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Offspring in response to parental female densities in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae: opiinae).

Translation provided by the authors.

The major natural enemies of tephritid fruit flies in Brazil are members of the families Braconidae, Figitidae, and Pteromalidae (Hymenoptera) (Garcia & Corseuil 2004). Parasitoid par·a·sit·oid  
n.
Any of various insects, such as the ichneumon fly, whose larvae are parasites that eventually kill their hosts.

adj.
Of or relating to a parasitic insect of this kind.
 mass rearing, required for biocontrol bi·o·con·trol  
n.
See biological control.



biocontrol  

See biological control.
 via augmentative aug·men·ta·tive  
adj.
1. Having the ability or tendency to augment.

2. Grammar Indicating an increase in the size, force, or intensity of the meaning of an adjacent word, as up does in eat up.

n.
 release, must be directed to optimize production of females rather than males (Carey et al. 1988). A higher female-biased sex ratio can be more efficient in applied biocontrol efforts with parasitoids because females can eliminate the target pest by oviposition oviposition

the act of laying or depositing eggs.
 and/or by feeding on host fluids themselves (King 2002). Therefore, understanding the different factors affecting off spring sex ratio of the parasitoid species to be mass reared is essential to get efficient parasitoid production (Wong & Ramadan 1992; Heimpel & Lundgren 2000).

In haplodiploid insects such as Hymenoptera, males develop from an unfertilized Adj. 1. unfertilized - not having been fertilized; "an unfertilized egg"
unfertilised, unimpregnated

infertile, sterile, unfertile - incapable of reproducing; "an infertile couple"
 haploid haploid /hap·loid/ (hap´loid)
1. having half the number of chromosomes characteristically found in the somatic (diploid) cells of an organism; typical of the gametes of a species whose union restores the diploid number.
 egg, but females originate from a fertilized fer·til·ize  
v. fer·til·ized, fer·til·iz·ing, fer·til·iz·es

v.tr.
1. To cause the fertilization of (an ovum, for example).

2.
 diploid diploid /dip·loid/ (dip´loid)
1. having two sets of chromosomes, as normally found in the somatic cells; in humans, the diploid number is 46.

2. an individual or cell having two full sets of homologous chromosomes.
 egg. Offspring sex-ratio control is primarily maternal (Godfray 1994), but several biotic biotic /bi·ot·ic/ (bi-ot´ik)
1. pertaining to life or living matter.

2. pertaining to the biota.


bi·ot·ic
adj.
1. Relating to life or living organisms.
 and abiotic factors can affect parasitoid progeny yield and off spring sex ratio (King 1987; Heimpel & Lundgren 2000). For example, the following factors have been identified in the Braconidae: host size, stage and age (Jarosik et al. 2003; Zenil et al. 2004), host species (Messing & Ramadan 2000; Quimio & Walter 2001), host plant (Jackson et al. 1996), host density (Harris & Bautista 1996), host contagion Contagion

The likelihood of significant economic changes in one country spreading to other countries. This can refer to either economic booms or economic crises.

Notes:
An infamous example is the "Asian Contagion" that occurred in 1997 and started in Thailand.
 with pathogens (Orr et al. 1994), parental age (Rungrojwanich & Walter 2000), density and sex ratio of parents (Lozano et al. 1997), dispersion behavior (Paranhos et at. 2007), superparasitism (Gonzalez et al. 2007), inbreeding (Stouthamer et al. 1992; Salin et al. 2004), local mate competition (Nishimura & Jahn 1996), multiple matings, postmating rest period, temperature in mating chambers, and storage temperatures for parents (Fuester et al. 2003).

Several species of braconid brac·o·nid  
n.
Any of several ichneumon flies of the family Braconidae, the larvae of which are parasitic on other insects.



[From New Latin Braconidae, family name, possibly from Greek
 parasitoids belonging to the subfamily subfamily /sub·fam·i·ly/ (sub´fam-i-le) a taxonomic division between a family and a tribe.

sub·fam·i·ly
n.
A taxonomic category ranking between a family and a genus.
 Opiinae have been mass reared and augmentatively released against economically important tephritid fruit fly species in tropical and subtropical sub·trop·i·cal  
adj.
Of, relating to, or being the geographic areas adjacent to the Tropics.


subtropical
Adjective

of the region lying between the tropics and temperate lands

 countries (Purcell 1998; Rendon et al. 2006). One such braconid is Diachasmimorpha longicaudata (Ashmead), a koinobiont larval-pupal endoparasitoid associated with numerous species of tephritid fruit flies (Wharton & Gilstrap 1983; Ovruski et al. 2000). This parasitoid species is currently considered to be one of the most significant biological control agents for augmentative release programs against fruit fly pests in Latin American (Gonzalez et al. 2007).

