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Hymenopteran parasitoids of Anastrepha fruit flies (Diptera: Tephritidae) reared from different hosts in Yucatan, Mexico.



Abstract

In order to carry on the detection and species inventory of hymenopteran parasitoids associated with fruit flies, we examined various tropical fruits growing at the Southern region of Yucatan. During a yearly cycle (Jun 2000 to Jun 2001), 9 host fruit species (including some varieties) were collected by 2 different methods. The first method involved weekly collection of ripened fruits that were transported to the laboratory ("Fruit-Lab"); and the second method was collection of fruits placed on the ground below the tree canopy ("Fruit-Beds"), and which remained in the field for two weeks, after which they were transported to the laboratory. Fruits obtained were counted and weighed, and the recovered pupae were quantified for each sample. As a whole, we sampled 4,470 fruits (850.8 Kg) from the 9 host plant species and varieties, which were infested in·fest  
tr.v. in·fest·ed, in·fest·ing, in·fests
1. To inhabit or overrun in numbers or quantities large enough to be harmful, threatening, or obnoxious:
 by 5 fruit fly species: Anastrepha ludens (Loew), A. obliqua (Macquart), A. serpentina (Wiedemann), A. striata Striata is an application software developer and service provider focused on significantly reducing the cost of traditional bill delivery. Striata provides secure, electronic document delivery by email, fax or SMS.  Schiner, and A. fraterculus (Wiedemann). The average 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
 in all samples was 3.69% represented by 11 hymenopteran species as follows: Braconidae, Doryctobracon areolatus (Szepligeti), and Opius bellus (Gahan); Figitidae, Aganaspis pelleranoi (Brethes), Aganaspis sp., Odontosema anastrephae Borgmeier and Odontosema sp.; Diapriidae, Coptera haywardi (Oglobin); Chalcididae, Dirhinus sp.; Pteromalidae, Spalangia endius Walker; Eurytomidae, Sycophila sp.; and Perilampidae, Euperilampus sp. On the basis of results in differences among samples for parasitism rates, fruit fly 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.
, and fruit fly host plant, parasitoid assemblages are analyzed and discussed.

Key Words: parasitism, fruit flies, host plants, natural enemies

Resumen

Con el proposito de realizar la deteccion e inventario de especies de parasitoides asociados con moscas de la fruta, se examinaron diversos frutos tropicales cultivados en la region Sur del estado de Yucatan. Durante el ciclo anual comprendido entre junio de 2000 a junio de 2001, se estudiaron nueve especies y variedades de frutos de la region, empleando dos metodos de colecta: el primero pri·me·ro  
n.
A gambling card game, popular in Elizabethan England.



[Alteration of Spanish primera, feminine of primero, first, from Latin
 se realizo por medio de la colecta semanal de frutos maduros transportados al laboratorio ("Fruit-Lab"); y el segundo El Segundo (ĕl sēgŭn`dō), industrial city (1990 pop. 15,223), Los Angeles co., S Calif., on Santa Monica Bay; inc. 1917. Its products include navigation and computer systems, aircraft parts, office machines, telephone apparatus, and  mediante la recoleccion de camas de frutos ("Fruit-Beds") colocados en el suelo bajo la cobertura de los arboles, los cuales permanecieron por dos semanas, y posteriormente trasladados al laboratorio. En ambos casos, los frutos fueron contados y pesados, ademas de la cuantificacion de pupas recuperadas en cada muestra. En total se recolectaron 4,470 frutos (850.8 Kg) de las nueve especies y variedades de plantas hospederas, las cuales resultaron infestadas por cinco especies de moscas de la fruta: Anastrepha ludens (Loew), A. obliqua (Macquart), A. serpentina (Wiedemann), A. striata Schiner, y A. fraterculus (Wiedemann). La proporcion de parasitismo en todas las muestras fue de 3.69% representado por 11 especies de himenopteros de las siguientes familias: Braconidae, Doryctobracon areolatus (Szepligeti), y Opius bellus (Gahan); Figitidae, Aganaspis pelleranoi (Brethes), Aganaspis sp., Odontosema anastrephae Borgmeier, and Odontosema sp.; Diapriidae, Coptera haywardi (Oglobin)); Chalcididae, Dirhinus sp.; Pteromalidae, Spalangia endius Walker; Eurytomidae, Sycophila sp.; and Perilampidae, Euperilampus sp.. Con base en estos resultados, se analizan y discuten las diferencias entre los indices de parasitismo, asi como entre los ensambles mosca- parasitoide y planta hospedera-parasitoide.

Translation provided by the authors.

**********

Diverse regional studies in Latin America Latin America, the Spanish-speaking, Portuguese-speaking, and French-speaking countries (except Canada) of North America, South America, Central America, and the West Indies.  have addressed the incidence of native parasitoids of the genus Anastrepha in countries such as Guatemala (Eskafi 1990), Costa Rica (Jiron & Mexzon 1989), Colombia (Yepes & Velez 1989; Carrejo & Gonzalez 1999), Venezuela (Katiyar et al. 1995; Boscan & Godoy 1996; Garcia & Montilla 2001), Brazil (Canal et al. 1995; Leonel et al. 1995; Guimaraes et al. 1999; Aguiar-Menezes et al. 2001), and Argentina (Ovruski 1995; Ovruski et al. 2004, 2005).

Previous studies have stated that as many as 18 parasitoid species of Anastrepha have been recorded in Mexico, including the exotic species Diachasmimorpha longicaudata (Ashmead) and Aceratoneuromyia indica (Silvestri), both of which have been considered as established (Ovruski et al. 2000). However, at least 6 other exotic species have been introduced into Mexico for control of A. ludens and A. obliqua (Jimenez-Jimenez 1955, 1956, 1963).

