New records and a voucher collection of parasitoid wasps (Hymenoptera) inhabiting agroforestry systems in the colombian amazon basin

Abstract

Cacao (Theobroma cacao) and copoazú (T. grandiflorum) agroecosystems represent a common source of income or many small-scale farmers in the Colombian Amazon basin. Most of these systems are set in low disturbance environments; they are considered biodiversity-friendly ecosystems inhabited by several groups of insects. In this study, we carried out a preliminary taxonomic inventory of the microhymenopteran parasitoids present in these agroforestry systems. Twenty-six localities of the Amazonian basin of Colombia were sampled using several insect collecting methods (Malaise trap, sweep net, pitfall, and rearing boxes). Collected specimens were curated and cataloged, establishing the first taxonomic voucher collection of parasitoids from the Colombian Amazon basin. We identified 767 specimens representing 64 species, 274 morphospecies, 143 genera and 20 families, 34 genera and 16 species of these being recorded for the first time in the country. The genus Gbelcia is reported for the first time from the Neotropical region. A new parasitoid-host relationship was found for Horismenus cupreus (Eulophidae) attacking larvae of Phyllocnistis sp. (Lepidoptera, Gracillariidae), which feeds on Annona montana (Annonaceae) leaves.

Keywords.
Plant hosts; Insect inventory; Insect taxonomy; Biological control; Insect biodiversity; Insect curatorship; Insect decline; Theobroma

INTRODUCTION

Museum collections based on insect collecting are among the most valuable resources for recognizing taxa from both simple and complex ecosystems, being important also in tracing historical data concerning local and widespread species and populations (Shaffer et al., 1998; Turney et al., 2015; Wagner, 2020). Even in agriculture, an activity in which pest management is a permanent activity, species inventories and reference collections of natural controllers, such as parasitoid wasps, still need to be carried out (Fernandez, 2000; Sääksjärvi et al., 2004; Lopez et al., 2009), since the proper identification of insects is the first step toward designing effective control strategies.

Cacao (Theobroma cacao L.) is one of the world’s most important perennial crops (Almeida & Valle, 2010), both socially and economically, mainly for 5 to 6 million farmers worldwide that depend on cocoa farming for their livelihood (WCF, 2014). Copoazu (T. grandiflorum (Willd. ex Spreng.)), an Amazonian species related to cacao, is a promising tree crop whose pulp and seeds may be used for a variety of food and cosmetic products, which contribute to the household income of family businesses in Colombia (Chaparro-Orozco & Lopez-Rodriguez, 2018). Both species are important crops in rural areas of Colombian, where they can be found being cultivated in agroecological systems, especially in small-scale, family-based economies that have preserved cacaos within mixed cropping systems (Espinal et al., 2005). These agroforestry systems have arisen as important alternatives for forest conservation and substitution of illicit crops for the country (Ortiz, 1993; Pineda-Jaimes, 2018).

Taxonomic inventories of beneficial insects such as parasitoid wasps are scarce in agroforestry systems. Most studies in agroecosystems have been carried out on insects of economic importance, e.g., pests (Miller, 1941; Conway, 1971; Entwistle, 1972; Keane & Putter, 1992; Ramirez-Cortés et al., 2008; Posada et al., 2011; Castillo, 2013; Srikumar & Shivarama, 2013), and pollinators (Winder, 1978; Adjaloo & Oduro, 2013; Mavisoy et al., 2013). This situation is similar for megadiverse countries such as Colombia, where taxonomic groups such as ants (Vergara & Serna, 2013; Fernandez et al., 2019) and bees (González et al., 2005; Parra & Londoño, 2013; Londoño-Carvajal et al., 2020) have been the focus of research efforts, but most other hymenopteran taxa remain poorly investigated. This is especially noticeable for parasitic wasps, in which only around 800 species have been recorded (Fernandez, 1995; Campos, 2001; Arias-Penna, 2004; Arias & Delvare, 2003; MBD, 2021; Noyes, 2021; SIB Colombia, 2021), representing about 0.8% of the total species predicted to occur in Colombia.

Parasitoid wasps constitute the most species-rich group of Hymenoptera, and the most common and abundant natural enemies of insect pests (Sharkey, 2007; Price et al., 2011). Nonetheless, the identification of microhymenopteran parasitoids often represents a challenging task due to their small size, high level of intraspecific variation of some taxa, the convergence of morphological traits, scarcity of taxonomic tools for their identification (Townes & Townes, 1966; Gebiola et al., 2012; Konstantinov & Namyatova, 2019), and the lack of representativeness of these species in voucher collections.

