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1 June 2013 Comparative Biology of Diachasmimorpha longicaudata(Hymenoptera: Braconidae) Reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae)
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Abstract

The braconid Diachasmimorpha longicaudata (Ashmead) is the most widely used parasitoid in biological control programs of tephritids in the Americas. Anastrepha fraterculus (Wiedemann) is a major fruit fly pest of exotic and native fruits in southern Brazil. However, life history parameters such as longevity, sex ratio, preoviposition, oviposition and post-oviposition periods, fecundity and fertility of D. longicaudata using A. fraterculus as host, have not been determined. These parameters were compared to those derived from the better known host, Ceratitis capitata (Wiedemann), the Mediterranean fruit fly. In the laboratory, A. fraterculus was at least as suitable a host for D. longicaudata as C. capitata. Female parasitoids derived from A. fraterculus were larger and had a higher net reproductive rate (R0). The mean numbers of superparasitism records were higher in A. fraterculus larvae (1.6 ± 0.22) than in C. capitata (0.4 ± 0.07). Other variables did not differ between hosts. Given suitable environments D. longicaudata may become established in A. fraterculus populations or successfully mass-reared on this host species and released.

Opiine braconids are widely used in the control of tephritid fruit flies because their relatively high host specificity and ability to inflict substantial mortality on their hosts (Aluja et al. 1990). About 100 species of braconids have been found parasitizing tephritid larvae worldwide, and many of these belong to the genera: Diachasmimorpha Viereck, Psyttalia Walker, Utetes Foster and Opius Wesmael (Wharton 1989). The Indo-Australian Diachasmimorpha longicaudata (Ashmead) is a koinobiont, solitary, synovigenic, larval-prepupal endoparasitoid of several tephritid genera that has been mass-reared and used in augmentative releases against important fruit fly species in tropical and subtropical countries (Montoya et al. 2000). Biological parameters of D. longicaudata have been studied on Anastrepha suspensa (Loew) (Ashley et al. 1976; Greany et al. 1976; Lawrence et al. 1976), Anastrepha ludens Loew (Montoya et al. 2003; Montoya et al. 2011) and Ceratitis capitata (Wiedemann) (Ovruski et al. 2003; Viscarret et al. 2006).

Although introduced to Brazil in 1990 (Carvalho & Nascimento 2002), D. longicaudata has been used sporadically and plans for further introductions and/or augmentation releases are still in early stages. In Brazil, D. longicaudata has been reared on the Mediterranean fruit fly, C. capitata, but less is known about its performance on the South American fruit fly, Anastrepha fraterculus (Wiedemann) (Kovaleski et al. 2000). This work aimed to evaluate biological parameters of D. longicaudata on A. fraterculus and provide data for mass-rearing this parasitoid.

MATERIALS AND METHODS

Puparia of C. capitata parasitized by D. longicaudata were provided by “Embrapa Mandioca e Fruticultura Tropical”, Cruz das Almas, state of Bahia, Brazil (Dr. Antônio Nascimento) and maintained according to the methods described by Carvalho et al. (1998). Host larvae were obtained from a laboratory culture established in 2007 from wild fruit flies. We used 16th to 28th generation fruit flies and 7th to 35th generation parasitoids.

Diachasmimorpha longicaudata Colony Rearing

Approximately 50 couples of D. longicaudata were maintained in cages (20 × 15 × 15 cm), covered by organdy screen and kept at 25 ± 2 °C; 65 ± 10% RH and 14:10 h L:D. Water and food were provided ad libitum. Diet consisted of water (120 ml), honey (120 ml), agar (0.8 g), ascorbic acid (0.05 g), and nipagin (0.005 g). Approximately 40 to 50 third instar larvae of C. capitata were introduced to the cages and exposed to parasitoids for 1 h in parasitism units made of organdy screen (225 cm2). Host larvae were placed in the center of the screen and the edges wrapped with a rubber band forming a spherical unit that was hung from the upper part of cage. Up to 3 units were hung in each cage per day. After exposure, larvae were transferred individually to 100 ml plastic vials with sterilized sand until emergence.

Anastrepha fraterculus and Ceratitis capitata Colony Rearing

The flies were reared using the methods described by Salles (1992) and Terán (1976), and maintained at 25 ± 2 °C; 65 ± 10% RH and 14:10 h L:D.

