Chrysopodes (Chrysopodes) divisus (Walker, 1853)

Silva, Patricia S., Tauber, Catherine A., Albuquerque, Gilberto S. & Tauber, Maurice J., 2013, Larvae of five horticulturally important species of Chrysopodes (Neuroptera, Chrysopidae): shared generic features, descriptions and keys, ZooKeys 262, pp. 39-92 : 43-51

Chrysopodes (Chrysopodes) divisus (Walker, 1853) Figs 2-9

Discussion.

Chrysopodes divisus is probably one of the most common and widespread of the Chrysopodes species. It has a large number of synonyms (see Adams and Penny 1985), and originally it was placed in the subgenus Chrysopodes (Neosuarius) . Recently it was moved to Chrysopodes (Chrysopodes) on the basis of adult characteristics ( Tauber 2010).

Adults of Chrysopodes (Chrysopodes) divisus are recognized by their relatively narrow costal cells, dark gradate veins, facial markings and very distinctive male and female genitalia. They can be identified using current keys and redescriptions ( Adams and Penny 1985, Freitas and Penny 2001).

Known geographic distribution.

Argentina, Brazil, British Guiana, Colombia, Cuba, Jamaica, Paraguay, Peru, Uruguay, and Venezuela ( Adams and Penny 1985, Freitas and Penny 2001).

Larval diagnosis.

Chrysopodes (Chrysopodes) divisus larvae (all instars) are relatively short, compact, and rotund. Their bodies are white to light cream-colored, with brown to light brown prothoracic sclerites; most of the long setae are cream-colored to light brown. The extensive brown head markings of Chrysopodes (Chrysopodes) divisus (all instars) are similar to those of Chrysopodes (Chrysopodes) lineafrons in that: (i) The confluent frontal markings, together with the dark brown intermandibular region, form an extensive dark brown, triangular to T-shaped mark on the anterior region of the head. (ii) The mesal and lateral arms of the epicranial markings are completely or partially confluent; together with the dark brown postfrontal markings, they cover most of the posterior and mesolateral regions of the head.

The first instar of Chrysopodes (Chrysopodes) divisus is distinguished from Chrysopodes (Chrysopodes) lineafrons by the lack of thorns on all cranial setae other than S1 and S11, metathorax with a large number of setae (n = 6-7) in row (R1) on posterior fold, and a large number of abdominal SMS on segments A1 to A5 (n> 30). Second and third instars (Semaphoront B) are characterizedby cranial setae that are all without thorns, prothorax that is white to cream-colored and without a conspicuous covering of brown spinules, and metathorax that has a large number of setae (n = 14-15) in row (R1), which, in the L3, is flanked laterally by a pair of long, smooth setae.

First instar.

(Semaphoront A). Body (Fig. 5A) short, globose, compact in shape, 2.5-2.9 mm long. Head (Figs 2A, 5B) 0.38-0.39 mm wide; mandibles 0.35-0.39 mm long (ratio, mandible length: head width = 0.95-1.02: 1). Dorsum of cranium predominantly brown, with wedge-shaped, white area posteromesally. Epicranial marking entire, light brown mesally, darker brown laterally. Postfrontal marking darker brown than most of epicranial marking, contiguous basally with distal margin of epicranial marking, extending to anterior base of antenna. Frontal marking paired, but fused mesally, dark brown anteriorly, narrow, extending anteriorly from midregion of cranium, bending toward inner basal margin of mandible. Intermandibular, clypeal area brown. Cranial setae light amber; S1, S11 long, thorny, others smooth, shorter.

Gena, ventral margin of cranium brown; genal marking with small white spot behind eye. Labial palpus tinged with light brown, slightly darker distally. Mandibles amber, with brown basolateral spot. Antenna with scape brownish, pedicel white basally, brown distally, flagellum light brown.

Thorax (Figs 2A, 5A) mostly cream to white, with sclerotized structures light to very light brown; episternum light brown. Legs white, with base of coxa light brown, femur (especially distal half) tinged with brown, dorsum of tibia, tarsus tinged with light brown; tarsal claws, empodia brown. LS cream to white; other setae white to cream.

