Print
Identity of parasitoid wasps (Hymenoptera, Braconidae and Eulophidae) reared from aquatic leaf-mining flies (Diptera, Ephydridae) on invasive Brazilian waterweed Egeria densa in South Africa
expand article infoSimon van Noort§, Rosali Smith|, Julie A. Coetzee|
‡ Iziko Museums of South Africa, Cape Town, South Africa
§ University of Cape Town, Cape Town, South Africa
| Rhodes University, Grahamstown, South Africa
Open Access

Abstract

The Brazilian waterweed, Egeria densa Planchon, 1849 (Hydrocharitaceae), is an invasive species in South Africa where it is a host plant for the aquatic leaf-miner Hydrellia egeriae Rodrigues-Júnior, 2015 (Ephydridae, Diptera). Efficacy of the biocontrol agent can potentially be affected by parasitoids. Three species of braconid parasitoid wasps were reared from puparia of Hydrellia egeriae. By comparison with the type specimens, these species have been determined to be Ademon lagarosiphonae van Achterberg, 2012 (Braconidae: Opiinae), Chaenusa anervata van Achterberg, 2012 and Chaenusa seminervata van Achterberg, 2012 (Braconidae: Alysiinae: Dacnusini), all previously recorded as parasitoids of an ephydrid dipterous aquatic leaf-miner, Hydrellia lagarosiphon Deeming, 2012, on Lagarosiphon major (Ridley, 1886) Moss ex Wager (Hydrocharitaceae) in South Africa. The chalcidoid, Janicharis africanus Gumovsky & Delvare, 2006 (Eulophidae), was also reared from Hydrellia egeriae and is possibly a hyperparasitoid of the braconids. South Africa is a new country record for J. africanus. We provide comprehensive images of all species including the braconid types and illustrated identification keys to the Afrotropical species of the two braconid genera are also provided. All images and online keys are available on WaspWeb (http://www.waspweb.org).

Keywords

Ademon, Alysiinae, aquatic weeds, biocontrol, Chaenusa, Entedoninae, Hydrellia egeriae, Hydrocharitaceae, Janicharis, Opiinae

Introduction

Egeria densa Planchon, 1849, Hydrocharitaceae (Brazilian waterweed; also known as leafy elodea or dense waterweed) is a rooted submerged aquatic macrophyte native to Brazil, Argentina and Uruguay (Cook and Urmi-König 1984; Cabrera Walsh et al. 2013). Stems are elongate, with a diameter of between 1 and 3 mm and irregular side branching (Cook and Urmi-König 1984). It prefers still to slow-moving water and can grow until it reaches the water surface (Yarrow et al. 2009). Leaves are small (10 to 44 mm long, 1.5 to 4.5 mm wide) and are characteristically grouped as four leaves per whorl (Cook and Urmi-König 1984). Vegetative growth occurs at double nodes on stems, which can either produce flowers, lateral branches or root buds (Yarrow et al. 2009). Egeria densa has been distributed around the world because it is an “oxygenator” and has a simple anatomy, making it an ideal aquarium and study plant (Yarrow et al. 2009; Coetzee et al. 2011a; June-Wells et al. 2012). Due to its ability to grow from fragments, it has established and become invasive in many countries (Hussner et al. 2017). In South Africa, it has taken advantage of open, eutrophic water following the successful management of floating aquatic weeds (Coetzee et al. 2011a). Egeria densa grows vigorously in eutrophic systems, which allows it to form dense uniform stands, with negative ecological, economic and societal impacts on the invaded system (Vundla et al. 2017; Smith et al. 2019).

A biocontrol investigation, conducted by the Centre for Biological Control at Rhodes University (South Africa) on the invasive Brazilian waterweed, produced four species of parasitoid wasps belonging to two families. These were reared from puparia of the ephydrid fly, Hydrellia egeriae Rodrigues-Júnior, 2015, a phytophagous biological control agent attacking Egeria densa. The Ephydridae contain a number of important naturally-occurring biological control agents of submerged invasive waterweeds (Wheeler and Center 2001; Baars et al. 2010; Coetzee et al. 2011a, b; Cabrera Walsh et al. 2013; Bownes 2014). These flies are attacked by braconid parasitoid wasps mainly belonging to the genera Ademon Haliday, 1833 and Opius Wesmael, 1835 (subfamily Opiinae); and Chaenusa Haliday, 1839 and Chorebus Haliday, 1833 (tribe Dacnusini, subfamily Alysiinae) (Yu et al. 2016). Both Ademon and Chaenusa contain aquatic parasitoid species of Hydrellia Robineau-Desvoidy, 1830 flies (Diptera, Ephydridae) (Kula and Zolnerowich 2008; van Achterberg and Prinsloo 2012; Kula and Harms 2016). We here provide determinations and photographs of the four species of parasitoid wasps recorded from puparia of the aquatic leaf-miner, Hydrellia egeriae developing on Brazilian waterweed Egeria densa to facilitate ongoing investigation into the efficacy of Hydrellia egeriae as a biocontrol agent in South Africa. We also provide illustrated identification keys to the species of the two braconid genera occurring in Africa.

Materials and methods

Photography

Images were acquired at SAMC with a Leica LAS 4.9 imaging system, comprising a Leica Z16 microscope with a Leica DFC450 Camera and 0.63× video objective attached. The imaging process, using an automated Z-stepper, was managed using the Leica Application Suite V. 4.9 software installed on a desktop computer. Diffused lighting was achieved using a Leica LED 5000 Dome.

