Translator Disclaimer
1 June 2008 Dacnusa cicerina (Hymenoptera: Braconidae: Alysiinae), A New Species of Endoparasitoid of Liriomyza cicerina (Diptera: Agromyzidae)
Author Affiliations +
Abstract

The larvae, pupa, adults, and venom apparatus of Dacnusa cicerina sp. n., an endoparasitoid of Liriomyza cicerina (Rondani), found on Cicer arietinum Linnaeus in Spain, are described, illustrated, and compared with those of allied species. The mature larva of Eurytoma sp., possibly a hyperparasitoid of D. cicerina, also is described, illustrated, and compared with those of allied species. Keys to discriminate adults are provided and morphological structures of phylogenetic value are discussed. The adults of D. cicerina are similar to those of Dacnusa rodriguezi Docavo & Tormos (1997). The immature larvae are similar to those of Dacnusa areolaris (Nees) and Dacnusa dryas (Nixon), and the mature larva is very similar to that of D. dryas, from which it differs in having scale-like sensilla (“setae”) on the thorax and abdomen. The cast skin of the final instar, like those described for Dacnusa Haliday, has a pleurostoma with well differentiated mandible processes and a long stipital sclerite. The venom apparatus of this species is very similar to that of Dacnusa flavicoxa Thomson, differing from it in length of the reservoir and the number of gland filaments. The mature larva of Eurytoma Illiger described here, despite its endoparasitoid nature, has well differentiated pleural and ventral setae.

From a study undertaken in 1987-1992 on Dacnusini (Hymenoptera: Braconidae: Alysiinae) and their agromyzid (Diptera: Agromyzidae) hosts in the Iberian Peninsula, data were gathered on the parasitoids of Liriomyza cicerina (Rondani), a species injurious to Cicer arietinum Linnaeus (chickpea) cultures. Although this species also feeds on Ononis and Hymenocarpus elsewhere, in the Mediterranean area it mainly feeds on chickpeas, for which it may be a serious pest.

In the study cited above, Dacnusa cicerina sp. n. was obtained from L. cicerina feeding on chickpea plants, and Eurytoma sp., a possible hyperparasitoid of D. cicerina, also was obtained. Another species of Braconidae, which has been observed parasitizing L. cicerina on chickpeas in Spain, Opius monilicornis Fischer (Garrido et al. 1992) also was found. Detailed information on the economic importance and the biology of L. cicerina has been given by Spencer (1973, 1976, 1990).

The genus Dacnusa Haliday belongs to the subfamily Alysiinae and to the tribe Dacnusini, most of whose members attack agromyzid flies. The classification and biology of this genus, which has approximately 77 European species (Achterberg 2004), have been studied by Griffiths (1964, 1966, 1968, 1984); Tobias (1995); and Belokobylskij et al. (1998). The structures that allow characterization of the final instar have been described in depth only in Dacnusa rodriguezi Docavo & Tormos (Pardo et al. 2000). Detailed studies addressing the variation in gland and reservoir morphology of the venom apparatus in species of Dacnusini recently have been conducted by Quicke et al. (1997) and Tormos et al. (2003).

The genus Eurytoma Illiger is the largest of the family Eurytomidae (Noyes 2001), and includes species displaying diverse larval feeding habits. This study addresses the larval morphology of an undetermined species of this genus, probably an hyperparasitoid of the new species of Dacnusa described here. A recent study of the mature larvae of Eurytoma has been carried out by Tormos et al. (2004).

Materials and Methods

Adults and exuviae of the final instar of D. cicerina, and imagos of Eurytoma sp. were obtained in Aug 1988 from pupae of L. cicerina whose larvae were mining leaves of C. arietinum in Ayora (Valencia, Spain). To collect specimens in both cases, we picked structures from plants that were infested with larvae of the agromyzids and placed them in plastic bottles of suitable dimensions whose openings were covered with gauze held in place with a rubber band. These receptacles were kept under environmental conditions of temperature, relative humidity (RH), and photoperiod. The methodology used for opening the puparium and preparing the cast skins was that proposed by Tormos et al. (2003).

