467
(O.Ol;NS 9
(43.6:)*** 13 (35.5;***
(91.0!$.. 583 (1.69;kJS
(16.1:*** 4 (SOi&**
11
341
10
(d&**
(199.8& 109 (27.1&
(O.Ol;NS 1 (l.66)2Ns
2,932 232 (326.12)***
103
20 (2.76pNS 112 ,73.,7,f***
***,
Windfallen
parasitoids
D. longicaudata
325 111 (46.61)***” 826 113 (71.63)*** 343 1117 (34.20)*** 784
a Number of pupae obtained from sampling windfallen peaches. b Psyttalia incisi, Tetrastichus giffardianus, and unemerged parasitoids. ’ Homogeneity x2 values in parentheses; df = 1. * P < 0.05; **, P < 0.01;
from
in 1988
P < 0.001;
NS,
not
significant;
(,3.1;***
x2.
% Parasitization 55.0 13.5 46.4 16.0 39.6 17.6 60.9 7.7 32.3 16.4 42.1 29.2 47.0 14.2
6
WONG
TABLE Comparison Populations: 1988
versus
Keokea
% Parasitism species Actual (x)
Location Control Kula Paired
t test
’ Data
3
of Mean Parasitization Kula
transformed
by arcsine
Maui,
Hawaii,
in
% D. tryoni of total
by all
parasitoid Actual (x)
2 2.20
20.37
recovered Transformed” (x xk SEM) 26.38
rt 2.71
46.10
+ 4.08
(n = 6) k 2.48
51.60
(n = 6) (t = 4.78; df P < 0.01)
5;
AL.
the present study, the level of measured parasitism was 47% but the true rate of parasitism was considerably higher. The reason for this was because the measured rate was limited to the parasitism that had occurred up to the time at which the fruit was collected, whereas the true rate of parasitism included that which continued up to the time all the fruit fly larvae had matured in the fruit. Tephritid eggs and young larvae artificially escaped parasitism due to removal of infested fruit from the field. Monthly collections of stem galls from lantana bushes showed only the lantana gall fly, E. xanthochaeta, and its parasitoids emerged from puparia (Table 4). D. tryoni was the most prominent parasitoid species reared. Eurytoma tephritidis Fullaway occurred at much lower frequencies. Parasitism was uniformly low throughout the collection, 10.9% in Kula and 12.1% in Keokea. High pupal mortality, caused in part by sampling of different age galls and handling, was recorded in all collections (Table 4). The augmentative releases of D. tryoni had no effect on the rate of parasitism of E. ranthochaeta, partly because lantana bushes were at least 25 m away from the nearest fruit trees. Factors such as habitat differences (pastureland versus fruit trees) and limited dispersal of D. tryoni in the presence of fruiting trees (T. T. Y. Wong, unpublished data) probably prevented higher rates of parasitism of D. tryoni on E. xanthochaeta in Kula. The sterile-insect release technique was used to suppress a Mediterranean fruit fly population in Kula. From December 1981 to June 1982, an average of 4 million irradiated flies were released by air and ground each week. A significant reduction of the C. capitata population, which was similar to that in the 1988 parasitoid releases, occurred in the Kula area compared with the
Rates of C. cupitatu
(Control),
Transformed” (x + SEM)
16.76 23.79 (n = 6) 42.71 46.08 (n = 6) (t = 4.48;df= P < 0.01)
ET
= 5;
proportion.
The x2 analysis of each parasitoid species showed significantly more parasitoids in Kula than in Keokea. Also, significantly (Student’s t test; t = 2.484, df = 5, P < 0.05) fewer C. capitata adults per fruit were obtained in the six samples of windfallen peaches in Kula than in Keokea. Moreover, a comparison of C. capitata populations showed a significantly higher rate of parasitism in Kula than in Keokea and this was attributed at least in part to significantly higher numbers of D. tryoni in Kula (Table 3). The predominance of D. tryoni over B. arisanus is a reversal of earlier studies. Haramoto and Bess (1970) reported that since 1951, B. arisanus had become the dominant parasitoid, replacing D. tryoni, and accounted for >90% of the total parasitization against C. capitata in coffee in Kona, Hawaii. Wong et al. (1984) and Wong and Ramadan (1987) reported that B. arisanus accounted for ~74% of the total parasitization in Kula. In
TABLE
4
Number of Stem Galls Collected from Young Stems of Lantana Bushes and Emergence of Diuchusmimorpha tryoni, Euryand Adult Lantana Flies from Eutretu xunthochueta Puparia in Kula (Eight Sites) and Keokea (Four Sites), Maui, Hawaii, in 1988
toma tephritidis,
Date January-March April-June July-September October-November Total
’ Percentage
parasitism
Location
No. galls counted
Kula Keokea Kula Keokea Kula Keokea Kula Keokea Kula Keokea
23,124 6,753 21,063 19,521 21,343 12,773 14,547 8,733 80,077 47,780
= No.
emerged
parasitoids/total
No. galls collected 632 262 748 519 772 414 731 437
No. flies emerged 58 25 61 57 83 72 44 35 246 189
1632 emerged
parasitoids
% galls from which insects emerged 11.4 9.5 8.8 12.3 11.9 20.5 6.3 9.4 9.6 13.2 + hosts
No.
