Research Article |
Corresponding author: Jose Fernandez-Triana ( cnc.braconidae@gmail.com ) Academic editor: Gavin Broad
© 2017 Jose Fernandez-Triana, Melanie Beaudin, Kees van Achterberg, Mawufe K. Agbodzavu, Stephen T.O. Othim, Faith W. Nyamu, Komi K.M. Fiaboe.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Fernandez-Triana J, Beaudin M, van Achterberg K, Agbodzavu MK, Othim STO, Nyamu FW, Fiaboe KKM (2017) DNA barcodes, expanded distribution, and redescription of Apanteles hemara Nixon, 1965 (Hymenoptera, Braconidae, Microgastrinae), a potential biocontrol species against amaranth leaf-webbers in Africa. Journal of Hymenoptera Research 58: 1-15. https://doi.org/10.3897/jhr.58.13361
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The microgastrine parasitoid wasp Apanteles hemara Nixon, 1965, is currently being considered as a potential biocontrol agent of amaranth leaf-webber pests in Africa. To facilitate future research and identification of the species, we characterize it from an integrative taxonomy perspective by providing a comprehensive morphological redescription, extensive illustrations (including the first images of the holotype), DNA barcodes, wasp biology, host data (Choreutidae and Crambidae caterpillars), and updated geographical distribution of the species (including eight new country records). Despite a wide distribution across four major biogeographical regions (mostly within the Old World tropics), the species seems to be relatively uniform from a molecular and morphological perspective, based on studied specimens from Africa and Asia.
Microgastrinae , Amaranthus , biocontrol, DNA barcode, geographical distribution, Africa
Apanteles hemara was described more than 50 years ago (
The host species attacked by A. hemara are also varied: it has been considered a regular solitary parasitoid of Tebenna micalis (Mann, 1857) (Choreutidae), wherever both species occur (
Due to the wide geographical distribution and host associations, the species was described four times under different names, and it currently has three synonyms (see below for more details on that).
In order to better characterize the species, this paper provides the first molecular information for Apanteles hemara (DNA barcodes), expands the known distribution to an additional eight countries, and presents the first color pictures of the species, including the holotype.
We studied specimens from the California Academy of Sciences (
Specimens from several countries (Kenya, Madagascar, Republic of the Congo, United Arab Emirates, and Yemen) were sampled for DNA barcodes (the 5’ region of the cytochrome c oxidase I (CO1) gene,
The holotype of A. hemara was photographed with a Leica DFC450 camera on a Leica M165 C microscope. Other specimens were photographed with a Keyence VHX-1000 Digital Microscope, using a lens 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. For the Leica camera, the Zerene Stacker program (http://zerenesystems.com/cms/stacker) was used; software associated with the Keyence System produced focused images taken with that camera. Plates were prepared using Microsoft PowerPoint 2010.
A map with the distribution of the species was generated using SimpleMappr (
Apanteles
hemara
Nixon, 1965. Original description
Apanteles
caboverdensis
Hedqvist, 1965. Synonymized by
Apanteles
proalastor
Hedqvist, 1965. Synonymized by
Apanteles
bulgaricus
Balevski & Tobias, 1980. Synonymized by
INDIA, Dehradun. Female (deposited in the Natural History Museum, London), examined.
DEMOCRATIC REPUBLIC OF THE CONGO: Iboubikro, Lesio-Loun Pk.; Pool, -3.2699 15.4711, 340mm, 25.xi.2008, coll. Braet & Sharkey, voucher code: CNCH2805 (1 specimen,
Afrotropical, Australian, Oriental and Palaearctic regions (Fig.
