Allorhogas uberlandiensis Joele & Zaldívar-Riverónı, 2019

Joele, Flávia R., Rezende, Uiara C., Samacá-Sáenz, Ernesto, Cardoso, João C. F., Oliveira, Denis C. & Zaldívar-Riverón, Alejandro, 2019, A new species of Allorhogas (Hymenoptera: Braconidae: Doryctinae) inducing ovule galls on Miconia chamissois Naudinı a potentially invasive shrub in the Brazilian cerrado, Journal of Natural History 53 (33), pp. 2073-2085 : 2073-2085

Allorhogas uberlandiensis Joele & Zaldívar-Riverónı new species ( Figure 1 (a – g))

Diagnosis. Allorhogas uberlandiensis sp. nov. is morphologically similar to A. minimus Centrella and Shaw, 2010 and A. granivorus Zaldívar-Riverón and Martínez, 2018 , though it can be distinguished from the latter two species by its larger body size (2.3 – 2.6 mm; 1.6 – 2.0 mm in A. granivorus , 0.8 – 1.4 mm in A. minimus ), face rugulose-coriaceous (coriaceous in A. minimus and A.granivorus ), shorter ovipositor size (0.2 times as long as metasoma; 0.4 in A. minimus , 0.5 in A. granivorus ) and by its association with M. chamissois ( M. calvescens and M. longifolia (Aublet) De Candolle in A. gravinorus and A. minimus , respectively). Also, this new species can be distinguished from A. minimus by having 20 – 21 flagellomeres (14 – 16 in A. minimus ); basal third of third tergite costate-rugulose, remaining area coriaceous (costate-rugulose on basal half to two-thirds, remaining area smooth in A. minimus ); and vertex, frons, temple, gena and clypeus rugulose-coriaceous (coriaceous in A. minimus ).

Description. Holotype female. Body size 2.5 mm, forewing length 2.2 mm. Colour: body colour dark brown to black ( Figure 1 (a)); scape, pedicel, and legs honey yellow; flagellum honey yellow, turning dark brown apically. Wings hyaline, pterostigma brown, veins light brown to brown. Ovipositor sheaths dark brown to black.

Head. Distinctly transverse in dorsal view, 3.0 times wider than its median length and 1.4 times wider than high. Occipital carina complete and reaching hypostomal carina before the base of mandible; inner margins of posterior ocelli (POL) as long as the ocellar diameter (OD), 0.7 times shorter than the distance between outer margin of posterior ocellus and eye (OOL). Vertex, frons, temple, gena and clypeus rugulose-coriaceous; frons excavation distinct, with sharp lateral margins. Face rugulose-coriaceous, with a median longitudinal carina anteriorly, with a convex, slightly coriaceous median area ( Figure 1 (b)). Eye 1.2 times longer than wide; eye width 2.1 times longer than the temple in dorsal view. Malar space 0.2 times eye height and 1.4 times longer than the width of hypoclypeal depression; mandibles bidentate. Antenna with 21 flagellomeres, first flagellomere about 4.0 times longer than wide, 1.3 times longer than the second flagellomere.

Mesosoma. 1.2 times longer than high ( Figure 1 (c)) and 1.5 times longer than wide. Pronotal collar short, not visible in dorsal view; pronotal furrow scrobiculate. Mesoscutum distinctly transverse in dorsal view, its median length 0.5 times its width; mesoscutal lobes coriaceous-rugose with extensive rugose areas surrounding notauli and lateral margins; median mesoscutal lobe with a median, scrobiculate stripe; notauli present, complete, and rugose-scrobiculate, finishing in a posterior strongly rugose median area ( Figure 1 (d)); scutellum slightly convex, coriaceous; prescutellar furrow with four transverse carinae. Propodeum entirely rugose-areolate, inner areas within areolae smooth, with basal areas delimited by two diverging carinae ( Figure 1 (d)). Mesopleuron rugose-coriaceous anteriorly, coriaceous medially and posteriorly, subalar sulcus scrobiculate-slightly rugulose; precoxal sulcus scrobiculate-slightly coriaceous, 0.6 times as long as mesopleuron.

Wings. Forewing 2.2 times longer than wide. Pterostigma 3.0 times longer than wide and 0.7 times as long as R ( Figure 1 (f)). Vein r 0.6 times as long as 3RSa, 0.2 times as long as 3RSb, and 0.7 times as long as vein r-m. Vein m-cu interstitial with 2RS, vein RS+Mb absent. Hindwing vein M+ CU 0.8 times as long as 1M, m-cu slightly curved towards wing apex ( Figure 1 (g)).

Legs. Protibia with a row of spines along the anterior margin. Metacoxa with a small but distinct basoventral tooth. Metafemur 3.1 times longer than wide.

Metasoma. First tergite wider than long, 0.8 times as long as apical width, rugulosecoriaceous basally, remaining area longitudinally costate-rugulose, anterior area delimited by transverse, curved carina; with two subparallel longitudinal dorsal carinae ( Figure 1 (d)). Second tergite costate-rugulose; suture between second and third tergites straight, slightly distinct; basal third of third tergite costate-rugulose, remaining area coriaceous ( Figure 1 (e)); remaining tergites entirely coriaceous. Ovipositor length about 0.2 times as long as metasoma.