Life History Traits of D. longicaudata Reared on A. fraterculus and C. capitata

Egg-Adult Phase

Five groups with 40–50 third-instar larvae of A. fraterculus (about 10-day-old) were exposed for 1 h to fifty 3–10-day-old experienced couples of D. longicaudata, previously reared on A. fraterculus larvae. The putatively parasitized larvae were placed individually in vials (25 ml) with sterilized sand and wet paper, and covered with plastic film. Larvae were maintained at 25 ± 2 °C; 65 ± 10% RH and 14:10 h L:D and observed every day for emergence. The same procedure was applied to third-instar larvae of C. capitata, which were exposed for 1 h to fifty 3–10-day-old experienced couples of D. longicaudata, previously reared on C. capitata larvae. The total developmental period (egg-adult) and immature viability of 215 and 225 parasitized larvae of A. fraterculus and C. capitata were recorded, respectively.

Longevity, Sex Ratio, Fecundity and Fertility

Two groups of D. longicaudata adults, one composed of 52 females and 56 males that had emerged from A. fraterculus, and another of 55 females and 54 males that emerged from C. capitata, were individually kept in plastic vials (140 mL) provided with food and water to determine the longevity of virgin adults. Females of these 2 groups did not receive larvae for oviposition during the experiment. We observed 10 parasitoid couples that had emerged from A. fraterculus, and were maintained with food and water ad libitum, and offered A. fraterculus larvae (10 per female) for 1 h oviposition periods in a daily basis. When a parasitoid female died, we reduced the number of larvae in order to keep the larva/female ratio, until all females had died. Each dead male was replaced to avoid competition for sexual partners and to guarantee the maximum reproductive potential by females. After exposure, the larvae were removed and kept at 25 ± 1 °C, 60 ± 10% RH and complete darkness. After 72 h the pupae were opened to count the number of parasitoid eggs and/or larvae, and the number of viable fruit fly larvae. We considered fertility as the number of parasitoid larvae and fecundity the number of larvae plus the number of eggs; superparasitism was evaluated by counting eggs and larvae inside the pupae. Longevity of mated D. longicaudata was also recorded. Fecundity, fertility and superparasitism of D. longicaudata reared on C. capitata or A. fraterculus were recorded for 25 couples on each host.

Morphometry of D. longicaudata Reared in A. fraterculus and C. capitata

We measured the length of the right hind tibia and the area of the right forewing of 100 D. longicaudata adult females and 100 adult males that emerged from A. fraterculus and C. capitata. These body parts were removed and photographed under an optical microscope and measured with a micrometer. The photos were analyzed and compared with the software Image Tool 3.00®. Mean larval weights of A. fraterculus and C. capitata were estimated by weighing 10 groups each of 10 larvae.

Data Analysis

Data were tested for normality by D'Agostino test and compared with a t-student or MannWhitney test. The sex ratio (sr) and fertility were calculated as described by Silveira Neto et al. (1976). The mean weight of larvae, tibia length and forewing area were compared between hosts by Kruskal-Wallis test. We estimated and compared the life table parameters, (net reproductive rate (R0), finite rate of increase (λ), rate of population increase (rm) and doubling time (TD)) of parasitoids reared on 2 hosts were estimated using the “Jackknife” technique (Meyer et al. 1986) following the procedures described in Maia et al. (2000) and Maia & Luiz (2006). The significance level used in all the tests was α = 0.05.

RESULTS

Life History Traits of D. longicaudata Reared on A. fraterculus and C. capitata

Egg-Adult Phase

The mean egg-adult development periods of D. longicaudata females and males were similar on both hosts. However, females had a longer lifespan than the males (H = 91.9402; df = 3; P < 0.05) (Table 1).

Longevity, Sex Ratio, Fecundity and Fertility

Virgin females that emerged from A. fraterculus lived longer than those emerged from C. capitata (t = -2.7008; df = 105; P = 0.008). By contrast, the longevities of mated females did not differ between hosts (t = -0.0776; df = 38; P = 0.9386). The longevities of virgin and mated males from both hosts was similar (t’ = 1.0727; df = 91.07; P = 0.2862 and U = 160; P = 0.4424, respectively) (Table 2).

TABLE 1.

