A new species of Uscanoidea Girault (Hymenoptera, Trichogrammatidae), an egg parasitoid of Monalonion dissimulatum Distant (Hemiptera, Miridae)

A new species of Uscanoidea Girault (Hymenoptera: Trichogrammatidae), Uscanoidea ricoi Viggiani, Gamboa & Pérez-Benavides, sp. nov. , is described and illustrated. The species is a solitary egg parasitoid of Monalonion dissimulatum Distant (Hemiptera: Miridae), the main insect pest on cocoa crops. An identification key for the described Uscanoidea species of the world is provided. The new species has a high potential for the biological control of the true bug M. dissimulatum in cocoa plantations in the Neotropical region.


Introduction
During a research project in cocoa (Theobroma cacao L.-Malvaceae) agroforestry systems in Colombia, several specimens of a Trichogrammatidae (Hymenoptera: Chalcidoidea) emerged from eggs of Monalonion dissimulatum Distant (Hemiptera: Miridae) from cocoa pods.The parasitoid was identified as a member of the subfamily Oligositinae, tribe Chaetostrichini, which, according to Owen et al. (2007) comprises several genera, including Adryas Pinto & Owen, Bloodiella Nowicki, Brachista Walker, Burksiella De Santis, Chaetostricha Walker, Kyuwia Pinto & George, Lathromeroidea Girault, Pseuduscana Pinto, Uscana Girault, Uscanoidea Girault, Zaga Girault, and Zagella Girault.Morphological comparison among these genera indicated the inclusion of the parasitoid in Uscanoidea.At present, Uscanoidea includes 12 rather different species whose members are distributed in the Oriental, Nearctic, and Neotropical regions (Pinto 2006;Noyes 2022).From comparison of the collected specimens with described species in Uscanoidea it emerged that the egg parasitoid of M. dissimulatum represents a new species.
In the Neotropical region, M. dissimulatum is the phytophagous bug that causes the highest incidence of fruit damage in cocoa plantations (Lavabre 1977;Vélez 1997;Schuh 2002Schuh -2013)).Nymphs and adults of M. dissimulatum are sucking bugs, producing punctures on cocoa pods (fruits) and feeding on the cells of the epicarp.When one to seven week old fruits 10 to 12 cm long are attacked, they turn black, harden, and die.Further, when maturing fruits are attacked, they produce small stunted seeds (almonds) (de Abreu 1977).
In South America, different cocoa agroecosystem productions are found, and most are considered agroforestry systems (Johns 1999;Sambuichi 2006;Suárez et al. 2018).In those plantations, which have a greater plant diversity and are managed under traditional technologies, most farmers do not control M. dissimulatum populations.However, the few that do employ synthetic insecticides.Considering this context, it is necessary to develop new pest management practices for phytophagous insects based on recognizing and using the natural diversity of beneficial insects associated with cocoa plantations, such as predators and parasitoids.
The aim of this paper is to describe a new species of Uscanoidea, which has potential value for M. dissimulatum pest control.

Methods
In the departments of Caquetá and Huila in Colombia, 251 cocoa plantations ranging from 1-32 hectares in size were sampled.In each plantation, a manual four-hour sampling was used to search for Monalonion dissimulatum eggs inside cocoa pods.Eggs of M. dissimulatum are typically inserted into cocoa pods, and localized by detecting the two lengthend aeropiles extending out from the anterior pole of the egg.
Cocoa pods containing M. dissimulatum eggs were collected in 23 localities, 12 in the municipalities of El Doncello, El Paujil, San Vicente del Caguán and Belén de los Andaquíes in the Department of Caquetá, and 11 in the municipalities of Agrado, Colombia, Neiva, Timaná, Rivera, and Paicol in the Department of Huila.The cocoa pods were transported in plastic bags placed inside a styrofoam box to the Laboratory of Entomology of the University of the Amazonia (LEUA) in the city of Florencia, Caquetá.
Mature Monalonion eggs, typically yellowish-white in color, were extracted manually under Olympus SZ61 stereomicroscope, using a blade, forceps, a pin, and a fine-tipped paintbrush.The eggs were placed into 15 × 15 × 8 cm plastic boxes with a top opening on the lid and sealed with muslin for aeration, simulating brood chambers.After emergence, any adult parasitoids were preserved in ethanol 96% before point mounting.Additionally, some specimens were slide mounted following the protocol proposed by Woolley and Dal Molin (2017), with the following modifications: 1) wings were removed and deposited directly in clove oil; 2) the parasitoid bodies were rinsed in 10% KOH for 15 to 45 minutes depending on the degree of sclerotization in a water bath; 3) each specimen was immersed in 10% glacial acetic acid for about 3 minutes, and then into distilled water, sequentially into 35%, 50%, 75%, and 96% ethanol, and then clove oil diluted with 96% ethanol in 1:1 and 3:1 ratios for at least 15 min each; 4) each specimen was then transferred to clove oil for at least 30 min before slide mounting; 5) on the slides, each appendage and head were separated from the body, covered with a thin layer of Canada balsam, and finally covered with a coverslip; 6) lastly, the slide-mounted specimens were placed into a lab oven at 50 °C for 4 to 5 days.Dry specimens were studied under an Olympus SZ61 stereomicroscope at 90× magnification, and slide-mounted specimens were examined with an Olympus CX21 optical microscope at 400× magnification.Photographs were taken with a LEICA M205A stereomicroscope with a built-in camera and a HITACHI TM4000Plus II Environmental Scanning Electron microscope.A distribution map of the species of Uscanoidea was plotted with the software QGIS version 3.26.2.
The curatorship of all specimens was carried out following the protocols established in the LEUA: 1) specimens sizing less than 15 mm are point mounted; 2) specimens sizing less than 3 mm are slide-mounted within the mounting medium (Hoyer, entelan, canadian balsam) according to the specialist of the insect group; 3) labels on both point-and slide-mounted contain the basic information regarding locality, geographic coordinates, altitude, date, and collector.A second label contains scientific information of the host (scientific and family names), and collecting method.