The Mediterranean fruit fly Mediterranean fruit fly: see fruit fly.
Mediterranean fruit fly
 or Med fly

Fruit fly (Ceratitis capitata) proven to be particularly destructive to citrus crops, at great economic cost.
 and several Anastrepha species are major pests of fruit crops worldwide and in Brazil. Parasitoid species were first reared on a C. capitata bisexual strain (Walder et al. 1995) in Brazil. Currently, in the Moscamed facility in Brazil the viability for mass rearing D. longicaudata on larvae Larvae, in Roman religion
Larvae: see lemures.
 of a genetic sexing (males-only) strain of a temperature sensitive lethal (tsl) C. capitata strain has been studied as part of an augmentative release program against C. capitata (Wiedemann) in the tropical fruit growing areas of northern Brazil (Lopes & Para nhos 2006; Paranhos 2007; Malavasi et al. 2007).

The objectives in the current study were to find the best parental ratio of females to males of D. longicaudata in rearing cages in order to get the highest female biased offspring in the rearing of D. longicaudata, and to verify the parasitism parasitism: see parasite.
parasitism

Relationship between two species in which one benefits at the expense of the other. Ectoparasites live on the body surface of the host; endoparasites live in their hosts' organs, tissues, or cells and often rely
 efficiency on C. capitata according to parental female densities.

MATERIAL AND METHODS

Study Site and Biological Material The study was conducted in the Laboratory of Radio-Entomology at CENA/University of Sao Paulo located in Piracicaba Town, Sao Paulo State, Brazil, in 1998. Laboratory conditions were 25-27[degrees]C, 60-85% RH, with a photoperiod photoperiod /pho·to·pe·ri·od/ (fo´to-per?e-od) the period of time per day that an organism is exposed to daylight (or to artificial light).photoperiod´ic

pho·to·pe·ri·od
n.
 of 12:12 h (L:D). The colony of D. longicaudata used in the experiments was raised and maintained on late third instars of the bisexual strain of C. capitata in the laboratory according to rearing methods described by Walder (2002).

Experimental Procedure

Adults of D. longicaudata were kept in aluminum-framed, mesh-covered experimental cages (30 x 30 x 30cm) provided with agar-agar a·gar   also a·gar-a·gar
n.
1. A gelatinous material derived from certain marine algae. It is used as a base for bacterial culture media and as a stabilizer and thickener in many food products.

2.
 (10 g), water (700 mL) and bee honey (300 mL). Males, which emerge before females, were collected and maintained inside experimental cages. After the second day, virgin females were collected just after emerging and also maintained in cages. Late-third instars of C. capitata (7 d old) from a wild bisexual strain were separated from artificial diet, irradiated at 60 Gy dose ([Co.sup.60] source, [gamma] rays) to avoid the emergence of flies, and used as hosts for all experiments. The irradiated naked larvae were placed in cylindrical PVC PVC: see polyvinyl chloride.
PVC
 in full polyvinyl chloride

Synthetic resin, an organic polymer made by treating vinyl chloride monomers with a peroxide.
 dishes (5 cm diameter, 1 cm height) that had the bottom side covered with organdy mesh. These oviposition units were exposed on the top screen of experimental cages for 40 min to female parasitoids. Ten irradiated late third instars of C. capitata in the oviposition units described above were offered daily to each female parasitoid from the 1st to 12th d of age. Three proportions of female/male parasitoids were tested independently: 20 females and 20 males (1:1 female/ male proportion), 60 females and 20 males (3:1), and 100 females and 20 males (5:1). Host larval larval

1. pertaining to larvae.

2. larvate.


larval migrans
see cutaneous and visceral larva migrans.
 density per female parasitoid was the same, al ways 10 larvae/female. Thus, in total 200, 600, and 1000 host larvae were offered per day and per experimental cage at the female densities noted above of 20, 60, and 100 female, respectively. The number of host larvae provided to surviving parasitoids was proportionally decreased as parental females died during the 12-day oviposition period. For each reared batch of parasitoids, 10 replicate experimental cages were used for each female/male parasitoid density, and each treatment was repeated 3 times with fresh parasitoids and host larvae. The cages were positioned at random on a table and kept under the laboratory conditions described above.

After exposure to the parasitoids, the fruit fly larvae were carefully transferred to plastic cups (250 mL) containing vermiculite ver·mic·u·lite  
n.
Any of a group of micaceous hydrated silicate minerals related to the chlorites and used in heat-expanded form as insulation and as a planting medium.
 as the pupation pu·pate  
intr.v. pu·pat·ed, pu·pat·ing, pu·pates
1. To become a pupa.

2. To go through a pupal stage.



pu·pa
 medium, and perforated lids to allow gas ex change. One cup was used for each treatment, maternal parasitoid age, and replicate. The cups containing pupae were kept under the laboratory conditions described above until the emergence of adult parasitoids. The number of male and female parasitoids emerged was recorded daily.

The following parameters were evaluated: (1) parental female productivity, calculated as the average number of live adult offspring (males + females) produced by a parental female (Bautista et al. 1998); (2) fecundity fecundity /fe·cun·di·ty/ (fe-kun´dit-e)
1. in demography, the physiological ability to reproduce, as opposed to fertility.