Given the lack of information regarding the identity of insects associated with cacao and copoazu crops in agroforestry systems of the Colombian Amazon basin and the scarce taxonomic records of parasitic wasps in Colombia, our primary aim was to carry out an inventory of the hymenopteran parasitoids inhabiting the above-mentioned crops. Our work consists of an initial alpha taxonomic effort in the cacao and copoazu farms located in the Amazon basin of Colombia. It was carried out by collecting, preserving, and curating parasitoid specimens from several farms. Identifications were based on the observation of morphological characters using available taxonomic identification tools. Thereby, we also managed to establish a cataloged voucher collection of the parasitoid wasps from the Colombian Amazon basin based on the collected specimens.

MATERIAL AND METHODS

Sampling localities and fieldwork

Adult specimens were collected in the departments (states) of Caquetá, Putumayo, and Amazonas (Fig. 1, Table 1), which are part of the Amazon basin region of Colombia. Between 2014 and 2018, we sampled 24 cacao and copoazu agroforestry farms. Overall, farm areas ranged from 1 to 5 ha and had a low level of technical crop production, with a mixture of different crops and a few timber trees or native forest. Each agroforestry farm was sampled using one Malaise and 10 pitfall traps for 60 days. The insects collected in Malaise traps were retrieved every 15 days (4 times). Pitfall traps were left operating for 24 hours every 15 days.

Figure 1
Sampling localities in the Amazonian basin of Colombia.

Table 1
Locations of the cacao agroforestry systems which were sampled.

Deparment (State)	Locality code	Latitude	Longitude	Altitude (m)
AMAZONAS	AM01	S 03°29′	W 70°12′	100
	AM02	S 04°08′47″	W 69°54′49″	70
	AM03	S 04°11′35″	W 69°56′23″	102
	AM04	S 04°11′38″	W 69°56′18″	96
	AM05	S 04°12′55″	W 69°56′26″	82
CAQUETÁ	CA01	N 01°22′03″	W 74°49′04″	278
	CA02	N 01°25′35″	W 75°30′57″	266
	CA03	N 01°29′59″	W 75°39′46″	300
	CA04	N 01°30′04″	W 75°36′22″	250
	CA05	N 01°30′06″	W 75°39′47″	263
	CA06	N 01°30′37″	W 75°40′21″	233
	CA07	N 01°40′02″	W 75°16′57″	337
	CA08	N 01°40′55″	W 75°18′30″	618
	CA09	N 02°07′11″	W 74°45′01″	270
	CA10	N 02°50′04″	W 74°46′08″	255
PUTUMAYO	PU01	N 00°28′01″	W 76°49′23″	316
	PU02	N 00°28′50″	W 76°30′18″	270
	PU03	N 00°39′27″	W 76°47′24″	325
	PU04	N 00°47′41″	W 76°38′49″	317
	PU05	N 00°47′42″	W 76°35′08″	317
	PU06	N 00°50′14″	W 76°38′06″	352
	PU07	N 01°07′06″	W 76°37′59″	584
	PU08	N 01°07′49″	W 76°39′56″	700
	PU09	N 01°11′28″	W 76°38′48″	352

Additionally, in every farm, we performed two active sampling efforts (once a month) using sweep nets and manual sampling during the two-month sampling period, between 10:00 and 15:00 hours. Manual sampling included a search for potential hosts of parasitoid wasps, including pupae, larvae, nymphs, and galls with signs of parasitism. The material found was placed inside insect breeding boxes (dimensions 20 × 10 × 5 cm), where a 5 × 5 cm hole was made in the lid of each box and covered with a muslin cloth. To avoid excess moisture, a piece of paper towel was placed inside each box. All collected and reared specimens were preserved in 76% ethanol.

Additional material

In addition to the previously described samples, we included in our collection other identified and curated parasitoid wasps (UNAB 5021, UNAB 1868, UNAB 3559, UNAB 3547, and UNAB 5562) housed at the Museo entomológico UNAB Facultad de Ciencias Agrarias, Bogotá, Universidad Nacional de Colombia, Bogotá, Colombia (UNAB), which were collected in cacao or copoazu crops in the Amazon region of Colombia, according to their label information.

Voucher collection and Imaging

Specimens were point-mounted, identified, cataloged (Excel database with location and biology information), and deposited in the Central Taxonomic Collection (CTC) of the UNAB museum (Martinez & Serna, 2015). Habitus (lateral view) photographs of pinned specimens were taken using a Canon 5D Mk II camera with an EF 100 mm f2.8, macro lens, and extension tubes.