D. tryoni 14
0 5 6 5 10 2 6 26 22 X 100.
parasitoids
emerged”
E. tephritidis 0 0 0 1 4 3
0 0 4 4
Total % parasitism 19.4 0 7.6 10.9 9.8 15.3 4.3 14.6 10.9 12.1
SUPPRESSION
OF
C. copitata
control area of Keokea (Wong et al., 1986). Plans to releases integrate the sterile insect and parasitoid in Kula in the near against the C. capitata population _ _ __ future have been developed; the two methods will likely be more effective and more ecologically acceptable than the use of insecticides (Knipling, 1979). The combination of these techniques will be useful in future eradication or suppression plans throughout the Hawaiian Islands and other fruit fly-infested areas, including the U.S. mainland. ACKNOWLEDGMENTS We thank J. E. Gilmore for administrative and technical assistance and E. F. Knipling for technical advice. We are grateful to Harris Chang, Kevin Gavagan, Dan Kawamoto, Dale Kanehisa, Mahmoud Kazan, Allen Marzan, Michael McKenney, and Keith Shigetani for providing fly larvae and parasitoids during this study.
REFERENCES Back, E. A., and Pemberton, C. E. 1918. The Mediterranean in Hawaii. U.S. Dep. Agric. Bull. 536. Beardsley, J. W. 1961. A review of the Hawaii Braconidae tera). Proc. Hawaii. Entomol. Sot. 17, 333-366.
fruit
fly
(Hymenop-
Bess, H. A. 1953. Status of Ceratitis capitata in Hawaii following the introduction of Dacus dorsalis and its parasites. Proc. Hawaii. Entomol. Sot. 15, 221-234. Bess, H. A., and Haramoto, F. 1961. Contributions to the biology and ecology of the oriental fruit fly,. Dacus dorsalis Hendel (Diptera: Tephritidae), in Hawaii. Hawaii Agric. Exp. Stn. Tech. Bull. 44. Greany, P. D., Tumlinson, J. H., Chambers, D. L., and Boush, G. M. 1977. Chemically mediated host finding by Biosteres (Opius) longicaudatus, a parasitoid of tephritid fruit fly larvae. J. Chem. Ecol. 2, 189-195. Haramoto, F. H., and Bess, H. A. 1970. dance of the oriental and Mediterranean their parasites. Proc. Hawaii. Entomol.
Recent studies on the abunfruit flies and the status of Sot. 20, 551-566.
Knipling, E. F. 1979. “The Basic Principles of Insect Population Suppression and Management.” U.S. Dept. Agric. Handbook 512. Nakagawa, S., Chambers, D. L., Urago, T., and Cunningham, R. T. 1971. Trap-lure combinations for surveys of Mediterranean fruit flies in Hawaii. J. Econ. Entomol. 64, 1211-1213. Nishida, T., Distributional
Harris, E. J., Vargas, loci and host fruit
R. I., and utilization
Wong, patterns
T. T. Y. 1985. of the Medi-
WITH
terranean Hawaii.
D.
7
tryoni
fruit Environ.
fiy, Ceratitis capitatu Entomol. 14, 602-606.
(Diptera:
Tephritidae),
in
Ramadan, M. M., Wong, T. T. Y., and Beardsley, J. W. 1989a. Survivorship, potential, and realized fecundity of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitata (Diptera: Tephritidae). Entomophaga 34, 291-297. Ramadan, M. M., Wong, T. T. Y., and Beardsley, J. W. 1989b. Insectary production of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capita& (Diptera: Tephritidae). Proc. Hawaii. Entomol. Sot. 29, in press. Snedecor, G. W., and Cochran, W. G. 1967. “Statistical Methods.” Iowa State Univ. Press, Ames. Tanaka, N., Steiner, L. F., Ohinata, K., and Okamoto, R. 1969. Lowcost larval rearing medium for mass production of oriental and Mediterranean fruit flies. J. Econ. Entomol. 62, 967-968. Van Zwaluwenburg, Entomol. Sot.
13,
R. H. 1947. 8.
Notes
and exhibitions.
Proc.
Hawaii.