2. ability to produce offspring rapidly and in large numbers.
, estimated as the average of female offspring by parental females at age, (mx) (Carey 1993); (3) off spring sex ratio, calculated as the number of female offspring divided by the sum of female and male offspring produced by surviving females at age x multiplied by 100; (4) percentage of parasitoid emergence, calculated as the number of adult parasitoids emerged divided by the total number of exposed host larvae; and (5) daily mortality of parental females and males at different female/male densities. Data on adult off spring, percent parasitism, and parental mortality rate were pooled at 2-day maternal age maternal age,
n the age of the mother at the period of conception.
 intervals.

Data Analysis

A completely randomized design was used. A two-way analysis of variance (ANOVA anova

see analysis of variance.

ANOVA Analysis of variance, see there
) with treatment and the maternal age interval as grouping factors was used to analyze the difference in parental female productivity and fecundity, offspring sex ratio, and percentage of adult parasitoid eclosion e·clo·sion  
n.
The emergence of an adult insect from a pupal case or an insect larva from an egg.



[French éclosion, from éclore, to open, from Old French, from Vulgar Latin
. Mean comparisons were analyzed by Tukey's honestly significant difference (HSD HSD Human Services Department
HSD High Speed Data
HSD Hillsboro School District (Hillsboro, OR)
HSD Hybrid Synergy Drive (Toyota/Lexus)
HSD High School Diploma
HSD Historical Society of Delaware
) test at P = 0.05. An arcsine square root transformation was applied to the percentage data to normalize normalize

to convert a set of data by, for example, converting them to logarithms or reciprocals so that their previous non-normal distribution is converted to a normal one.
 their distribution. However, original means ([+ or -] SEM) are used for data presentation. A Kruskal-Wallis one way analysis of variance on ranks and Median comparisons test (P = 0.05) was performed to analyze the difference in the number of parental female and male deaths among treatments and maternal age intervals, because normality and homoscedasticity assumptions were not met and data transformations were unsuccessful.

RESULTS

Overall, the mean live progeny produced by a female during 12 d of life at 1:1 female/male rate was 2.7-, and 4.7- times higher than in high parental female density treatments ([F.sub.2,100] = 170.45, P < 0.0001) (Table 1). A similar trend was re corded for mean fecundity yield by females throughout the 12 d of a test ([F.sub.2,100] = 133.11, P < 0.0001 (Table 1). The overall progeny production (mean [+ or -] SEM) was not different among the 3 parasitoid female/male densities (711.3 [+ or -] 33.6, 791.7 4.8, and 750.3 [+ or -] 11.9 parasitoids at 1:1, 3:1, and 5:1 female/male densities, respectively) ([F.sub.2,6] = 3.75, P = 0.0877). In all 3 female/male ratios evaluated during the 12-d period, both the cumulative fecundity and progeny produced every 2 d in creased significantly after the maternal age interval 1-2 d post eclosion, and did not increase or de crease significantly after parental female age 5-6 d ([F.sub.5,100] = 20.48, P < 0.0001 and [F.sub.5,100] = 18.32, P < 0.0001, respectively) (Table 1). Overall, the mean sex ratio of offspring was not significantly different for all three treatments ([F.sub.2,100] = 0.38, P = 0.6865) (Table 2). Approximately 70% of the total progeny produced were females during the 12-d period at 1:1, 3:1, and 5:1 female/male densities. A male-biased sex ratio was recorded at maternal age interval 1-2 d. Thereafter, offspring sex ratio was female-biased and the female proportion, ranging between 70 and 86%, did not increase or decrease significantly (Table 2).

There was a difference ([F.sub.2,100]) = 206.80, P < 0.0001) in the mean percentage of parasitoid emergence when compared among the 1:1 female/ male density and the highest parental female density treatments (Table 2). Moreover, the analysis of parasitoid emergence showed a highly significant difference between parental female age intervals ([F.sub.5,100]) = 40.21, P < 0.0001). In all treatments, the parasitoid emergence produced by 1-2 d-old females was significantly lower than in older maternal ages (Tukey test, P < 0.05) (Table 2). The highest percentage of parasitoid emergence was recorded for 7-8-d-old females in 1:1, 3:1 and 5:1 female/male ratios, although there was no significant difference (Tukey test, P < 0.05) with lower maternal age intervals (3-4 and 5-6 d old) nor with higher maternal age intervals (9-10 and 11-12 d old) (Table 2). There was a significant difference (H (2, n = 108) = 17.95, P < 0.0001) in the total number of parental female deaths at end of the 12-d period between the different female/male densities. Approximately, 3 and 12 times as many females died at the 3:1 and 5:1 female/male densities, respectively, as compared to the 1:1 female/male density (0.06 [+ or -] 0.04 females). Thus, there was no significant difference between the observed and expected number of female deaths at the 3:1 female/ male density, but a greater number of females died at the 5:1 female/male ratio than would be expected ([chi square chi square (kī),
n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies.
] = 16.71, df = 2, P = 0.0002). On the contrary, changes in female/male densities did not significantly influence the total number of parental male deaths (H (2, n = 108) = 2.14, P = 0.3428). The number of males dead at the 3:1 and 5:1 female/male densities only was 1.3 and 2.3 times the number occurring at the 1:1 female/male density (0.22 [+ or -] 0.09 females, mean [+ or -] SEM), respectively. There was no significant difference in the number of female deaths among maternal age intervals at the 1:1, 3:1 and 5:1 female/male densities (H (5, n = 36) = 4.12, P = 0.35326; H (5, n = 36) = 4.67, P = 0.4579; H (5, n = 36) = 11.5, P = 0.0574, respectively).