Taxonomic identification

In this study we included de following families: Scelionidae, Platygastridae, Braconidae, Chalcididae, Pteromalidae, Eulophidae, Eurytomidae, Eucharitidae, Mymaridae, Encyrtidae, Eupelmidae, Perilampidae, Signiphoridae, Torymidae, Diapriidae, Figitidae, Evaniidae, Ceraphronidae, Bethylidae, Chrysididae, and Dryinidae. We employed the following identification keys, diagnoses, and descriptions: Chrysididae: Morgan (1984); Dryinidae: Olmi & Virla (2014); Bethylidae: Evans (1965), Terayama (2003), Azevedo (2014), Barbosa & Azevedo (2018), and Alencar & Azevedo (2020); Evaniidae: Deans (2006); Braconidae: Wharton et al. (1997); Figitidae: Forshage & Nordlander (2008), Buffington (2009), and Van-Noort et al. (2015); Platygastroidea: Masner (1980) and Chen et al. (2018); Diapriidae: Nixon (1980) and Masner & Garcia (2002); Chalcidoidea: Gibson et al. (1997) and Hanson & Gauld (2006); Chalcididae: Burks (1960) and Delvare (1992); Encyrtidae: Noyes (1980, 2010) and Trjapitzin et al. (2008); Eulophidae: Hansson (2009); Eucharitidae: Burks et al. (2015, 2018); Eupelmidae: Gibson (1995, 2004) and Pérez-Benavides et al. (2016); Eurytomidae: Gates (2008); Mymaridae: Huber (2015); Pteromalidae: Strand (1911).

To verify species distributions, we consulted Fernandez (1995), the NSF (National Science Foundation) database (2006), MBD (Biological Diversity database) (2021), Hansson (2019), and Noyes (2021). When a species determination was not possible using the available taxonomic tools, specimens were identified as morphospecies. For Platygastroidea, we followed the proposed classification of Chen et al. (2021), in which the superfamily is classified into eight families. Specimens of Ichneumonidae and Proctotrupidae (> 1,000 specimens) were not identified due to a lack of experience in these groups. We examined the specimens using a Nikon stereomicroscope using 60-120× magnification and direct lighting of 150 W.

RESULTS

We curated 767 parasitoid wasp specimens (Table 2). The greatest number of collected specimens were in the families Scelionidae (148 specimens), Braconidae (140), Chalcididae (97), and Pteromalidae (75) (Fig. 2A), while families with the least number of individuals were Chrysididae (5), Signiphoridae (3), Dryinidae (1), and Torymidae (1). Chalcidoidea and Platygastroidea contained over 37% of the total parasitoid wasps collected and curated (Table 2, Fig. 2A). We identified a total of 64 species and 274 morphospecies from 147 different genera, 20 families, and eight superfamilies (Table 2): Diaprioidea (16 species/morphospecies; 11 genera; 1 family) (Fig. 3A-C), Cynipoidea (30; 14; 1) (Fig. 3D-F), Chalcidoidea (159; 66; 11) (Fig. 4), Chrysidoidea (20; 11; 3), Ceraphronoidea (8; 2; 1), Evanioidea (10; 4; 1), Ichneumonoidea (39; 16; 1), and Platygastroidea (60; 24; 2) (Fig. 5). The largest number of genera happened in the families Scelionidae (18), Pteromalidae (17), Braconidae (16), and Figitidae (14) (Fig. 2B). On the other hand, the most species-rich superfamilies were Chalcidoidea (159 species) and Platygastroidea (60 species) (Table 2), while the most species-rich families comprised Chalcididae (50), Scelionidae (42), Braconidae (39), and Figitidae (30) (Fig. 2B).

Table 2
List of the parasitic wasps associated with cacao species in the Colombian Amazon basin*.