Inventories of native parasitoids of Anastrepha fruit flies have been conducted in commercial orchards at Morelos and Chiapas (McPhail & Bliss 1933; Baker et al. 1944; Aluja et al. 1990), but also in wild environments associated with native fruit fly hosts in Nuevo Leon (Plummer & McPhail 1941; Gonzalez-Hernandez & Tejada 1979), Veracruz (Hernandez-Ortiz et al. 1994; Lopez et al. 1999), and Chiapas (Aluja et al. 2003). Inventories have not been done in many other fruit growing regions of Mexico.

Anastrepha ludens (Loew), A. obliqua (Macquart), A. serpentina (Wiedemann), A. striata Schiner, A. fraterculus (Wiedemann), A. ampliata Hernandez-Ortiz, and A. pallens (Coquillett) have been recorded from the state of Yucatan (Hernandez-Ortiz et al. 2002). The first 4 species are significant pests in fruit crops in Mexico and most of the Neotropics (Hernandez-Ortiz & Aluja 1993). Fruit fly control in Yucatan has generally involved use of pesticides (CESVY 2000), and very little is known of the native hymenopteran parasitoid communities. An earlier regional study showed the presence in Yucatan of certain Opiinae (Braconidae) that potentially parasitize par·a·sit·ize
v.
To live on or in a host as a parasite.



parasitize

to live on or within a host as a parasite.
 Anastrepha species, including Doryctobracon Ender, Utetes Foerster, and Opius Wesmael (Delfin-Gonzalez & Leon 1997), although sampling methods in that study were not focused on host collection. Thus, specific relationships between Anastrepha and 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
 species remain unknown.

The present study focuses on the search for and inventory of parasitoids that attack Anastrepha species, as well as determination of the relationships between fruit flies, host plants, and parasitoids in the fruit growing region A growing region is an area suited by climate and soil conditions to the cultivation of a certain type of crop. Most crops are cultivated not in one place only, but in several distinct regions in diverse parts of the world.  of southern Yucatan, which mainly consists of mixed orchards of citrus, mango mango (măng`gō), evergreen tree of the Anacardiaceae (sumac family), native to tropical E Asia and now grown in both hemispheres. The chief species, Mangifera indica, is believed to have been cultivated for about 6,000 years. , sapodilla, guava guava (gwä`və), small evergreen tree or shrub of the genus Psidium of the family Myrtaceae (myrtle family), native to tropical America and grown elsewhere for its ornamental flowers and edible fruit. , and red mombin.

Materials and Methods

The study was carried out in mixed commercial orchards in the Yaax-Hom Fruit Unit, 5 km from the Lol-Tun archaeological site, Oxkutzcab municipali ty, in southern Yucatan (20[degrees]18'N, 89[degrees]42'W). Surrounding native vegetation is semi-evergreen tropical forest (Flores Flores, town, Guatemala
Flores (flōrəs), town (1990 est. pop. 2,200), capital of Petén department, N Guatemala. Flores was built on an island in the southern part of Lake Petén Itzá and on the site of the
 & Espejel 1994). Collection of fruit samples occurred from Jun 2000 to Jun 2001, and included 9 host plant species during their fruit-growing seasons: sour orange, Citrus aurantium L. (Aug 2000 to Jan 2001); Valencia orange, C. sinensis (L.) Osbeck var. valenciana (Oct 2000 to Mar 2001); Ruby grapefruit, C. paradisi MacFad (Jul 2000 to Jan 2001); star apple, Chrysophyllum cainito Noun 1. Chrysophyllum cainito - evergreen tree of West Indies and Central America having edible purple fruit star-shaped in cross section and dark green leaves with golden silky undersides
caimito, star apple

fruit tree - tree bearing edible fruit
 L. (Jan to Mar 2001); mango, Mangifera indica L. c.v. Cordoba cor·do·ba  
n.
See Table at currency.



[American Spanish córdoba, after Francisco Fernández de Córdoba (1475?-1526?), Spanish explorer.]

Noun 1.
, criollo Criollo

native Spanish-American light horse or riding pony. Includes a number of ethnic varieties, e.g. Argentine Criollo. Any color, 13.3 to 15 hands high. Originated from a mixture of Arab, Barb and Andalusian.
, pico de loro, and manglova (Mar to Jul 2001); sapodilla, Manilkara zapota (L.) P. Royen (Sept to Dec 2000); mamey sapote The mamey sapote (Pouteria sapota) is a species of tree that is native to southern Mexico and northern South America. The tree is cultivated in Central America, the Caribbean, and South Florida for its melon, which is commonly eaten in many Latin American countries. , Pouteria sapota (Jacq.) H. Moore & Stearn (Apr to Jul 2001); guava, Psidium guajaua L. (Jun to Sep 2000; Febr, April to Jun 2001); and red mombin, Spondias purpurea Noun 1. Spondias purpurea - common tropical American shrub or small tree with purplish fruit
jocote, mombin, mombin tree

mombin - purplish tropical fruit

fruit tree - tree bearing edible fruit
 L. c.v. San Juan San Juan, city, Argentina
San Juan (săn wän, Span. sän hwän), city (1991 pop. 353,476), capital of San Juan prov., W Argentina. It is a commercial and industrial center in an agricultural region.
, tuxpana, and chi-abal (Apr to May 2001).

Fruits were sampled during the fruiting season of each host plant, according to according to
prep.
1. As stated or indicated by; on the authority of: according to historians.