To study the different larval stages of D. cicerina, in Jun 1990, we collected leaves of C. arietinum that were mined by L. cicerina, and took them to the laboratory, where they were placed in the same kind of receptacle as above and kept under environmental conditions. The parasitoids that emerged from the host puparia were fed with honey impregnated on strips of blotting paper or with sugar and water. Females aged between 24 and 72 h were placed individually in Petri dishes (9 × 1.5 cm) and provided daily with leaves of C. arietinum infested with larvae of different stages of L. cicerina. To study the larval development of the parasitoid, parasitized material was kept in a chamber at 21-23°C, 60-80 RH, and a photoperiod of 16L:8D, and the hosts were periodically dissected. Where possible, these observations were complemented with the dissection of specimens of hosts parasitized in the field. These dissections allowed us to study the mature larva of an undetermined species of Eurytoma. All dissections were performed in 0.9% saline solution. To study the development of the larvae of D. cicerina, the methodology of Tormos et al. (2003) was used. For the microscopic preparation of the larval stages of both the braconid and the eurytomid, the methods of Tormos et al. (2003, 2004) were employed.

The venom apparatus was prepared and drawn according to the method described by Quicke et al. (1992, 1997) with clorazol black staining for dry museum specimens. The venom apparatus was treated with a hydroxide solution, after which the soft tissue could be removed. It was then possible to observe the characteristics of the remaining chitinous gland intima, which are not apparent from examination of an intact gland and reservoir. The material examined (adults, immature stages, and venom apparatus) is deposited at the “Torres Sala” Entomological Foundation (Valencia, Spain).

The terminology for the body morphology, biometric data, and wing venation of the adults of Dacnusa follows Wharton et al. (1997). The terminology used in the description of the different structures of the immature stages of the braconid and of the eurytomid is that used by Tormos et al. (2003, 2004). The terminology used for characteristics of the gland and reservoir parts of the venom apparatus follows Tormos et al. (2003).

Results and Conclusions

Dacnusa cicerina sp. n. (Fig. 1a-d)

Type Material. SPAIN: Valencia: Ayora (30SXJ6825), 25-VI-1988 (date of host capture)/8-11-VIII-1988 (emergence date of the parasitoids): Holotype: ♀, from puparium of L. cicerina (host)/on C. arietinum (host’s food plant). Paratypes: 1 ♀, 1 ♂, ditto.

Holotype, length of body 1.7 mm.

Head--Width of head 2.0 times its length, 1.9 times distance between eyes. Height of head 1.3-1.5 times its length. Antenna with 23 antennomeres; maxillary palpi moderately long; length of eye in dorsal view 0.8 times temple; fairly smooth medially and finely setose towards sides and at center of its foremost part; clypeus width 0.70 times distance between eyes; mandible three-toothed, expanded apically, 0.5 times length of head, with middle tooth long and pointed. Mesosoma--Length of mesosoma 1.3 times its height, 1.9 times its width; pronotum with a median pit; sternaulus smooth, weak, short; metapleuron setose towards the posterior coxae; notauli weakly impressed; mesoscutum with dorsal pit, largely smooth, shiny, setose, with setae longer in its middle-posterior part, covering all its surface; scutellar sulcus simple; surface of propodeum wrinkled and finely setose. Wings--Pterostigma moderately wide and dark, 2.0 times longer than R1; 3Rsb sinuate; m-cu antefurcal. Legs--Hind tarsus shorter than hind tibia. Metasoma--Petiole glabrous, as long as wide apically, with large dorsope; third tergite smooth, without setae on its base; ovipositor sheath not extending beyond apical tergite in retracted position. Color--Head and mesosoma black; face black; clypeus dark brown; labrum and palpi yellow; antennae dark brown, centre of mandibles orange-yellow; legs pale yellow, with slightly darkened tarsi; wings hyaline, with dark pterostigma; metasoma brownish, becoming darker apically.

Allotype--Similar to ♀, but pterostigma wider and dark.

Differential Diagnosis. This new species is similar to D. rodriguezi, from which it is distinguished by the following character states: (a) mandibles expanded, with middle tooth pointed; (b) sternaulus smooth; and (c) first metasomal tergite brownish, glabrous, as long as wide apically.

Etymology: The specific name of this species refers to Liriomyza cicerina, of which it is a parasitoid.