Variation. Body size 2.3 – 2.6 mm. Flagelomeres 20 – 21. Forewing length 2.2 – 2.3 mm.

Etymology. The name of this species refers to the city of Uberlândia, situated in the state of Minas Gerais, Brazil, from where the type specimens were collected.

Material examined. Holotype ( DCBU UFSCar). Female. Brazil, Minas Gerais, Uberlândia, Reserva particular do Clube Caça e Pesca Itororó de Uberlândia ( CCPIU). 18°58 ʹ 59 ” S- 48°17 ʹ 44 ” W, galled fruits of Miconia chamissois Naudin (Melastomataceae) , 09.viii.2018. Paratypes: 11 females ( DCBU UFSCar, CNIN UNAM), same data as holotype; DNA voucher nos CNIN 4121, GenBank accession nos MN 646957 ( COI), MN 646959 (28S).

Biological information

A total of 25 adult specimens of A. uberlandiensis were reared from 30 ‘ fruit-like ’ galls of M. chamissois that were collected during August 2018 ( Figure 2 (a – e)). Dissection of the ‘ fruit-like ’ galls showed that the pistil has an ovary divided into four locules, each having an ovule with axial placentation. Larvae and pupae of A. uberlandiensis were observed within ovule galls present in the floral buds of M. chamissois , stopping the floral anthesis. As a physiological consequence of gall induction on the ovules, the ovary wall hypertrophies forming a ‘ fruit-like ’ gall, which contains up to four wasps. The fruitlike galls have a global-shape that is three to four times bigger than the actual fruits. Since these structures contain up to four ovule galls, they have a tetrad-like arrangement ( Figure 2 (e)).

The ovule gall (inside the fruit-like gall) produced by A. uberlandiensis is capsular, with an oval shape, formed by a single larval chamber, covered by a nutritive tissue from which the insect directly feeds. The external tissue layer is thicker, and when the larva turns into pupa it works as a cocoon. The ‘ fruit-like ’ galls are, on the other hand, mostly red and occasionally with greener parts ( Figure 2 (c – d)), which are apparently driven by differential regimes of light and the consequent anthocyanin accumulation pattern ( Bomfim et al. 2019). The ‘ fruit-like ’ galls that protect the ovule galls differ from the actual fruits because, although both are generally green when start forming, the latter turn violet when they mature ( Figure 2 (c)).

Phylogenetic relationships

The phylogram derived from the Bayesian analysis ( Figure 3 ) did not recover the monophyly of Allorhogas , though some of the relationships involved did not have significant support. The topology contained a significantly supported main Allorhogas clade with 14 of its 18 examined species (PP = 0.99). However, A. coccolobae + A. scotti were more related to the representative species of Labania, Ficobolus and Mononeuron (PP = 0.51), whereas A. crassifemur and A. ingavera appeared in a clade together with the member of Monitoriella (PP = 0.42).

Within the main Allorhogas clade, there is a significantly supported subclade containing the five species that are associated with Melastomataceae host plant species (PP = 1.0). The remaining members of the Allorhogas clade with host plant records, on the other hand, did not appear grouped together, but most of their relationships were weakly supported.

Uncorrected COI distances between A. uberlandiensis and the remaining members associated with Melastomataceae ranged from 7.4 (with A. minimus ) to 10.3% (with A. clidemiae ). COI distances between the new species and the additional members of the Allorhogas clade, on the other hand, varied from 9.6 ( A. amuzgo ) to 13.4% ( A. jaliscoensis ).

Figures

Figure 1. Allorhogas uberlandiensis sp. nov. (female, holotype): (a) habitus, lateral view; (b) head, frontal view; (c) head and mesosoma, lateral view; (d) mesosoma, dorsal view; (e) metasoma, dorsal view; (f) forewing; (g) hindwing.

Figure 2. Galls induced by Allorhogas uberlandiensis sp. nov. on the floral buds of its host plant, Miconia chamissois Naudin (Melastomataceae). (a) photograph of ‘cerrado’ biome showing plants of M. chamissois. (b) plant of M. chamissois. (c) fruits and ‘fruit-like’ galls. (d) internal longitudinal view of a ‘fruit-like’ gall showing the locules (GL) formed by the ovary hypertrophy. (e) internal transversal view showing the four locules, each one occupied by an ovule-gall. The insect remains inside the ovule-gall capsule until its emergence from pupa (IE).Afterwards,wings start to expand untilit is still inside the fruit-like gall and after it leaves (EA) byopening another hollow (see in C;FLG).IF –Immature fruit,MF –Mature Fruit,FLG – Fruit-like gall, GL – Gall locule, IA – Emerged Adult, IE – Insect emergence, EOG – Empty Ovule-gall.

Figure 3. Bayesian phylogram for the examined species of Allorhogas derived from the concatenated analysis with the COI and 28S markers. The black dots indicate the nodes with posterior probability bigger than 0,95. The name of the new species is shown in bold.