2. In keeping with: according to instructions.

3.
 availability of mature fallen fruits under the trees by means of 2 different methods as follows:

(1) Fruit-Lab Samples. Fruits were weekly sampled, placed in 20-liter containers with a substrate of soil from the collection site, covered with wire mesh wire mesh, wire netting ntela metálica  and topped with a fine-mesh screen to prevent contamination. Samples were taken to the laboratory where they were counted, weighed, and reviewed daily. The recovered pupae were separated in small plastic containers for adult fly and parasitoid emergence.

(2) Fruit-Bed samples. This method was implemented once a sufficient amount of fruits were available. Collected fruits were arranged in "fruit-beds" under the tree canopy, consisting of a plastic tarp covered with soil, containing a known number of fruits previously weighed. "Fruit-beds" remained in the field for 2 weeks and were observed. All pupae recovered were taken to the laboratory in small plastic containers for adult fly and parasitoid emergence.

Percent of parasitism (PP) was recorded as PP = a/(a + b) 100, where a = Number of recovered parasitoids; and b = Number of emerged adult flies in each sample (Steck et al. 1986). Correlation analysis (Statistica 1999) was used to compare mean fruit weight of host sampled (calculated as the [Log.sub.(10)] of fruit weight), infestation infestation /in·fes·ta·tion/ (-fes-ta´shun) parasitic attack or subsistence on the skin and/or its appendages, as by insects, mites, or ticks; sometimes used to denote parasitic invasion of the organs and tissues, as by helminths.  index (calculated as the number of larvae/Kg fruit), and percentage of parasitoids recovered in each sample.

Specimens of fruit flies and parasitoids were determined by VHO VHO Vrij Historisch Onderzoek
VHO Video Heat Online
VHO Video Hub Office
VHO Vertical Handover
VHO Volatile Halogenated Organics
 and HDG HDG Heading
HDG Haus der Geschichte (German)
HDG Hot Dip Galvanized
HdG Havre de Grace
HDG Hab Dich Gern (German)
HDG Heavy-Duty Gasoline-Powered Vehicle
HDG Heeresdisziplinargesetz
, respectively. Voucher specimens are deposited in the Insect Collections (IEXA) of the Instituto de Ecologia (Xalapa, Veracruz), and in the Regional Entomological en·to·mol·o·gy  
n.
The scientific study of insects.



ento·mo·log
 Collections (CERUY) of the Universidad Autonoma de Yucatan (Merida, Yucatan). Botanical samples were identified by personnel of the Botanical Department of the UADY and deposited in the Herbarium herbarium, collection of dried and mounted plant specimens used in systematic botany. To preserve their form and color, plants collected in the field are spread flat in sheets of newsprint and dried, usually in a plant press, between blotters or absorbent paper.  of this institution. Botanical nomenclature Botanical nomenclature is the formal naming of plants, from a scientific point of view. It has a long history, going back perhaps to Theophrastos, but anyway back to the period when Latin was the scientific language throughout Europe.  is based on Terrel et al. (1986), and parasitoid nomenclature nomenclature /no·men·cla·ture/ (no´men-kla?cher) a classified system of names, as of anatomical structures, organisms, etc.

binomial nomenclature
 follows Ovruski et al. (2000).

Results

Altogether, 4,470 fruits (850.8 kg) from 9 host species (including 4 mango varieties and 3 red mombin varieties) were examined and found to be infested by 5 Anastrepha species. All the citrus hosts (C. aurantium, C. sinensis, and C. paradisi) were infested by A. ludens, and 1 specimen of A. serpentina was recovered from ruby grapefruit and 2 from sour orange. A single specimen of A. fraterculus was found in sour orange. The hosts of the family Sapotaceae Noun 1. family Sapotaceae - tropical trees or shrubs with milky juice and often edible fleshy fruit
sapodilla family, Sapotaceae

dicot family, magnoliopsid family - family of flowering plants having two cotyledons (embryonic leaves) in the seed which usually
 (C. cainito, P. sapota and M. zapota) were only infested by A. serpentina, and all S. purpurea varieties were infested by A. oblique. The mango varieties (M. indica) were infested by A. ludens (53.4%) and A. obliqua (45.9%), and 2 specimens of A. serpentina were recovered. The guava fruits (Psidium guajaua) were infested by A. fraterculus (84.2%) and A. striata (15.8%).

In total, 12,929 larvae Larvae, in Roman religion
Larvae: see lemures.
 and pupae were recovered from the sampled fruits. Although the number of fruits collected by each sampling method were equivalent, the "Fruit-Lab" samples exhibited a higher degree of infestation (2,227 fruits, with 8,511 recovered pupae), than that left in the "Fruit-Bed" samples (2,243 fruits, with 4,418 recovered pupae). The highest infestation indices per host were observed in P. guajaua (103.2 larvae/Kg), S. pupurea (all varieties with 83.3 to 44 larvae/Kg), C. cainito (40.4 larvae/Kg), P. sapota (29.6 larvae/Kg), and C. aurantium (22.5 larvae/ Kg). The lowest infestation rates occurred in M. indica (all varieties with 15.9 to 0.3 larvae/ Kg), M. zapota (15.7 larvae/Kg), C. sinensis (4.2 larvae/Kg), and C. paradisi (3.1 larvae/Kg). Sample sizes in some of these low-infestation hosts were relatively small. In total, 9,223 fruit fly viable pupae were recovered during the study, which produced 8,883 adult flies and 340 parasitoid specimens. Average parasitism of all fruit flies was 3.69% (Table 1).