DURATION (DAYS) (MEAN ± SE) OF THE EGG TO ADULT DEVELOPMENT OF DIACHASMIMORPHA LONGICAUDATA FEMALES AND MALES REARED ON ANASTREPHA FRATERCULUS AND CERATITIS CAPITATA [25 ± 2 °C; 65 ± 10% RH; 14:10 H L:D].

t01_412.gif

Virgin individuals of D. longicaudata, regardless the host, lived longer (31 ± 1.19 days) than mated ones (17.7 ± 1.21 days) (t’ = 7.8427; df = 229.11; P < 0.0001) (Table 2).Virgin females reared on A. fraterculus lived longer than virgin males from the same host (t’ = 5.2652; df = 89.50; P < 0.0001), but there was no difference between the longevities of the sexes when mated (U = 90.50; P = 0.3615). Conversely, for insects reared from C. capitata, the mean longevity of virgin females did not differ from that of males (t = -0.07832; df = 107; P = 0.4352), while mated females lived longer than males (U = 201; P = 0.0305) (Table 2).

On the first day of parasitoid emergence, only males emerged from both hosts. On the second day of emergence, males predominated. From the third day onwards the female ratio increased. The sex ratio of D. longicaudata on A. fraterculus (0.59) was similar to that on C. capitata (0.55) (χ2 = 1.978; df = 1; P = 0.1776) (Fig. 1).

The mean daily fecundity (U = 4.50; P = 0.0947), total (t =1.3987; df = 8, P = 0.1994) and mean fertility (χ2 = 1.141; df = 1; P = 0.3599) were similar in D. longicaudata emerged from A. fraterculus and C. capitata. The preoviposition (t = 1.0; df = 4; P = 0.3739), oviposition (U = 10; P = 0.6015) and post-oviposition (t’ = -0.7977; df = 4.38; P = 0.4697) periods did not differ for females reared on the 2 hosts (Table 3). Superparasitism was recorded during all the oviposition period in the wasps reared from both hosts. The mean number of superparasitism records per day and per female were higher on A. fraterculus (1.6 ± 0.22) than on C. capitata (0.4 ± 0.07) (U = 164; P = 0.0002). Up to 3 parasitoid eggs were recorded in a single C. capitata larva, while in A. fraterculus we recorded up to 6 eggs (Fig. 2).

Based on generation time (T), net reproductive rate (R0), finite rate of increase (ë), infinitesimal rate of increase (rm) and doubling time (DT), the fitness of D. longicaudata reared on A. fraterculus was higher than when reared on C. capitata (Table 4).

TABLE 2.

MEAN LONGEVITY (DAYS) (± SE) OF VIRGIN AND MATED DIACHASMIMORPHA LONGICAUDATA FEMALES AND MALES REARED ON ANASTREPHA FRATERCULUS AND CERATITIS CAPITATA [25 ± 2 °C; 65 ± 10% RH; 14:10 H L:D].

t02_412.gif

Fig. 1.

Daily sex ratio of Diachasmimorpha longicaudata reared on Anastrepha fraterculus (fi01_412.gif) and on Ceratitis capitata (fi02_412.gif) [25 ±2 °C; 65 ± 10% RH; 14:10 H L:D]. A sex ratio value that is greater than 0.5 represents a population with more females than males. A sex ratio of less then 0.5 represents a population with more males than females.

f01_412.jpg

Fig. 2.

Daily number of superparasitisms observed per Diachasmimorpha longicaudata female on Ceratitis capitata (Dl(Cc)) and Anastrepha fraterculus (Dl(Af)).

f02_412.jpg

Morphometry of D. longicaudata Reared in A. fraterculus and C. capitata

Third-instar larvae of A. fraterculus were heavier (0.0203 ± 0.00027 g) than those of C. capitata (0.0121 ± 0.00025 g)(t = - 22.4084; df = 18, P < 0.0001). Females that emerged from A. fraterculus had a larger wing area (F = 1.7393; df = 211; P < 0.0001) and longer tibia length (F = 3.5723; df = 220; P < 0.0001) than those derived from C. capitata. Males reared from A. fraterculus also had larger wings (F = 2.3671; df = 201; P < 0.0001) and longer tibiae (F = 2.0931; df = 204; P < 0.0001). Females were always larger than males regardless the host species (Table 5).

DISCUSSION

The longer lifetime observed for D. longicaudata females compared to males can be related to additional time required for maturation of reproductive organs (Ramadan et al. 1992). This seems be a pattern in braconids, as recorded in Diachasmimorpha tryoni (Cameron) (Hurtrel et al. 2001), Biosteres persulcatus Silvestri (Ibrahim et al. 1993) and Biosteres arisanus (Sonan) (Bautista et al. 1998). Moreover, male parasitoids usually emerge sooner, which expedites locating emerging females and ensures mating. The maledominated sex ratio on the first and second day of emergence may be a strategy increases the likelihood of males copulating newly emerged females (Godfray 1994). The shorter longevity of mated females compared to virgin females may be related to the energy used for copulation and oviposition (Greany et al. 1976).