Wharton, R. A., and Gilstrap, F. E. 1983. Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Cerutitis and Dacus s.1. (Diptera: Tephritidae). Ann. Entomol. Sot. Amer. 76, 721-742. Wong, T. T. Y., Nishimoto, J. I., and Mochizuki, N. 1983. Infestation patterns of Mediterranean fruit fly and the oriental fruit fly (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Environ. Entomol. 12,1031-1039. Wong, T. T. Y., Mochizuki, N., and Nishimoto, J. I. 1984. Seasonal abundance of parasitoids of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Environ. Entomol. 13, 140-145. Wong, T. T. Y., McInnis, D. O., Kobayashi, R. M., and Nishimoto, J. I. 1985. Distribution and seasonal abundance of adult male Mediterranean fruit flies (Diptera: Tephritidae) in Kula, Maui, Hawaii. J. Econ. Entomol. 78, 552-557. Wong, T. T. Y., Kobayashi, R. M., and McInnis, D. 0. 1986. Mediterranean fruit fly (Diptera: Tephritidae): Methods of assessing the effectiveness of sterile insect releases. J. Econ. Entomol. 79,15011506. Wong, T. T. Y., and Ramadan, M. M. 1987. Parasitization of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. J. Econ. Entomol. 80, 77-80. Wong, T. T. Y., Ramadan, M. M., McInnis, D. O., and Mochizuki, N. 1990. Influence of cohort age and host age on oviposition activity and offspring sex-ratio of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitatu (Diptera: Tephritidae). J. Econ. Entomol., in press. Yamada, T., Nakagawa, S., and Kamasaki, H. 1962. Identification of three species of reared Hawaiian fruit fly pupae. Proc. Hawaii. Entomol. Sot. 8, 319-321.
CONTROL
1,
2-7
(1991)
Augmentative Releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to Suppress a Mediterranean Fruit Fly (Diptera: Tephritidae) Population in Kula, Maui, Hawaii TIM T. Y. WONG, Tropical
Fruit
and
Vegetable
M. M. RAMADAN, Research
Laboratory, Received
D. 0. MCINNIS, Agricultural May
N. MOCHIZUKI,
Research 21,199O;
accepted
The Mediterranean fruit fly, Ceratitis cupituta (Wiedemann), and the oriental fruit fly, Dacus dorsalis Hendel, are serious pests of fruits and vegetables in Hawaii. C. capitata was introduced into Hawaii from Australia in 1910 (Back and Pemberton, 1918) and D. dorsalis was introduced from the Pacific Islands about 1945 (Van Zwaluwenberg, 1947; Bess and Haramoto, 1961). Both species became widespread immediately after their establishment. However, within 5 years of the arrival of D. dorsalis, the distribution patterns of C. capitata changed. Associated with competition with D. dorsalis and a high rate of parasitism, C. cupituta became scarce at low elevation but remained abundant in upland areas (Bess, 1953). At present, C. capitata is isolated in
$3.00
0 1991 by Academic Press, Inc. of reproduction in any form reserved.
October
Department
of Agriculture,
Honolulu,
Hawaii
96804
2,199O
MATERIALS
AND
METHODS
Larvae of C. capitata were reared by the methods of Tanaka et al. (1969) and were used as host larvae for rearing D. tryoni. Our laboratory colony of D. tryoni was established in 1981 with adults emerged from parasitized C. capitata pupae from infested peaches that had been collected in Kula, Maui. Adult D. tryoni cohorts were kept in screened cages (26 cm3) at a capacity of 400 2
1049.9644/91
U.S.
AND J. C. HERR
patches throughout the major Hawaiian Islands, with its largest populations found in Kula, Maui, and Kona, Hawaii (Haramoto and Bess, 1970, Nishida et al., 1985). Wong et al. (1984) and Wong and Ramadan (1987) found that nearly all peach fruits in Kula were infested with fruit flies; approximately 50% of adult insects that emerged were C. capitata, 25% were D. dorsalis, and the remaining 25% were parasitoids of both fruit fly species. Biosteres arisanus Fullaway, an egg-larval parasitoid, was the dominant species and accounted for 374% and the two larval parasitoids, Diachasmimorpha longicaudata (= Biosteres longicaudatus) (Ashmead) and Diachasmimorpha tryoni (= Biosteres tryoni) (Cameron), accounted for 15 and lo%, respectively, of the parasitoids recovered (Wong and Ramadan, 1987). The rationale for augmentative releases of parasitoids has been considered and discussed by Knipling (1979). However, the utility of this method of insect suppression in the field has not been fully demonstrated with fruit flies. The present paper reports on the suppression of a C. capitata population by augmentative releases of D. tryoni in the Kula area from March to June 1988. D. tryoni is selected over other braconids because it is amenable to mass rearing in the laboratory. Also, in Hawaii, D. tryoni is relatively host specific. It successfully develops in C. capitata larvae and in the larvae of two stem gall-forming tephritids, the lantana gall fly, Eutreta xanthochaeta Aldrich, and Procecidochares utilis Stone, but it is unable to develop on D. dorsalis (Haramoto and Bess, 1970).
