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Title: Evaluation of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae)
reared on a genetic sexing strain of Ceratitis capitata (Wied.) (Diptera: Tephritidae).
Article Type: Regular Article
Section/Category:
Keywords: Keywords: Diachasmimorpha longicaudata; Ceratitis capitata; life table analysis; genetic sexing
strain; integrated pest management; biological control; sterile insect technique.
Corresponding Author: Dr. Mariana Mabel Viscarret, PhD
Corresponding Author's Institution: INTA
First Author: Mariana Mabel Viscarret, PhD
Order of Authors: Mariana Mabel Viscarret, PhD; Rubén La Rossa, MSc; Diego Fernando Segura, BSc;
Sergio Marcelo Ovruski, PhD; Jorge Luis Cladera, PhD
Manuscript Region of Origin:
Abstract: Abstract
If a genetic sexing strain of C. capitata could be used to produce sterile males and parasitoids at the same
time, significant amount of resources could be saved in comparison with the production of these two
biological agents separately. We studied here the major biological parameters comparing two strains of the
parasitoid Diachasmimorpha longicaudata, one of them reared on a wild type strain of Ceratitis capitata:
DL(+), and the other on a genetic sexing strain of C. capitata: DL(sw). The mean longevity, fecundity and
sexual proportion of their respective offspring showed no significant difference. Moreover, no difference was
observed in population parameters such as mean generation time, net reproductive rate, finite rate of
increase, doubling time, and intrinsic rate of increase. The conclusion is reached that, rearing the parasitoid
on this particular genetic sexing strain of C. capitata does not produce any negative effect on the biological
parameters studied. The biological parameters of other artificially reared parasitoids on the Tephritidae is
reviewed in two tables.
Cover Letter
April 19th, 2005
Biological Control
Editorial Office
525 B Street, Suite 1900
San Diego, CA 92101-4495, USA
I am sending you the manuscript “Evaluation of the parasitoid Diachasmimorpha
longicaudata (Ashmead) (Hymenoptera: Braconidae) reared on a genetic sexing strain of
Ceratitis capitata (Wied.) (Diptera: Tephritidae)”. I would appreciate you evaluate the
possibility to publish it in your journal.
Thank you very much for your kindness,
Dra. Mariana M. Viscarret
Instituto de Genética "Ewald A. Favret"
Instituto Nacional de Tecnología Agropecuaria
Casilla de Correo 25 (1712) Castelar.
Buenos Aires, Argentina.
TE/FAX: +54-11-4-4500805/1876
E-mail: mviscarret@cnia.inta.gov.ar
* Manuscript
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Evaluation of the parasitoid Diachasmimorpha longicaudata (Ashmead)
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(Hymenoptera: Braconidae) reared on a genetic sexing strain of Ceratitis
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capitata (Wied.) (Diptera: Tephritidae).
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Viscarret, Mariana M.1; La Rossa, Rubén2; Segura, Diego F.1; Ovruski, Sergio M.3;
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Cladera, Jorge L.1
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Agropecuaria, Castelar, Buenos Aires, Argentina.
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Instituto de Genética “Ewald A. Favret”. Instituto Nacional de Tecnología
Instituto de Microbiología y Zoología Agrícola. Instituto Nacional de Tecnología
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Agropecuaria, Castelar, Buenos Aires, Argentina.
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Miguel de Tucumán, Argentina.
CONICET, FML-CIRPON, Instituto Superior de Entomología-FCNeIML-UNT, San
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----------------------------------------------------------------------------------------------------------------Corresponding author: Instituto de Genética “Ewald A. Favret”. INTA Castelar. C. C.
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25 (1712), Castelar, Buenos Aires, Argentina.
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Phone/Fax: +54-11-4-4500805/1876
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E-mail address: mviscarret@cnia.inta.gov.ar
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Abstract
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If a genetic sexing strain of C. capitata could be used to produce sterile males and
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parasitoids at the same time, significant amount of resources could be saved in
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comparison with the production of these two biological agents separately. We studied
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here the major biological parameters comparing two strains of the parasitoid
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Diachasmimorpha longicaudata, one of them reared on a wild type strain of Ceratitis
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capitata: DL(+), and the other on a genetic sexing strain of C. capitata: DL(sw). The
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mean longevity, fecundity and sexual proportion of their respective offspring showed
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no significant difference. Moreover, no difference was observed in population
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parameters such as mean generation time, net reproductive rate, finite rate of
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increase, doubling time, and intrinsic rate of increase. The conclusion is reached that,
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rearing the parasitoid on this particular genetic sexing strain of C. capitata does not
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produce any negative effect on the biological parameters studied. The biological
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parameters of other artificially reared parasitoids on the Tephritidae is reviewed in
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two tables.