Depositories

CASC California Academy of Sciences, San Francisco, USA (Curator: Brian Fisher);

CIRAD Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Curator: Philippe Lachenaud);

MNHN Muséum national d’Histoire naturelle, Paris (Curator: Bernardo Santos);

NHMUK Natural History Museum, London (Curator: Gavin Broad);

RMNH Naturalis Biodiversity Center, Leiden (Curator: Luc Willemse);

SAMC Iziko South African Museum, Cape Town, South Africa (Curator: Simon van Noort);

SANC National Collection of Insects, ARC, Pretoria (Curator: Vivienne Uys).

Results

Four parasitoid wasp species belonging to two families (Braconidae and Eulophidae) were reared from puparia of Hydrellia egeriae on Egeria densa. The three braconids, through comparison with the type specimens, were determined to be Ademon lagarosiphonae van Achterberg, 2012 (Opiinae), Chaenusa anervata van Achterberg, 2012 and Chaenusa seminervata van Achterberg, 2012 (Alysiinae), described from specimens reared from an aquatic ephydrid leafminer, Hydrellia lagarosiphon Deeming, 2012 on Lagarosiphon major, (Ridley, 1886) Moss ex Wager also of the family Hydrocharitaceae. The chalcidoid, Janicharis africanus Gumovsky & Delvare, 2006 (Eulophidae) was also reared from this ephydrid fly and is likely a hyper-parasitoid of the braconids.

All images included in this paper, as well as additional images and online interactive keys to the braconid species are available on WaspWeb (http://www.waspweb.org) (van Noort 2021):

http://www.waspweb.org/Ichneumonoidea/Braconidae/Alysiinae/index.htm

http://www.waspweb.org/Ichneumonoidea/Braconidae/Opiinae/index.htm

http://www.waspweb.org/Ichneumonoidea/Braconidae/Keys/index.htm

http://www.waspweb.org/Chalcidoidea/Eulophidae/Entedoninae/Janicharis/index.htm

Family Braconidae

Subfamily Alysiinae Leach, 1815

Tribe Dacnusini Foerster, 1862

Chaenusa Haliday, 1839

Alysia (Chaenusa) Haliday, 1839: 19. Type species: Bracon conjungens Nees von Esenbeck, 1812 (1811), by monotypy; type destroyed.

Chorebidea Viereck, 1914: 32. Type species: Alysia (Chorebus) nereidum Haliday, 1839, by original designation and monotypy. Treated as Chaenusa (Chorebidea) Viereck, 1914 (Zaykov 1986).

Chorebidea Nixon, 1943: 28. Preoccupied. Type species: Alysia (Chorebus) naiadum Haliday, 1839, by original designation and monotypy.

Chorebidella Riegel, 1950: 125. Type species: Chorebidella bergi Riegel, 1950, by original designation and monotypy.

Diagnosis

See Kula and Zolnerowich 2008.

Distribution

Afrotropical, Australian, Nearctic, Neotropical, Oriental and Palaearctic Regions (Kula and Zolnerowich 2008; Yu et al. 2016).

Key to the Afrotropical species of the genus Chaenusa Haliday

Modified after van Achterberg and Prinsloo 2012.

1 Vein 2–1A of forewing completely developed, resulting in a closed first subdiscal cell (A); vein 1-SR+M of forewing absent or, when present, largely unsclerotised (A); apical half of metasoma of female largely depressed (B); body black; face strongly narrowed in females, ventrally narrower than high (C) (subgenus Chaenusa Haliday, 1839) 2
Vein 2–1A of forewing largely absent, resulting in an open first subdiscal cell (a); vein 1-SR+M of forewing sclerotised, complete (a); apical half of metasoma of female strongly compressed; body largely reddish-brown; female face slightly wider than high (subgenus Chorebidea Viereck, 1914) Chaenusa testacea
2 Frons (fr) and face polished (A); face and eyes (ep) sparsely pubescent (A); each scutellar fovea (sf) with 2 or 3 longitudinal septa (A); first tergite (1t) longer than posteriorly wide, laterally strigous, medially rugulose (B); vein 1-SR+M of forewing pigmented, but largely unsclerotised (C); distal end of pterostigma (pt) comparatively elongate (C) Chaenusa seminervata
Frons (fr) and face granulate (a); face and eyes (ep) densely pubescent (a); each scutellar fovea (sf) with no obvious longitudinal septa (a); first tergite (1t) as long as posteriorly wide, overall rugulose without longitudinal strigae (b); vein 1-SR+M of forewing absent (c); distal end of pterostigma (pt) comparatively shorter and more robust (c) Chaenusa anervata

Chaenusa (Chaenusa) anervata van Achterberg, 2012

Figs 1, 2, 3, 4

Holotype

South Africa • female; Mpumalanga Prov., Lydenburg Fisheries, Lydenburg; 25°11'S, 30°48'E; 21.xi.2008; J.R. Baars, J.A. Coetzee, G.D. Martin; ex leaf-miner on Lagarosiphon major Hydrocharitaceae (SANC examined).

Figure 1. 

Chaenusa anervata Holotype female TYPH01927 (SANC) A habitus, lateral view B habitus, dorsal view C head and mesosoma, lateral view D head and mesosoma, dorsal view E head, anterior view F head, ventrolateral view.