Results
Sixty eight individuals of Uscanoidea ricoi, sp.nov.were reared from the same (68) number of eggs of Monalonion, of which six were slide-mounted and the remainder point-mounted.
Etymology.The specific epithet is named in honor of Leonidas Rico Martínez, President (Rector) of Universidad de la Amazonia (Florencia, Caquetá, Colombia), (from 2011 to 2016).He supported the foundation of the LEUA, with the aim of investigating the diversity of insects present in the Colombian's Amazon.
Examined material.Holotype.at least four types of traditional agroforestry systems for cocoa are recognized (1-complex diversified multistrata, 2-low diversity with regular trees, 3-low diversity with clustered trees, and 4-high density of Musaceae), depending on the diversity of the associated trees (Suárez et al. 2018).In the traditional cocoa agroforestry arrangements in Caquetá and Huila departments, plant species such as Albizia guachapele

Discussion
The genus Uscanoidea was described by Girault (1911) as follows: "A genus allied with and resembling Uscana Girault and Uscanella Girault but differing from the former in having a pointed conic-ovate abdomen which is longer than the thorax, in bearing a shorter somewhat swollen and compact 2-jointed antennal club and in lacking a ringjoint in the antennae; from the latter genus it is practically similar in the form of the antennae, but differs in the absence of the ring-joint, in the short marginal cilia of the fore wing, the more distinct and denser discal ciliation, the shorter marginal and stigmal veins and the longer, more pointed abdomen".Doutt and Viggiani (1968) revised the type material of both mentioned genera and made corrections to the original description.The distinction of Uscanoidea from Uscana was based mostly on the club number segments (3 in Uscanoidea and 4 in Uscana) and the length of the ovipositor (long in Uscanoidea and short in Uscana).After the type species U. nigriventris Girault, 2 new species from China were included in Uscanoidea (Lin 1994).The author defines both genera as having a 4-segmented club, but Uscana with "forewing moderately rounded, marginal vein slender and straight; 4 segments of club distinctly separated" and Uscanoidea with "forewing greatly broad and nearly truncate apically, marginal vein not very slender, usually with cluster of setae, club segmentation irregular and oblique, segmented differently in different view".Pinto (2006) extends the limits of the genus including species with "male and female antennal club 5-segmented" and "propodeal disc and metanotum usually subequal in length".The same author synonymizes the genus Gnorimogramma De Santis (1972) under Uscanoidea.The diagnosis of the latter genus by Pinto (2006) includes in Uscanoidea only species having antenna with 2 anelli and 5 asymmetrical club segments; most of the other characteristics appear mostly of specific and not generic value.Consequently, at present, the genus Uscanoidea sensu Pinto remains a complex of heterogeneous species without a common identity.Particularly marked are the variations of the antennal shape shown in the known species included in the genus, which need further studies to confirm the present assessment of Uscanoidea.It is a matter of fact that the morphological differences between Uscanoidea and Uscana still remain uncertain.However, biologically the two genera are different, the known hosts of Uscanoidea are Hemiptera and of Uscana are Coleoptera (Bruchidae) (Fursov 1995).
For the majority of the Uscanoidea species, biological data are lacking.However, what is known is that U. aliciae was reared from eggs of Mahanarva (Ipiranga) rubicunda (=Mahanarva rubicunda indentata) (Walker) (Hemiptera: Cercopidae) (De Santis 1972), both U. parviclavata and U. silvestrii were reared from eggs of Campylenchia hastata (Fabricius) (Hemiptera: Membracidae), and U. silvestrii was reared from eggs of an unidentified membracid (De Santis 1997).Lastly, Pinto (2006)  Prophanurus (=Telenomus) bodkini is incorrect as a taxonomic identity.Even so, during all these years in Colombia this incorrect information continues to be cited.We did an exhaustive search around the information included in Vélez (1997), to be able to make this statement.We even visited the entomological collection where Dr. Vélez worked and there is no evidence of this.In Latin America, other Monalonion species harm crops of economic importance.Among others, M. velezangeli is a polyphagous pest insect in plantations of Coffea arabica L. (Rubiaceae), Eucalyptus grandis W. Hill (Myrtaceae), Mangifera indica L. (Anacardiaceae), Persea americana Mill.(Lauraceae), Psidium guajaba L. (Myrtaceae), and Rubus glaucus Benth.(Rosaceae) (Torres et al. 2012;Ocampo et al. 2018).Exhaustive searches for Uscanoidea parasitoids for different Monalonion species should be conducted.

Figures 26 -
Figures 26-30.Habitat and host of Uscanoidea ricoi sp.nov.26 cocoa plantations in agroforestry system 27 eggs at the moment of emergence of the nymphs of Monalonion dissimulatum 28 nymphs of M. dissimulatum host feeding on cocoa pod 29 adult of M. dissimulatum feeding on cocoa pod 30 collection of cocoa pods with M. dissimulatum eggs parasitized.