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Keywords: Diachasmimorpha longicaudata; Ceratitis capitata; life table analysis;
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genetic sexing strain; integrated pest management; biological control;sterile insect
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technique.
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Introduction
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There are two economically important fruit flies pests in Argentina: the
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Mediterranean fruit fly, Ceratitis capitata (Wiedemann), and the South American fruit
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fly, Anastrepha fraterculus (Wiedemann) (Maddison and Bartlett, 1989). The annual
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losses by direct damage have been estimated between 15 and 20% of the national
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fruit yield (Aruani et al., 1996). Furthermore, the presence of any of these dipteran
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species cause quarantine restrictions for fruit exportation (Senasa, 1998).
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Different methods have been used worldwide to control fruit flies species. The
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sterile insect technique (SIT) and the augmentative biological control (ABC) through
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the use of fruit fly parasitoids are two environmentally acceptable strategies to control
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fruit flies. Integration of these two techniques would be highly desirable. Theoretical
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studies (Barclay, 1987; Knipling, 1992), have shown that augmentative parasitoids
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releases used in conjunction with the SIT have a synergistic effect to suppress
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tephritid population: the joint expected effect is stronger than the sum of the expected
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effects of each of the control method employed alone. Moreover, the integration of
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the mass production of sterile males and parasitoids may result in a considerable
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reduction of costs compared to producing these agents separately. This encourages
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the joint use of these two methodologies (SIT and ABC) to control fruit flies.
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Diachasmimorpha longicaudata (Ashmead) is a larval parasitoid of fruit flies.
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This parasitoid wasp has been reported in numerous countries in Southeastern Asia,
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where it parasitizes at least 14 species of the genus Bactrocera (Bess et al., 1961;
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Clausen et al., 1965; Wharton and Gilstraps, 1983). Following its introduction to
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several other countries, D. longicaudata has been reported parasitizing Bactrocera
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dorsalis (Hendel), C. capitata (Wiedemann), and some species of the genus
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Anastrepha (Montoya et al., 2000). Likewise, this parasitoid has been used in ABC
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strategies in several countries (Clausen et al., 1965; Vargas et al., 1993; Sivinski et
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al., 1996).
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In Argentina, SIT has been successfully applied to control C. capitata (Aruani
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et al., 1996; De Longo et al., 2000). However less attention has been paid to the use
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of parasitoid wasps as biological control agents (Ovruski et al., 1999). The natural
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parasitism of C. capitata and A. fraterculus in wild and cultivated fruits is very low,
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due fundamentally to the inability of the native braconid parasitoids to attack these
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tephritids (Ovruski et al., 2004). During the years 60´s and 80´s, several small scale
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releases of D. longicaudata were conducted, without enough subsequent evaluations
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(Ovruski et al., 2004). Recently, D. longicaudata has been reported in Argentina ´s
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northeastern province of Misiones (Schliserman et al., 2003).
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The objective of the present study is to use life table analysis to evaluate a
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genetic sexing strain of C. capitata as potential host for a mass rearing program of D.
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longicaudata. We worked with a genetic sexing strain of C. capitata based on a
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mutation of the gene sw affecting the rate of development (Manso and Lifschitz,
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1992). In this strain females have a longer developmental time than males (Delprat
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et al., 2002) so they can be separated from males early in their life cycle (Viscarret et
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al., 2004). Female larvae could be used for rearing parasitoids to release in ABC
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programs, while the male larvae (previous irradiation at pupal stage) could be used
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for the SIT after their emergence.
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Material and Methods
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The parasitoids and fruit flies used in this study were reared at Laboratorio de
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Insectos, Instituto de Genética (INTA, Castelar). Ceratitits capitata wild type strain
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was MI94 (originated from the colony reared in the Mendoza Insectary, Argentina,
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introduced into the lab at INTA Castelar Argentina, on September 1994), and the
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genetic sexing strain was Cast 191 (Delprat et al., 2002). The colony of D.
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longicaudata was initiated with individuals coming from CIRPON, San Miguel de
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Tucumán (Ovruski et al., 2003).