DISCUSSION

Our results indicated that providing the experimental rearing cages with higher numbers than 20 parental females did not affect the sex ratio of their offspring nor did it result in significantly greater progeny production, or fecundity. Female biased progeny resulted in all tests from parasitoid females older than 2 d in agreement with observations by Ashley & Chambers (1979) on D. longicaudata parasitizing Anastrepha suspensa (Loew). These authors worked with 3 different parental parasitoid densities in the rearing cages but a 1:1 female/male ratio was always maintained. On the other hand, Ramadan et al. (1994) indicated that the female offspring of Fopius arisanus (Sonan), an opiine egg parasitoid of tephritid flies, was influenced by changes in the pa rental parasitoid density when eggs of Bactrocera dorsalis (Hendel) were exposed to different parasitoid female/cage densities. However, these authors pointed out that the offspring sex ratios al ways favored males. With exception of recorded data by Baeza Larios et al. (2002), female-biased sex ratios in populations of D. longicaudata have been recorded in the field on Bactrocera correcta (Bezzi) in Central Thailand (Kitthawee 2000), under conditions of mass-rearing on B. dorsalis (Wong & Ramadan 1992; Wong 1993; Messing et al. 1993; Purcell et al. 1994; Vargas et al. 2002) and on Anastrepha ludens (Loew) (Cancino et al. 2002a,b; Montoya et al. 2000a,b; Cancino & Montoya 2004; Gonzalez et al. 2007), and from laboratory rearing on A. suspensa (Greany et al. 1976; Ashley & Chambers 1979), on Bactrocera papayae Drew & Hancock (Petcharat & Petcharat 1997), on Anastrepha obliqua (Macquart) and A. ludens (Eben et al. 2000), on C. capitata (Ovruski et al. 2003), on both wild and genetic sexing strains of C. capitata (Viscarret et al. 2006), and on Anastrepha fraterculus (Wiedemann) (Ovruski et al. 2007).

In contrast to our data, Viscarret et al. (2006) found no influence of D. longicaudata female age on sex ratio of progeny obtained from C. capitata puparia. It is possible that the difference between the data of Viscarret's et al. (2006) and our data might be due to the distinct preoviposition and oviposition periods of the D. longicaudata females recorded, as was noted by Avilla & Albajes (1984), in the opiine P. concolor reared on C. capitata and Bactrocera oleae Gmel. During the preoviposition period, D. longicaudata females tend to mate and to mature ovarian eggs (Wong & Ramadan 1992). Nevertheless, emerged females during the first 24 h have been recorded ovipositing, but with few off spring resulting (Greany et al. 1976), mainly males (Ashley & Chambers 1979). Viscarret et al. (2006) reported preoviposition and oviposition periods of approximately 3-4 d and 23-28 d, respectively, while we only recorded offspring sex ratios throughout the 12-d oviposition period. In general, short oviposition periods for D. longicau-data, which ranged between 9 and 16 d, have been reported in the literature (Ashley & Chambers 1979; Wong & Ramadan 1992; Vargas et al. 2002). Changes in the offspring sex ratios as the parental female aged have been reported in other opiine larval parasitoid species, such as P. fletcheri (Wong & Ramadan 1992; Wong 1993), Diachasmi morpha tryoni (Cameron) (Ramadan et al. 1989a,b; Wong et al. 1990; Wong & Ramadan 1992), and in the opiine egg parasitoid F. arisanus (Ramadan et al. 1994; Bautista et al. 1998). In general, newly emerged females as well as older females produce male-biased sex ratios (Wong et al. 1990).

The offspring sex ratio biased toward females in D. longicaudata found in the present study may reflect the fertilization of parasitoid eggs as a result of successful mating irrespective of the parental female/male ratio; or/and may indicate differential survival of the sexes during parasitoid post-embryonic development; or/and may reveal a greater number of female eggs deposited in the presence of conspecifics. These hypotheses have been documented as probable factors influencing offspring sex ratios (King 1993; Godfray 1994; He impel im·pel  
tr.v. im·pelled, im·pel·ling, im·pels
1. To urge to action through moral pressure; drive: I was impelled by events to take a stand.