Paratypes

South Africa • 1 female; KwaZulu-Natal Prov., Mooi River, Mearns Dam; 29°25'S, 29°97'E; 18.xi.2008; J.R. Baars, J.A. Coetzee, G.D. Martin; ex leaf-miner on Lagarosiphon major Hydrocharitaceae (RMNH not seen) • 1 male: Underberg, Farm Dam on Bushman’s Nek road; 30°27'S, 29°14'E; 16.xi.2008 (SANC examined) • 1 male; Mooi River, Mearns Weir, 29°15'S, 29°57'E, 17.xi.2008 (RMNH not seen).

Figure 2. 

Chaenusa anervata Holotype female TYPH01927 (SANC) A propodeum and metasoma, dorsal view B propodeum and metasoma, lateral view C scutellum, metanotum and propodeum, dorsal view D first tergite, dorsal view E wings F data labels.

Other material

South Africa • 1 male; KwaZulu-Natal, Midmar Dam, 29°32'21.35"S, 30°11'40.15"E, June 2019, R. Smith, Collected from Egeria densa infestation with Hydrellia egeriae pupae, reared in lab, MDMR-FOR-R05, SAM-HYM-P092803 (SAMC).

Biology

Parasitoid of aquatic leaf-mining flies (Ephydridae): Hydrellia lagarosiphon on Lagarosiphon major (Hydrocharitaceae) and Hydrellia egeriae on Egeria densa (Hydrocharitaceae).

Figure 3. 

Chaenusa anervata Paratype male (SANC) A habitus, lateral view B habitus, dorsal view C head, anterior view D wings, inset: data labels.

Distribution

South Africa.

Comments

According to van Achterberg and Prinsloo (2012), this species is similar to Chaenusa glabra Kula, 2009 (India, Pakistan), which has a two-segmented labial palp (three-segmented in C. anervata and C. seminervata), females with 12–14 antennal segments (at least 15 in C. anervata and 16–18 in C. seminervata) and males with 14–17 segments (22 in C. anervata and 17–24 in C. seminervata). The body is brown or brownish-yellow as opposed to black in C. anervata and C. seminervata (van Achterberg and Prinsloo 2012). Other sexually dimorphic characters in C. anervata encompass the forewing pterostigma, which is light brown in females and dark brown in males; the male first metasomal tergite is generally longer (1.1–1.3 times its apical width) than in the female (1.1 times apical width) (van Achterberg and Prinsloo 2012); in addition, the compound eyes in females converge far more strongly (narrowest ventral width of face 0.55× broadest dorsal width) towards the clypeus than in the males (narrowest ventral width of face 0.90× broadest dorsal width); however, the overall relative dimensions of the face relative to the broadest width just below the toruli are equivalent in the two sexes, being slightly wider than high (females H:W = 9:10; males H:W = 10:11).

Figure 4. 

Chaenusa anervata male SAM-HYM-P092803 (SAMC) A habitus, lateral view B habitus, dorsal view C head, anterior view D wings, inset: data labels.

Chaenusa (Chaenusa) seminervata van Achterberg, 2012

Figs 5, 6, 7, 8, 9

Holotype

South Africa • female; Mpumalanga Prov., Lydenburg Fisheries, Lydenburg; 25°11'S, 30°48'E; 21.xi.2008; J.R. Baars, J.A. Coetzee, G.D. Martin; ex leaf-miner on Lagarosiphon major Hydrocharitaceae (SANC examined).

Figure 5. 

Chaenusa seminervata Holotype female TYPH01928 (SANC) A habitus, lateral view B habitus, dorsal view C head and mesosoma, lateral view D head and mesosoma, dorsal view E head, anterior view F head, ventrolateral view.

Paratypes

South Africa • 1 female; Mpumalanga Prov., Belfast, Lakenvlei Wetland; 25°60'S, 30°05'E (RMNH not seen) • 1 male; KwaZulu-Natal Prov., Stillwater Dam, Rosetta; 29°30'S, 29°97'E; 17.xi.2008; J.R. Baars, J.A. Coetzee, G.D. Martin; ex leaf-miner on Lagarosiphon major Hydrocharitaceae (RMNH not seen) • 4 males; Dieu Donne Farm Dam, Sani Pass; 29°68'407"S, 29°48'949"E; 16.xi.2008; J.R. Baars, J.A. Coetzee, G.D. Martin; reared from leaf-miner on Lagarosiphon major (Hydrocharitaceae) (SANC examined, RMNH not seen).

Figure 6. 

Chaenusa seminervata Holotype female TYPH01928 (SANC) A propodeum and metasoma, dorsal view B propodeum and metasoma, lateral view C mesosoma and first tergite, dorsal view D propodeum and first tergite, dorsal view E wings F data labels.

Other material

South Africa • 1 male; KwaZulu-Natal, Midmar Dam, 29°32'21.35"S, 30°11'40.15"E, June 2019, R. Smith, collected from Egeria densa infestation with Hydrellia egeriae pupae, reared in lab, MDMR-FOR-R01, SAM-HYM-P092800 (SAMC) • 1 female, idem, except MDMR-FOR-R02, SAM-HYM-P092801 (SAMC) • 1 male, idem, except MDMR-FOR-R04, SAM-HYM-P092802 (SAMC) • 1 male, idem, except MDMR-FOR-R09, SAM-HYM-P092804 (SAMC) • 1 male, idem, except MDMR-FOR-R10, SAM-HYM-P092805 (SAMC) • 1 male, idem, except MDMR-FOR-R14, SAM-HYM-P092806 (SAMC).

Figure 7. 

Chaenusa seminervata female SAM-HYM-P092801 (SAMC) A habitus, lateral view B habitus, dorsal view C head and mesosoma, lateral view D head and mesosoma, dorsal view E head, anterior view F head, ventrolateral view.