Diachasmimorpha tryoni (Cameron), a larval parasitoid, was mass-reared in the laboratory and was used to suppress a wild Mediterranean fruit fly, Ceratitis capitata (Wiedemann), population in a nonisolated area (13 km’) of Kula, Maui, Hawaii. Weekly releases of D. tryoni, averaging 272,000 parasitoids per release, were made from March 10 to June 22, 1988. Trap catches of male C. capitata adults began to decline 8 weeks after the first release, and catches remained low throughout the summer months. However, in the control area of Keokea, adult catches began to increase in April and reached a peak in early July that was similar to that of previous years. The percentage of parasitism of C. capitata by D. tryoni was significantly higher for the six weekly collections of infested peaches in Kula than in the control area of Keokea: an average of 47.0% parasitism in Kula compared with 14.2% in Keokea. Of the total parasitoids, a significantly higher percentage of D. tryoni was recovered in fruit samples from Kula than in those from Keokea. Moreover, the number of C. capitata per fruit was significantly lower in the treated area than in the control area. 0 1991 Academic Press, Inc. KEY WORDS: Insecta; Ceratitis capitata; Diachasmimorpha tryoni; parasitoid releases.
Copyright All rights
Service,
J. I. NISHIMOTO,
SUPPRESSION
OF
C. cupitata
males and 400 females per cage. Honey, streaked on the top screen, was the source of food and water for adult wasps. The oviposition unit was a modified petri dish (9 cm in diameter and ~0.5 cm deep). Tight-fitting lids with organdy covers were used to hold C. capitata larvae inside the dishes. Third-instar hosts (about 800) mixed in artificial rearing media were packed into each oviposition unit and were exposed to parasitoids for 3 to 4 h. Parasitoid females readily oviposited through the organdy into the larvae. To allow introduction and removal of oviposition units from the outside without causing injury or loss of parasitoids, a screened opening to accommodate oviposition units was made in the bottom of the cage. After exposure to parasitoids, host larvae were removed from the oviposition units and consolidated along with additional rearing media in plastic trays (30 X 48 X 2.5 cm) which were then kept in wooden holding cabinets (91 X 183 X 61 cm). When mature, host larvae vacated the larval diet; they popped out and fell into plastic containers (30 X 48 X 14 cm) of vermiculite for pupation. Seven days later, puparia were sifted from vermiculite and held on screened trays (53 X 67 X 2 cm) in screened emergence cabinets (76 X 155 X 63 cm). Flies emerged from unparasitized pupae about 10 to 13 days after pupation and died within 2 days of adult life because no food was provided; the remainder of the puparia contained immature parasitoids. These parasitized puparia were collected and distributed in small paper bags to be placed in cohort cages to maintain the colony or were placed in plastic containers hanging from branches of fruit trees for field release. Male D. tryoni emerged 16 to 18 days after oviposition and females followed 2 days later at 26 + 1°C and 60 f 10% RH. Biological data and mass-rearing procedures for D. tryoni have been reported by Ramadan et al. (1989a,b) and Wong et al. (1990). The study area [1.8 X 7.3 km (13 km2)] on the slopes of Mount Haleakala (summit elevation, 3056 m) in Kula, Maui, with elevations ranging from 700 to 1200 m, was selected because prior study had shown it to be an area where fruits were heavily infested with C. capitata (Wong et al., 1983). Although the Kula area is not isolated, it is bordered on all sides by moderately dry rangeland that is currently used for livestock grazing. Fruit trees occurred along roadsides, in yards of residences, and in gulches. The Keokea area of 2.6 km2 (about 1.1 km south of Kula) was used as a control site because fruit-fly host trees, climatic conditions, and elevation were similar to those in the Kula area. Keokea served as a control for a test using sterile fly releases to suppress a C. capitata population in Kula in 1981-1982. Infestation patterns and parasitoids of C. capitata from loquat and peach fruits as well as adult fly trap catch data from Keokea were similar to those from the Kula area (Wong et al., 1986). White plastic containers (3.8 liters, 14 cm deep X 20 cm diameter) were
WITH
D. tryoni
3