This species can be identified with the keys provided by Docavo & Tormos (1997, page 387) modified as follows:

Males

  1. 159 (144) Antennae 22-23 segmented. Mandibles three-toothed, not expanded. First metasomal tergite dark brownish red, 1.7 times longer than wide apically. Pterostigma narrower than in Dacnusa melicerta (Nixon) (Fig. 4). Sternaulus absent. Body 1.3 mm. Parasitoid of Liriomyza dracunculi Hering, L. artemisicola de Meijere. Center, Central Ural; East Germany; Austria

  2. 159’ (215) Antennae 20-23 segmented. Mandibles three-toothed, expanded. First metasomal tergite 1.3 times, or less, longer than wide apically. Pterostigma much longer than the R1 (Fig. 4b, see Docavo & Tormos 1997). Sternaulus present

  3. 159” (144) Antennae 20-22 segmented. Mandibles weakly expanded, with middle tooth blunt (Fig. 2). First metasomal tergite black, 1.3 times longer than wide apically. Sternaulus weakly crenulate. Body 1.5 mm. Parasitoid of Chromatomyia horticola (Goureau). Spain

  4. 159” (144) Antennae 23 segmented. Mandibles expanded, with middle tooth long and pointed (Fig. 1b). First metasomal tergite brownish, glabrous, as long as wide apically. Sternaulus smooth. Body 1.7 mm. Parasitoid of Liriomyza cicerina (Rondani). Spain

Females

  1. 214 (215) Antennae 21-24 segmented. Mandibles three-toothed, not expanded. First metasomal tergite reddish dark brown, slightly pubescent, 1.7 times longer than wide apically. Pterostigma yellowish dark brown, parallel-sided, few longer than R1. Sternaulus absent. Body 1.3 mm

  2. 214’ (215) Antennae 20-23 segmented. Mandibles three-toothed, expanded. First metasomal tergite 1.3 times, or less, longer than wide apically. Pterostigma much longer than the R1 (Fig. 4a, to see Docavo & Tormos 1997). Sternaulus present

  3. 214” (215) Antennae 20-22 segmented. Mandibles weakly expanded, with middle tooth blunt. First metasomal tergite (petiole) black, fairly glabrous, 1.3 times longer than wide apically (Fig. 3). Pterostigma dark brown, much longer than the R1. Sternaulus crenulated (Fig. 2, see Docavo & Tormos 1997). Body 1.5 mm

  4. 214” (215) Antennae 23 segmented. Mandibles expanded, with middle tooth long and pointed (Fig. 1a). First metasomal tergite (petiole) brownish, glabrous, as long as wide apically (Fig. 1d). Pterostigma dark brown, much longer than the R1. Sternaulus smooth (Fig. 1c). Body 1.7 mm

Females and males of D. cicerina can be also distinguished from those of D. basirufa Tobias, in Belokobylskij et al. (1998: 339, 340, 353) after the following modifications:

Males

  1. 56 (55) 1st-3rd metasomal tergite brownish-yellow

  2. --First tergite black. Antennal segments more than 24

  3. 57 (56) Radial cell almost not shortened. Pterostigma long, narrow, yellowish. 1st-3rd flagellar segments yellow. Antenna 25-segmented; median segments about twice as long as wide. 1.7 mm (Fig. 128, 5, see Belokobylskij et al. (1998)). Primorskiy Territory

  4. --Radial cell shortened. Pterostigma wider, brown. Antenna 20-23-segmented, dark; median segments 2-2.5 times as long as wide

  5. 57’ (57) Antennae 22-23 segmented. Mandibles three-toothed, not expanded. First metasomal tergite dark brownish red, 1.7 times longer than wide apically. Pterostigma narrower than in Dacnusa melicerta (Nixon) (Fig. 4). Sternaulus absent. Body 1.1-1.5 mm. Magadan Province, Primorskiy Kray

  6. --Antennae 20-23 segmented. Mandibles three-toothed, expanded. First metasomal tergite 1.3 times, or less, longer than wide apically. Pterostigma much longer than the R1 (Fig. 4b, see Docavo & Tormos 1997). Sternaulus present

  7. 57” (57’) Antennae 20-22 segmented. Mandibles weakly expanded, with middle tooth blunt (Fig. 2). First metasomal tergite black, 1.3 times longer than wide apically. Sternaulus weakly crenulate. Body 1.5 mm. Parasitoid of Chromatomyia horticola (Goureau). Spain

  8. --Antennae 23 segmented. Mandibles expanded, with middle tooth long and pointed (Fig. 1b). First metasomal tergite brownish, glabrous, as long as wide apically. Sternaulus smooth. Body 1.7 mm. Parasitoid of Liriomyza cicerina (Rondani). Spain

