Research Article |
Corresponding author: Jose Fernandez-Triana ( cnc.braconidae@gmail.com ) Academic editor: Elijah Talamas
© 2021 Farial Krache, Malika Boualem, Jose Fernandez-Triana, Amber Bass, Judit Arnó, Fouzia Benourad.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Krache F, Boualem M, Fernandez-Triana JL, Bass A, Arnó J, Benourad F (2021) First record in Africa of the parasitoid Dolichogenidea gelechiidivoris (Hymenoptera: Braconidae) on tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) from tomato fields in Algeria. Journal of Hymenoptera Research 88: 115-131. https://doi.org/10.3897/jhr.88.75279
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The Neotropical parasitoid wasp Dolichogenidea gelechiidivoris (Marsh, 1975) (Hymenoptera: Braconidae), one of the most important biocontrol agents of the South American tomato pinworm Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae), is reported for the first time from Africa, from tomato grown in open fields and greenhouses in several regions of Algeria. Color photos of specimens from Algeria, Spain and South America, as well as the holotype and one paratype are provided. Morphological and molecular details to better characterize and recognize the species are also provided. We speculate that D. gelechiidivoris arrived accidentally to Algeria from Spain, where it has recently been reported. The consequences for future biocontrol projects against T. absoluta in Africa are discussed.
Tuta absoluta, Afrotropical region, Microgastrinae, tomato, biological control, species diagnosis, DNA barcoding, accidental introduction
The past decade has seen Africa invaded by the tomato pinworm Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae), an important pest native to South America that causes severe crop losses when not controlled. The first reported record of the pest out of its continent of origin was from Spain in 2006 (
Biological control is often considered one of the most economical and environmentally sustainable means of managing native as well as exotic pests and crop diseases (
In Africa (Nigeria, Tunisia, Algeria and Morocco), the parasitoid complex of T. absoluta that has so far been recorded through field monitoring and surveys include the larval parasitoids Dolichogenidea appellator (Telenga, 1949) and several species in the genera Apanteles Foerster and Bracon Fabricius (Hymenoptera: Braconidae) as well as egg parasitoids in the genus Trichogramma Westwood (Hymenoptera: Trichogrammatidae) (
Among Braconidae subfamilies, Microgastrinae is a critically important group of parasitoid wasps estimated to include 17,000–50,000 species worldwide (
The microgastrine species Dolichogenidea gelechiidivoris (Marsh, 1975), originating from the Neotropics, is a koinobiont solitary endoparasitoid of T. absoluta and a few other closely related species (
The International Centre of Insect Physiology and Ecology (icipe) in Kenya, in collaboration with the International Potato Center (CIP) in Peru, also identified D. gelechiidivoris as an effective endemic natural enemy of T. absoluta in their native range (Peruvian central highlands) and imported specimens of the parasitoid wasp into Kenya from Peru in 2017 for studies of its feasibility as a candidate for classical biological control of T. absoluta in Africa (
In this paper we present the first record of D. gelechiidivoris from Africa, recovered as a parasitoid of T. absoluta in tomato grown in open fields and greenhouses in Algeria. We also provide morphological and molecular information to better diagnose this parasitoid wasp species and discuss the significance of its finding for future biocontrol projects against T. absoluta in Africa.
In December 2020, one species of Microgastrinae was reared from larvae of T. absoluta collected in tomato fields of the municipality of Stidia, along the Bay of Arzew and 15 km SW from the city of Mostaganem. The locality is characterized by a mild Mediterranean climate. The same wasp species was later found in greenhouses growing tomatoes in other municipalities of Mostaganem province (Table
Collecting sites of specimens of Dolichogenidea gelechiidivoris parasitizing Tuta absoluta in Algeria.
Site | Collection dates | Field characteristics |
---|---|---|
Stidia | 16/12/2020; 01/05/2021 | Open fields and greenhouses |
Mazaghran | 21/04/2021 | Greenhouses |
Hassi Mameche | 26/04/2021 | Greenhouses |
Hadjadj | 26/05/2021 | Greenhouses |
Ain Tadles | 05/06/2021 | Greenhouses |
Sidi Ali | 28/06/2021 | Greenhouses |
The identification of the parasitoid wasp species was made by one of the authors (JFT) in the Canadian National Collection of Insects (
For morphological terms we follow several published references (see details in
Photographs were taken with a Keyence VHX-1000 Digital Microscope, using lenses with a range of 10–130×. Multiple images were taken of a structure through the focal plane and then combined to produce a single in-focus image using the software associated with the Keyence System. Plates were prepared using Microsoft PowerPoint 2010 and later saved as .tiff files.
