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Laboratory biological parameters of Trichogramma fuentesi (Hymenoptera: Trichogrammatidae), an egg parasitoid of Cactoblastis cactorum (lepidoptera: pyralidae).

In the late 1980s, a phycitine moth native to South America, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), was found in south Florida (Dodd 1940; Dickel 1991; Zimmermann et al. 2001). The moth has been considered an important ecological and economic threat to Opuntia opuntia

Any plant of the genus Opuntia, the largest genus of the cactus family. Native to the New World, it has characteristic small bristles with backward-facing barbs.
 spp. cactus particularly in the Southwestern U.S. and in Mexico. Current management techniques involve pest population monitoring with sex pheromone pheromone

Any chemical compound secreted by an organism in minute amounts to elicit a particular reaction from other organisms of the same species. Pheromones are widespread among insects and vertebrates (except birds) and are present in some fungi, slime molds, and algae.
 baited traps, field sanitation through removal of infested plants, and area wide control through inundative releases of sterile C. cactorum adult males (Hight hight  
adj. Archaic
Named or called.

[Middle English, past participle of highten, hihten, to call, be called, from hehte, hight, past tense of hoten
 et al. 2005; Bloem et al. 2007). In addition to these management efforts, biological control by egg parasitoids in the genus Trichogramma has been suggested (Bennett & Habeck 1995; Pemberton & Cordo 2001; Logarzo et al. 2008; Paraiso et al. 2011).

Trichogramma spp. are facultative gregarious egg parasitoids that have been used as inundative biological control agents against a wide range of agricultural pests including corn borers, sugarcane borers, and cotton bollworm bollworm, name for the larvae of two different moths. The pink bollworm is a serious pest of cotton, and the corn earworm, or cotton bollworm, attacks cotton, corn, and other crops.  (Li 1994; van Lenteren 2000; Godin & Boivin 2000). Trichogramma wasps are particularly efficient against lepidopteran lepidopteran

Any of the more than 155,000 species constituting the order Lepidoptera (Greek: “scaly wing”): butterflies, moths, and skippers. The name refers to the dusting of minute scales that covers the wings and bodies of these insects.
 pests that lay their eggs in clusters such as the European pine shoot borer (Rhyacionia buoliana Denis & Schiffermuller: Tortricidae), and the European corn borer (Ostrinia nubilalis Hiibner: Pyralidae) (Dahlsten & Mills 1999; Kogan et al. 1999).

Previous surveys for natural enemies in North Florida led to the discovery of T. pretiosum (Riley) and T. fuentesi Torre attacking C. cactorum (Paraiso et al. 2011). Inundative releases of several Trichogramma spp., such as T. exiguum Pinto & Platner against heliothine pests of cotton (Suh et al. 2000), or against the Nantucket pine tip moth (Rhyacionia frustrana (Comstock): Tortricidae) in Virginia pine (Pinus virginiana Mill.) (Philip et al. 2005), have failed to provide an adequate level of pest suppression. Therefore, prior to field release it is important to undertake detailed studies of biological and ecological characteristics of prospective agents (van Lenteren et al. 2003; Dannon et al. 2010). Some of the important characteristics that need to be studied to optimize rearing conditions and release strategy of T. fuentesi against C. cactorum include: sex ratio, longevity, and influence of parasitoid par·a·sit·oid  
Any of various insects, such as the ichneumon fly, whose larvae are parasites that eventually kill their hosts.

Of or relating to a parasitic insect of this kind.
 and host age on parasitism parasitism: see parasite.

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
 and 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.

Trichogramma wasps require a source of carbohydrate to maintain basic physiological activities (Romeis et al. 2005). Generally, raisins and pure or diluted honey are used in experimental studies as a source of food to maintain Trichogramma adult rearing cultures (Morrison 1985). The presence and nutritional quality of a supplemental source of food have been reported to increase the longevity of Trichogramma spp. (Laetimia et al. 1995; Oliveira et al. 2003). In addition, a source of carbohydrate can, in some cases, influence fecundity and egg resorption resorption /re·sorp·tion/ (re-sorp´shun)
1. the lysis and assimilation of a substance, as of bone.