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The D. longicaudata strain reared on C. capitata MI94 was named DL(+),
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whereas the one reared on Cast 191 was named DL(sw), because females are sw-
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//sw-.
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Experimental procedure
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Fifteen couples (< 24h old) were set from both strains of parasitoids. Each
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female represented a replicate. When the male of any couple died, it was replaced by
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another male of similar age until the female died. All couples were provided water
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and honey throughout the assay.
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An oviposition unit (a Petri dish, 3 cm diameter, covered with a mesh)
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containing seven-days-old larvae of C. capitata (ad libitum) was offered to each
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couple every other day. The exposition period lasted five hours. Afterwards, larvae
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were kept in a vial with medfly fresh artificial diet (Terán, 1977). Vermiculite was used
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as pupation substrate. The pupae obtained from each exposition and for each couple
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were separated and kept in flasks until the parasitoids and fruit flies emerged.
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For each replicate, the number of pupae obtained, the number and sex of
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parasitoid offspring and the number of fruit flies emerged, were recorded every other
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day. Female survival was also registered.
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Larvae and pupae were maintained at T (mean ± standard error): 24.61ºC ±
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0.33ºC, HR (mean ± standard error): 65.00% ± 2.75%, and continuous light. Adults
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were kept at T: 22.90ºC ± 2.90ºC, RH: 47.73% ± 1.66%, and 12L:12D photoperiod.
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Preovipositional
period,
ovipositional
period,
longevity,
survival,
fecundity, and sexual proportion
After all data were registered we calculated the following variables:
1) mean preovipositional period (Σ number of days until the i female begun to
lay eggs / initial number of females);
2) mean ovipositional period (Σ number of days during which the female i laid
eggs / number of initial females);
3) mean longevity of the adult female (Σ lifespan of the i female / initial number
of females);
4) mean survival by age (lx), (number of female at age x / initial number of
females);
5) specific fecundity by age (mx), (mean number of female offspring by female
at age x);
6) mean fecundity (Σ number of female offspring of the i female / total number of
females); and
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7) mean diary sexual proportion ([Σ number of female offspring of the i female in
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the j day / Σ total number of offspring of the i female in the j day] / number of
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remaining females in the j day).
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One-Way ANOVA was used to compare between parasitoid strains for
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preovipositional period, ovipositional period, mean fecundity, mean longevity, and
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mean diary sexual proportion, as all this variables satisfied the assumptions required
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by that test.
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Population parameters
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The following population parameters were estimated using the program
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“TABLAVI” (La Rossa and Kahn, 2003):
1) Net reproductive rate (R0): average number of individuals (females in this
case) produced by one female along its life (Begon et al., 1988);
2) finite rate of increase (λ): factor by which a population increases in size from
time t to time t+1(Ravinovich, 1980);
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3) intrinsic rate of increase (rm): rate at which the population increases in size. It
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is the change in the population size per individual per unit of time (Begon et al.,
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1988);
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4) mean generation time (T): mean time between the birth of an individual and
the birth of its offspring (Begon et al., 1988); and
5) doubling time (t): time required for the population to reach a twofold increase
in size (Messenger, 1964).
All the estimated parameters were compared with a T test (Steel and Torrie,
1980).
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Results
Preovipositional
period,
ovipositional
period,
longevity,
survival,
fecundity, and sexual proportion.
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Both strains of D. longicaudata presented a preovipositional period. There was
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no significant difference (F(1,25) = 0.10, P = 0.75) between DL(sw) (mean ± standard
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error: 3.23±0.62 days) and DL(+) (mean ± standard error: 3.57 ± 0.81 days).
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The ovipositional period did not show significant difference between strains
(F(1,25) = 2.91, P = 0.10) (28±2.56 days for DL(sw) and 22.57 ± 1.87 days for DL(+)).
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The mean longevity of female was not significantly different between parasitoid
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strains (F(1,26) = 2.45, P = 0.13) (Table 1), but the females of the strain DL(sw)
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showed higher survival (l50= 39 days) than those of DL(+) (l50= 33days) (Fig. 1).