Females

  1. 114 (106) Mesosoma entirely dark colored

  2. --First metasomal tergite yellowish brown

  3. 117 (114) Sternauli absent

  4. --Sternauli present

  5. 117’ (114) Median segments of antenna 2.5 times as long as wide; basal segments of antenna dark. Pterostigma weakly wedge-shaped. Antenna 21-24-segmented. Only first metasomal tergite pale colored, but infuscate medially. 1.3-1.4 mm

  6. --Median segments of antenna 1.5-1.8 times as long as wide; four basal segments of antenna yellow. Pterostigma lineal (in male elongate wedge-shaped and as in female pale colored). Antenna 21-22-segmented. First-third metasomal tergite pale yellowish brown. 1.1-1.4 mm

  7. 117” (114) Antennae 20-22 segmented. Mandibles weakly expanded, with middle tooth blunt. First metasomal tergite (petiole) black, fairly glabrous, 1.3 times longer than wide apically (Fig. 3). Stigma dark brown, much longer than the R1. Sternaulus crenulated (Fig. 2, see Docavo & Tormos 1997). Body 1.5 mm

  8. --Antennae 23 segmented. Mandibles expanded, with middle tooth long and pointed (Fig. 1a). First metasomal tergite (petiole) brownish, glabrous, as long as wide apically (Fig. 1d). Stigma dark brown, much longer than the R1. Sternaulus smooth (Fig. 1c). Body 1.7 mm

Immature Stages of D. cicerina sp. n. (Figs. 5a-d, 6a, b)

The first instar was found in different larval stages of the host; second and third instars were only found in host pupae.

Larva. 1st instar. General Aspect (Fig. 5a). Body [length (l) and width (w) (at the level of the mesothoracic segment): 0.5 × 0.15 mm] with head well defined and 13 body segments, caudate, vermiform, transparent, curved to the ventral side. Last abdominal segment slightly modified into a short blunt, rounded organ in the form of a tail (l = 80-85 μm, number of specimens = 3), with 25 setae (l = 50-70 μm) distributed in a fan around the anus. Segments 2-12 with a row of short setae (l = 7-12 μm) on their posterodorsal part, the numbers corresponding to 8 (mesothorax), 12 (metathorax), and between 17 and 35 (abdominal segments). Cranium (Fig. 5b) (length and width: 160 × 170 μm) with sclerites strongly sclerotized with the exception of the epistoma (weakly sclerotized). Mouthparts: Mandibles well defined, with an oblong molar lobe and one blade (l = 32 μm) sharp, curved, and well sclerotized.

2nd instar. General Aspect (5c). Body [l = 1 mm; w (at the level of the mesothoracic segment) = 0.20 mm] cylindrical, long with respect to mesothoracic width, slightly spindle-shaped at ends. Integument bare. Without cephalic sclerites or mouthparts.

3rd instar. General Aspect (5d). Typical Hymenopteriform (l = 1.70, w = 0.60 mm), with head, thoracic and abdominal segments well defined; yellowish. Integument with scale-like sensilla (“setae”) (l = 3 μm) covering the thoracic and abdominal segments, except the intersegmental zones and around the spiracles and anus. Nine pairs of spiracles (diameter (di) = 8 μm), with the atrium and closing apparatus well differentiated, one pair on the prothorax and another on the anterior edge of each of the first eight abdominal segments.

Pupa. Exarate. Without cocoon.

Exuvia of Final Instar. Of the 2 exuviae available for study only 1 was measured. General aspect. Tegument weakly sclerotized, except spiracles and scale like sensilla (setae) [l = 3 μm]. Spiracles (Fig. 6a) situated on prothorax and first 8 abdominal segments; atrium (atr) [di = 6 μm] sparingly developed, round, unarmed, separated from the closing apparatus (ca) [l = 11 μm, w = 9 μm] by a section of the trachea (t) [l = 52 μm, a = 5-7 μm]. Cranium (Fig. 6b) [w (maximum) = 0.50 mm, h (taken from the base of the mandibles) = 0.20 mm] reduced; weakly sclerotized; with sensilla (se) [di = 3 μm] and setae (st) [l = 3 μm]; orbital antennal circular (a) [di = 0.08 mm], weakly protuberant; pleurostoma (plst), superior (app) and inferior (ppp) mandible processes, hypostoma (h) and stipital sclerite (sl) well differentiated and sclerotized; the latter joined to the labial sclerite (ls), which is weakly sclerotized. Mouthparts. Mandibles (md) [l = 0.06 mm] with broad base and relatively long blade, curved, thin, unarmed (smooth) unidentate, sclerotized; maxillary (mp) and labial (lp) palpi circular, slightly protuberant, with a highly developed sensilla [di = 6 μm] in the case of the labial palpi, and with two sensilla, one of them highly developed [di = 5 μm] and the other minute [di = 2 μm] in the case of the maxillary palpi; salivary orifice well defined (so) (l = 12 μm).