2. reabsorption.

 in parasitoids (Heimpel et al. 1997). Female parasitoid age is another biological characteristic that can affect the success of an inundative biological control agent (Amalin et al. 2005). Studies have shown that trichogrammatids under or over a certain age are not able to parasitize par·a·sit·ize
To live on or in a host as a parasite.


to live on or within a host as a parasite.
 their hosts (Rajapakse 1992; Amalin et al. 2005). Host age also impacts the level of parasitism since trichogrammatid parasitoids favor young host eggs (Sequeira & Mackauer 1988; Amalin et al. 2005), and younger hosts generate parasitoid offspring that are characterized by greater fitness (Sequeira & Mackauer 1994).

In the present study, we examined the influence of 3 types of supplemental food sources on the longevity of T. fuentesi in the laboratory. In addition, optimum age for oviposition oviposition

the act of laying or depositing eggs.
 by female T. fuentesi was assessed in order to furnish information for optimizing inundative releases against C. cactorum. This paper provides information on the influence of supplemental food sources, parasitoid female age, mating and host age on parasitism rates, number of parasitoid progeny, number of emerged parasitoid per parasitized eggs, and sex ratio.


Rearing Procedures and General Methods

Experiments were conducted at the USDA-Agricultural Research Service and the Florida A&M University Center for Biological Control laboratory in Tallahassee, Florida. Trichogramma fuentesi females used in the study came from a rearing colony originating from field collected material. Species identity was confirmed by DNA DNA: see nucleic acid.
 or deoxyribonucleic acid

One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes.
 ITS 2 sequences performed by Dr. R. Stouthamer (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. , University of California, Riverside The University of California, Riverside, commonly known as UCR or UC Riverside, is a public research university and one of ten campuses of the University of California system. , California). Cactoblastis cactorum eggs derived from a colony maintained on artificial diet were used as hosts during parasitoid rearing and for the experiments. To culture T. fuentesi, host eggsticks were glued on note card strips (4 x 2 cm) with non-toxic carpenter's glue (Elmer's[R] glue, Elmer's Products Inc., Columbus, Ohio). The note card strips were placed into plastic petri dishes (9 x 2 cm) lined with filter paper (Ahlstrom[R], Mt. Holly Springs, Pennsylvania). A fresh raisin was glued on a 1 x 1 cm note card in the center of each petri dish pe·tri dish
A shallow circular dish with a loose-fitting cover, used to culture bacteria or other microorganisms.

Petri dish

a shallow, circular, glass or disposable plastic dish used to grow bacteria on solid media such as agar.
 to provide a supplemental source of food to emerging wasps. Petri dishes were sealed with parafilm[R] (Pechiney-Plastic Packaging, Menasha, Wisconsin) and arranged on plastic trays lined with moist wipes to increase relative humidity relative humidity
The ratio of the amount of water vapor in the air at a specific temperature to the maximum amount that the air could hold at that temperature, expressed as a percentage.
 to 60-80% RH. The cultures were maintained in a growth chamber at 28 [+ or -] 1 [degrees]C, 16:8 h L:D. Additional growth chambers maintained at 25 [+ or -] 1 [degrees]C, 16:8 h L:D and 60-80% RH were used for incubation of experimental units in all experiments. At 25 [+ or -] 1 [degrees]C, C. cactorum eggs require an average of 26 d to hatch (McLean et al. 2006).

Effect of Presence and Type of Diet on Female Parasitoid Longevity

We tested the effect of no supplemental source of food, presence of undiluted honey, or presence of raisins on the longevity of female parasitoids. Individual, newly emerged (0-24 h-old) T. fuentesi females were collected from the rearing colony and placed in a plastic petri dish (3.5 x 1 cm) lined with filter paper (Ahlstrom[R], Mt. Holly Springs, Pennsylvania). A source of food consisting of either a drop of honey or a raisin was added to the center of each container. A set of control petri dishes did not have any supplemental source of food. Petri dishes were sealed with parafilm and arranged on a plastic tray lined with moist paper wipes to maintain the relative humidity. The containers were incubated and checked daily until all females died. Each treatment was replicated 20 times.