Biology

Parasitoid of aquatic leaf-mining flies (Ephydridae): Hydrellia lagarosiphon on Lagarosiphon major (Hydrocharitaceae) and Hydrellia egeriae on Egeria densa (Hydrocharitaceae).

Figure 8. 

Chaenusa seminervata female SAM-HYM-P092801 (SAMC) A metasoma, dorsal view B metasoma, lateral view C scutellum, metanotum, propodeum and first tergite, dorsal view D first tergite, dorsal view E wings, inset: data labels F vertex of head.

Distribution

South Africa.

Comments

The Neotropical species Chaenusa aurantium Kula & Martinez, 2009 was reared from an undescribed species of Hydrellia in Argentina under evaluation for control of Egeria densa in the United States (Kula et al. 2009). Chaenusa seminervata keys to C. aurantium (terminal maxillary palpomere is brown) in the key to New World species (Kula and Zolnerowich 2008; Kula et al. 2009), but it is distinct from C. aurantium in head colour, sculpture and setation of the frons, as well as mesoscutal, mesopleural and propodeal sculpture. Sexual dimorphism of Chaenusa seminervata is exhibited in the following characters: females with 16–18 antennal segments, males with 17–24 segments; the forewing pterostigma is light brown in females and dark brown in males; in addition, the compound eyes in females converge less strongly (narrowest ventral width of the face 0.75× broadest dorsal width) towards the clypeus than in C. anervata, but still more strongly than in males (narrowest ventral width of the face 0.81× broadest dorsal width); however, the overall relative dimensions of the face relative to the broadest width just below the toruli are equivalent in the two sexes, being slightly wider than high (females H:W = 10:12; males H:W = 9:11).

Figure 9. 

Chaenusa seminervata male SAM-HYM-P092802 (SAMC) A habitus, lateral view, inset: data labels B habitus, dorsal view C head and mesosoma, lateral view D head, anterior view.

Chaenusa (Chorebidea) testacea (Granger, 1949)

Chorebidea testacea Granger, 1949.

Syntypes

Madagascar • 2 females, 1 male; (MNHN). Types not seen.

Biology

Unknown.

Distribution

Madagascar.

Subfamily Opiinae Blanchard, 1845

Tribe Opiini Blanchard, 1845

Subtribe Ademonina Fischer, 1964

Ademon Haliday, 1833

Ademon Haliday, 1833: 266. Type species: Bracon decrescens Nees von Esenbeck, 1812 (1811), by monotypy; type destroyed.

Lytacra Foerster, 1863: 266. Type species: Lytacra stygia Foerster, 1863, by monotypy and original designation.

Giardinaia de Stefani-Perez, 1902. Type species: Giardinaia urinator de Stefani, 1902, by monotypy.

Analostania Viereck, 1916. Type species: Analostania tenuipes Viereck, 1916, by monotypy and original designation.

Diagnosis

Heavily-sculptured body with presence of an epicnemial carina (= prepectal carina), more or less developed ventrally; occipital carina complete dorsally; malar suture absent; crenulate depression above eye present; vein SR1 of forewing incomplete, not reaching the wing margin and resulting in an open marginal cell; medio-posteriorly scutellum with continuation of lateral elevated area; hind tibia, tarsus and tarsal claws very slender; second metasomal tergite distinctly longer than third tergite and second metasomal suture distinct (Wu et al. 2014; Wharton 2021).

Distribution

Afrotropical, Nearctic, Oriental and Palaearctic Regions (van Achterberg and Prinsloo 2012).

Key to the Afrotropical species of the genus Ademon Haliday

Line drawings modified from van Achterberg and Prinsloo 2012.

1 Vein 3-SR of forewing 5.0 times as long as vein r; vein 1-SR+M slightly sinuate; vein r-m inclivous (A) Ademon angolanus
Vein 3-SR 2.1–3.5 times as long as vein r; vein 1-SR+M usually strongly sinuate; vein r-m vertical or nearly so (a) Ademon lagarosiphonae

Ademon angolanus Fischer, 1963

Holotype

Angola • female; CAS-TYPE-10370 (CASC). Not seen.

Biology

Unknown.

Distribution

Angola.

Ademon lagarosiphonae van Achterberg, 2012

Figs 10, 11, 12, 13, 14, 15, 16

Holotype

South Africa • female Mpumalanga, Lydenburg Fisheries, Lydenburg, 25°11'S, 30°48'E, 21.xi.2008, J.R. Baars, J.A. Coetzee, G.D. Martin, reared from leaf-miner on Lagarosiphon major (Hydrocharitaceae) (SANC examined).

Figure 10. 

Ademon lagarosiphonae Holotype female TYPH01926 (SANC) A habitus, lateral view B habitus, dorsal view C head and mesosoma, lateral view D head and mesosoma, dorsal view E head, anterior view F head, ventroanterior view.

Paratypes

South Africa • 1 female, 1 male; same data as for holotype (SANC examined).

Figure 11. 

Ademon lagarosiphonae Holotype female TYPH01926 (SANC) A head and mesosoma, laterodorsal view B metasoma, lateral view C metasoma, dorsal view D metasomal terminal tergites, dorsal view.