UNAB Catal	Sampling methods	Taxon	Number of specimens	Sampling localities	Host	Previous records
		ICHNEUMONOIDEA
		BRACONIDAE	140
5010	SW	Aleiodes sp.	7	PU04, PU05, PU06, PU08
5553	SW	Apanteles carpatus (Say, 1836)	3	PU07
1477	MN	Apanteles sp.	9	CA06	Reared from larva of Notodontidae on leaf of Cedrela sp. (Meliaceae)
1365	SW	Aphaereta sp.	1	CA03
1364	SW	Bracon sp.	1	CA03
3427-3428	MT	Chelonus sp.1-sp.2	3	CA06, PU06
1042	MN	Cotesia sp.	7	CA03	Reared from larva of Manduca sexta (Sphingidae) on Solanaceae
3440	MT	Cyclaulacidea sp.	1	CA06
3416-3420	SW	Digonogastra sp.1-sp.5	7	PU03, PU05, PU06, PU07, PU08
1476	SW	Heterospilus achi Marsh, 2013	7	CA01
3430	SW	Heterospilus levitergum Marsh, 2013	2	CA01
3431	SW	Heterospilus tres Marsh, 2013	2	CA03
3432-3239, 3822	SW	Heterospilus sp.1-sp.9	17	CA01, CA03, PU01, PU07	sp.9: Reared from root galls on Ficus sp. associated with species of Eurytomidae, Braconidae and Ichneumonidae
1474	MN	Hypomicrogaster sp.	19	CA01	Reared from larva of Sphingidae on Jussiaea linifolia (Onagraceae)
3823	MN	Labania ficophagaBelokobylskij & Zaldívar-Riverón, 2015**	6	PU07	Reared from root galls on Ficus sp. associated with species of Eurytomidae, Braconidae, and Ichneumonidae. The biology is similar to that found by Belokobylskij et al., 2015	Costa Rica (Belokobylskij et al., 2015)
3441	SW	Lasiphorus sp.	1	PU06
1367	MN	Lysiphlebus sp.	12	CA08
1366	MN	Lysiphlebus testaceipes Cresson, 1880	26	CA07, CA08	Reared from Toxoptera sp. on Citrus sp.
3421-3426	MT	Lytopylus sp.1-sp.6	6	CA06, PU05, PU06, PU07, PU09
5552	SW	Notiospathius sp.	2	PU03, PU07
1363	SW	Praon sp.	1	CA03
		CHRYSIDOIDEA
		BETHYLIDAE	19
5125	MN	Anisepyris angulatus Santos & Azevedo, 2000*	1	AM02		Brazil (Barbosa & Azevedo, 2018)
5124	MT	Anisepyris borladiBarbosa & Azevedo, 2018*	2	CA04		Brazil, Bolivia, Paraguay (Barbosa & Azevedo, 2018)
1193	SW	Anisepyris fortunatusEvans, 1965*	1	PU07		Costa Rica, Ecuador, Guiana (Barbosa & Azevedo, 2018)
3925-3928	SW, MT	Apenesia sp.1-sp.4	6	CA06, PU07
3923, 5132	MT	Bakeriella lata Kawada & Azevedo, 2003*	2	CA04		Brazil (Azevedo, 2014)
3224	MT	Bakeriella reclusa (Evans, 1969)*	1	CA06		El Salvador, Costa Rica, Ecuador, Bolivia (Azevedo, 2014)
5127-5128	MT, SW	Dissomphalus sp.1-sp.2	2	CA04, PU09
5126	MT	Epyris sp.	1	AM04
5129-5130	MN, MT	Pristocera sp.1-sp.2	2	AM03, AM04
5123	SW	Rhabdepyris (Trichotepyris) sp.	1	CA04
		CHRYSIDIDAE	5
3931	MT	Adelphe paradoxa (Ducke, 1902)	3	CA06
3617-3618	MT	Caenochrysis sp.1-sp.2	2	CA06, CA07
		DRYINIDAE	2
5131	SW	Gonadryinus hansoni Olmi, 1991	1	PU05
662	MT	Gonatopus sp.	1	CA06
		CERAPHRONOIDEA
		CERAPHRONIDAE	12
5011-5012	SW	Aphanogmus sp.1-sp.2	2	CA03
1448-1449, 4136-4139	SW, MT, MN	Ceraphron sp.1-sp.6	10	CA03, CA06, CA07
		CHALCIDOIDEA
		CHALCIDIDAE	100
5025	SW	Brachymeria annulata (Fabricius, 1793)	2	CA04, PU08
3525	MN	Brachymeria mnestor Walker, 1841	2	CA06	Reared from pupa of Pieridae on Duranta sp. (Verbenaceae)
1041, 1345, 1348	SW, MT	Brachymeria sp.1-sp.3	9	CA03, CA04, CA06, CA07, PU06
1865	SW	Conura albomaculata (Ashmead, 1904)	1	CA09
1872	MT	Conura apicalis (Ashmead, 1904)	1	PU09