Influence of Female Parasitoid Age and Mating Status on Parasitism

The effect of female parasitoid age on percentage of host eggs parasitized was tested for wasps ranging from 2-6 d old. One-d old unmated female parasitoids were isolated from the rearing colony and individually transferred to petri dishes (3.5 x 1 cm) lined with filter paper, as described above. In addition, newly emerged (0-24 h) females and males were collected from the rearing colony and stored in a petri dish for 24 h to allow mating. Mated and unmated females were transferred individually into petri dishes (3.5 x 1 cm) lined with filter paper. The experimental arena did not have a source of food for the wasps. Adult female parasitoids, without food, lived an average of 4 d (data from above Experiment). Eggsticks were replaced daily until the females were 5 d old. Petri dishes were sealed with parafilm and arranged on a plastic tray lined with moist paper wipes and incubated at 25 [+ or -] 1 [degrees]C, 16:8 h L:D and 60-80% RH. Individual females were exposed to 60, 2-d old, C. cactorum eggs. The experiment was replicated 20 times. The number of parasitized eggs was determined on a daily basis and the rates of parasitism for these mated females were compared against unmated.

Influence of Host Age on Percent Parasitism

Cactoblastis cactorum females lay an average of 70-90 eggs/eggstick (Zimmermann & Perez-Sandi 2006). Eggs hatch in approximately 3 wk (Zimmermann et al. 2001). A no-choice experimental design was used to assess the influence of 10 different C. cactorum host age groups (1, 6, 7, 9, 11, 12, 13, 14, 15, and 20 d old). Three day old, randomly chosen, honey-fed, mated female parasitoids were isolated from the rearing colony and each placed in an individual petri dish (3.5 x 1 cm) lined with filter paper. Sixty host eggs belonging to one of the different age groups were placed in the center of each petri dish. Eggsticks were removed after 48 h and individually transferred into plastic cups (30 mL) for 10 d to allow all parasitoids to emerge. Each treatment was replicated 20 times and the percent parasitism, total number of emerged parasitoids, number of emerged parasitoids per parasitized eggs, and sex ratio were determined.

Statistical Analysis

The effect of presence and type of diet on female parasitoid longevity and influence of host age on number of egg parasitized by T. fuentesi were analyzed by analysis of variance (PROC (language) PROC - The job control language used in the Pick operating system.

["Exploring the Pick Operating System", J.E. Sisk et al, Hayden 1986].
 ANOVA anova

see analysis of variance.

ANOVA Analysis of variance, see there
 & PROC GLM GLM Global Language Monitor
GLM Global Marine (stock symbol)
GLM Graduated Length Method (ski instruction)
GLM Good Looking Mom (used in pediatric practices)
GLM God Loves Me
). In addition, the effect of host egg age on level of parasitism, number of progeny, number of successfully emerged eggs, and percentage of females produced was analyzed by polynomial polynomial, mathematical expression which is a finite sum, each term being a constant times a product of one or more variables raised to powers. With only one variable the general form of a polynomial is a0xn+a  regression. A logistic regression was used to analyze the effect of T. fuentesi age and whether the female wasp was mated or unmated on the level of parasitism. A one way analysis of variance (PROC LOGISTIC) with Firth correction was applied to the proportion of eggs parasitized by T. fuentesi. Comparison of the number of eggs parasitized versus mated and unmated T. fuentesi females at each age was evaluated using Tukey least mean comparison test. A Bonferroni approach was used to adjust the alpha value for the pairwise comparisons. The SAS (1) (SAS Institute Inc., Cary, NC, A software company that specializes in data warehousing and decision support software based on the SAS System. Founded in 1976, SAS is one of the world's largest privately held software companies. See SAS System.  Statistical Software Version 9.2 (SAS Institute, Cary, North Carolina North Carolina, state in the SE United States. It is bordered by the Atlantic Ocean (E), South Carolina and Georgia (S), Tennessee (W), and Virginia (N). Facts and Figures

Area, 52,586 sq mi (136,198 sq km). Pop.
) was used to perform the statistical analyses.