DNA barcodes were obtained from specimens collected in Algeria and Spain. DNA was extracted destructively from the hind leg of 4 specimens with the DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA, USA). Modifications to the manufacturer’s protocol from
Sequences were deposited in the Barcode of Life Data Systems (BOLD; http://www.boldsystems.org). A dataset containing all available sequences of D. gelechiidivoris (ours and others previously obtained from specimens in South America) was created in BOLD and assigned a doi for future reference (dx.doi.org/10.5883/DS-DOLIGELE). A Neighbour joining (NJ) tree with the 16 sequences of the species over 600 base pairs (bp) was built using BOLD standard parameters.
The parasitoid wasp specimens reared in Algeria from T. absoluta on tomato were identified as D. gelechidiivoris, based on the original description (Marsh, 1975) and comparison with the species holotype, one paratype and other material deposited in the
Female holotype of Dolichogenidea gelechiidivoris, Colombia, voucher code USNMENT00831760.
Additional corroboration of the species identity came from Algerian specimens from which DNA barcodes were obtained and were a perfect match to specimens from South America and Spain (Fig.
Female paratype of Dolichogenidea gelechiidivoris, Colombia, voucher code CNC678061.
A total of 25 species of Dolichogenidea have been so far recorded from Africa (
At present, there are no keys to separate African species of Dolichogenidea, but the following combination of morphological characters should suffice to characterize and unequivocally recognize D. gelechiidivoris among all other described species of the genus in Africa: 1) antenna shorter than body; 2) anteromesoscutum mostly shiny, covered with white setae and with relatively sparse but evenly distributed and well-marked punctures; 3) mesoscutellar disc shiny with punctures that are comparatively shallower and more sparse than in anteromesoscutum; 4) polished area (lunules) of the lateral side of the axillar complex about half the height of lateral side; 5) propodeum mostly smooth and shiny on anterior half, posterior half rugose medially, with rugae near nucha and forming lower part of an areola; 6) metasoma relatively short and slightly compressed laterally; 7) first mediotergite (T1) mostly parallel-sided, but slightly narrowing near posterior margin; 8) T1 smooth on anterior half, rugose on posterior half; 9) second mediotergite (T2) relatively transverse, its width at posterior margin more than 3.0× its medial length, with lateral sides oblique and posterior margin sinuate (shape of T2 varies slightly and it is sometimes less transverse in some specimens from all geographical areas examined); 10) T2 mostly sculptured, with small area smooth along posterior margin; 11) ovipositor sheaths about same length (or slightly shorter) than metatibia length, ovipositor evenly down curved; 12) fore wing with pterostigma relatively thick, light coloured (pale yellow-brown) but with thin brown margins; 13) fore wing vein R1 comparatively short, its length about the same than pterostigma length, but less than 2.5× the distance between its end and end of vein 3RS; 14) most veins in wings either light brown to yellow-brown or transparent; 15) legs mostly dark brown to black but with posterior 0.1–0.2 of femora and most of tibiae yellow to yellow brown (specimens from Algeria and some specimens from Spain we have examined have darker tibiae, which can be mostly dark brown to black); 16) body color mostly black, including tegula and humeral complex.
Especially, the following characters are useful to recognize the species: the sculpture of propodeum; sculpture and shape of T1 and T2; color and shape of pterostigma; short vein R1; relative short antenna and metasoma relatively compressed laterally. Among the specimens included in the following study, the morphological variation was relatively minor (with some specimens having slightly darker legs and slightly less transverse T2 shape), thus the species is fairly recognizable and uniform.
Dolichogenidea appellator (Telenga, 1949) is the only other species of Dolichogenidea from Africa which has been recorded parasitizing Tuta absoluta in the continent (
From a molecular perspective, D. gelechiidivoris is also clearly distinctive and diagnosable. The specimens with available data in BOLD come from six different countries, Algeria, Chile, Colombia, Peru, Spain and Venezuela. They comprise 19 sequences, with 16 of them over 600 bp (15 representing full barcodes). Out of the three short sequences (107–164 bp) two are especially important as they were retrieved from paratype specimens housed in the
Although South American specimens of D. gelechiidivoris, from Peruvian central highlands, were brought to Kenya in 2017 by researchers at icipe, they have only been studied in laboratory conditions for potential classical biological control of T. absoluta (
The documentation in this paper of D. gelechiidivoris already established in Africa (at least in northern areas of the continent) is very relevant for the future of biological control of T. absoluta in the continent. Since this wasp species occurred spontaneously in tomato crops but autonomous spreading to isolated fields seems limited, it is possible to recommend its mass rearing and augmentation release for its rapid establishment in other areas, and to include its management in combination with other biocontrol agents in the IPM programs of T. absoluta in the region.
We are grateful for the excellent comments and suggestions provided by the reviewers Kaoru Maeto, Ilgoo Kang and Sergey Belokoblylskij as well as the editor Elijah Talamas, which considerably improve the final version of this paper. The work of JFT and AB was supported by Project J-002276 “Systematics of beneficial arthropods in support of resilient agroecosystems”, from Agriculture and Agri-Food Canada. JA was supported by Horta.Net and the CERCA Programmes of the Generalitat de Catalunya.