Apanteles hemara can be recognized by having antenna slightly shorter than body length, with flagellomere 14 length 1.3–1.6 × its width; vein R1 about four times as long as distance between ends of veins R1 and 3RS; hind legs with black coxa, yellow trochanter and trochantellus, brown metafemur, metatibia yellow on anterior 0.5–0.6 and brown on posterior 0.4–0.5, metatibial spurs white, and metatarsus brown; propodeum mostly smooth, but with entire areola entirely defined by strong carinae; tergites 1 and 2 with strong, longitudinal striation; and ovipositor sheats shorter than metatibia (0.7–0.9 ×). Apanteles hemara belongs to the ater species group (sensu
Body color mostly black, tergites 3+ dark brown, laterotergites and sternites 3+ light yellow-brown. Head black, except for dark orange-brown labrum, light yellow-white palpi and dark brown antennae. Front and middle legs yellow (except for coxae and mesofemur light yellow-brown to brown); hind leg with black coxa, yellow trochanter and trochantellus, brown metafemur, metatibia yellow on anterior 0.5–0.6 and brown on posterior 0.4–0.5, metatibial spurs white, and metatarsus brown. Wings with most veins transparent or white, except for brown veins R1, r, 2RS and M; pterostigma mostly brown, with a very small white spot at base. Anteromesoscutum and scutellar disc with relatively coarse and dense punctures (distance between punctures smaller than diameter of individual puncture). Propodeum mostly smooth, with areola entirely defined by strong carinae. Tergites 1 and 2 with strong, longitudinal striation, contrasting with remaining tergites which are smooth. Body measurements (in mm) and ratios. Body length: 2.50–3.20, fore wing length: 2.50–3.00, ovipositor sheaths: 0.62–0.84, metafemur: 0.65–0.77, metatibia length: 0.87–0.95, tergite 1 0.36–0.49. Length of flagellomeres: 1st (0.18–0.22), 2nd (0.18–0.22), 3rd (0.17–0.21), 14th (0.08–0.10), 15th (0.08–0.10) and 16th (0.12). Length/width of flagellomere 2: 2.75–3.14; length/width of flagellomere 14: 1.28–1.60. Head height/width: 0.82–0.88; head slightly narrowing towards mandibles, width at clypeus base 0.88–0.88 × head width at antennal base. Malar line 1.12–1.50 × mandibular base. Ocular ocellar line 1.67–2.00 × posterior ocellus diameter; interocellar distance 1.71–2.17 × posterior ocellus diameter. Scutellar disc length 1.09–1.15 × width at base. Maximum height of mesoscutellum lunules 0.42–0.56 × maximum height of lateral face of mesoscutellum. Tergite 1 widening from anterior margin to two thirds of tergite length, then slightly narrowing towards posterior margin; tergite 1 length 1.64–2.09 × tergite width at posterior margin; tergite widths (at anterior margin/maximum width/posterior margin): 0.19–0.25/0.27–0.30/0.22–0.25. Tergite 2 width at posterior margin 2.31–2.64 × length medially. Tergite 2 length medially 0.48–0.64 × tergite 3 length medially. Metafemur length 3.25–3.67 × metafemur width. Pterostigma length 2.55–2.86 its width. Vein R1 length 1.15–1.27 × pterostigma length. Vein r length 1.82–2.20 × vein 2RS length.
Despite the widespread distribution of the species across four major biogeographical regions (mostly Old World tropics), the specimens we examined were very similar morphologically (Figs
Solitary parasitoid (Fig.
A total of 17 DNA barcodes were obtained from the specimens we studied. All sequences but one were over 600 base pairs (bp) long, with most representing full barcodes (658 bp). Additional sequences representing the species are found in BOLD, but we could not examine those specimens because they belong to projects that are not public yet. Overall, there are currently 32 sequences belonging to A. hemara in BOLD, 24 of them being public records and 19 being barcode compliant (Fig.
Details of the Barcode Index Number Registry for Apanteles hemara, data from BOLD (http://v4.boldsystems.org/).
In Kenya, the parasitoid was collected during outbreaks of two amaranth leaf-webber species, Spoladea recurvalis and Udea ferrugalis on two species of amaranth, Amaranthus cruentus L. and A. dubius L. It was successfully reared under laboratory conditions on both amaranth leaf-webber species at ICIPE. However, it failed to attack the leafworm species Spodoptera littoralis (Boisduval, 1833) and S. exigua (Hübner, 1808) (Noctuidae). During population dynamics studies carried out under field conditions at high and mid altitude levels in Central Kenya, field parasitism rates on S. recurvalis as low as 3% were obtained during outbreak periods while parasitism rates as high as 25 to 75% were achieved outside outbreak periods. These observations prompted studies for potential augmentative biological control strategies for early interventions aiming at preventing or reducing outbreaks of the amaranth leaf-webbers in farmers’ fields. Under laboratory conditions (25 ± 2°C, 60 ± 10% RH and 12L:12D photoperiod), A. hemara demonstrated high performance on S. recurvalis and U. ferrugalis both through high direct parasitism rates and significant non-reproductive mortalities caused to the hosts. The parasitized caterpillars can easily be distinguished from non-parasitized ones within the first two days after the parasitoid’s oviposition in the larva, through a significant reduction in feeding, movement and the lack of windowing on the leaf epidermis. Subsequently their growth rate is reduced and within four days after the parasitoid’s oviposition, parasitized caterpillars are considerably smaller in size than their non-parasitized counterparts, turn creamish and will all die whether the parasitoid successfully emerged or not. The developmental times are 12 and 13 days for male and female parasitoids respectively. Apanteles hemara is currently being considered for a conservative and augmentative biological control program against the amaranth leaf-webbers in Africa.
Gavin Broad (NHM, London, UK) kindly loaned the holotype specimen for study. The research at ICIPE was carried out with financial support from the German Federal Ministry of Economic Cooperation and Development (BMZ).