placed in nearly all of the 480 peach trees located in Kula (Wong et al., 1983). Paper bags holding parasitized pupae were slit across the top and placed into the containers at weekly intervals when fruits were in season. Male parasitoids usually began emerging on the day of release and females about 2 days later. Emerging parasitoids escaped by flying out of eight l-cm-diameter holes near the tops of the containers. Seasonal distribution and abundance of adult male C. capitata were determined with 250 plastic traps baited with trimedlure in the Kula area from 1978 to 1981 (Wong et al., 1985). In the present study, we reduced the number to 100 traps, or approximately every other trap site of the original distribution, and placed 25 traps in the Keokea area to detect and monitor the adult population. Trapped flies (>99% males) were removed weekly by the methods of Nakagawa et al. (1971). The trap catches of 1988 in Kula were used to compare with those of a high catch year of 1978 and a moderate catch year of 1979, as well as with those in Keokea during 1982,1983, and 1988. Traps were in place for only these years. No yearly collection data were omitted from analysis. Weekly from June to early July 1988, we collected windfallen peaches on the ground. These fruit samples were brought back to the laboratory, counted, weighed, and placed in screen-sided fiberglass containers (30 X 50 X 15 cm), at 26 k 2°C and 60 t 10% RH. Four to five days later, each fruit was examined, discarded if not infested, or held for 2 or more weeks if infested. Mature tephritid larvae were collected, counted, and placed in plastic cups containing moistened fine white sand and were covered with screened lids (144 mesh/cm2). About 6-8 days after pupation, all puparia were examined under a stereomicroscope, and C. capitata and D. dorsalis were separated using differences in the anterior puparial characters as described by Yamada et al. (1962). Puparia of each tephritid species were then held in separate plastic cups with screened lids for emergence. Numbers of adults were recorded, and parasitoids were identified to species using published keys (Beardsley, 1961; Wharton and Gilstrap, 1983). The total percentage parasitism was determined by dividing the total number of parasitoids by the total of C. capitata and parasitoids eclosed. In Kula, eight sites (15 X 15 m per site) with lantana bushes, Lantana camara L., were selected for monitoring the potential impact of the parasitoid releases on the lantana gall fly, Eutreta xanthochaeta Aldrich, at monthly intervals from January to November 1988. In Keokea, four sites were selected. At each site, galls on freshly grown shoots were counted; then about 3 to 5% of the galls were cut from shoots randomly and were brought back to the laboratory, weighed, and held individually in plastic cups with screen lids. All insects that emerged from the galls were recorded. Plans to monitor the population of the other nontarget species P. utilis
4
WONG
TABLE
ET
1
sitism and percentage D. tryoni of total parasitoids in Kula and Keokea were compared with a-paired t test. data were transformed using the arscine procedure before analysis (Snedecor and Cochran, 1967).
Number of Diachasmimorpha tryoni Released and Number of Release Sites on Peach Trees in Kula, Maui, Hawaii, in 1LY”” OPP
Month
NO. weekly releases
March April May June
4 4 4 3
No. parasitoids Total
released
Average/week
l&X2,350 1,194,120 1,313,361 510,648
265,587 298,530 328,340 170,216
NO. release sites
Average No. parasitoids/ site/week
144 191 169 67
1844 1563 1943 2540
RESULTS
,
,
,
,
/
l
I
I
IIIIIIIIIIl
,
,
,
,
,
,
,
AND
DISCUSSION
From March 9 to June 22, 1988, 4.1 million laboratory-reared D. tryoni, an average of 272,000 parasitoids per week, with a range of 170,000 to 328,000 parasitoids per week, were released into the Kula area of Maui to suppress larvae of C. capitata infesting peach fruits (Table 1). The number of release sites varied from week to week because of fruit development and maturation rates at different altitudes. However, in most instances, parasitoids were released wherever fruits were present on each peach tree or adjacent tree. During the peak of peach production in April and May, the average number of parasitoids released per site per week ranged from 1563 to 1943. Emerging D. tryoni males were observed to hover near the containers and mated with females as the latter emerged. Copulation occurred for about 10 to
had been made, but this was not done because few or none of its host plant, Ageratina adenophoria (Spreng), were found in Kula or Keokea. The x2 procedure was used to compare differences in the proportion of each parasitoid species for each fruit collection date and the total fruits collected from Kula and Keokea. Student’s t test was used to compare differences in C. capitata adults obtained from windfallen peaches from both Kula and Keokea. Percentage para-
6,
AL.
,
,
,
,
,
,
,
,
,
/
,
,
,
,
4-
2G n l!z”. a
12
IIIIIIIIIIII
% E
KULA IO-
\ \ 2
2 9
w”
8-
nI -
‘a
\
/
a----m -
1978
o-----o
1988
1979
\
:
I
6-
4-
2-
o-
1/1,,,1(1,,,,,,,,,,,/,,,(1 5 19 2 16 JAN FEE
FIG. 1. Comparison period between arrows
of male represents
C.
I
I5 MAR
29
12
26 APR
capituta trap catches parasitoid
release
IO
24 MAY
7
21 JUN
in Kula (1978-1979 during 1988.
5
I9
2
JUL and
1988)
I6 30 AUG and Keokea
13 27 SEP
II 25 OCT
(1982-1983
8
22 NOV
and 1988),
6 20 DEC Maui,
Hawaii.