T1: Row of three very small setae (R1) at anteromesal base of LTs. Sc1 brown mesally, basolaterally, with cream colored interior; S2Sc1 small, immediately above S1Sc1. S1 long, S3 intermediate-length. T2: Spiracle with lips of atrium protruding above integumental surface. Sc1, Sc2, transparent; Sc3 marked with light brown; S 2Sc3 variable, medium-length to long; S2 smaller. T3: S1Sc1, S2Sc1 present, S1Sc2 very small, sometimes absent, S2Sc2 usually present. Posterior fold with row (R1) of six (sometimes seven) long, thorny, pointed setae on chalazae with ovate, light brown marks anteriorly; lateral two chalazae on each side juxtaposed.

Abdomen (Figs 5C-D) white to cream-colored, with LTs, LDTs tinged with light brown.

A1: Dorsum with ten to twelve SMS in single anterior row, with 34-42 SMS in double to triple row posteriorly; spiracles at end of posterior row, without distinguishable SSp. A2: Dorsum with ~10 SMS in single anterior row, with ~44 SMS in double to triple posterior row; anterior row bending posteriorly at each end, coalescing with setae in posterior row; spiracle at end of posterior row, with SSp near anterodistal margin. A3-A5: Dorsum with ~8 (A3, A4) or 6-7 (A5) SMS in single anterior row, with ~36 (A3), ~32 (A4), ~26 (A5) SMS in double to triple posterior row; anterior row bending posteriorly at each end, coalescing with posterior row; spiracle with SSp anteroventrally. A6: Anterior region with four SMS; spiracle with SSp mesally. A7: Anterior region with pair of microsetae; spiracle with SSp mesally. A8: Venter with two pairs of medium-length setae posteriorly, one pair of short setae slightly anteriorly.

Second and third instars.

(Semaphoront B). Body (Figs 6E, 7 A–B) length 3.3-3.4 mm (L2), 5.7-6.3 mm (L3); surface white to cream-colored, with light to dark brown integumental spinules somewhat dense, dark on pronotum; primary pronotal, mesonotal sclerites brown to dark brown, other dorsal marks small, brown; sclerites around coxae dark brown, abdomen with light to very light brown stripe laterally.

Head (Figs 3A, 4A, 6 A–B, 7 C–D) cream-colored, with extensive brown and dark brown markings. Epicranial marking undivided, with mesal and lateral arms distinguishable, but broadly connected throughout, both arms in contact with posterior margin of head; lateral arm dark brown basally, lighter distally, extending from distal ~one-fourth of posterior cranial suture to lateral base of mandible; mesal arm light brown, extending from base of head, becoming confluent with postfrontal marking. Postfrontal marking very dark brown, narrow throughout, extending to inner base of scape. Frontal marking dark brown, with left, right arms contiguous with each other and with intermandibular marking, forming broad, triangular, dark brown anterior marking. Clypeolabral region distal to anterior marking cream-colored. Gena cream-colored, with brown marking basally, becoming lighter brown, forking near midregion, extending to base of eye. Mandible, maxilla dark brown laterally and distally, amber mesally, base with dark brown mesal mark. Labial palpus: basal segment cream-colored with light brown mesally; mesal segment ringed with light brown laterally, cream-colored mesally, with terminal subsegment brown; terminal segment dark brown basally, light brown distally. Antenna: scape, basal, mesal sections of pedicel cream-colored to amber, distal section of pedicel very light brown, flagellum light brown. Venter cream-colored to white; margin of cranium brown to dark brown; cardo, stipes brown; base of mentum with light brown patch.

All cephalic setae smooth, pointed; S1 slightly robust, medium length, S11 long, S2-10, S12 short to medium length; Vx setae fairly long, robust; with one to two pairs of secondary setae. Anterior margin of head protruding, straight with angled lateral margins; mesal pair of anterior setae much longer than two lateral pairs.

