Research Article |
Corresponding author: Jean Gamboa ( jagamboat@unal.edu.co ) Academic editor: Petr Janšta
© 2024 Jean Gamboa, Lucía Pérez-Benavides, Esaú Ospina-Peñuela, Francisco Serna, Gennaro Viggiani.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gamboa J, Pérez-Benavides L, Ospina-Peñuela E, Serna F, Viggiani G (2024) A new species of Uscanoidea Girault (Hymenoptera, Trichogrammatidae), an egg parasitoid of Monalonion dissimulatum Distant (Hemiptera, Miridae). Journal of Hymenoptera Research 97: 191-206. https://doi.org/10.3897/jhr.97.111008
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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.
Antennal club, biological control, cocoa, fore wing, genitalia
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
In the Neotropical region, M. dissimulatum is the phytophagous bug that causes the highest incidence of fruit damage in cocoa plantations (
In South America, different cocoa agroecosystem productions are found, and most are considered agroforestry systems (
The aim of this paper is to describe a new species of Uscanoidea, which has potential value for M. dissimulatum pest control.
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
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.
Genus Uscanoidea was identified using the keys in
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.
Female (Figs
Uscanoidea ricoi sp. nov., female 1 habitus, lateral view 2 antenna 3 setae on antenna 4 mesoscutum 5 metanotum and propodeum 6 metasoma 7 hypopygium 8 fore wing 9 hind wing 10 fore leg 11 mid leg 12 hind leg; c1 – first club segment, c2 – second club segment, md – metanotum disc; pd – propodeum disc.
Male (Fig.
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.
Holotype. Colombia • ♀; Caquetá, El Doncello, Vda. Los Laureles, Fca. Los Matapollos; 01°41'53"N, 75°17'48"W; 620 m alt.; 30 Jul. 2022; E. Ospina and L. Pérez leg.; emerged from an egg of Monalonion dissimulatum collected in cacao pod; LEUA-51438. Holotype is deposited in Laboratory of Entomology of the University of the Amazonia (LEUA), Florencia, Caquetá, Colombia (LEUA), section Central Taxonomic Collection (CTC).
Paratypes. Colombia • ♂ (Allotype); same data of holotype; LEUA-51442; deposited in LEUA • 2 ♀♀; same data of holotype; LEUA-51439/51440; LEUA • 5 ♀♀ and 4 ♂♂; Caquetá, El Doncello, Vda. La Ceiba, Fca. Bethel; 01°43'48"N, 75°16'55"W; 511 m alt.; 05 Jul. 2022; L. Pérez and E. Ospina leg.; emerged from egg of Monalonion dissimulatum collected in cacao pod; LEUA-51441; deposited in MUSA • 1 ♀; Caquetá, Belén de los Andaquíes, Vda. Agua Dulce, Fca. El Morichal; 01°20'34"N, 75°49'10"W; 328 m alt.; 13 Oct. 2021; L. Pérez and E. Ospina leg.; LEUA-51413; LEUA • 1 ♀; Caquetá, El Doncello, Vda. El Recreo, Fca. La Siberia; 01°42'53"N, 75°17'22"W; 452 m alt.; 06 Sep. 2022; Y. Rodríguez leg.; LEUA-51420; LEUA • 1 ♀ and 1 ♂; same collection data as for preceding; 18 Jul. 2021; L. Pérez and E. Ospina leg.; LEUA-51421/51422; LEUA • 1 ♂; Caquetá, El Doncello, Vda. La Ceiba, Fca. Bethel; 01°43'48"N, 75°16'55"W; 511 m alt.; 10 Ago. 2022; E. Ospina and L. Pérez leg.; LEUA-51408; LEUA • 5 ♀♀ and 3 ♂♂; same collection data as for preceding; 19 Jul. 2021; L. Pérez and E. Ospina leg.; LEUA-51959/51960/51961/51962/51963/51964/51965/51966; LEUA • 1 ♂; Caquetá, El Doncello, Vda. Los Laureles, Fca. Los Matapollos; 01°41'53"N, 75°17'48"W; 620 m alt.; 19 Jul. 2021; E. Ospina leg.; LEUA-51424; LEUA • 2 ♀♀ and 3 ♂♂; same collection data as for preceding; 06 Sep. 2022; L. Pérez leg.; LEUA-51426/51427/51428/51429/51430; LEUA • 1 ♂; Caquetá, El Doncello, Vda. Serranía, Fca. La Playa; 