The
SUPPRESSION
OF
‘2. cupitutu
20 s and then females flew off to nearby fruit trees. Females were found on the surface of leaves and fruits. Greany et al. (1977) reported that D. longicaudata was attracted to fermentation products emanating from rotting fruit, a probable site for the location of host larvae. In our study, rotting fruit was attractive, irrespective of the presence of host larvae, and attraction was attributed to microbial fermentation products rather than to kairomones from host larvae. On many occasions in the field, we observed D. longicaudata and D. tryoni sitting, probing, and ovipositing into fruits on the ground. Figure 1 shows the seasonal trends of wild male C. capitata caught by traps placed in Kula for 1978, 1979, and 1988 and in Keokea for 1982, 1983, and 1988. In Keokea, trap catches for all 3 years began to increase in April and the peaks reached in July 1988 were higher than those reached in the other 2 years. In Kula, the catch patterns for 1978 and 1979 were similar to those in Keokea, but in 1988 the population reached a peak in late April and then began to decline rapidly before increasing again to a smaller peak in early July. Wong et al. (1985) reported that the increase in population each year in April was the result of infested loquat fruits appearing in the winter months and that the peak population in the summer months was from infested peaches in the spring. They also found that adult catches were
Date
Numbers
Location
No. pupae”
of C. cupitutu in Kula No. C. capitatu and parasitoids
Pupae and and Keokea
1
Kula Control
1,191 1,030
1,129 970
621 131
June
8
Kula Control
4,646 1,089
4,511 947
2093 152
June
14
Kula Control
2,206 1,119
2,106 1,021
835 180
June
21
Kula
2,428
2,271
1384
June
28
Control Kula Control
2,805 1,402 1,712
2,483 1,314 1,617
191 425 266
July
6
Kula Control
819 578
774 527
326 154
12,105 7,565
5684 1074
Kula Control
18,399 11,305
tryoni
5
2
Their Parasitoids (Control), Maui,
Collected Hawaii, No.
Total parasitoids
June
Total
D.
significantly correlated with the number of infested fruits. In this study, we found that a similar peak in trap catches occurred 8-12 weeks after the peak in fruit infestations. This lag time provided an indication of the minimum total time required for C. capitata to complete development in fruit, to pupate, and finally to be trapped as adults. In 1988, fruit production and tephritid infestation were similar or perhaps higher than those in previous years. Therefore, we conclude that the reduction in trap catches in May and June of 1988 in Kula was the result of the augmentative releases of D. tryoni because trap catches began to decrease about 8 weeks after the beginning of the releases on March 9. The decline in trap catches in May and June indicated that the ratio of parasitoid females to C. capitata females was sufficient to cause and decline in population. In April, when the C. capitata population began to increase, the ratio of parasitoid females to C. capitata females decreased, with the lowest ratio in the week of April 26. This resulted in a peak in C. capitata numbers about 10 weeks later on July 5. Table 2 presents numbers of C. capitata and parasitoids collected from windfallen peaches on six dates in 1988 at Kula and Keokea. The percentages of parasitization based upon eclosion of adults ranged from 32.3 to 60.9% for Kula and from 7.7 to 29.2% for Keokea.
TABLE Total
WITH
B. arisanus
(4.8:;* 63 169 (174.06)*** 196 131 (29.96)*** 2,537 733 (201.72)***
Peaches
D. tryoni
Other@
1
260
35
(O.Pl)‘NS 51
(36.7;;** 1,172
(3.9$ 44
t9.2:** 16
(104.4:*** 467
(O.Ol;NS 9
(43.6:)*** 13 (35.5;***
(91.0!$.. 583 (1.69;kJS
(16.1:*** 4 (SOi&**
11
341
10
(d&**
(199.8& 109 (27.1&
(O.Ol;NS 1 (l.66)2Ns
2,932 232 (326.12)***
103
20 (2.76pNS 112 ,73.,7,f***
***,
Windfallen
parasitoids
D. longicaudata
325 111 (46.61)***” 826 113 (71.63)*** 343 1117 (34.20)*** 784
a Number of pupae obtained from sampling windfallen peaches. b Psyttalia incisi, Tetrastichus giffardianus, and unemerged parasitoids. ’ Homogeneity x2 values in parentheses; df = 1. * P < 0.05; **, P < 0.01;
from
in 1988
P < 0.001;
NS,
not
significant;
(,3.1;***
x2.