Head width across eyes, 0.53-0.59 mm (L2), 0.78-0.83 mm (L3); mandible length, 0.52-0.56 mm (L2), 0.81-0.90 mm (L3); ratio mandible length to head width = 0.92-1.0: 1 (L2), 1.0-1.1: 1 (L3). Tip of mandible with six teeth mesally.

Cervix brownish dorsally, slightly darker laterally; venter cream-colored mesally, light brown laterally; white ventrally.

Thorax (Figs 3A, 4A, 6 B–C, 6E, 7 A–B, 8A) white to cream-colored; dorsum, especially pronotum tinged with brown, the darkness of which depends on density, color of integumental spinules; with sclerites, markings brown; LTs white to cream-colored, with LS amber. Venter white to cream-colored, unmarked. Legs: coxa white, with brown on basodorsal surface; trochanter cream-colored to white, base of femur cream-colored, becoming brownish mesally, cream-colored at tip; tibia white with brown setae; tarsus tinged with light brown; empodium brown; claws amber.

T1: LT with 14-17 (L2), 17-19 (L3) LS. Sc1 large, rhomboid, extending around posterior base of LT, darker brown laterally than mesally. Sc2 triangular, appearing as paired brown marks, with two small, irregularly shaped sclerites (brown) above; sometimes small brown spots anteriorly. S2, S3 smooth. T2: Anterior sclerite (Sc1) light brown to brown; spiracles on prominent protuberances. Posterior subsegment with Sc2 light brown; Sc3 pronounced, brown. LT with 12-13 (L2), 16-19 (L3) LS. T3: Sc1 transparent. LT with 11-13 (L2), 13-18 (L3) LS. Posterior fold with 14 to 15 robust, thorny setae; L3 sometimes with additional pair of long, smooth, pointed setae laterally, arising from smaller chalazae.

Abdomen (Figs 6 D–F, 7 A–B, 8 B–C) white to cream-colored, tinged with light brown, with small light brown to brown spots anterior to bases of LTs; spots more diffuse on A5-A8; white fat-body visible beneath integument; setae mostly light brown to amber-colored. A6, A7 each with pair of large, dark brown marks surrounding LDTs. A8 with pair of dark brown marks mesal to spiracles; A9 with pair of large, dark brown marks anterolaterally, dark brown mark mesally; A10 with inverted U-shaped, dark brown mark. Venter white to cream-colored, unmarked, except with some light brown pigmentation ventrolaterally on S5-S9 (some specimens); tip of A10 with pair of small, abutting, triangular dark brown marks.

A 1: Dorsum with ~78-88 (L2), 142-172 (L3) SMS in two double-triple transverse bands between spiracles. A2-A5: Dorsum with 64-112 (L2), 120-196 (L3) SMS in two broad transverse bands. LTs each with 11-21 (L2), 29-40 (L3) LS: one to five robust, thorny, blunt to spatulate LS on distal surface; remaining LS long, smooth, hooked, in large patch on dorsal surface. A6: Dorsum with transverse band of 20-30 (L2), 56-66 (L3) SMS across anterior of segment; midsection with one to two pairs of smooth setae, mesal pair hooked (similar to SMS), lateral pair short, pointed. LT with nine to eleven (L2), ten to eleven (L3) LS of various sizes. A7: Dorsum with one to two pairs of very small setae (S1, S2) anteriorly, between spiracles; LDTs each with one medium-length, robust, thorny, blunt to spatulate LDS, one to two smaller, smooth, pointed LDS; pair of very small setae between LDTs. LT with ten to 13 (L2), ten to 14 (L3) LS of various sizes. A8: Anterior region with one to two pairs of very small setae (S1, S2). Venter with pair of medium-length setae between LTs, two to three smaller setae slightly anteroventral to LTs. A9: Dorsum with one pair of very small setae anteriorly. Middle and posterior regions with two transverse rings of setae extending around segment; each ring with ~14-16 short to medium-length setae, several in each ring robust. A10: Dorsum with several pairs of small setae on V-shaped anterior sclerites, one slightly anterior to terminus. Two pairs of robust lateral setae. Venter with ~five pairs of small setae in V-shaped pattern, posterior row of microsetae anterior to terminus.

Egg.