2. To drive forward; propel.
 & Lundgren 2000). Other possible explanations could involve genetic mechanisms such as the presence of high sex allele allele (əlēl`): see genetics.
allele

Any one of two or more alternative forms of a gene that may occur alternatively at a given site on a chromosome.
 diversity within the laboratory culture of D. longicaudata, as was documented by Heimpel & Strand (1999) and Antolin et al. (2003) for a commercial mass rearing culture of the braconid, Habrobracon hebetor Say. Recently, superparasitism has also been proposed to explain the presence of female biased sex ratio in D. longicaudata, especially at high parasitoid female/rearing cage densities (Gonzalez et al. 2007).

Our results showed that more D. longicaudata females inside rearing cages without varying the parasitoid female of C. capitata larvae ratio did not significantly increase the overall offspring production, nor was the percentage of adult parasitoid emergence favored. Moreover, we showed that the highest parasitoid female productivity and fecundity were found at 1:1 female/male per cage density whereas the lowest productivity and fecundity were recorded at 5:1 female/male ratio. These results could be attributed to negative effects of overcrowding parental females inside experimental rearing cages at the upper parasitoid densities, such as: (1) a higher prevalence of aggressive local competition among females for sites on the parasitization unit (Ashley & Chambers 1979; Ramadan et al. 1994), which can affect their habitual oviposition behavior (Lawrence 1978); (2) a significantly greater number of parental female deaths (Ashley & Chambers 1979); and (3) a extremely higher host larvae mortality produced by the parasitoid females (Montoya et al. 2000b; Gonzalez et al. 2007). Our data and personal observations correspond well with both the first and second assumptions. Although in the current study the percentage of host larval mortality did not occur because irradiated C. capitata larvae were used as hosts for parasitoids, our results on parasitoid emergence suggest, in agreement with Montoya et al. (2000b) and also with the previous Ashley & Chambers' (1979) data, that a low parasitoid female/cage density should be maintained to optimize the production of D. longicaudata.

In conclusion, the results of the current study on progeny production efficiency of D. longicau data females may facilitate the advancement of an optimum mass-rearing system using C. capitata for this parasitoid species in Brazil. Nonetheless, as previously recommended by Montoya et al. (2000b) and more recently by Gonzalez et al. (2007), additional improvements in mass rearing process of D. longicaudata, particularly directed at the assessment of the parasitoid/host larvae proportion, host exposure time, and size of host exposure area, are needed to get an efficient large scale production of this fruit fly parasitoid. Thus, the host exposure period should be mainly chosen according to the parasitoid female/host ratio, which is correlated with the parental female age (Ramadan et al. 1989b). Furthermore, the quality of host larvae (e.g. size, age, and instars) must be cautiously controlled to achieve successful laboratory or factory mass rearing of D. longicaudata as pointed out by Wong & Ramadan (1992).

ACKNOWLEDGMENTS

We express our gratefulness to Donald McInnis for reviewing the original manuscript. Financial support was provided by the FINEP (2660/05)-Brazil, Banco do Nordeste (BNB BNB Bed 'n Breakfast
BNB Banco do Nordeste do Brasil (Brazil)
BNB Banque Nationale de Belgique
BNB Bulgarian National Bank
BNB British National Bibliography
BNB Bad News Bears (movie) 
)-Brazil, and CONICET CONICET Consejo Nacional de Investigaciones Científicas Y Técnicas (National Council for Science and Technology, Argentina)  Argentina (Grant PIP No. 5129/05).

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JACKSON, D. M., S. F. NOTTINGHAM, W. S. SCHLOTZHAU ER, R. J. HORVAT, V. A. SISSON, M. G. STEPHENSON, T. FOARD, AND R. M. MCPHERSON. 1996. Abundance of cardiochiles nigriceps (Hymenoptera: Braconidae) on Nicotiana nicotiana (nĭkō'shēā`nə), any plant of the genus Nicotiana of the family Solanaceae (nightshade family). Most species are herbs native to tropical America, although there are a few North American species and several  species (Solanaceae). Environ. Entomol. 25:1248-1255.

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LAWRENCE, P. O., P. D. GREANY, J. L. NATION, AND R. M. BARANOWSKI. 1978. Oviposition behavior of Biosteres longicaudatus, a parasite of the Caribbean fruit fly Anastrepha suspensa. Ann Entomol. Soc. America 17:253-265.

LOPES, F. S. C., AND B. A. J. PARANHOS. 2006. Criacao do parasit6ide Diachasmimorpha longicaudata (Hymenoptera: Braconidae) sobre larvas de Ceratitis capitata (Diptera: Tephritidae) linhagem tsl Vienna 8, pp. ,107-114 In JORNADA DE INICIAQAO CIENTIFICA DA EMBRAPA EMBRAPA Empresa Brasileira de Pesquisa Agropecuária (Brazilian Agricultural Research Corporation)  SEMI-ARIDO, 1., 2006, Petrolina. Embrapa Semi-Arido, 2006. (Embrapa Semi-Arido. Documentos, 197).

LOZANO, C., N. A. C. MDD MDD Major depressive disorder, see there , M. A. JERVIS, AND M. CAM POS (1) See point of sale and packet over SONET.

(2) "Parent over shoulder." See digispeak.