Effect of Presence and Type of Diet on Female Parasitoid Longevity

The provision of a food supplement had a significant influence on the survival of female parasitoids as indicated for each food source. Without a supplemental food source, females survived the shortest period; an average of 4 [+ or -] 0.58 d (F = 23.14, df = 1, 12, P < 0.001, [R.sup.2] = 0.85). Females supplied with a raisin or honey supplement lived for 8 [+ or -] 0.07 d (F = 595.03, df = 1, 12, P < 0.001, [R.sup.2] = 0.99) and 11 [+ or -] 0.79 d (F = 670.73, df = 1, 12, P < 0.001, [R.sup.2] = 0.99), respectively. Type of food (raisin or honey) significantly affected the longevity of female parasitoids (F = 43.20, df = 2, 57, P < 0.001, [R.sup.2] = 0.60). The longest survival time was 16 d for a female fed honey.

Influence of Female Parasitoid Age and Mating Status on Percent Parasitism

The number of parasitized eggs varied significantly with female parasitoid age (F = 20.86, df = 4, 190, P < 0.0001). The number of parasitized eggs was the highest for 2 and 3 d old female parasitoids and declined rapidly thereafter (Table 1). In addition, successful parasitism increased when females were mated (F = 21.14, df = 1, 190, P < 0.0001). Unmated females had none to a low level of parasitism after the third day. In contrast, parasitized eggs were still recovered after the fifth day with mated females (Table 1).

Influence of Host Age on Percent Parasitism

Numbers of eggs parasitized and emerged parasitoids per eggstick declined with age of host eggs (F = 19.53, df = 3, 196, P < 0.0001; and F = 16.53, df = 3, 196, P < 0.0001, respectively) (Table 2). The relationship between host egg age and the number of eggs parasitized was best represented by a cubic polynomial equation (y = 4.81 - 1.02x + 0.074[x.sup.2] - 0.0018[x.sup.3], [R.sup.2] = 0.23). Trichogramma fuentesi displayed a preference for 1 d old host eggs, and the highest level of parasitism and number of progeny produced was recorded for 1 d old host eggs. Female parasitoids did not produce any progeny in host eggs older than 14 d (Table 2). A cubic polynomial equation also described the relationship between egg age and the number of parasitoids that emerged (y = 16.17 - 3.56x + 0.27[x.sup.2] - 0.0065[x.sup.3], [R.sup.2] = 0.20). However, host egg age did not have a significant influence on the sex ratio or on the total number of parasitoids emerging per parasitized egg (Table 2). Although polynomial regression revealed significant relationships between host egg age and the number of parasitized eggs and the number of parasitoids per eggstick, only about 20% of the variation in the data was explained by our models. The high significance lends credibility to the reality of the influence of host egg age, but additional factors are important in explaining the variation in our data.


This study provides information on the biological parameters of T. fuentesi, a potential inundative biological control agent for C. cactorum. Although there is considerable amount of information on the biology of some Trichogramma spp., little is known on this particular species. Trichogramma fuentesi has been recorded in the neotropics including Argentina, Colombia, Mexico, Peru, and Venezuela and in several U.S. states (Alabama, California, Florida, Louisiana, New Jersey, South Carolina South Carolina, state of the SE United States. It is bordered by North Carolina (N), the Atlantic Ocean (SE), and Georgia (SW). Facts and Figures