Other material

South Africa • 1 male; Eastern Cape, East London, Nahoon River; 32°57'45.41"S, 27°54'41.59"E; 12 December 2018; R. Smith; Collected from Egeria densa infestation with Hydrellia egeriae pupae; SAM-HYM-P095098 (SAMC) • 1 female: idem; except for 9 May 2019; R. Smith; Collected from Egeria densa infestation with Hydrellia egeriae pupae; reared in lab; NHN-FOR-R01; SAM-HYM-P092742 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R01; SAM-HYM-P092743 (SAMC) • 1 female: idem; except for NHN-FOR-R02; SAM-HYM-P092744 (SAMC) • 1 male: idem; except for NHN-FOR-R03; SAM-HYM-P092746 (SAMC) • 1 male: idem; except for NHN-FOR-R04; SAM-HYM-P092748 (SAMC) • 1 female: idem; except for NHN-FOR-R05; SAM-HYM-P092750 (SAMC) • 1 female: idem; except for NHN-FOR-R06; SAM-HYM-P092752 (SAMC) • 1 male: idem; except for July 2019; NHN-WINTER-FOR-R03; SAM-HYM-P092747 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R04; SAM-HYM-P092749 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R05; SAM-HYM-P092751 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R06; SAM-HYM-P092753 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R07; SAM-HYM-P092756 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R08; SAM-HYM-P092757 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R09; SAM-HYM-P092759 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R10; SAM-HYM-P092760 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R11; SAM-HYM-P092761 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R12; SAM-HYM-P092764 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R13; SAM-HYM-P092765 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R14; SAM-HYM-P092767 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R15; SAM-HYM-P092768 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R16; SAM-HYM-P092769 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R17; SAM-HYM-P092770 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R18; SAM-HYM-P092771 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R19; SAM-HYM-P092772 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R20; SAM-HYM-P092773 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R21; SAM-HYM-P092774 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R22; SAM-HYM-P092775 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R23; SAM-HYM-P092776 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R24; SAM-HYM-P092777 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R25; SAM-HYM-P092778 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R26; SAM-HYM-P092779 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R27; SAM-HYM-P092780 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R28; SAM-HYM-P092781 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R30; SAM-HYM-P092782 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R31; SAM-HYM-P092783 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R32; SAM-HYM-P092784 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R33; SAM-HYM-P092785 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R34; SAM-HYM-P092786 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R35; SAM-HYM-P092787 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R36; SAM-HYM-P092788 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R37; SAM-HYM-P092789 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R38; SAM-HYM-P092790 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R39; SAM-HYM-P092791 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R40; SAM-HYM-P092792 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R41; SAM-HYM-P092793 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R42; SAM-HYM-P092794 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R43; SAM-HYM-P092795 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R44; SAM-HYM-P092796 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R45; SAM-HYM-P092797 (SAMC) • 1 male: idem; except for NHN-WINTER-FOR-R46; SAM-HYM-P092798 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R47; SAM-HYM-P092799 • 1 male; KwaZulu-Natal; Midmar Dam; 29°32'21.35"S, 30°11'40.15"E; June 2019; R. Smith; Collected from Egeria densa infestation with Hydrellia egeriae pupae; reared in lab; MDMR-FOR-R03; SAM-HYM-P092745 (SAMC) • 1 male: idem; except for MDMR-FOR-R06; SAM-HYM-P092754 (SAMC) • 1 male: idem; except for MDMR-FOR-R07; SAM-HYM-P092755 (SAMC) • 1 male: idem; except for MDMR-FOR-R08; SAM-HYM-P092758 (SAMC) • 1 male: idem; except for MDMR-FOR-R11; SAM-HYM-P092762 (SAMC) • 1 female: idem; except for MDMR-FOR-R12; SAM-HYM-P092763 (SAMC) • 1 male: idem; except for MDMR-FOR-R13; SAM-HYM-P092766 (SAMC).

Figure 12. 

Ademon lagarosiphonae Holotype female TYPH01926 (SANC) A scutellum, metanotum and propodeum, dorsal view B metasomal tergites 1–2, lateral view C forewing D data labels.

Biology

Parasitoid of aquatic leaf-mining flies (Ephydridae): Hydrellia lagarosiphon on Lagarosiphon major (Hydrocharitaceae) and Hydrellia egeriae on Egeria densa (Hydrocharitaceae).

Distribution

South Africa.

Comments

This species exhibits a disparate range of colour forms, from being completely black (Figs 14 A–F; 15 A–F; 16A, B) through to being completely yellowish-orange, as in the holotype (Figs 10 A–F; 11 A–D; 12 A, B) with intermediate grades present (Figs 13A, B; 16E, F). This extent of intra-specific colour difference is also present in the Palaearctic type species of the genus, A. descrescens (Nees, 1812 [1811]) (van Achterberg and Prinsloo 2012).

Figure 13. 

Ademon lagarosiphonae Paratype female (A, B) and paratype male (C, D) (SANC) A habitus, lateral view B habitus, dorsal view, inset: data labels C habitus, lateral view, inset: data labels D habitus, dorsal view.

Figure 14. 

Ademon lagarosiphonae female SAM-HYM-P092756 (SAMC) A habitus, lateral view B habitus, dorsal view C head and mesosoma, lateral view D head and mesosoma, dorsal view E head, anterior view F head, ventroanterior view.

Figure 15. 

Ademon lagarosiphonae female SAM-HYM-P092756 (SAMC) A head and mesosoma, laterodorsal view B metasoma, lateral view C metasoma, dorsal view D metasomal terminal tergites, dorsal view.

Figure 16. 