The recovered parasitoids included the following 11 species: the larval-pupal parasitoids D. areolatus (Szepligeti) and Opius bellus (Gahan) (Braconidae); Aganaspis pelleranoi (Brethes), Aganaspis sp., Odontosema anastrephae Borgmeier and Odontosema sp. (Figitidae); and the pupal pu·pa  
n. pl. pu·pae or pu·pas
The nonfeeding stage between the larva and adult in the metamorphosis of holometabolous insects, during which the larva typically undergoes complete transformation within a protective cocoon or
 parasitoids Coptera haywardi (Oglobin) (Diapriidae), Dirhinus sp. (Chalcididae), and Spalangia endius Walker (Pteromalidae). In addition, 2 other parasitoid species in the genera genera, in taxonomy: see classification.  Sycophila sp. (Eurytomidae) and Euperilampus sp. (Perilampidae) were recorded for the first time in Anastrepha.

Relationships between fruit fly-parasitoids among samples showed that A. ludens was attacked in Citrus spp Citrus spp.,
n See extract, citrus seed.
. by 5 parasitoids, which accounted for 29.3% of overall species, while in M. indica only 2 parasitoid species were recorded with 0.6%. In this sense, A. obliqua was parasitized in Spondias purpurea by 5 parasitoid species (16.7%); A. serpentina was attacked by 5 parasitoids (25.6%) infesting 3 hosts of the family Sapotaceae; and the Psidium guajaua fruits infested by A. striata/A. fraterculus were parasitized by 8 species (27.8%).

Odontosema anastrephae was found in 7 host plant species representing 43.2% of all recovered parasitoids with highest proportions in Psidium guajaua and Citrus aurantium. Coptera haywardi represented by 16.2% of parasitoids was found in 6 hosts; Doryctobracon areolatus (14.2%) was present in 4 hosts, particularly in C. cainito; and Spalangia endius only accounted for 6.5% of the overall recorded parasitism, but it was found in 4 different fruit hosts (Table 2).

Parasitism observed between 2 sampled collections revealed that specimens recovered from "Fruit-Bed" samples were higher than those recovered from the "Fruit-Lab" samples with 68.5% and 31.5%, respectively. In this sense, species as C. haywardi, O. anastrephae, S. endius, and Dirhinus sp. were dominant in "Fruit-Beds" accounting for 65% of all parasitoid specimens. On the contrary, the dominant species observed in "Fruit-Lab" samples were D. areolatus, Sycophila sp. and Euperilampus sp., which accounted for 21.2%. Table 3 shows the proportions of parasitoids by hosts obtained from each sampling method.

Correlation analysis between average fruit weight (Log Fruit Weight) and the infestation index (Mean Larvae/kg Fruit) were significant (r = -0.695; P = 0.005), indicating that as average weight increased in the different fruit species, the degree of infestation in the sample decreased. In contrast, there was not a significant correlation between the average fruit weight and the percentage of parasitism (r = -0.090; P = 0.758), and no correlation between infestation index and the percentage of parasitism among samples (r = 0.270; P = 0.350).

Discussion

All parasitoid species reported here are first records for Anastrepha in Yucatan. No previous published records exist in literature of the genera Sycophila sp. (Eurytomidae) and Euperilampus sp. (Perilampidae) as parasitoids in Anastrepha (Ovruski et al. 2000). In this sense, Eurytoma siuinskii Gates & Grissell (Eurytomidae) was recently described attacking field populations of A. obliqua in Mexico (Gates & Grissell 2004). The eurytomids also occur as parasites in Cynipidae, Pteromalidae, Eurytomidae, Tanaostigmatidae, and Agaonidae (Grisell & Schauff 1990; DiGiulio 1997), and members of the family Perilampidae are hyperparasitoids of Ichneumonidae (Darling 1997). However, since the tephritid pupae were separated from the fruit and counted before adult emergence, these may be cases of hyperparasitism hy·per·par·a·sit·ism
n.
A condition in which a secondary parasite develops within a previously existing parasite.
. These results should be further investigated.

The genus Dirhinus (Chalcididae) has been reported as a pupal parasite in Brachycerous Diptera widely distributed Adj. 1. widely distributed - growing or occurring in many parts of the world; "a cosmopolitan herb"; "cosmopolitan in distribution"
cosmopolitan

bionomics, environmental science, ecology - the branch of biology concerned with the relations between organisms
 throughout the world 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. , with 3 known species in the USA (Burks 1947), and about 15 native species yet to be studied in regions ranging from Indiana (USA) to central Argentina (Boucek 1992). Unpublished data for Mexico indicate the presence of at least D. buscki (Crawford), D. schwarzi (Crawford), D. texanus (Ashmead), and D. giffardii (Silvestri) (data provided by Alejandro Gonzalez-Hernandez and Serguei Triapitsyn), although there are probably 1 or 2 more species with cosmopolitan distribution In biogeography, a biological category of living things is said to have cosmopolitan distribution if this category can be found almost anywhere around the world. See "cosmopolitan" for etymology.

An example of a cosmopolitan species is the Painted Lady butterfly.
 (Robert A. Wharton, Texas Wharton is a city in Wharton County, Texas, United States. The population was 9,237 at the 2000 census. It is the county seat of Wharton CountyGR6. Geography
Wharton is located at  (29.316939, -96.
 A & M University, personal communication).

Dirhinus giffardi is the unique species reported attacking fruit flies in the Neotropics, a native western African species introduced in Israel around 1950 (Podoler & Mazor 1981), and in Latin American countries of Puerto Rico Puerto Rico (pwār`tō rē`kō), island (2005 est. pop. 3,917,000), 3,508 sq mi (9,086 sq km), West Indies, c.1,000 mi (1,610 km) SE of Miami, Fla.  (1935-1937), Costa Rica (1955), Peru (1960), Colombia (1970), and Bolivia (1971), and in Florida, USA (1977-1979) (Ovruski et al. 2000). In Mexico, it has been introduced in the states of Morelos and Oaxaca (Jimenez-Jimenez 1956), however there is no evidence that it is established in these regions. The Dirhinus species reported in this paper is very similar to D. schwarzi and D. giffardii, representing an undescribed species, and a new record of a native parasitoid for A. obliqua and A. serpentina.