At oviposition, light yellowish green to green, with white micropyle; ovoid, 0.82 to 1.06 mm long, 0.36 to 0.43 mm wide. Stalk smooth, hyaline, 2.89 to 6.80 mm long.

Larval specimens examined.

Numerous lots, each originating from a single gravid female collected in Brazil, Bahia: Cruz das Almas, VI-19-96 (Tauber Lots 96:017C, 96:018B, 96:019B, 96:019D); Camacan, Reserva Serra Bonita, 800 m., X-3 to 7-2005 (Tauber Lot 2005:032). Distrito Federal, Brasília, X-22 and 23-2003 (Tauber Lots 2003:035, 2003:036, 2003:038). Minas Gerais, Lavras, UFLA Campus, coffee orchard, X-12-2005 (Tauber Lot 2005:020); Lavras, Parque Ecológico Cachoeiras do Rio Bonito, X-14-2005 (Tauber Lot 2005:028). Rio de Janeiro: Conceição de Macabu, Santo Agostinho, V-21-2002 (Tauber Lot 2002:020); Conceição de Macabu, Fazenda Carrapeta, II-28-2002, IV-29 to V-6-2003 (Albuquerque Lot 2002:05, Tauber Lot 2003:007); Santa Maria Madalena, Terras Frias, III-30-1999 (Tauber Lot 99:043). Rio Grande do Sul: Cachoeira do Sul, São Nicolau, I-16-2007 (Tauber Lots 2007:023A, 2007:023B). Two field-collected L3 from RJ, Conceição de Macabu, Santo Agostinho, V-2-2003.

Biology.

Adults and larvae of this species were collected on shrubs in disturbed, dry forest habitats. Adults are agile; they exhibit fast, evasive flight, usually inward toward the interior of the bush or tree.

Based on the following observations, we think that Chrysopodes (Chrysopodes) divisus adults may enter a diapause-mediated dormancy. Adults collected during the spring in Minas Gerais (Parque Ecológico Cachoeiras do Rio Bonito) were yellow to yellowish brown, and they had a greasy appearance. In addition, their prothoracic stripes were pronounced, broad and relatively dark reddish brown. In the lab, reproduction by these adults did not oc cur until after they had been held under warm, long-day conditions with ample food and water for over a week. Moreover, reproduction was correlated with the assumption of bright green coloration, the loss of some of the reddish brown coloration on the thorax, and a narrowing of the prothoracic stripes. In other Chrysopini adults, e.g., species of Chrysoperla, changing behavioral and color patterns like those described for Chrysopodes (Chrysopodes) divisus have been shown to be part of the diapause syndrome ( Tauber et al. 1986).

In the lab, eggs from all the lots listed above were deposited separately (with isolated stalks), in small groups with no particular pattern; the stalks were sticky, but without droplets. During the first 24 hours after oviposition, the eggs were bright yellowish green to green, without spots. On the second day, they began to develop a bluish brown color, with grey or brownish mottling which became more pronounced as hatching approached (Fig. 9). At 24 ± 1°C, hatching occurred within six to eight days (lots from three females collected in Cruz das Almas, n = 17 - 48 eggs/female).

In one case, a small proportion (n = 2 of 28) of the eggs laid by a female from Minas Gerais had a prolonged incubation period (approximately one week to ten days longer than the usual six- to eight-day incubation period). They were a dark bluish brown color during the period of delay. The cause of the prolongation is unknown; however, the resulting larvae developed normally and appeared healthy.

Larvae of Chrysopodes (Chrysopodes) divisus carry pieces of woody plant material and other dry debris on their backs. In the rearings (24 ± 1°C) from three females collected at Cruz das Almas, development of the various stages required: L1, 5-8 days; L2, 5-7 days; L3, 5-9 days; cocoon, 16-20 days; complete development from oviposition to adult emergence, 40-48 days. Among the offspring of each of the three females, the sex ratio was approximately 1: 1 (n = 19-33 individuals / female). The developmental and reproductive responses of Chrysopodes (Chrysopodes) divisus to a broad range of temperatures are reported elsewhere (Silva et al. in prep.).