Area, 31,055 sq mi (80,432 sq km). Pop. (2000) 4,012,012, a 15.
, and Texas) (Fry 1989; Pinto 1999). Its primary hosts are mainly noctuid species (Fry 1989; Wilson & Durant 1991; Pintureau et al. 1999; Querino & Zucchi 2003). Trichogramma wasps require sugar as a source of energy to sustain major physiological processes (Romeis et al. 2005). In nature, Trichogrammatids may obtain sugar from floral nectar, extra-floral nectar, honeydew, and plant sap (Wackers 2005). Food deprived parasitoids will first search for food resources before they search for hosts (Hegazi et al. 2000). In addition, sugar feeding influences overall individual flight, foraging behavior (Forsse et al. 1992; Pompanon et al. 1999; Romeis et al. 2005), and longevity (Oliviera et al. 2003). Hegazi et al. (2000) observed that honey-deprived T. cacoeciae Marchall only attacked one host patch whereas fed females were more likely to move to a second host egg patch. Females without supplemental sources of food in our study never lived more than 5 d while fed females lived an average of 11 d on honey and 8 d on raisin. Honey contains proteins, enzymes, fructose fructose (frŭk`tōs), levulose (lĕv`yəlōs'), or fruit sugar, simple sugar found in honey and in the fruit and other parts of plants. , glucose, and amino acids (Vela vela

plural of velum.
 et al. 2007). The main sugars of raisins are fructose and glucose with minimal amounts of sucrose. They are a good source of vitamins, minerals, and phytochemicals (Williamson & Carughi 2010). Although a comparison of nutritional quality was not done between the different types of food to document their influence on insect physiology, the difference in longevity may be explained by the greater accessibility of carbohydrates in honey compared with raisin.

Various studies have shown that the age of parasitoids can affect the level of parasitism (Hentz 1998; Honda & Kainoh 1998). This information is important in deciding at what age parasitoids should be released in the field to obtain a significant level of parasitism (Amalin et al. 2005). The highest level of parasitism was observed in 2 d old unmated parasitoids and 2-3 d old mated females (Table 1). The level of parasitism decreased after the third d until the death of the parasitoids. Mating status (mated or unmated) may affect oviposition behavior of parasitoids (Hardy et al. 2007). In our study, the percent parasitism did not significantly increase for mated females except for 3 d old females (Table 1). The 2 d old mated and unmated females parasitized the same number of eggs (Table 1). Therefore, inundative releases of 2 d old mated T. fuentesi females should be used against C. cactorum eggs to increase control levels.

A range of ages of C. cactorum eggs coexist in the field during the flight period. Trichogramma spp. generally prefers younger host eggs (Godin & Boivin 2000; Takada et al. 2000). The number of Trichogrammatid progeny decreases significantly with older host eggs (Miura & Kobayashi 1998; Takada et al. 2000) due to depletion of essential nutrients (Ruberson & Kring 1993) or host embryo cephalic cephalic /ce·phal·ic/ (se-fal´ik) pertaining to the head, or to the head end of the body.

1. Of or relating to the head.

 capsule sclerotization (Guang & Oloo 1990). In our study, the highest level of parasitism and number of parasitoid progeny was observed on 1 d old host eggs (Table 2). The number of eggs parasitized decreased as the host eggs age increased. Trichogramma fuentesi females did not parasitize C. cactorum eggs older than 13 d old (Fig. 1). Although sex allocation was not influenced by host age, female-biaised progeny were observed in all experimental treatments (Table 2). Female Trichogramma preferentially lay a higher percentage of females in younger host eggs due to their implication with higher fitness.


Our results showed that honey must be provided in mass reasing programs to establish a sustainable population of T. fuentesi in the laboratory. Two to 3 d old mated T. fuentesi females should be released in the field to obtain a significant level of parasitism. Trichogramma fuentesi displayed a preference for younger host eggs. Therefore, the inundative releases of this egg parasitoid should be timed to coincide with the beginning of C. cactorum oviposition period and/or frequent releases made to attack newly layed C. cactorum eggs.