Ademon lagarosiphonae females SAM-HYM-P092756 (A–D), SAM-HYM-P092796 (E), SAM-HYM-P092744 (F) (SAMC) A scutellum, metanotum and propodeum, dorsal view B metasomal tergites 1–2, lateral view C forewing D data labels E habitus, lateral view, inset: data labels F habitus, lateral view, inset: data labels. Figures E and F illustrate intermediate colour forms.

Family Eulophidae

Entedoninae Foerster, 1856

Janicharis Gumovsky & Delvare, 2006

Type species

Janicharis africanus Gumovsky & Delvare, 2006, by monotypy and original designation.

Janicharis africanus Gumovsky & Delvare, 2006

Fig. 17

Holotype

Cameroon • female; Maroua, Djarengol; Malaise trap; 26.ix.1984; G. Delvare (MNHN not seen).

Paratypes

Cameroon • 3 females, idem (CIRAD) • 3 females, idem (RMNH) • Nigeria • Oyo, Ibadan, Iita Compound; x.1987; J. Noyes (NHMUK) • Madagascar • Lac Alaotra; on Oryza sativa, 17.x.1991; P. Bousses (CIRAD). Paratypes not seen.

Other material

South Africa • 1 female: Eastern Cape, East London, Nahoon river; 32°57'45.41"S, 27°54'41.59"E; NHN-WINTER-FOR-R02; July 2019; R. Smith; reared in laboratory; ex Hydrellia egeriae pupa collected from host plant Egeria densa; SAM-HYM-P092807 (SAMC) • 1 female: idem; except for NHN-WINTER-FOR-R29 and SAM-HYM-P092808 (SAMC) • 1 female: idem; except for: February 2019; R. Smith; Collected from Egeria densa infestation with Hydrellia egeriae pupae; SAM-HYM-P095099 (SAMC) • 1 male: idem; except for SAM-HYM-P095100 (SAMC).

Diagnosis

Uniquely defined by two large foveae situated anterio-medially on propodeum; anterolateral propodeal strip wide, somewhat angulate above spiracle. Characters shared with morphologically-similar congeners: pronotum dorsally reduced, placed significantly below the level of mesoscutum; propodeum with anterolateral propodeal strips; anterior propodeum with basal cup and foveae on sides; metanotum with anteriorly-delimited foveae at sides of dorsellum; long postmarginal vein (Gumovsky et al. 2006).

Biology

Previously unknown. Here, we record the species as a parasitoid associated with immature stages of the aquatic ephydrid fly Hydrellia egeriae, having been reared from puparia along with specimens of Ademon lagarosiphonae and Chaenusa seminervata and hence is potentially a hyperparasitoid attacking the braconids rather than the fly. The eulophid subfamily Entedoninae harbours a wide range of life style strategies including species that are usually solitary or gregarious endoparasitoids (more rarely ectoparasitoids or hyper-parasitoids) of concealed dipteran, lepidopteran, coleopteran, hymenopteran or hemipteran larvae or rarely of eggs or pupae. Janicharis africanus is morphologically similar to the genera Hakuna Gumovsky & Delvare, 2006 and Pediocharis Bouček, 1988 (Gumovsky et al. 2006) and may, therefore, exhibit similar lifestyle strategies. The monotypic species Hakuna matata Gumovsky & Bouček, 2006 was reared from conical insect galls on a forest plant and each gall contained several pupae in separate cells; adult wasps emerged through a single hole at the apex of the gall. Based on these notes by the collector, Gumovsky et al. (2006) hypothesised H. matata to be a parasitoid of the gall former. Biology of Pediocharis is unknown and, together with the lack of detail concerning the biology of Hakuna, makes it difficult to predict whether J. africanus is, indeed, a hyper-parasitoid or not. A more remote possibility of morphological congeneric similarity for Janicharis is to Chrysocharis Foerster, 1856 (Gumovsky et al. 2006), but this genus contains a very broad range of lifestyle strategies, including endo- and ectoparasitoids and facultative hyperparasitoids (Yu et al. 2016), which does not provide any further enlightenment as to potential possibilities for Janicharis. The only recourse is to pursue direct investigation of the biology for J. africanus in the field.

Distribution

Cameroon, Nigeria, Madagascar and South Africa (new country record).

Comments

The reared specimens were identified by corroboration of morphological character attributes with the original description and type photographs of J. africanus (Gumovsky et al. 2006). The genus is monotypic.

Figure 17. 

Janicharis africanus female SAM-HYM-P092808 (SAMC) A habitus, lateral view B habitus, dorsal view C head, anterior view D data labels.

Discussion

This paper contributes towards an understanding of the impact of parasitoid wasps on potential biocontrol agents of invasive waterweeds, specifically that of Brazilian waterweed, which is targeted by biocontrol agents in the genus Hydrellia. Numerous studies have been conducted in the New World and Oriental Region assessing, in particular, species delimitation and host relationships of Chaenusa species (Kula et al. 2006; Kula and Zolnerowich 2008; Kula 2009; Kula et al. 2009; Kula and Harms 2016). Efficacy of the biocontrol agent can potentially be affected by parasitoids and the extent to which these Chaenusa parasitoid wasps, as well as species of Ademon and Janicharis, affect these waterweed biocontrol programmes in various parts of the world is under ongoing investigation, including in South Africa (Rosali Smith, in prep.). Janicharis africanus may be a hyper-parasitoid of the braconids, further complicating the impact of the biocontrol efficacy of Hydrellia egeriae, although if it is a hyper-parasitoid, this species should potentially have a positive impact on the biocontrol programme. Elucidation of the precise lifestyle strategy of J. africanus is under ongoing investigation by the Centre for Biological Control at Rhodes University (South Africa). Ramifications of adaptation by the indigenous parasitoids, documented in this paper, to introduced hosts released as potential biocontrol agents against targeted invasive species in South Africa, will be detailed in an accompanying publication (Smith, Coetzee, van Noort, in prep). This paper provides a taxonomic contribution towards resources that will facilitate identification of parasitoid wasps reared in the process of establishing effective control programmes for invasive waterweeds in Africa.