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There was not difference between strains for mean fecundity (F(1,26)=0.006,
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P=0.96) (Table 1). The strain DL(sw) reached its highest fecundity between the 11th
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and 27th day of its lifespan (Fig. 2), with three peaks on the days 15 (4.75 ± 1.06
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females /female), 19 (4.82 ± 0.99 females / female) and 25 (4.92 ± 1.50 females /
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female). The DL(+) strain reached the highest fecundity between the days 11 and 27
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with two peaks on 15 (6.67 ± 1.18 females / female) and 19 (6.69 ± 1.30 females /
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female) days. Both strains showed similar curves (Fig. 2).
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The mean diary sexual proportion of offspring was high for both parasitoid
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strains between the third and 30th day of female life span, approximately. The means
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(± standard errors) for this period were 0.62 (±0.03) for DL(+) and 0.67 (±0.05) for
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DL(sw) (Fig. 3). Values observed from day 31 onward are irrelevant due to low
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survival of the parental female. The overall proportion of female offspring was similar
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in both parasitoid strain (F(1,26)=0.15, P=0.70) (Table 1).
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Population parameters
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The mean generation time (T), the net reproductive rate (R0), the finite rate of
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increase (λ), the doubling time (t) and the intrinsic rate of increase (rm) did not differ
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between parasitoid strains (Table 2).
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Discussion
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The two strains of parasitoids compared here show similar biological
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characteristics. All the variables estimated indicate that rearing the parasitoid on the
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fruit fly genetic sexing strain Cast191 does not affect its biological quality.
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For all the variables registered, the existence of some differences between our
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results and the ones obtained by other authors can be satisfactorily explained by
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different environmental conditions and host species used. The ovipositional period
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registered in the present work is longer than cited in the literature for D. longicaudata
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and other fruit fly parasitoids (Table 3). The longevity registered in the present study
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was, in general, higher than that registered for other parasitoids, except for Psyttalia
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cosyrae (Wilkinson) using C. capitata and C. cosyra (Walker) as hosts (Mohamed et
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al. 2003) (Table 3).
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In relation to female survival, Ramadan et al. (1995) described a similar curve
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for F. vandenboschi but with a more pronounced slope. Mohamed et al. (2003)
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reported, for P. cosyrae, curves similar to those found in this work. In the case of D.
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longicaudata (host: B. dorsalis) Vargas et al. (2002) observed a higher mortality rate
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at the beginning of their life span, but a similar pattern after the initial period.
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Graphical estimation of l50 for all the mentioned species, produced lower values than
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the ones observed in this assay. This lower value of l50 was also registered by
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Cancino and Yoc (1993) for D. longicaudata.
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The highest fecundity of different species of fruit flies parasitoids, including D.
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longicaudata, on different host occurs between the 7th and 15th day of the adult
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female life span (Greany et al., 1976; Ashley and Chambers, 1980; Cancino and Yoc,
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1993; Bautista et al., 1998; Rungrojwanich and Walter, 2000). However, Zenil et al.
223
(2004), registered for F. arisanus a high diary number of offspring extended to the
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25th day of the adult female life. Similarly, in the present study higher percentage of
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parasitism was observed in older females. However, the fecundity curve (Fig. 2) was
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similar to those reported in other fruit fly parasitoid species (Greany et al., 1976;
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Ashley and Chambers, 1980; Bautista et al., 1998; Rungrojwanich and Walter, 2000,
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Vargas et al., 2002; Zenil et al., 2004).
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Many variables influence the oviposition behavior of this kind of parasitoids.
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The previous ovipositional experience has showed to be a factor that increases the
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oviposition as well as the number of eggs in the ovarioles. The presence of males, a
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suitable rearing medium and a higher “host : parasitoid” ratio are also positive stimuli
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(Lawrence et al., 1978; Lawrence et al., 2000; Ashley and Chambers, 1980;
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Ramadan et al., 1995; Cancino, 1998; Rungrojwanich and Walter, 2000). In our work
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females were offered larvae throughout their life span, as well as food, water and
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males. The “hosts : female” ratio was set in order to allow females to show their
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maximum fecundity.
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Regarding the female offspring sex proportion for both parasitoid strains the
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values observed here were similar to those cited by other authors(Table 3). The
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exception there are the low value data registered for Psyttalia incisi (Silvestri) and P.
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fletcheri (Silvestri) (Vargas et al., 2002) and Diachasmimorpha krausii (Fullaway)
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(Rungrojwanich and Walter, 2000).