% Parasitization 55.0 13.5 46.4 16.0 39.6 17.6 60.9 7.7 32.3 16.4 42.1 29.2 47.0 14.2
6
WONG
TABLE Comparison Populations: 1988
versus
Keokea
% Parasitism species Actual (x)
Location Control Kula Paired
t test
’ Data
3
of Mean Parasitization Kula
transformed
by arcsine
Maui,
Hawaii,
in
% D. tryoni of total
by all
parasitoid Actual (x)
2 2.20
20.37
recovered Transformed” (x xk SEM) 26.38
rt 2.71
46.10
+ 4.08
(n = 6) k 2.48
51.60
(n = 6) (t = 4.78; df P < 0.01)
5;
AL.
the present study, the level of measured parasitism was 47% but the true rate of parasitism was considerably higher. The reason for this was because the measured rate was limited to the parasitism that had occurred up to the time at which the fruit was collected, whereas the true rate of parasitism included that which continued up to the time all the fruit fly larvae had matured in the fruit. Tephritid eggs and young larvae artificially escaped parasitism due to removal of infested fruit from the field. Monthly collections of stem galls from lantana bushes showed only the lantana gall fly, E. xanthochaeta, and its parasitoids emerged from puparia (Table 4). D. tryoni was the most prominent parasitoid species reared. Eurytoma tephritidis Fullaway occurred at much lower frequencies. Parasitism was uniformly low throughout the collection, 10.9% in Kula and 12.1% in Keokea. High pupal mortality, caused in part by sampling of different age galls and handling, was recorded in all collections (Table 4). The augmentative releases of D. tryoni had no effect on the rate of parasitism of E. ranthochaeta, partly because lantana bushes were at least 25 m away from the nearest fruit trees. Factors such as habitat differences (pastureland versus fruit trees) and limited dispersal of D. tryoni in the presence of fruiting trees (T. T. Y. Wong, unpublished data) probably prevented higher rates of parasitism of D. tryoni on E. xanthochaeta in Kula. The sterile-insect release technique was used to suppress a Mediterranean fruit fly population in Kula. From December 1981 to June 1982, an average of 4 million irradiated flies were released by air and ground each week. A significant reduction of the C. capitata population, which was similar to that in the 1988 parasitoid releases, occurred in the Kula area compared with the
Rates of C. cupitatu
(Control),
Transformed” (x + SEM)
16.76 23.79 (n = 6) 42.71 46.08 (n = 6) (t = 4.48;df= P < 0.01)
ET
= 5;
proportion.
The x2 analysis of each parasitoid species showed significantly more parasitoids in Kula than in Keokea. Also, significantly (Student’s t test; t = 2.484, df = 5, P < 0.05) fewer C. capitata adults per fruit were obtained in the six samples of windfallen peaches in Kula than in Keokea. Moreover, a comparison of C. capitata populations showed a significantly higher rate of parasitism in Kula than in Keokea and this was attributed at least in part to significantly higher numbers of D. tryoni in Kula (Table 3). The predominance of D. tryoni over B. arisanus is a reversal of earlier studies. Haramoto and Bess (1970) reported that since 1951, B. arisanus had become the dominant parasitoid, replacing D. tryoni, and accounted for >90% of the total parasitization against C. capitata in coffee in Kona, Hawaii. Wong et al. (1984) and Wong and Ramadan (1987) reported that B. arisanus accounted for ~74% of the total parasitization in Kula. In
TABLE
4
Number of Stem Galls Collected from Young Stems of Lantana Bushes and Emergence of Diuchusmimorpha tryoni, Euryand Adult Lantana Flies from Eutretu xunthochueta Puparia in Kula (Eight Sites) and Keokea (Four Sites), Maui, Hawaii, in 1988
toma tephritidis,
Date January-March April-June July-September October-November Total
’ Percentage
parasitism
Location
No. galls counted
Kula Keokea Kula Keokea Kula Keokea Kula Keokea Kula Keokea
23,124 6,753 21,063 19,521 21,343 12,773 14,547 8,733 80,077 47,780
= No.
emerged
parasitoids/total
No. galls collected 632 262 748 519 772 414 731 437
No. flies emerged 58 25 61 57 83 72 44 35 246 189
1632 emerged
parasitoids
% galls from which insects emerged 11.4 9.5 8.8 12.3 11.9 20.5 6.3 9.4 9.6 13.2 + hosts
No.
D. tryoni 14
0 5 6 5 10 2 6 26 22 X 100.
parasitoids
emerged”
E. tephritidis 0 0 0 1 4 3
0 0 4 4
Total % parasitism 19.4 0 7.6 10.9 9.8 15.3 4.3 14.6 10.9 12.1
SUPPRESSION
OF
C. copitata
control area of Keokea (Wong et al., 1986). Plans to releases integrate the sterile insect and parasitoid in Kula in the near against the C. capitata population _ _ __ future have been developed; the two methods will likely be more effective and more ecologically acceptable than the use of insecticides (Knipling, 1979). The combination of these techniques will be useful in future eradication or suppression plans throughout the Hawaiian Islands and other fruit fly-infested areas, including the U.S. mainland. ACKNOWLEDGMENTS We thank J. E. Gilmore for administrative and technical assistance and E. F. Knipling for technical advice. We are grateful to Harris Chang, Kevin Gavagan, Dan Kawamoto, Dale Kanehisa, Mahmoud Kazan, Allen Marzan, Michael McKenney, and Keith Shigetani for providing fly larvae and parasitoids during this study.