The exotic species Diachasmimorpha longicaudata and Aceratoneuromyia indica were not recorded during the present study, but both have been documented as established and as having significant parasitism indices in Costa Rica (Wharton et al. 1981) and Mexico (Aluja et al. 1990) respectively, though both these studies were only concerned with coffee and mango orchards. Spalangia endius is a remarkable record, since it has been recorded from Anastrepha in Florida, though rarely reared from tephritids (Ovruski et al. 2000).

The majority of the published papers on Anastrepha parasitoids indicate that D. areolatus (Braconidae) is the most important native parasitoid species, having the highest parasitism indices in the Neotropical region in countries such as Mexico (Hernandez-Ortiz et al. 1994; Lopez et al. 1999), Guatemala (Eskafi 1990), Costa Rica (Jiron & Mexzon 1989), Colombia (Yepes & Velez 1989; Carrejo & Gonzalez 1999), Venezuela (Katiyar et al. 1995), Brazil (Canal et al. 1995; Leonel et al. 1995; Aguiar-Menezes & Menezes 1997; Aguiar-Menezes et al. 2001), and Argentina (Ovruski et al. 2004, 2005).

On the basis of our results, O. anastrephae (Figitidae) is the dominant species occurring in 7 host plants attacked by 5 Anastrepha species. This species is considered a koinobiont parasitoid of Anastrepha larvae (Ovruski et al. 2000), though most of the recovered specimens were found in the Fruit-Bed samples, particularly from Citrus species and guava accounting for 87.7%. Such differences in the parasitism indices may be related to parasitoid biological factors, such as the ability of O. anastrephae to reach their host larvae by entering wounds in fruit located on the ground (Sivinski et al. 1997, 2000).

Comparisons between fruit weight and infestation rates among different hosts showed that the number of larvae was larger in small fruits but decreased as fruit size increased. This coincides with results observed for A. suspensa in Florida (USA), when fruit sizes and infestation indices were compared for 6 host species (Sivinski 1991).

Previous hypothesis on parasitism levels have been attributed in part to physical difficulties in locating immature stages within large fruits (Sivinski 1991). However, our comparisons between fruit weight of 14 hosts and the parasitism rates of the 11 parasitoid species showed no correlation. This may be due to the fact that more sample sizes are needed in order to test this hypothesis, or that the native parasitoid community has only become recently adapted to certain exotic fruit species included in our analysis, such as Citrus spp. and M. indica.

The low level of parasitism (3.69%) observed in this study is probably due to orchard management practices, in which destruction of fallen fruit and periodic pesticide use (CESVY 2000), could have a negative impact on parasitoid populations. Similar studies carried out in Brazil reported similar species diversity and levels of parasitism (Uchoa-Fernandes et al. 2003). Based on the parasitoid species diversity that attack the Anastrepha fruit flies in Yucatan, further studies need to be focused on the biology and ecology of certain native parasitoids such as O. anastrephae, C. haywardi, and D. areolatus as promising biological control agents.

Acknowledgments

The authors thank Luis Hernandez Puch for allowing access to his family's orchard for this research. Thanks are due to 2 anonymous reviewers for helpful suggestions on the earlier version of the manuscript. This study was partially supported by the project "Relaciones huesped-parasitoide y caracterizacion de la comunidad de braconidos (Hymenoptera: Parasitica) en el estado de Yucatan" funded by the CONACYT CONACYT Consejo Nacional de Ciencia y Tecnología (National Board of Science and Technology; Mexico, Bolivia, Paraguay) , Mexico (Ref: 25016-N), and by the project "Ecologia y sistematica de insectos fitofagos y saprofagos", funded by the Instituto de Ecologia, A.C. (Ref: 902-08/128).

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Aguiar-Menezes, E. L., E. B. Menezes, P. S. Silva, A. J. Bittar, and P. C. R. Cassino Cassino, town, Italy
Cassino (käs-sē`nō), town (1991 pop. 32,787), in Latium, central Italy, in the Apennines, on the Rapido River. It is a commercial and agricultural center, and the site of a Fiat auto assembly plant.
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Aluja, M., J. Guillen, P. Liedo, M. Cabrera, E. Rios, G. De La Rosa De La Rosa is a surname in the Spanish language meaning of the Rose
  • Pedro de la Rosa
  • Jorge de la Rosa
  • Rogelio de la Rosa
  • Nelson de la Rosa
  • Lidia de la Rosa
, H. Celedonio, and D. Mota. 1990. Fruit infesting tephritids (Diptera: Tephritidae) and associated parasitoids in Chiapas, Mexico. Entomophaga 35:39-48.

Aluja, M., J. Rull, J. Sivinski, A. L. Norrbom, R. A. Wharton, R. Macias-Ordonez, F. Diaz-Fleischer, and M. Lopez. 2003. Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the tropical rainforest Tropical rainforests are rainforests generally found near the equator. They are common in Asia, Africa, South America, Central America, and on many of the Pacific Islands.  biosphere biosphere, irregularly shaped envelope of the earth's air, water, and land encompassing the heights and depths at which living things exist. The biosphere is a closed and self-regulating system (see ecology), sustained by grand-scale cycles of energy and of  reserve of Montes mon·tes  
n.
Plural of mons.
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Comite Estatal de Sanidad Vegetal vegetal /veg·e·tal/ (vej´e-t'l) vegetative (defs. 1, 2, and 3).

veg·e·tal
adj.
1. Of, relating to, or characteristic of plants.