Acknowledgements

We thank Denis Brothers, Mark Shaw, Cees van Achterberg and an anonymous reviewer for their critical reviews that improved the manuscript. This research was funded through the Department of Environmental Affairs, Natural Resource Management Programme’s Working for Water programme. Further funding for this work was provided by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation of South Africa (grant nos. 89967, 109244 and 109683 to Martin Hill, SARCHi Chair). Simon van Noort was funded by a South African NRF FBIP grant no. 98115.

References

  • Achterberg C van, Prinsloo GL (2012) Braconidae (Hymenoptera: Opiinae, Alysiinae) reared from aquatic leaf-mining Diptera on Lagarosiphon major (Hydrocharitaceae) in South Africa. African Entomology 20(1): 124–133. https://doi.org/10.4001/003.020.0116
  • Baars JR, Coetzee JA, Martin G, Hill M, Caffrey J (2010) Natural enemies from South Africa for biological control of Lagarosiphon major (Ridl.) Moss ex Wager (Hydrocharitaceae) in Europe. Hydrobiologia 656(1): 149–158. https://doi.org/10.1007/s10750-010-0427-0
  • Blanchard E (1845) Histoire Naturelle des Insecte Leurs Moeurs, Leurs Métamorphoses et Leur Classification ou Traite Elementaire D’entomologie. Tome Premier. Librairie de F. Didot Freres, Paris, 398 pp.
  • Bouček Z (1988) Australasian Chalcidoidea (Hymenoptera). A biosystematic revision of genera of fourteen families, with a reclassification of species. CAB International, Wallingford, Oxon, U.K., Cambrian News Ltd. Aberystwyth, Wales, 832 pp.
  • Bownes A (2014) Suitability of a leaf-mining fly Hydrellia sp., for biological control of the invasive aquatic weed, Hydrilla verticillata in South Africa. BioControl 59(6): 771–780. https://doi.org/10.1007/s10526-014-9615-6
  • Cabrera Walsh G, Dalto YM, Mattioli FM, Carruthers RI, Anderson LW (2013) Biology and ecology of Brazilian elodea (Egeria densa) and its specific herbivore, Hydrellia sp., in Argentina. BioControl 58(1): 133–147. https://doi.org/10.1007/s10526-012-9475-x
  • Coetzee JA, Bownes A, Martin GD (2011a) Prospects for the biological control of submerged macrophytes in South Africa. In: Moran VC, Hoffmann JN, Hill MP (Eds) Biological Control of Invasive Alien Plants in South Africa (1992–2010). African Entomology 19(2), 469–487. https://doi.org/10.4001/003.019.0203
  • Coetzee JA, Hill MP, Byrne MJ, Bownes A (2011b) A review of the biological control programmes on Eichhornia crassipes (C.Mart.) Solms (Pontederiaceae), Salvinia molesta D.S.Mitch. (Salviniaceae), Pistia stratiotes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragaceae) and Azolla filiculoides Lam. (Azollaceae) in South Africa. African Entomology 19(2): 451–468. https://doi.org/10.4001/003.019.0202
  • De Stefani-Perez T (1902) Osservazioni biologische sopra un Braconide aquatico, Giardinaia urinator, a descrizione di due altri Imenotteri nuovi. Zoologische Jahrbücher Abteilung für Systematik 15: 625–634. https://doi.org/10.5962/bhl.part.19039
  • Deeming JC (2012) A new species of Hydrellia Rob. Desv. (Diptera: Ephydridae) developing in Lagarosiphon major (Hydrocharitaceae) in South Africa. African Entomology 20(2): 217–221. https://doi.org/10.4001/003.020.0206
  • Fischer M (1963) Die Opiinae der äthiopischen Region (Hymenoptera: Braconidae). Beiträge zur Entomologie 13(5/6): 662–747.
  • Fischer M (1964) Die Opiinae der nearktischen Region (Hymenoptera, Braconidae). I. Teil. Polskie Pismo Entomologiczne 34: 197–530.
  • Foerster A (1856) Hymenopterologische Studien. 2. Chalcidiae und Proctotrupii. Aachen, 152 pp.
  • Foerster A (1862) Synopsis der Familien und Gattungen der Braconiden. Verhandlungen des Naturhistorischen Vereins der Preussischen Rheinlande und Westfalens 19: 225–288.
  • Granger C (1949) Braconides de Madagascar. Mémoires de l’Institut Scientifique de Madagascar (A) 2: 1–428.
  • Gumovsky A, Bouček Z, Delvare G (2006) New genera and species of Afrotropical Entedoninae (Hymenoptera, Eulophidae). Zoologische Mededelingen, Leiden 80–1(4): 73–85.
  • Haliday AH (1833) An essay on the classification of the parasitic Hymenoptera of Britain, which correspond with the Ichneumones minuti of Linnaeus. Entomological Magazine 1(3): 259–276.
  • Hussner A, Stiers I, Verhofstad MJJM, Bakker ES, Grutters BMC, Haury J, van Valkenburg JLCH, Brundu G, Newman J, Clayton JS, Anderson LWJ, Hofstra D (2017) Management and control methods of invasive alien freshwater aquatic plants: A review. Aquatic Botany 136: 112–137. https://doi.org/10.1016/j.aquabot.2016.08.002