Host size may affect sex ratio, particularly of idiobionts, because more females are produced from larger hosts (Ueno 1999; Ode & Heinz 2002). As expected of a koinobiont parasitoid, we did not observe such effect in our study. Host size may have a direct influence on parasitoid size (Godfray 1994), as demonstrated in this study. Larger parasitoids may have higher levels of fertility and fecundity (Jervis 2005). However, the heavier females reared from A. fraterculus larvae did not have higher fertility or fecundity. Differences in host size or quality may not necessarily influence reproductive parameters. Some parasitoids may allocate resources to host searching, having a somehow fixed reproductive budget (Cicero et al. 2011). In fact, parasitoids are able to compensate for differences in host quality by modifying their resource allocation strategy (Cicero et al. 2012). The higher incidence of superparasitism in A. fraterculus may be related to the size of the larvae and the parasitism unit. Anastrepha fraterculus is larger than C. capitata, while the parasitism units were the same size for both hosts. Thus, parasitoid females contacted fewer larvae of A. fraterculus than of C. capitata. Superparasitism by D. longicaudata appears to be common. Superparasitized hosts were recorded even in the presence of unparasitized larvae with no apparent detrimental effects on the offspring's demographic parameters (Montoya et al. 2012).

TABLE 3.

PREOVIPOSITION, OVIPOSITION AND POST-OVIPOSITION PERIODS (DAYS) (MEAN ± SE), DAILY FECUNDITY AND TOTAL FECUNDITY (MEAN ± SE), FERTILITY (%) (MEAN ± SE)) OF DIACHASMIMORPHA LONGICAUDATA REARED ON ANASTREPHA FRATERCULUS (DL (AF)) (N = 11) AND ON CERATITIS CAPITATA (DL (Cc)) (N = 25) [25 ± 2 °C; 65 ± 10% RH; 14:10 H L:D].

t03_412.gif

TABLE 4.

NET REPRODUCTIVE RATE (R0), INFINITESIMAL RATE OF INCREASE (RM), FINITE RATE OF INCREASE (fi03_412.gif), MEAN (T) (DAYS), AND DOUBLING TIME (DT) (DAYS) (VALUES ± SE) OF DIACHASMIMORPHA LONGICAUDATA REARED ON ANASTREPHA FRATERCULUS AND ON CERATITIS CAPITATA [25 ± 2 °C; 65 ± 10% RH; 14:10 H L:D].

t04_412.gif

Differences in the size of parasitoids produced by different hosts should be taken into account in biological control projects. The parasitoid size may influence their host searching efficiency (Lawrence et al. 1976).

In summary, in the laboratory A. fraterculus was at least as suitable as a host as C. capitata for D. longicaudata. Female parasitoids derived from A. fraterculus had a higher net reproductive rate (R0) and produced larger individuals. The number of superparasitism records was higher in A. fraterculus than in C. capitata;other variables, such as longevity, sex ratio, preoviposition, oviposition and post-oviposition periods, fecundity and fertility did not differ between the host species. Given suitable environments, D. longicaudata may become established in Brazilian A. fraterculus populations or successfully mass-reared and released for augmentative biocontrol.

TABLE 5.

RIGHT FOREWING AREA (MM2) (MEANS ± SE) AND HIND TIBIA LENGTH (MM) OF FEMALES AND MALES OF DIACHASMIMORPHA LONGICAUDATA REARED FROM ANASTREPHA FRATERCULUS (DL (AF)) AND FROM CERATITIS CAPITATA (DL (Cc)) [25 ± 2 °C; 65 ± 10% RH; 14:10 H L:D].

t05_412.gif

ACKNOWLEDGMENTS

We thank Dra. Aline Barcellos for the critical revision and valuables comments and to CNPq for fellowships awarded to the authors and the financial support (grant 475287/2010-0).

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Rafael Narciso Meirelles, Luiza Rodrigues Redaelli, and Cláudia Bernardes Ourique "Comparative Biology of Diachasmimorpha longicaudata(Hymenoptera: Braconidae) Reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae)," Florida Entomologist 96(2), (1 June 2013). https://doi.org/10.1653/024.096.0204
Published: 1 June 2013
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