We thank Shalom Benton (FAMU FAMU Florida Agricultural and Mechanical University
FAMU Federación Argentina de Mujeres Universitarias (Spanish)
FAMU Federation of Australian Maritime Unions
FAMU Fault Alarm Monitor Unit
) for field collection and laboratory assistance, Chris Albanese, Michael Getman, and John Mass (USDA-ARS-CMAVE, Tallahassee) for field assistance, and Susan Drawdy and Robert Caldwell (USDA-ARS-CPMRU, Tifton) for an ample supply of cactus moth eggsticks. This work is funded under the FAMU, USDA-APHIS Cooperative Agreement, 07-10-8100-0755-CA. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.


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OULIMATHE PARAISO (1), STEPHEN D. HIGHT (2), MOSES Moses (mō`zĭs), Hebrew lawgiver, probably b. Egypt. The prototype of the prophets, he led his people in the 13th cent. B.C. out of bondage in Egypt to the edge of Canaan.  T. K. KAIRO (1), STEPHANIE BLOEM (3), JAMES E. CARPENTER (4) AND STUART REITZ (2)

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(2) USDA-ARS, Center for Medical Agricultural and Veterinary Entomology, Tallahassee, FL 32308

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(4) USDA-ARS, Crop Protection and Management Research Unit, Tifton, GA 31793

Age of Female T. Mean # of Eggs Parasitized ([+ or -] S.E.) *
fuentesi (Days)
n = 20

                          Mated                   Unmated

2                  5.4 [+ or -] 0.97 a A   4.0 [+ or -] 1.06 a A
3                  5.9 [+ or -] 1.39 a A   1.8 [+ or -] 0.78 b B
4                  2.8 [+ or -] 0.75 b A   0.0 [+ or -] 0.05 c B
5                  0.9 [+ or -] 0.65 c A   0.0 [+ or -] 0.00 c B
6                  0.0 [+ or -] 0.00 d A   0.0 [+ or -] 0.00 c A

* Means with different lower case letter in columns or capital
letter in rows are significantly different according to Tukey's
Least Mean Comparison test at P < 0.002.


Age of                 Mean # ([+ or -] S.E.) *
Host (Days)

               Eggs Parasitized           Emerged

1             4.0 [+ or -] 1.28 a   13.2 [+ or -] 4.70 a
6             0.5 [+ or -] 0.25 b   2.0 [+ or -] 0.89 b
7             0.6 [+ or -] 0.43 b   1.0 [+ or -] 0.55 b
9             0.8 [+ or -] 0.34 b   2.8 [+ or -] 1.43 b
11            0.3 [+ or -] 0.21 b   1.4 [+ or -] 0.82 b
12            0.3 [+ or -] 0.15 b   1.6 [+ or -] 0.87 b
13            0.2 [+ or -] 0.20 b   0.6 [+ or -] 0.65 b
14            0                     0
15            0                     0
20            0                     0

Age of             Mean # ([+ or -] S.E.) *
Host (Days)

                   Emerged          % Females
               Parasitized Egg

1             3.4 [+ or -] 0.80   60 [+ or -] 14
6             5.5 [+ or -] 1.34   98 [+ or -] 2
7             2.0 [+ or -] 0.58   50 [+ or -] 29
9             3.3 [+ or -] 0.75   50 [+ or -] 0
11            5.8 [+ or -] 1.17   81 [+ or -] 9
12            6.5 [+ or -] 2.73   71 [+ or -] 5
13            3.2 [+ or -] 0.00   85 [+ or -] 0
14            -                   -
15            -                   -
20            -                   -

* Means within a column with different letters are
significant according to Tukey's Least Mean Comparison
test at P < 0.05. Since no significant relationship was
found between age of host egg and number of parasitoids
per parasitized egg or percent females, means were not
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Author:Paraiso, Oulimathe; Hight, Stephen D.; Kairo, Moses T.K.; Bloem, Stephanie; Carpenter, James E.; Rei
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2012
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