POS - point of sale
. 1997. Effects of parasitoid spatial heterogeneity, sex ratio and mutual interference on the interaction between the olive bark beetle Phloeotribus scarabaeoides (Col., Scolytidae) and the pteromalid parasitoid Cheiropachus quadrum (Hym., Pteromalidae). J. Appl. Entomol. 121: 521-528.

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MONTOYA, P., P. LIEDO, B. BENREY, J. CANCINO, J. F. BARRERA, J. SIVINSKI, AND M. ALUDA. 2000a. Biological Control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative re leases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol. Control 18: 216-224.

MONTOYA, P., P. LIEDO, B. BENREY, J. CANCINO, J. F. BARRERA, J. SIVINSKI, AND M. ALUDA. 2000b. Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Ann. Entomol. Soc. America 93(1):47-54.

NISHIMURA, K., AND G. C. JAHN. 1996. Sex allocation of three solitary ectoparasitic wasp species on bean weevil larvae: sex ratio change with host quality and local mate competition. J. Ethology ethology, study of animal behavior based on the systematic observation, recording, and analysis of how animals function, with special attention to physiological, ecological, and evolutionary aspects.  14: 27-33.

ORR, D. B., L C. LEWIS, AND J. J.OBRYCKI. 1994. Behavior and survival in corn plant of Ostrinia nubilalis (Lepidoptera: Pyralidae) larvae when infected with Nosema Nosema /No·se·ma/ (no-se´mah) a genus of intracellular protozoa, including N. ocula´rum, which causes corneal infections.

Nosema

a genus of protozoa in the class Microsporea.
 pyrausta (Microspora: Nosematidae) and parasitized by Macrocentrus grandii (Hymenoptera: Braconidae). Environ. Entomol. 23: 1020-1024.

OVRUSKI, S. M., M. ALUDA, J. SIVINSKI, AND R. WHAR TON. 2000. Hymenopteran parasitoids on fruit--infesting tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Int. Pest Manag. Rev. 5:81-107.

OVRUSKI, S. M., C. COLIN, A. SORIA, L. ORONO, AND P. SCHLISERMAN. 2003. Introducci6n y establecimiento en laboratorio de Diachasmimorpha tryoni y Diachasmimorpha longicaudata (Hymenoptera: Braconidae, Opiinae) para el control biologico de Ceratitis capitata (Diptera: Tephritidae, Dacinae) en la Argentina. Rev. Soc. Entomol. Arg. 62: 49-59.

OVRUSKI, S. M., L. E. ORONO, P. SCHLISERMAN, AND S. NUREZ CAMPERO. 2007. The effect of four fruit species on the parasitization rate of Anastrepha fraterculus (Diptera: Tephritidae, Trypetinae) by Diachasmi morpha longicaudata (Hymenoptera: Braconidae, Opiinae) under laboratory rearing conditions. Biocontrol Science & Technology 17: 1079-1085.

PARANHOS, B. A. J. 2007. Biofabrica Moscamed Brasil: tecnologia ambientalmente segura no combate as pragas. In SIMPOSIO DE MANGA DO VALE DO SAO FRANCISCO, 2., 2007, Juazeiro. Palestras. Petrolina: Embrapa Semi-Arido, 2007. 1 CD-ROM. (Embrapa Semi-Arido. Documentos, 198).

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PETCHARAT, J., AND J. PETCHARAT. 1997. Biology of Diachasmimorpha longicaudata Ashmead (Hymenoptera: Braconidae): a larval-pupal parasitoid of the oriental fruit fly Bactrocera papayae Drew& Hancock. Kaen Kaset Kaen Agricult. J. 25: 30-35.

PURCELL, M. F. 1998. Contribution of biological control to integrated pest management Integrated Pest Management (IPM), planned program that coordinates economically and environmentally acceptable methods of pest control with the judicious and minimal use of toxic pesticides.  of tephritid fruit flies in the tropics tropics, also called tropical zone or torrid zone, all the land and water of the earth situated between the Tropic of Cancer at lat. 23 1-2°N and the Tropic of Capricorn at lat. 23 1-2°S.  and subtropics. Int. Pest Manag. Rev. 3: 63-83.

PURCELL, M. F., C. G. JACKSON, J. P. LONG, AND M. A. BATCHLOR 1994. Influence of guava ripening on parasitism levels of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), by Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) and other parasitoids. Biol. Control 4: 396-403.

QUIMIO, G. M., AND G. H. WALTER 2001. Host preference and host suitability in an egg-pupal fruit fly parasitoid, Fopius arisanus (Sonan) (Hym., Braconidae). J. Appl. Entomol. 125: 135-140.

RAMADAN, M. M., F. CHANG, AND R. H. MESSING. 1994. Influence of parasitoid age, host species, and exposure periods on the reproductive autput of Diachas mimorpha longicaudata (Hymenoptera: Bra conidae), In Abstracts of the 4th International Symposium on Fruit Flies of Economic Importance, Florida, USA.