Description and Comments of Venom Apparatus (Fig. 7)

The venom apparatus exhibits the characters specified by Quicke et al. (1997) for Dacnusa: (a) an undivided reservoir; (b) a reservoir neck region without narrowing; (c) a reservoir more than six times longer than maximally wide; (d) a secondary venom duct absent; (e) an extensively branched venom gland; (f) a venom gland inserted at the extreme posterior end of the reservoir; and (g) a secondary venom duct that is not narrow. The venom apparatus of Dacnusa cicerina is very similar to that of D. flavicoxa Thomson (both species are included in the subgenus Pachysema Foerster), the morphological differences being that the reservoir length is more than 12 times longer than maximally wide in D. cicerina (less than 12 times in D. flavicoxa) and that the number of gland filaments is 6 in D. cicerina, while D. flavicoxa has 8 filaments (Fig. 7).

Notes on the Hyperparasitoid Eurytoma sp. (Fig. 8a, b)

A mature larva of this genus was collected, together with a second larval instar of D. cicerina, from a puparium of L. cicerina at Ayora (Valencia, Spain) on 10-VI-1989. This appears to indicate that Eurytoma sp. probably oviposits into the phytophagous host, representing then a hyperparasitoid of D. cicerina (Sullivan 1999). An adult male Eurytoma sp. was obtained on 15-VIII-1988, from the same locality, from a puparium of L. cicerina that was originally collected on 6-VI-1988.

General aspect (Fig. 8a). Body (l = 2.2 mm, w = 0.61 mm), shape varying between barrel-shaped and cylindrical, anterodorsal protuberances present on thoracic segment 3 (th3) and first nine abdominal segments (a1-a9), with three thoracic and ten abdominal segments. Color yellowish. Weakly sclerotized, except for mandibles (md), spiracles (sp) and setae. Anus small, subterminal, transverse. Pleural lobes scarcely developed. Tegument setose, with: (a) dorsal setae (l = 62-120 μm): two pairs of setae on (th1-a7), a pair on the (a8) and (a9); (b) dorsal terminal setae (l = 30 μm): one pair; (c) pleural setae (l = 55-110 μm): four pairs on (th1-a2); two pairs on (a3-a9); (d) ventral setae (l = 150-420 μm): one pair on (th1-a9), (sp) on (th2), (th3), and on (a1-a7); atrium of spiracle (l = 20 μm, d maximum = 10 μm) funnel-shaped, with approximately twelve chambers; closing apparatus of spiracle (l = 7 μm; w = 3 μm) adjacent to atrium. Cranium (Fig. 8b). Wider than high (w = 210 μm, height (from apex of cranium to base of (md)) = 105 μm), narrower than (th1), weakly sclerotized, with two pairs of setae (l = 4-5 μm): superior frontal setae (l = 4 μm), hypostomal setae (l = 5 μm). antenna approximately 2.5 times as long as broad, located below middle of cranium, with two small sensilla on apex. Clypeus and labrum without setae or sensilla; epipharynx with a pair of small sensilla (a). Tentorium with the pleurostoma and its anterior and posterior pleurostomal processes sclerotized and differentiated. Epistoma almost indistinct, and very weakly sclerotized. Mouthparts. (md) (l = 5 μm, w = 3 μm) sclerotized, more heavily sclerotized at their blade, unidentate, with a wide base; maxillae (mx) and labium (lum) completely fused: (mx) with a pair of maxillary setae (l = 4 μm) and a protuberant maxillary papilla (4 × 2 μm); (lum) without setae, with a pair of small prelabial sensilla.

Discussion

The first instar of D. cicerina can be considered of the caudate-mandibulate type, according to the classifications of Clausen (1962) and Hagen (1964). Its larva is similar to the first instar of Dacnusa areolaris (Nees) (Haviland, 1922) and Dacnusa dryas (Nixon) (Guppy & Meloche 1987). Like D. areolaris, it has a semicircle of stouter setae arranged fanwise round the anus. Like D. dryas, it has rows of setae on the posterodorsal part of several body segments. The strongly sclerotized mandibles of this first instar could serve to break the chorion; alternatively, they could contribute to preventing super- or multiparasitoidism, as has been indicated for the caudate-mandibulate larvae of Alysiinae (Tormos et al. 2003).