REFERENCES Back, E. A., and Pemberton, C. E. 1918. The Mediterranean in Hawaii. U.S. Dep. Agric. Bull. 536. Beardsley, J. W. 1961. A review of the Hawaii Braconidae tera). Proc. Hawaii. Entomol. Sot. 17, 333-366.
fruit
fly
(Hymenop-
Bess, H. A. 1953. Status of Ceratitis capitata in Hawaii following the introduction of Dacus dorsalis and its parasites. Proc. Hawaii. Entomol. Sot. 15, 221-234. Bess, H. A., and Haramoto, F. 1961. Contributions to the biology and ecology of the oriental fruit fly,. Dacus dorsalis Hendel (Diptera: Tephritidae), in Hawaii. Hawaii Agric. Exp. Stn. Tech. Bull. 44. Greany, P. D., Tumlinson, J. H., Chambers, D. L., and Boush, G. M. 1977. Chemically mediated host finding by Biosteres (Opius) longicaudatus, a parasitoid of tephritid fruit fly larvae. J. Chem. Ecol. 2, 189-195. Haramoto, F. H., and Bess, H. A. 1970. dance of the oriental and Mediterranean their parasites. Proc. Hawaii. Entomol.
Recent studies on the abunfruit flies and the status of Sot. 20, 551-566.
Knipling, E. F. 1979. “The Basic Principles of Insect Population Suppression and Management.” U.S. Dept. Agric. Handbook 512. Nakagawa, S., Chambers, D. L., Urago, T., and Cunningham, R. T. 1971. Trap-lure combinations for surveys of Mediterranean fruit flies in Hawaii. J. Econ. Entomol. 64, 1211-1213. Nishida, T., Distributional
Harris, E. J., Vargas, loci and host fruit
R. I., and utilization
Wong, patterns
T. T. Y. 1985. of the Medi-
WITH
terranean Hawaii.
D.
7
tryoni
fruit Environ.
fiy, Ceratitis capitatu Entomol. 14, 602-606.
(Diptera:
Tephritidae),
in
Ramadan, M. M., Wong, T. T. Y., and Beardsley, J. W. 1989a. Survivorship, potential, and realized fecundity of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitata (Diptera: Tephritidae). Entomophaga 34, 291-297. Ramadan, M. M., Wong, T. T. Y., and Beardsley, J. W. 1989b. Insectary production of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capita& (Diptera: Tephritidae). Proc. Hawaii. Entomol. Sot. 29, in press. Snedecor, G. W., and Cochran, W. G. 1967. “Statistical Methods.” Iowa State Univ. Press, Ames. Tanaka, N., Steiner, L. F., Ohinata, K., and Okamoto, R. 1969. Lowcost larval rearing medium for mass production of oriental and Mediterranean fruit flies. J. Econ. Entomol. 62, 967-968. Van Zwaluwenburg, Entomol. Sot.
13,
R. H. 1947. 8.
Notes
and exhibitions.
Proc.
Hawaii.
Wharton, R. A., and Gilstrap, F. E. 1983. Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Cerutitis and Dacus s.1. (Diptera: Tephritidae). Ann. Entomol. Sot. Amer. 76, 721-742. Wong, T. T. Y., Nishimoto, J. I., and Mochizuki, N. 1983. Infestation patterns of Mediterranean fruit fly and the oriental fruit fly (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Environ. Entomol. 12,1031-1039. Wong, T. T. Y., Mochizuki, N., and Nishimoto, J. I. 1984. Seasonal abundance of parasitoids of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Environ. Entomol. 13, 140-145. Wong, T. T. Y., McInnis, D. O., Kobayashi, R. M., and Nishimoto, J. I. 1985. Distribution and seasonal abundance of adult male Mediterranean fruit flies (Diptera: Tephritidae) in Kula, Maui, Hawaii. J. Econ. Entomol. 78, 552-557. Wong, T. T. Y., Kobayashi, R. M., and McInnis, D. 0. 1986. Mediterranean fruit fly (Diptera: Tephritidae): Methods of assessing the effectiveness of sterile insect releases. J. Econ. Entomol. 79,15011506. Wong, T. T. Y., and Ramadan, M. M. 1987. Parasitization of the Mediterranean and oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. J. Econ. Entomol. 80, 77-80. Wong, T. T. Y., Ramadan, M. M., McInnis, D. O., and Mochizuki, N. 1990. Influence of cohort age and host age on oviposition activity and offspring sex-ratio of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitatu (Diptera: Tephritidae). J. Econ. Entomol., in press. Yamada, T., Nakagawa, S., and Kamasaki, H. 1962. Identification of three species of reared Hawaiian fruit fly pupae. Proc. Hawaii. Entomol. Sot. 8, 319-321.