  • June-Wells M, Vossbrinck CR, Gibbons R, Bugbee G (2012) The aquarium trade: A potential risk for nonnative plant introductions in Connecticut, USA. Lake and Reservoir Management 28(3): 200–205. https://doi.org/10.1080/07438141.2012.693575
  • Kula RR (2009) A new species of Chaenusa (Hymenoptera: Braconidae) reared from Hydrellia pakistanae and Hydrellia sarahae laticapsula (Diptera: Ephydridae) infesting Hydrilla verticillata (Alismatales: Hydrocharitaceae) in India and Pakistan. The Florida Entomologist 92(1): 139–146. https://doi.org/10.1653/024.092.0121
  • Kula RR, Harms N (2016) A new species of Chaenusa Haliday sensu lato (Hymenoptera: Braconidae) from the Nearctic Region. Proceedings of the Entomological Society of Washington 118(1): 101–108. https://doi.org/10.4289/0013-8797.118.1.101
  • Kula RR, Zolnerowich G (2008) Revision of New World Chaenusa Haliday sensu lato (Hymenoptera: Braconidae: Alysiinae), with new species, synonymies, hosts, and distribution records. Proceedings of the Entomological Society of Washington 116(1): 1–60. https://doi.org/10.4289/0013-8797-110.1.1
  • Kula RR, Zolnerowich G, Ferguson CJ (2006) Phylogenetic analysis of Chaenusa sensu lato (Hymenoptera: Braconidae) using mitochondrial NADH 1 dehydrogenase gene sequences. Journal of Hymenoptera Research 15: 251–265.
  • Kula RR, Martínez JJ, Cabrera Walsh G (2009) Supplement to revision of New World Chaenusa Haliday sensu lato (Hymenoptera: Braconidae: Alysiinae). Proceedings of the Entomological Society of Washington 111(3): 641–655. https://doi.org/10.4289/0013-8797-111.3.641
  • Nees von Esenbeck CG (1811) (1812 [1811]) Ichneumonides Adsciti, in Genera et Familias Divisi. Magazin Gesellschaft Naturforschender Freunde zu Berlin 5: 3–37.
  • Planchon JE (1849) Sur L’ Anacharis alsinastrum, plante anglaise supposée nouvelle avec un synopsis des espèces d’Anacharis en d’Apalanthe et des descriptions de quelques hydrocharidées nouvelles. Annales des Sciences Naturelles. Botanique Series 3 11: 79–80.
  • Riegel GT (1950) A new genus and species of Dacnusini (Hym.: Braconidae). Entomological News 61: 125–129.
  • Robineau-Desvoidy JB (1830) Essai sur les Myodaires. Mémoires Preséntes par divers Savans a l’Académie Royale des Sciences de l’Institut de France, et Imprimés par son Ordre Sciences Mathématiques et Physiques 2(2): 1–813.
  • Rodrigues-Júnior FA, Mathis WN, Hauser M (2015) Argentine Hydrellia Robineau-Desvoidy (Diptera, Ephydridae): New species and key to identification. Zootaxa 3957(1): 131–136. https://doi.org/10.11646/zootaxa.3957.1.11
  • Smith R, Mangan R, Coetzee JA (2019) Risk assessment to interpret the physiological host range of Hydrellia egeriae, a biocontrol agent for Egeria densa. BioControl 64(4): 447–456. https://doi.org/10.1007/s10526-019-09942-4
  • van Noort S (2021) WaspWeb: Hymenoptera of the Afrotropical region. http://www.waspweb.org [Accessed: 4/January/2021]
  • Viereck HL (1916) One new genus and five new species of Ichneumon-flies. Proceedings of the Biological Society of Washington 29: 165–172.
  • Vundla T, Blignaut JN, Crookes DC (2017) Aquatic weeds: To control or not to control. The case of the Midmar Dam, KwaZulu-Natal, South Africa. African Journal of Agricultural and Resource Economics 12(4): 412–429.
  • Wesmael C (1835) Monographie des Braconides de Belgique. Nouveaux. Mémoires de l’Academie Royale des Sciences et Belles-lettres Bruxelles 9: 1–252.
  • Wheeler GS, Center TD (2001) Impact of the biological control agent Hydrellia pakistanae (Diptera: Ephydridae) on the submersed aquatic weed Hydrilla verticillata (Hydrocharitaceae). Biological Control 21(2): 168–181. https://doi.org/10.1006/bcon.2001.0927
  • Wu Q, He J-H, Chen X-X (2014) The genus Ademon Haliday (Hymenoptera: Braconidae: Opiinae) from China, with descriptions of two new species. Zootaxa 3794: 294–298. https://doi.org/10.11646/zootaxa.3794.2.8
  • Yarrow M, Marín VH, Finlayson M, Tironi A, Delgado LE, Fischer F (2009) The ecology of Egeria densa Planchon (Liliopsida: Alismatales): a wetland ecosystem engineer? Revista Chilena de Historia Natural 82(2): 299–313. https://doi.org/10.4067/S0716-078X2009000200010
  • Yu DS, van Achterberg C, Horstman K (2016) Taxapad 2016, Ichneumonoidea 2015. Nepean, Ontario. Database on flash-drive.
  • Zaykov AN (1986) Description of two new Dacnusini species (Hymenoptera, Braconidae). Acta Zoologica Bulgarica 32: 52–55.