The second instar is fairly similar to the mature larva, having lost the tail, tegumental differentiations, cephalic sclerites and mouthparts; it is very similar to those of D. dryas (Guppy & Meloche 1987) and Dacnusa sibirica Telenga (Croft & Copland 1994).

The mature larva is very similar to that described for D. dryas (Guppy & Meloche 1987), from which it differs by having scale-like sensilla (“setae”) on the thorax and abdomen. Differences in the cephalic sclerites are addressed in the discussion of the exuviae. The description of D. areolaris (Haviland 1922) does not allow comparative studies to be carried out.

The cast skin of the final instar of D. cicerina, like those described for Dacnusini, displays simple, unarmed mandibles and a reduction in the labial sclerite (Capek 1970, 1973). It shares a pleurostoma with well-differentiated mandible processes and a long stipital sclerite with those of the genus Dacnusa. The only appreciable differences from D. rodriguezi and D. dryas (species whose mature larvae have been adequately described) lie in the presence/absence, type, number and arrangements of tegumental differentiations: spinules, setae, and sensilla. Unlike D. rodriguezi, D. cicerina does not have spinules on the tegument; the tegumental sensilla are scale-like (not bluntly pointed) and the labial palpi only have 1 sensillum. Unlike those of D. dryas, the tegumental, thoracic, and abdominal sensilla are scale-like (not bluntly pointed) and the maxillary palpi have 2 sensilla.

The mature larva of Eurytoma sp. shares the following character states with other known Eurytoma spp.: (a) body mainly barrel-shaped, broader in mid-region; (b) head hemispherical, without pronounced clypeus, with hypostomal setae longer or about as long as half the width of the labrum, and with inconspicuous and unpigmented craneal sclerites; (c) integument with setae arranged in distinct rows along all body segments, and with ventral setae arranged in paired rows; (d) atrium of spiracle long. Like E. nodularis Boheman, this larva has the antennae located below the middle of the cranium and more than 2 dorsal setae present on abdominal segments A6-7; the cranium, without FI setae, is similar to that of E. heriadi Zerova.

This mature larva can be characterized and distinguished from the similar mature larvae of Eurytoma: E. nodularis and E. heriadi, by the combination of the following character states: (a) tegument with two pairs of setae on (th1-a7); (b) cranium without inferior frontal setae or setae on genae; and (c) epipharynx with a pair of small sensilla. Additionally, it has an atrium with 12 chambers, an intermediate number between those of E. nodularis (14) and E. heriadi (10). The smaller size of this larva may represent a morpho-functional adaptation to its possible nature as hyperparasitoid.

Acknowledgments

We are indebted to G. C. D. Griffiths (University of Alberta, Canada) and I. Docavo (Universidad de Valencia, Spain) for corroboration of the determinations of the agromyzid host and braconid parasitoid, respectively. María Jesús Verdú (I.V.I.A., Spain) confirmed the determination of the Eurytoma. Thanks to Sergey Alexandrovich Belokobylskij (Zoological Institute of Russia) and Charles Godfray (University of Oxford, UK) for observations on and critical reading of the manuscript. This study was carried out in the laboratories of the Departamento de Protección Vegetal, I.V.I.A. (València, Spain). Financial support for this paper was provided from the Junta de Castilla y León, project SA012A05, and Fundación Entomológica “Torres-Sala”

References Cited

1.

C. Van Achterberg 2004. Fauna Europaea. Symphyta & Ichneumonoidea.  http://www.faunaeur.org/Google Scholar

2.

S. A. Belokobylskij, V. I. Tobias, M. J. Sharkey, and A. Taeger . 1998. Fam. Braconidae. pp. 8-656 In P. A. Lehr [ed.], Key to Insects of the Russian Far East. Neuropteroidea, Mecoptera, Hymenoptera. Vol. 4, pt. 3. Vladivostok: Dal’nauka (in Russian, English abstr.). Google Scholar

3.

M. Capek 1970. A new classification of the Braconidae (Hymenoptera) based on the cephalic structures of the final instar larva and biological evidence. Canadian Entomol 102:846–875. Google Scholar

4.