RAMADAN, M. M., T. T. Y. WONG, AND J. W. BEARDSLEY 1989a. Insectary production of Biosteres tryoni (Cameron) (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitata (Wiedeamann) (Diptera: Tephritidae). Proc. Hawaiian Entomol. Soc. 29:41-48.

RAMADAN, M. M., T. T. Y. WONG, AND J. W. BEARDSLEY 1989b. Survivorship survivorship n. the right to receive full title or ownership due to having survived another person. Survivorship is particularly applied to persons owning real property or other assets, such as bank accounts or stocks, in "joint tenancy. , potential and realized fecundity of Biosteres tryoni (Hymenoptera: Braconidae), a larval parasitoid of Ceratitis capitata (Wiedeamann) (Diptera: Tephritidae). Entomophaga 34: 291-297.

RENDON, P., J. SIVINSKI, T. HOLLER, K. BLOEM, M. LOPEZ, A. MARTINEZ, AND M. ALUJA. 2006. The effects of sterile males and two braconid parasitoids Fopius arisanus (Sonan) and Diachasmimorpha kraussii (Fullaway) (Hymenoptera) on caged population of Mediterranean fruit flies, Ceratitis capitata (Wied.) (Diptera: Tephritidae) at various sites in Guatemala. Biol. Control 36: 224-231.

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LARA Lawsuit Abuse Reduction Act of 2004
LARA Light Armed Reconnaissance Aircraft
LARA Lakeland Agricultural Research Association
LARA Labor Aerospace Research Agenda
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BEATRIZ J. P (1), MARIA DE LOURDES Z. COSTA (2), SERGIO M. OVRUSKI (3), RENATA M. ALVES (4), LUCIMARA BLUMMER (5) AND JULIO M. M. WALDER (2)

(1) Brazilian Agricultural Research Corporation (Embrapa-Tropical Semi-Arid), Laboratory of Fruit Flies, BR 428, km 152, C.P. 23, 56.302-970, Petrolina--PE, Brazil (2) CENA--University of Sao Paulo, Laboratory of Food Irradiation and Radio-Entomology, Av. Centendrio, 303, 13.416-000, C.P. 96, Piracicaba--SP, Brazil (3) PROIMI Biotecnologia--CONICET, Division Control Biologico de Plagas, Laboratorio Moscas de la Fruta, Avda. Belgrano y Pje. Caseros, (T4001MVB MVB Multivesicular Body
MVB Magdeburger Verkehrsbetriebe
MVB Multifunction Vehicle Bus
MVB Multimedia Viewer Book
MVB Multifunctional Vehicle Bus
MVB Moisture Vapor Barrier
MVB Multivibrator
MVB Minimum Variance Beamformer
MVB MicroVax Business
) San Miguel de Tucuman San Mi·guel de Tu·cu·mán   or Tucumán

A city of northern Argentina at the foot of an eastern range of the Andes north-northwest of Córdoba. The country's independence was proclaimed here in July 1816. Population: 833,000.
, Argentina (4) ESALQ- University of Sao Paulo, Department of Entomology entomology, study of insects, an arthropod class that comprises about 900,000 known species, representing about three fourths of all the classified animal species. , Av. Padua Dias, 11, 13.418-900, C.P. 9, Piracicaba-SP, Brazil (5) University of Earth, Departament of Agronomy agronomy (əgrŏn`əmē), branch of agriculture dealing with various physical and biological factors—including soil management, tillage, crop rotation, breeding, weed control, and climate—related to crop production. , Quadra 203- Area Especial Lote 32, Recanto das Emas, Brasilia-DF, Brazil
TABLE 1. OFFSPRING PRODUCTION OF DIACHASMIMORPHA LONGICAUDATA
REARED ON CERATITIS CAPITATA IRRADIATED LARVAE AT DIFFERENT
MATERNAL AGE INTERVALS AND PARASITOID FEMALE/MALE DENSITIES

                           Female productivity
                         (mean [+ or -] SEM)(a)

Maternal age          Female/male densities
intervals
(days)                     1:1                  3:1

1-2               0.07 [+ or -] 0.04 a    0.04 [+ or -] 0.01 a
3-4               0.26 [+ or -] 0.03 b    0.11 [+ or -] 0.01 ab
5-6               0.35 [+ or -] 0.03 c    0.13 [+ or -] 0.02 b
7-8               0.35 [+ or -] 0.01 c    0.14 [+ or -] 0.01 b
9-10              0.38 [+ or -] 0.02 c    0.13 [+ or -] 0.01 b
11-12             0.37 [+ or -] 0.02 c    0.11 [+ or -] 0.01 b
Overall mean(b)   0.32 [+ or -] 0.02 A    0.12 [+ or -] 0.01 B

                   Female productivity           Fecundity
                  (mean [+ or -] SEM)(a)  (mean [+ or -] SEM)(a)

Maternal age      Female/male densities   Female/male densities
intervals
(days)                    5:1                     1:1