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It is well known that the sexual proportion can be affected by different
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variables, such as larval stage, age and size of the host, time of exposition to the
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parasitoids and age of the female. In Fopius vandenboschi
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Bactrocera dorsalis (Hendel)), Ramadan et al (1995) registered an increase of female
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offspring when females were exposed to the second or early third larval stage, but
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the proportion of females was lower when using first larval stage, and no female
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emerged from late third larvae. Likewise, Messing and Ramadan (2000) registered
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for Diachasmimorpha krausii (Fullaway) a higher percentage of female offspring
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parasitizing on intermediate third larval stage of Bactrocera latifrons (Hendel) and on
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early third larval stage of C. capitata. In the case of F. arisanus (Sonan) the
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production of females increased with the age of the host (Zenil et al., 2004). Refering
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to host size, Messing and Ramadan (2000) described for D. krausii a greater bias
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towards females when rearing was done on B. latifrons (bigger larvae) than on C.
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capitata (smaller larvae). This result has also been observed in D. longicaudata
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(hosts: Anastrepha ludens (Loew) and B. dorsalis) and other fruit flies parasitoids of
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the Opiinae family (Cancino and Yoc, 1993; Messing et al., 1993). In the present
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work these hypothesis have not been tested, but our results are, in general, similar to
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those cited by the authors for the stages preferred by this parasitoid (Table 3). Even
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though the age of the female is also mentioned as a factor that affects the sexual rate
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(Bautista et al., 1998; Ramadan et al., 1994), no clear tendency was observed in the
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present assay.
(Fullaway) (host:
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Population parameters
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The population parameters estimated for D. longicaudata in the present work
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are, mostly, similar to those observed by Vargas et al. (2002) and Bautista et al.
268
(1998) (Table 4). The values registered here for R0 and T were somewhat higher
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than those observed by the mentioned authors for D. longicaudata and the other
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parasitoids studied. However, Zenil et al. (2004) registered for F. arisanus, lower R0
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values when the host was A. ludens and higher R0 when it was C. capitata and A.
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serpentina. Temperature and, probably, the host species, could have influenced our
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results.
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It is important to point out that no genetic sexing strains of C. capitata, neither
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in Argentina nor in other countries, has ever been used before with the double
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purpose of rearing male flies for SIT and parasitoids for ABC. Our results are
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promissory since they indicate that the medfly sexing strain, Cast191, could be used
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to produce sterile males and parasitoids simultaneously. Therefore this study is an
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original contribution to the integration of these two techniques in pest management
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programs for fruit flies control.
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Acknowledgements
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We thank Dr. Silvia López and Lic. Alejandro Pietrek for their valuable comments and
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suggestions on an early version of this article, and Leonela Carabajal Paladino,
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Cynthia Cagnotti, Romina Russo and María Eugenia Utgés for helping in the
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laboratory.
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This work was supported by the grant PICTO 12909 from Agencia Nacional de
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Promoción Científica y Tecnológica-Instituto Nacional de Tecnología Agropecuaria to
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J.L.C., and S. M. O.
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18
433
Figure 1: Survival of adult females (number of female to start the age interval x /
434
initial number of females) for strains DL(+) and DL(sw) of Diachasmimorpha
435
longicaudata.
436
Figure 2: Mean diary fecundity (number of females/female/day) for strains DL(+) and
437
DL(sw) of Diachasmimorpha longicaudata (± standard error).
438
Figure 3: Mean diary sexual proportion (F/M+F) for strains DL(+) and DL(sw) of
439
Diachasmimorpha longicaudata (± standard error).
19
Figure
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Figure
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Figure
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Tables
1
Table 1: Longevity, mean fecundity and sexual proportion (Mean ± standard error),
2
for DL(sw) and DL(+) parasitoid strains of Diachasmimorpha longicaudata. Variables
3
were compared using a One-way ANOVA.
4
Parameter
D. longicaudata D. longicaudata
P
(sw)
(+)
Longevity (days)
34.08±3.13
28.33±2.07
0.13
Mean fecundity (♀/♀)
32.92±5.055
32.53±5.652
0.96
Sexual proportion (♀/(♀+♂)
0.55±0.04
0.56±0.05
0.70
5
6
1
7
Table 2: Population parameters estimated for strains DL(sw) and DL(+) of
8
Diachasmimorpha longicaudata (Mean ± standard error). Variables were compared
9
using a T test.