2.
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Flores, G. S., and I. Espejel. 1994. Tipos de vegetacion de la Peninsula de Yucatan. Etnoflora Yucatanense 3: 1-135.

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Gates, M. W., and E. E. Grissell. 2004. A new species of Eurytoma (Hymenoptera: Eurytomidae) attacking the Mango Fruit Fly Anastrepha obliqua (Macquart) (Diptera: Tephritidae), pp. 147-159 In Perspectives on Biosystematics bi·o·sys·tem·at·ics  
n. (used with a sing. verb)
The statistical analysis of data obtained from genetic, biochemical, and other observational studies to assess the taxonomic relationships of organisms or populations, especially within an
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biodiversity

Quantity of plant and animal species found in a given environment. Sometimes habitat diversity (the variety of places where organisms live) and genetic diversity (the variety of traits expressed
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Guimaraes, J. A., R. A. Zucchi, N. B. Diaz, M. F. De Souza De Souza or D'Souza is a common Portuguese family name. Although it is still quite common outside Portugal -- especially in Brazil and India --, Souza is the old spelling of present-day Sousa.  Filho, and M. Uchoa. 1999. Especies de Eucoilinae (Hymenoptera: Cynipoidea: Figitidae) parasitoides de larvae frugivoras (Diptera: Tephritidae e Lonchaeidae) no Brasil. Ann. Soc. Entom. Brasileira 28: 263-273.

Hernandez-Ortiz, V., and M. Aluja. 1993. Listado de especies del genero neotropical Anastrepha (Diptera: Tephritidae) con notas sobre su distribucion y plantas hospederas. Folia Entomol. Mexicana 88:89-105.

Hernandez-Ortiz, V., R. Perez-Alonso, and R. A. Wharton. 1994. Native parasitoids associated with the genus Anastrepha (Diptera: Tephritidae) in Los Tuxtlas The Los Tuxtlas region, very broadly, occupies parts of south central Veracruz state, in east central Mexico. The region includes the Sierra de los Tuxtlas and stretches from Laguna Alvarado, along the Gulf of Mexico, to Laguna del Ostión, then along the westernmost tributaries of , Veracruz, Mexico. Entomophaga 39: 171-178.

Hernandez-Ortiz, V., P. Manrique-Saide, H. Delfin-Gonzalez, and L. Novelo-Rincon. 2002. First report of Anastrepha compressa in Mexico and new records for other Anastrepha species in the Yucatan Peninsula (Diptera: Tephritidae). Florida Entomol. 85:389-391.

Jimenez-Jimenez, E. 1955. Liberacion de enemigos naturales de las plagas agricolas en Mexico en el ano de 1954. Parasitos (genero Opius) de la mosca mexicana de la fruta (Anastrepha spp.). Revista Fitofilo 10: 70-71.

Jimenez-Jimenez, E. 1956. Las moscas de la fruta y sus enemigos naturales. Revista Fitofilo 16: 4-11.

Jimenez-Jimenez, E. 1963. Avances y resultados del control biologico en Mexico. Revista Fitofilo 38: 34-37.

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See under Distribution.

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Leonel, F. L., Jr., R. A. Zucchi, and R. A. Wharton. 1995. Distribution and tephritid hosts (Diptera) of braconid parasitoids (Hymenoptera) in Brazil. Int. Jour. Pest Manag. 41: 208-213.

Lopez, M., M. Aluja, and J. Sivinski. 1999. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera:Tephritidae) in Mexico. Biol. Control 15: 119-129.

McPhail, M., and C. I. Bliss. 1933. Observations on the Mexican Fruit Fly and Some Related Species in Cuernavaca, Mexico in 1928 and 1929. U.S. Dept. Agric. Circular 255: 1-24.

Ovruski, S. 1995. Pupal and larval larval

1. pertaining to larvae.

2. larvate.


larval migrans
see cutaneous and visceral larva migrans.
 parasitoids (Hymenoptera) obtained from Anastrepha spp. and Ceratitis capitata (Dipt.: Tephritidae) pupae collected in four localities of Tucuman Province, Argentina. Entomophaga 40: 367-370.

Ovruski, S., M. Aluja, J. Sivinski, and R. A. Wharton. 2000. Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the Southern United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. : diversity, distribution, taxonomic tax·o·nom·ic   also tax·o·nom·i·cal
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Of or relating to taxonomy: a taxonomic designation.



tax
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Ovruski, S. M., P. Schliserman, and M. Aluja. 2004. Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in northwestern Argentina. Biol. Control. 29: 43-57.

Ovruski, S. M., R. Wharton, P. Schliserman, and M. Aluja. 2005. Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and its associated native parasitoids (Hymenoptera) in feral feral

untamed; often used in the sense of having escaped from domesticity and run wild.
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Podoler, H., and M. Mazor. 1981. Dirhinus giffardii Silvestri (Hymenoptera: Chalcididae) as a parasite of 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.
, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Acta Oecologica 2: 299-309.

Sivinski, J. 1991. The influence of host fruit morphology morphology

In biology, the study of the size, shape, and structure of organisms in relation to some principle or generalization. Whereas anatomy describes the structure of organisms, morphology explains the shapes and arrangement of parts of organisms in terms of such
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Sivinski, J., M. Aluja, and M. Lopez. 1997. Spatial and temporal distribution of parasitoids of Mexican Anastrepha species (Diptera: Tephritidae) within the canopies of fruit trees. Ann. Entom. Soc. Am. 90: 604-618.

Sivinski, J., J. Pinero, and M. Aluja. 2000. The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biol. Control 18: 258-269.

Statistica. 1999. Software for PC Statistical Analysis. Statsoft, Inc., Tulsa, OK.