1-2               0.02 [+ or -] 0.01 a    0.03 [+ or -] 0.02 a
3-4               0.06 [+ or -] 0.01 b    0.18 [+ or -] 0.03 b
5-6               0.07 [+ or -] 0.01 b    0.28 [+ or -] 0.02 c
7-8               0.08 [+ or -] 0.01 b    0.28 [+ or -] 0.01 c
9-10              0.07 [+ or -] 0.01 b    0.30 [+ or -] 0.02 c
11-12             0.07 [+ or -] 0.01 b    0.29 [+ or -] 0.02 c
Overall mean(b)   0.07 [+ or -] 0.01 C    0.23 [+ or -] 0.02 A

                              Fecundity
                           (mean [+ or -] SEM)(a)

Maternal age               Female/male densities
intervals
(days)                    3:1                     5:1

1-2               0.02 [+ or -] 0.01 a    0.01 [+ or -] 0.01 a
3-4               0.07 [+ or -] 0.01 ab   0.05 [+ or -] 0.01 b
5-6               0.11 [+ or -] 0.01 b    0.06 [+ or -] O.01 b
7-8               0.12 [+ or -] 0.01 b    0.07 [+ or -] O.01 b
9-10              0.10 [+ or -] 0.01 b    0.05 [+ or -] O.01 b
11-12             0.09 [+ or -] 0.01 b    0.05 [+ or -] 0.01 b
Overall mean(b)   0.09 [+ or -] 0.08 B    0.05 [+ or -] 0.01 C

(a) Means in the same row followed by a different capital letter
differ significantly (Tukey's test, P < 0.05).

(b) Means within a column followed by the same small
letter do not differ significantly (Tukey's test, P < 0.05).

TABLE 2. OFFSPRING SEXUAL RATE AND PERCENTAGE OF PARASITOID
EMERGENCE AT DIFFERENT D. LONGICAUDATA FEMALE AGE INTERVALS
AND PARASITOID FEMALE/MALE PROPORTIONS.

                               Sex Ratio (% female
                               progeny) (mean
                               [+ or -] SEM) (a)

Maternal age                   Female/male densities
intervals
(days)                      1:1                     3:1

1-2                24.45 [+ or -] 11.45 a   27.53 [+ or -] 12.46 a
3-4                69.99 [+ or -] 3.02 b    70.01 [+ or -] 2.83 b
5-6                79.64 [+ or -] 2.67 b    82.70 [+ or -] 2.91 b
7-8                77.83 [+ or -] 2.96 b    85.86 [+ or -] 2.63 b
9-10               79.17 [+ or -] 3.21 b    78.97 [+ or -] 3.27 b
11-12              78.67 [+ or -] 2.86 b    74.70 [+ or -] 3.62 b
Overall mean (b)   68.28 [+ or -] 8.89 A    69.94 [+ or -] 8.79 A

                   Sex Ratio (% female      Parasitoid Emergence (%)
                   progeny) (mean           mean [+ or -] SEM) (a)
                   [+ or -] SEM) (a)

Maternal age       Female/male densities    Female/male densities
intervals
(days)                      5:1                     1:1

1-2                30.06 [+ or -] 13.59 a   0.72 [+ or -] 0.37 a
3-4                70.50 [+ or -] 4.62 b    2.58 [+ or -] 0.33 b
5-6                82.22 [+ or -] 2.67 b    3.48 [+ or -] 0.29b
7-8                85.25 [+ or -] 1.73 b    3.78 [+ or -] 0.12 b
9-10               76.82 [+ or -] 2.74 b    3.56 [+ or -] 0.16 b
11-12              79.21 [+ or -] 3.25 b    3.68 [+ or -] 0.21 b
Overall mean (b)   70.68 [+ or -] 8.37 A    2.97 [+ or -] 0.48 A

                               Parasitoid Emergence (%)
                               (mean [+ or -] SEM) (a)

Maternal age                   Female/male densities
intervals
(days)                      3:1                     5:1

1-2                0.38 [+ or -] 0.17 a     0.23 [+ or -] 0.10 a
3-4                0.95 [+ or -] 0.05 ab    0.62 [+ or -] 0.05 b
5-6                1.08 [+ or -] 0.02 b     0.71 [+ or -] 0.05 b
7-8                1.15 [+ or -] 0.01 b     0.83 [+ or -] 0.03 b
9-10               1.07 [+ or -] 0.03 b     0.70 [+ or -] 0.06 b
11-12              0.98 [+ or -] 0.08 b     0.66 [+ or -] 0.17 b
Overall mean (b)   0.94 [+ or -] 0.11 B     0.63 [+ or -] 0.09 B

(a) Means within a column followed by the same letter do not differ
significantly (Tukey's test, P < 0.05).

(b) Means in the same row followed by a different capital letter
differ significantly (Tukey's test, P < 0.05).
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Author:Paranhos, Beatriz J.; De Lourdes Z. Costa, Maria; Ovruski, Sergio M.; Alves, Renata M.; Blummer, Luc
Publication:Florida Entomologist
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Geographic Code:3BRAZ
Date:Dec 1, 2008
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