10
D. longicaudata D. longicaudata
Population parameter
P
(sw)
(+)
11
T (Mean generation time, days)
39.373±0.552
37.933±0.681
0.12
Ro (Net reproductive rate,♀/♀)
33.844±5.140
32.537±5.651
0.87
٨ (Finite rate of increase, per day)
1.099±0.004
1.102±0.006
0.69
t (Doubling time, days)
7.360±0.280
7.111±0.378
0.61
rm (Intrinsic rate of increase, day-1)
0.094±0.004
0.098±0.005
0.55
12
13
2
3
14
Table 3: Biological parameters of fuit flies parasitoids.
15
Species
Oviposition
Fecundity
period
Longevity
Sexual rate
(days)
Experimental
Authors
Conditions
(days)
Fopius arisanus (a)
11.0±1.78
119.40±24.71
17.30±3.89
-
T: 26±2ºC ;
Vargas et al.,
RH : 60±10%
2002
0.57±0.08
T: 26±2ºC ;
Vargas et al.,
(Female
RH : 60±10%
2002
57±4.6
26±2ºC ;
Ramadan et
(Female
RH: 60±10%
al., 1995
(eggs/F)
F. vandenboschi (a)
11.0±1.50
33.38±5.92
22.0±4.35
(eggs/F)
proportion)
F. vandenboschi (a)
6.1±1.1
33.3±6.0
(eggs/F)
22.0±1.3
percentage)
4
Diachasmimorpha
9.33±1.64
longicaudata (a)
93.00±3.88
15.67±4.10
(eggs/F)
0.59±0.05
T: 26±2ºC ;
Vargas et al.,
(Female
RH : 60±10%
2002
0.49±0.10
T: 26±2ºC ;
Vargas et al.,
(Female
RH : 60±10%
2002
0.64±0.05
T: 26±2ºC ;
Vargas et al.,
(Female
RH : 60±10%
2002
T: 25ºC
Mohamed et
RH: 60-70%
al. 2003
T: 25ºC
Mohamed et
RH: 60-70%
al. 2003
proportion)
Psyttalia incisi (a)
16.50±2.08
90.90±12.98
36.60±3.89
(eggs/F)
proportion)
P. fletcheri (b)
8.80±0.81
69.30±11.21
13.40±3.89
(eggs/F)
proportion)
P. cosyrae (c)
P. cosyrae (d)
55.0±4.2
77.5±3.9
5
D. tryoni (c)
6.60±0.78
50.40±6.67
13.40±3.89
(eggs/F)
0.55±0.6
T: 26±2ºC ;
Vargas et al.,
(Female
RH : 60±10%
2002
0.28±0.03
T: 25±1ºC ;
Rungrojwanich
(Male
RH: 60±5%
and Walter
proportion)
D. krausii (e)
111.7±11.29
27.6±4.55
((F+M)/F)
proportion)
(2000)
16
17
The hosts were: (a): Bactrocera dorsalis . (b) Bactrocera cucurbitae.
(c)
Ceratitis capitata. (d) Ceratitis cosyra. (e) Bactrocera tryoni.
6
7
Table 4: Population parameters of fruit flies parasitoids. T (mean generation time,
days); R0 (net reproductive rate, female/female); ٨ (finite rate of increase, per
day); t (doubling time, days); rm (intrinsic rate of increase/day)
Species
T
R0
٨
Fopius arisanus (a)
27.3
27.4
1.13
t
rm
Authors
0.12
Vargas et al.,
2002
F. arisanus (a)
26.69
16.21
1.11
6.3
0.10
Bautista et al.,
1998
F. arisanus (b)
117.4±0.8
Zenil et al.,
2004
F. arisanus (c)
14.5±0.4
Zenil et al.,
2004
F. arisanus (d)
58.0±0.7
Zenil et al.,
2004
F. vandenboschi
30.3
10.1
1.08
0.08
(a)
Diachasmimorpha
2002
27.2
28.2
1.13
0.12
longicaudata (a)
D. tryoni (b)
Vargas et al.,
Vargas et al.,
2002
27.8
16.4
1.11
0.10
Vargas et al.,
2002
Psyttalia incisi (a)
33.4
29.4
1.12
0.10
Vargas et al.,
2002
8
P. fletcheri (e)
28.3
21.5
1.11
0.11
Vargas et al.,
2002
The hosts were: (a): Bactrocera dorsalis . (b) Ceratitis capitata. (c) Anastrepha
ludens. (d)Anastrepha serpentina. (e)Bactrocera cucurbitae.
9
10