M. Capek 1973. Key to the final instar larvae of the Braconidae (Hymenoptera). Acta Inst. For. Zvolenensis 259-268. Google Scholar

5.

C. P. Clausen 1962. Entomophagous Insects. McGraw-Hill, New York & London. Google Scholar

6.

P. Croft and J. W. Copland . 1994. Larval morphology and development of the parasitoid Dacnusa sibirica (Hym., Braconidae) in the leafminer host Chromatomyia syngenesiae. Entomophaga 39:85–93. Google Scholar

7.

I. Docavo and J. Tormos . 1997. A new species of Dacnusa (Hymenoptera: Braconidae) from Spain. Entomol. News 108:382–388. Google Scholar

8.

A. Garrido, J. Tormos, and F. Beitia . 1992. Explanatory notes on Agromyzids (Dipt.) injurious to chickpea and their parasitoids (Hym.: Braconidae, Eulophidae). Ann. Soc. Entomol. France (N.S.) 28:111–112. Google Scholar

9.

G. C D. Griffiths 1964. The Alysiinae (Hym., Braconidae) parasites of the Agromyzidae (Diptera). I. General questions of taxonomy, biology and evolution. Beitr. Entomol 14:823–914. Google Scholar

10.

G. C D. Griffiths 1966. The Alysiinae (Hym., Braconidae) parasites of the Agromyzidae (Diptera). II. The parasites of Agromyza Fallén. Beitr. Entomol 16:551–605. Google Scholar

11.

G. C D. Griffiths 1968. The Alysiinae (Hym., Braconidae) parasites of the Agromyzidae (Diptera). VII. The parasites of Cerodontha Rondani s.l. Beitr. Entomol 18:63–152. Google Scholar

12.

G. C D. Griffiths 1984. The Alysiinae (Hym., Braconidae) parasites of the Agromyzidae (Diptera). VII. Supplement. Beitr. Entomol 34:343–362. Google Scholar

13.

J. C. Guppy and F. Meloche . 1987. Life history and description of the immature stages of Dacnusa dryas (Nixon) (Hymenoptera: Braconidae), a European parasite of the alfalfa blotch leafminer (Diptera: Agromyzidae) in eastern Canada. Cananadian Entomol 119:281–285. Google Scholar

14.

K. S. Hagen 1964. Developmental stages of parasites. pp. 186-246 In P. Debach [ed.], Biological Control of Insects Pests and Weeds. Chapman & Hall, London. Google Scholar

15.

M. D. Haviland 1922. On the larval development of Dacnusa areolaris Nees (Braconidae), a parasite of Phytomyzinae (Diptera), with a note on certain chalcid parasites of phytomyzids. Parasitology 14:167–173. Google Scholar

16.

J. S. Noyes 2001. World Chalcidoidea Database on CD-Rom. ETI. Netherlands. Google Scholar

17.

J. Pardo, J. Tormos, and R. Jiménez, R . 2000. Particularidades morfológicas del último estado larvario de Dacnusa rodriguezi, especie parasitoide de Chromatomyia horticola (Hymenoptera, Braconidae; Diptera, Agromyzidae). Fragm. Entomol 32:299–303. Google Scholar

18.

D. L J. Quicke, J. Tunstead, J. V. Falcó, and P. M. Marsh . 1992. Venom gland apparatus in cyclostome braconid wasps with special reference to the subfamily Doryctinae (Insecta, Hymenoptera, Braconidae). Zool. Scr 21:403–416. Google Scholar

19.

D. L J. Quicke, K. Van Achterberg, and H. C. Godfray . 1997. Comparative morphology of the venom gland and reservoir in opiine and alysiine braconid wasps (Insecta, Hymenoptera, Braconidae). Zool. Scr 26:23–50. Google Scholar

20.

K. A. Spencer 1973. Agromyzidae (Diptera) of Economic Importance. Ser. Entomol., 9. W. Junk (ed.). The Hague. Google Scholar

21.

K. A. Spencer 1976. The Agromyzidae (Diptera) of Fennoscandia and Denmark. Fauna ent. Denmark. 5, part 1-2, 1-304 pp. 305-606. Google Scholar

22.

K. A. Spencer 1990. Host specialization in the world Agromyzidae (Diptera). Kluwer Academic Publishers. London. Google Scholar

23.

D. J. Sullivan 1999. Hyperparasitism: Mutitrophic ecology and behavior. Annu. Rev. Entomol 44:291–315. Google Scholar

24.