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fruit-eating.
 flies (Diptera, Tephritoidea) reared from fruits of the cerrado of the state of Mato Grosso do Sul Mato Grosso do Sul (pron. IPA: ['ma.tu 'gɾo.su du suw] [1]) is one of the states of Brazil. Neighbouring states are (from north clockwise) Mato Grosso, Goiás, Minas Gerais, São Paulo and Paraná. , Brazil. Rev. Brasileira Entom. 47: 181-186.

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Vicente Hernandez-Ortiz (1), Hugo Delfin-Gonzalez (2), Andres Escalante-Tio (2) and Pablo Manrique-Saide (2)

(1) Instituto de Ecologia A.C., Km 2.5 carretera antigua a Coatepec No. 351, Congregacion El Haya Apartado Postal 63, C.P. 91000, Xalapa, Veracruz, Mexico

(2) Universidad Autonoma de Yucatan, Facultad de Medicina Veterinaria y Zootecnia, Depto. de Zoologia Apartado Postal 4-116, Merida, Yucatan, Mexico
TABLE 1. HOST PLANT SAMPLED AND RECOVERED FRUIT FLY PUPAE AND
PARASITOIDS OF ANASTREPHA SPECIES IN YUCATAN MEXICO. MANGIFERA INDICA:
1 = VAR. CORDOBA; 2 = VAR. CRIOLLO; 3 = VAR. PICO DE LORO; 4 = VAR.
MANGLOVA; SPONDIAS PURPUREA: 1 = VAR. SAN JUAN; 2 = VAR TUXPANA, 3 =
VAR. CHI-ABAL.

                                   Total fruit      Mean fruit
Host plant       Fruit sampled     weight (Kg)      weight (Kg)

C. aurantium          558             90.40            0.162
C. sinensis           732            138.60            0.189
C. paradisi           251            124.40            0.496
Ch. cainito           200             22.80            0.114
M. indica 1           325             64.70            0.199
M. indica 2            29              4.60            0.159
M. indica 3           225             87.00            0.387
M. indica 4           234            105.90            0.453
Ma. zapota            454             83.60            0.184
Po. sapota             92             72.80            0.791
Ps. guajava           442             26.80            0.061
S. purpurea 1         716             26.80            0.037
S. purpurea 2         138              1.75            0.013
S. purpurea 3          74              0.65            0.009

All samples          4470            850.8             0.232

                  Infestation      Total pupae
Host plant        (larvae/Kg)       recovered      Pupae viable

C. aurantium        22.50              2037             1630
C. sinensis          4.24               587              438
C. paradisi          3.15               392              269
Ch. cainito         40.40               918              514
M. indica 1          2.80               179              110
M. indica 2         15.90                73               67
M. indica 3          0.33                29               23
M. indica 4          1.20               127               81
Ma. zapota          15.70              1310             1084
Po. sapota          29.60              2157             1940
Ps. guajava        103.20              2765             1773
S. purpurea 1       83.30              2232             1188
S. purpurea 2       44.00                77               73
S. purpurea 3       70.80                46               33

All samples         31.2             12929             9223

                                   Parasitoids
Host plant       Flies emerged       emerged       Parasitism %

C. aurantium         1578                52             3.19
C. sinensis           414                24             5.48
C. paradisi           245                24             8.92
Ch. cainito           447                67            13.04
M. indica 1           108                 2             1.82
M. indica 2            67                 0             0.00
M. indica 3            23                 0             0.00
M. indica 4            81                 0             0.00
Ma. zapota           1072                12             1.11
Po. sapota           1932                 8             0.41
Ps. guajava          1679                94             5.30
S. purpurea 1        1133                55             4.63
S. purpurea 2          72                 1             1.36
S. purpurea 3          32                 1             3.03

All samples          8883               340             3.69

TABLE 2. PARASITOID SPECIES EMERGED BY HOST FRUIT SPECIES UNDER 2
DIFFERENT SYSTEMS OF COLLECTION. M. INDICA; 1 = VAR. CORDOBA; S.
PURPUREA; 1 = VAR. SAN JUAN; 2 = VAR. TUXPANA; 3 = VAR. CHI-ABAL.
ACRONYMS FOR PARASITOID SPECIES ARE AS FOLLOWS: DAR = D. AREOLATUS;
OBEL = O. BELLUS; CHAY = C. HAYWARDI; APELL = A. PELLERANOI; ASP
= AGANASPIS SP.; OANAS = O. ANASTREPHAE; OSP = ODONTOSERNA SP.;
SPEND = S. ENDIUS; DSP = DIRHINUS SP.; SYSP = SYCOPHILA SP.; ESP
= EUPERILAMPUS SP.

Hosts             Parasitoids      Oar         Obel        Chay

C. aurantium      Fruit Lab         0           0           0
                  Fruit beds        0           0           8
C. sinensis       Fruit Lab         0           0           0
                  Fruit beds        0           0           6
C. paradisi       Fruit Lab         0           0           0
                  Fruit beds        0           0           1
Ch. cainito       Fruit Lab        30           0           0
                  Fruit beds        5           0           7
M. indica 1       Fruit Lab         0           0           0
                  Fruit beds        0           0           0
Ma. zapota        Fruit Lab         0           0           0
                  Fruit beds        0           0           9
S. purpurea 1     Fruit Lab         5           0           0
                  Fruit beds        0           0           0
S. purpurea 2     Fruit Lab         0           0           0
                  Fruit beds        0           0           0
S. purpurea 3     Fruit Lab         1           0           0
                  Fruit beds        0           0           0
Po. sapota        Fruit Lab         0           0           0
                  Fruit beds        0           0           0
Ps. guajava       Fruit Lab         6           2           0
                  Fruit beds        1           0          24