01°41'52"N, 75°18'05"W; 621 m alt.; 18 Jul 2021; L. Pérez and E. Ospina leg.; LEUA-51437; LEUA • 1 ♀ and 2 ♂♂; Caquetá, El Paujil, Vda. La Providencia, Fca. El Coralito; 01°32'23"N, 75°29'12"W; 320 m alt.; 20 Ago. 2021; L. Pérez and E. Ospina leg.; LEUA/51969/51970/51971; LEUA • 1 ♀ and 1 ♂; Caquetá, El Paujil, Vda. La Rivera, Fca. La Fortuna; 01°36'50"N, 75°19'47"W; 663 m alt.; 18 Ago. 2021; L. Pérez and E. Ospina leg.; LEUA-51433/51434; LEUA • 1 ♀; Caquetá, San Vicente del Caguán, Vda. Alto Pocetas, Fca. La Chinita; 02°16'21"N, 74°40'40"W; 375 m alt.; 10 Sep. 2021; E. Ospina and L. Pérez leg.; LEUA-51976; LEUA • 2 ♀; Caquetá, San Vicente del Caguán, Vda. Buenos Aires, Fca. La Jardinera; 02°17'05"N, 74°40'46"W; 605 m alt.; 26 Sep. 2021; E. Ospina and L. Pérez leg.; LEUA-51406/51407; LEUA • 1 ♀; Caquetá, San Vicente del Caguán, Vda. La Reforma No. 2, Fca. La Victoria; 02°16'50"N, 74°41'44"W; 422 m alt.; 09 Oct. 2021; L. Pérez and E. Ospina leg.; LEUA-51423; LEUA • 2 ♀♀; Caquetá, San Vicente del Caguán, Vda. Sotará, Fca. Villanueva; 02°01'29"N, 74°51'42"W; 293 m alt.; 11 Sep. 2021; L. Pérez and E. Ospina leg.; LEUA-51412/51977; LEUA • 1 ♀; same collection data as for preceding, Fca. Parcela 4; 02°01'44"N, 74°50'55"W; 302 m alt.; 04 Oct. 2021; L. Pérez and E. Ospina leg.; LEUA-51435; LEUA • 2 ♀♀ and 2 ♂♂; Huila, Agrado, Vda. La Galda, Fca. El Trapiche; 02°14'52"N, 75°46'19"W; 827 m alt.; 23 Feb. 2022; E. Ospina and L. Pérez leg.; LEUA-51414/51415/51416/51417; LEUA • 2 ♀♀; same collection data as for preceding, Fca. Santana; 02°15'02"N, 75°46'23"W; 829 m alt.; 23 Feb. 2022; E. Ospina and L. Pérez leg.; E. Ospina and L. Pérez leg.; LEUA-51980/51981; LEUA • 1 ♀; Huila, Colombia, Vda. Horizonte Bajo, Fca. La Fortuna; 03°25'54"N, 74°46'05"W; 793 m alt.; 25 Ago. 2021; E. Ospina and L. Pérez leg.; LEUA-51410; LEUA • 4 ♀♀; Huila, Colombia, Vda. Ariari, Fca. La Esperanza; 03°25'58"N, 74°46'16"W; 782 m alt.; 25 Ago. 2021; E. Ospina and L. Pérez leg.; LEUA-51972/51973/51974/51975; LEUA • 1 ♀ and 1 ♂; Huila; Neiva; Vda. Floragaita; Fca. El Tesoro; 02°52'45"N, 75°08'21"W; 928 m alt.; 26 Oct. 2021; E. Ospina and L. Pérez leg.; LEUA-51978/51979; LEUA • 1 ♂; Huila, Paicol, Vda. El Alto, Fca. Alemania; 02°27'12"N, 75°46'44"W; 916 m alt.; 15 May. 2022; E. Ospina and L. Pérez leg.; LEUA-51436; LEUA • 1 ♀; Huila, Timaná, Vda. Cascajal, Fca. Las Palmeras; 01°55'17"N, 75°56'59"W; 1250 m alt.; 28 May. 2022; L. Pérez and E. Ospina leg.; LEUA-51982; LEUA • 1 ♀ and 1 ♂; Huila, Rivera, Vda. El Guadual, Fca. La Primavera; 02°47'09"N, 75°14'03"W; 793 m alt.; 31 Jul. 2021; L. Pérez and E. Ospina leg.; LEUA-51431/51432; LEUA • 2 ♀♀ and 1 ♂; Huila, Rivera, Vda. Mesitas, Fca. La Balsa; 02°44'47"N, 75°14'57"W; 894 m alt.; 29 Jul. 2021; E. Ospina and L. Pérez leg.; LEUA-51409/51418; LEUA • 1 ♂; same collection data as for preceding; Fca. Caracolí; 02°44'49"N, 75°14'57"W; 869 m alt.; 28 Jul. 2021; E. Ospina and L. Pérez leg.; LEUA-51425; LEUA • 1 ♀ and 1 ♂; Huila; Rivera; Vda. El Viso; Fca. La Labranza; 02°45'22"N, 75°15'22"W; 760 m alt.; 28 Jul. 2021; E. Ospina and L. Pérez leg.; LEUA-51967/51968; LEUA. All additional material emerged from eggs of Monalonion dissimulatum collected in cocoa pod.
Uscanoidea ricoi, sp. nov., is a solitary parasitoid of eggs of Monalonion dissimulatum (Hemiptera: Miridae: Bryocorinae: Monaloniini) (Figs
Twelve species of Uscanoidea have been recorded worldwide: Argentina (4), Bermuda (1), Brazil (3), China (5), Jamaica (1), Panama (1), and United States of America (1) (
Specimens of Uscanoidea ricoi, sp. nov., were collected in cocoa plantations intermixed within assortments of abundant vegetation (Fig.