W. I. Tobias 1995. Subfamily Alysiinae. pp. 156-386 In G. S. Medvedev [ed.], Keys to the Insects of the European Part of the URSS. Vol. III. Hymenoptera. Part V. Science Publishers, Inc. Lebanon (in Russian, English abstr.). Google Scholar

25.

J. Tormos, X. Pardo, R. Jiménez, J. D. Asís, and S. F. Gayubo . 2003. Descriptions of adults, immature stages and venom apparatus of two new species of Dacnusini: Chorebus pseudoasphodeli sp. n., parasitic on Phytomyza chaerophili Kaltenbach and C. pseudoasramenes sp. n., parasitic on Cerodontha phragmitophila Hering (Hymenoptera: Braconidae: Alysiinae; Diptera: Agromyzidae). Eur. J. Entomol 100:393–400. Google Scholar

26.

J. Tormos, J. D. Asís, S. F. Gayubo, and M. A. Martín . 2004. Descriptions of the Final instar of Eurytoma nodularis and E. heriadi (Hymenoptera: Eurytomidae). Florida Entomol 87:278–282. Google Scholar

27.

R. A. Wharton, P. M. Marsh, and M. J. Sharkey . 1997. Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special publications of the International Society of Hymenopterists, Washington, DC. Google Scholar

Appendices

Fig. 1.

Dacnusa cicerina sp. n. (♀): a--head in lateral view; c--detail of mesopleuron showing the sternaulus; d--petiole in dorsal view. Dacnusa cicerina sp. n. (♂): b--left mandible.

i0015-4040-91-2-170-f01.gif

Figs. 2-4. 2--Dacnusa rodriguezi (♂): mandible in lateral view. 3--D. rodriguezi (♀): a--petiole in dorsal view; 4--Dacnusa austriaca (♀): anterior wing according Tobias (1995).

i0015-4040-91-2-170-f02.gif

Fig. 5.

Dacnusa cicerina sp. n.: 5--Larval phase: a--1st instar (lateral view); b--mandibles and head sclerites; c--2nd instar (lateral view); d--3rd instar (general aspect).

i0015-4040-91-2-170-f05.gif

Figs. 6-7. Dacnusa cicerina sp. n.: 6--Larval phase: exuvia of final instar: a--spiracle; b--cephalic structures 7. Venom apparatus of D. cicerina sp. n. showing the terminology used for the venom gland and reservoir parts. Lettering: antennal orbit (a), anterior pleurostomal process (app), atrium (at), closing apparatus (ca), venom gland (dg), secondary venom duct (f), gland filament (sack) (e), epistoma (epst), hypostoma (h), labial palpi (lp), labial sclerite (ls), mandible (md), maxillary palpi (mp), pleurostoma (plst), posterior pleurostomal process (ppp), reservoir with spiral sculture (r), mesothoracic, metathoracic and abdominal setae (s), anal setae (sa), scale like setae (“setae”) (sc), sensilla (se), stipital sclerite (sl), salivary orifice (so), spiracle (sp), setae (st), trachea (t).

i0015-4040-91-2-170-f06.gif

Fig. 8.

Eurytoma sp.: a--mature larva in lateral view; b--cranium. Lettering: abdominal segments (a1-9), antenna (an), anal segment (as), anterodorsal protuberances (adp), base of mandibles (ba), blade of mandible (bl), clypeus (clp), dorsal setae (d), dorsal terminal seta (dt), sensilla of the epipharynx (epx): a), superior frontal setae (fs), hypostomal setae (hy), labrum (lm), labium (lum), mandibles (md), maxillae (mx), pleural setae (p), pleural lobes (pl), spiracles (sp), thoracic segments (th1-3), ventral setae (v).

i0015-4040-91-2-170-f08.gif
Josep Tormos, Xavier Pardo, Josep Daniel Asís, and Severiano F. Gayubo "Dacnusa cicerina (Hymenoptera: Braconidae: Alysiinae), A New Species of Endoparasitoid of Liriomyza cicerina (Diptera: Agromyzidae)," Florida Entomologist 91(2), 170-178, (1 June 2008). https://doi.org/10.1653/0015-4040(2008)91[170:DCHBAA]2.0.CO;2
Published: 1 June 2008
JOURNAL ARTICLE
9 PAGES


SHARE
ARTICLE IMPACT
Back to Top