Total specimens   Fruit Lab        42           2           0
                  Fruit beds        6           0          55

% parasitism      FLab + FBeds     14.1         0.6        16.2

Parasitoids          Apell         Asp        Oanas        Osp

Fruit Lab              1            0           1           1
Fruit beds             0            0          38           0
Fruit Lab              0            0           1           0
Fruit beds             0            0          10           0
Fruit Lab              0            0           0           0
Fruit beds             0            0          23           0
Fruit Lab              0            0          12           0
Fruit beds             0            0          13           0
Fruit Lab              0            0           1           0
Fruit beds             0            0           0           0
Fruit Lab              0            0           0           0
Fruit beds             0            0           3           0
Fruit Lab              0            0           0           0
Fruit beds             0            0           0           0
Fruit Lab              0            0           0           0
Fruit beds             0            0           0           0
Fruit Lab              0            0           0           0
Fruit beds             0            0           0           0
Fruit Lab              0            0           0           0
Fruit beds             0            0           0           0
Fruit Lab              7            1           3           1
Fruit beds             5            0          42           0

Fruit Lab              8            1           18          2
Fruit beds             5            0          129          0

FLab + FBeds           3.8          0.3         43.2        0.6

Parasitoids          Spend         Dsp         Sysp

Fruit Lab              0            0           0
Fruit beds             3            0           0
Fruit Lab              0            0           0
Fruit beds             7            0           0
Fruit Lab              0            0           0
Fruit beds             0            0           0
Fruit Lab              0            0           0
Fruit beds             0            0           0
Fruit Lab              0            0           1
Fruit beds             0            0           0
Fruit Lab              0            0           0
Fruit beds             0            0           0
Fruit Lab              0            0           8
Fruit beds            10           15           1
Fruit Lab              0            0           1
Fruit beds             0            0           0
Fruit Lab              0            0           0
Fruit beds             0            0           0
Fruit Lab              0            4           0
Fruit beds             0            0           0
Fruit Lab              0            0           0
Fruit beds             2            0           0

Fruit Lab              0            4          10
Fruit beds            22           15           1

FLab + FBeds           6.5          5.6         3.2

                                               % by
Parasitoids           Esp         Totals      sample

Fruit Lab              0            3           0.9
Fruit beds             0           49          14.4
Fruit Lab              0            1           0.3
Fruit beds             0           23           6.8
Fruit Lab              0            0           0.0
Fruit beds             0           24           7.1
Fruit Lab              0           42          12.4
Fruit beds             0           25           7.3
Fruit Lab              0            2           0.6
Fruit beds             0            0           0.0
Fruit Lab              0            0           0.0
Fruit beds             0           12           3.5
Fruit Lab             16           29           8.5
Fruit beds             0           26           7.7
Fruit Lab              0            1           0.3
Fruit beds             0            0           0.0
Fruit Lab              0            1           0.3
Fruit beds             0            0           0.0
Fruit Lab              4            8           2.3
Fruit beds             0            0           0.0
Fruit Lab              0           20           5.9
Fruit beds             0           74          21.7

Fruit Lab             20          107          31.5
Fruit beds             0          233          68.5

FLab + FBeds           5.9        340         100

TABLE 3. RELATIONSHIP FRUIT FLY-PARASITOID SPECIES RECOVERED
FROM ALL SAMPLED HOSTS EXPRESSED IN PERCENTAGES.

                                                 A. ludens/
Fruit fly                       A. ludens        A. obliqua

Hosts                          Citrus spp.       M. indica

Parasitoids

Odontosema anastrephae            21.4              0.3
Odontosema sp.                     0.3              0.0
Aganaspis pelleranoi               0.3              0.0
Aganaspis sp.                      0.0              0.0
Doryctobracon areolatus            0.0              0.0
Opius bellus                       0.0              0.0
Coptera haywardi                   4.4              0.0
Spalangia endius                   2.9              0.0
Dirhinus sp.                       0.0              0.0
Sycophila sp.                      0.0              0.3
Euperilampus sp.                   0.0              0.0

Parasitism %                      29.3              0.6

Fruit fly                      A. obliqua      A. serpentina

                                                Ch. cainito,
                                Spondias         P. sapota,
Hosts                           purpurea         M. zapota

Parasitoids

Odontosema anastrephae             0.0              8.2
Odontosema sp.                     0.0              0.0
Aganaspis pelleranoi               0.0              0.0
Aganaspis sp.                      0.0              0.0
Doryctobracon areolatus            1.8             10.3
Opius bellus                       0.0              0.0
Coptera haywardi                   0.0              4.7
Spalangia endius                   2.9              0.0
Dirhinus sp.                       4.4              1.2
Sycophila sp.                      2.9              0.0
Euperilampus sp.                   4.7              1.2

Parasitism %                      16.7             25.6

                               A. striata/
Fruit fly                     A. fraterculus    Parasitism %

Hosts                          P. guajava        All hosts

Parasitoids

Odontosema anastrephae            13.3             43.2
Odontosema sp.                     0.3              0.6
Aganaspis pelleranoi               3.5              3.8
Aganaspis sp.                      0.3              0.3
Doryctobracon areolatus            2.1             14.2
Opius bellus                       0.6              0.6
Coptera haywardi                   7.1             16.2
Spalangia endius                   0.6              6.4
Dirhinus sp.                       0.0              5.6
Sycophila sp.                      0.0              3.2
Euperilampus sp.                   0.0              5.9

Parasitism %                      27.8            100.0
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Author:Hernandez-Ortiz, Vicente; Delfin-Gonzalez, Hugo; Escalante-Tio, Andres; Manrique-Saide, Pablo
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1MEX
Date:Dec 1, 2006
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