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.
Most cocoa agroecosystems border on the introduced grasses Brachiaria decumbens Stapf (Poaceae) and B. humidicola (Rendle) Scheweick or border other agroecosystems such as Saccharum officinarum L. (Poaceae), H. brasiliensis, C. arabica, Erythroxylum coca Lam. (Erythroxylaceae) and Musa paradisiaca L. (Musaceae) or border stubble, secondary forests and primary forests. Extensive livestock production systems predominate in the region and there are high rates of deforestation.
The genus Uscanoidea was described by
Unfortunately, the type and syntype material of U. nigriventris are in very poor condition (
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) (
1 | Antenna with funicle and club | 2 |
– | Antenna without funicle | 4 |
2(1) | Club elongate, 4.0× as long as wide; genitalia tubular, 4.0× as long as wide, with distal half very narrow | U. aliciae |
– | Club ovate, less than 2.0× as long as wide | 3 |
3(2) | Genitalia with basal half ovate, with ventral medial keel and chelate structures | U. aduncatum |
– | Genitalia tubular with a large anterodorsal aperture and with two ventral setae | U. oviclavata |
4(1) | Ovipositor longer than metasoma | 5 |
– | Ovipositor not longer than metasoma | 6 |
5(4) | Ovipositor base at level of mesocoxae | U. silvestrii |
– | Ovipositor base at level of tegula | U. iperterebrata |
6(4) | Fore wing fringe with longest setae as long as discal setae | 7 |
– | Fore wing fringe with longest setae longer than discal setae | 8 |
7(6) | Club 2.3× as long as wide; fore wing length/width ratio 5.0× | U. hastata |
– | Club 1.7× as long as wide; fore wing length/width ratio 4.5× | U. parviclavata |
8(6) | Fore wing infumate from base to level of stigma vein level | U. ovata |
– | Fore wing hyaline | 9 |
9(8) | Club at least 3.0× as long as wide | 10 |
– | Club at most 2.0× as long as wide | U. nigriventris |
10(9) | Female club with maximum length of C5 2.0× width | U. acuminata |
– | Female club C5 at least 3.0× as long as wide | 11 |
11(10) | Fore wing length/width ratio greater than 1.6 | U. marilandica |
– | Fore wing length/width ratio at most 1.6 | 12 |
12(11) | Female club segment C5 as long as in the male; genitalia tubular, parallel sided, 3.0× as long as wide, with two ventral setae | U. apiclavata |
– | Female club segment C5 longer than in the male; genitalia tubular but not parallel sided, 4.4× as long as wide, without ventral setae | U. ricoi |
The high anthropogenic pressure on natural ecosystems leads to cocoa agroforestry systems becoming the vegetation coverage that provides suitable habitats and food for different groups of insects. In a sampling carried out at the Matapollos farm located in El Doncello, Caquetá, 40 cocoa pods with Monalonion dissimulatum eggs were collected. From each pod, between 15 to 25 M. dissimulatum eggs were obtained, for a total of 719 eggs. The percentage of parasitoidism of U. ricoi, sp. nov., in M. dissimulatum eggs reached 87,9%. Therefore, it seems that cocoa in agroforestry system plantations ensures natural biological control of this phytophagous insect.
The parasitoid wasp U. ricoi, sp. nov., shows high potential as a biological agent against M. dissimulatum in cocoa plantations (Figs
This work corresponds to the first record, arguably the second record, of the plant bug parasitoid of M. dissimulatum.
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) (
We thank the Ministry of Science, Technology and Innovation (Ministerio de Ciencia, Tecnología e Innovación) – MINCIENCIAS and the General Royalty System (Sistema General de Regalías) – SGR for funding the Research Project “STUDY OF THE DIVERSITY, POPULATION DYNAMIC AND BIOTIC POTENTIAL OF PREDATORS AND PARASITOIDS THAT CONTROL TRUE BUGS OF THE GENUS Monalonion IN COCOA PLANTATIONS OF THE STATES OF HUILA AND CAQUETÁ FLORENCIA (ESTUDIO DE LA DIVERSIDAD, DINÁMICA POBLACIONAL Y POTENCIAL BIÓTICO DE DEPREDADORES Y PARASITOIDES CONTROLADORES DE CHINCHES VERDADERAS DEL GÉNERO Monalonion EN PLANTACIONES DE CACAO DE LOS DEPARTAMENTOS DE HUILA Y CAQUETÁ FLORENCIA)” [code BPIN 2020000100513], approved by Agreement Number 100 of November 24, 2020, from which this study has derived. To María Bermúdez, Yulieth Rodríguez, Loreisy Andrade, Eidy Martínez, and Sebastián Valencia for their support in sampling and laboratory activities. To Yennifer Carreño and Éric Córdoba for their support in taking photographs and preparing the figures for publication. To Lizeht Gamboa for the administrative support during the execution of the Research Project. To the Supervision Support Group of the Research Project, including Juan Suárez, Karen Obregón, Paulo Murcia, Olga González, and Diego Vega.