1886	SW	Conura decisa (Walker, 1862)	4	PU05, PU06, PU07, PU08
1032	MN, SW	Conura dimidiata (Fabricius, 1804)	4	CA04, PU02, PU05
1866	SW	Conura enocki (Ashmead, 1904)	1	PU06
3527	SW	Conura marginata Ashmead, 1904	1	PU03
3465	SW	Conura mesomelas Walker, 1862	1	PU07
3429	MT	Conura nigrita (Howard, 1894)	1	PU09
5021	SW	Conura nigropetiolata Ashmead, 1904	1	AM05
1868	SW	Conura quadripunctata (Fabricius, 1804)	1	AM01
1033, 1036, 1350-1354, 3531-3549, 3559, 5022, 5024	MN, MT, SW, PT	Conura sp.1-sp.29	58	AM04-05, CA03-04, CA07-09, PU03, PU05, PU07-09	sp.11: Reared from pupa of Pieridae on Duranta sp. (Verbenaceae)
1190	SW	Haltichella hydara (Walker, 1842)	1	CA03
2530	SW	Haltichella ornaticornis Cameron, 1884	2	CA03, CA04
2531-2532	SW	Haltichella sp.1-sp.2	2	CA03
1189	SW	Notaspidium sp.	2	CA03
1356	SW, MT	Stypiura sp.	3	CA03, CA06
		ENCYRTIDAE	11
663, 3821	MT	Aenasius sp.1-sp.2	2	CA06, CA07
2537	SW	Anagyrus sp.	1	CA03
1473	MT	Caenohomalopoda sp.**	1	CA06		Algeria, Cayman Islands, China, India, Indonesia, Japan, Guam, North Korea, Puerto Rico, South Africa, South Korea, United States of America, Vietnam (Noyes, 2021)
1433	MT	Cerchysiella sp.	1	CA06
1463	MT	Cercobelus sp.**	1	CA06		Armenia, Azerbaijan, Belgium, Costa Rica, Czechoslovakia, Denmark, Finland, France, Germany, Hungary, India, Lithuania, Moldova, Montenegro, Netherlands, Norway, Russia, Sweden, United Kingdom (Noyes, 2021)
2538	MT	Coelopencyrtus sp.	1	CA06
2536	MT	Encyrtus infelix (Embleton, 1902)	1	CA06
3820, 3919	MT, SW	Ooencyrtus sp.1-sp.2	2	CA06, PU01
1436	MT	Tetracnemoidea sp.	1	CA06
		EUCHARITIDAE	23
4133	MN	Dicoelothorax sp.	1	CA05
1820	MN, MT, SW	Kapala sp.	14	CA03, CA04, CA06, PU09
5027	MN	Lirata luteogaster Cameron, 1884**	1	CA06		Brazil, Costa Rica, Ecuador, Mexico, Panama, Venezuela (Noyes, 2021)
1460, 3783	MT, SW	Orasema sp.	2	CA03, CA06
5110	SW	Orasema erwiniBurks, Mottern & Heraty, 2015*	1	CA04		Brazil, Ecuador, Peru (Burks et al., 2015)
5111	SW	Orasema evansiBurks, Heraty & Dominguez, 2018*	1	CA04		Costa Rica, Dominican Republic, Honduras, Nicaragua, Panama, St Vincent & Grenadines, Trinidad & Tobago, United States of America (Burks et al., 2018)
5112	SW	Orasema susanae species group	3	PU02, PU06, PU09
		EULOPHIDAE	45
5039	MT	Ametallon sp.	1	CA06
1197	SW	Aprostocetus (Aprostocetus) sp.	1	CA03
3817	MN	Aprostocetus gala (Walker, 1847) pos.	2	CA03	Reared from Cecidomyiidae on leaf galls of Manihot esculenta (Euphorbiaceae)*
3832-3835	MT, SW	Aprostocetus sp.1-sp.4	4	CA06, CA08, CA09, PU09
5040	SW	Chrysonotomyia sp.	1	PU03
3818	SW	Deutereulophus sp.**	1	CA03		Australasia, Nearctic, Neotropics, Paleartic (Noyes, 2021)
4091	MN	Elachertus sp.	6	CA01		Reared from Gracillariinae on Chrysophyllum cainito (Sapotaceae)
5043	SW	Entedon sp.	2	CA03
3826-3837	SW	Euderus sp.1-sp.2	2	CA01, CA03
5042	SW	Hadrotrichodes sp.	3	CA03
3830	MT	Horismenus bennetti Schauff, 1987*	1	CA06		Costa Rica, Trinidad & Tobago (Noyes, 2021)
5037	SW	Horismenus chydaeusHansson, 2009*	2	CA03		Belize, Costa Rica, Dominican Republic, Ecuador, Honduras, Peru (Noyes, 2021)
4093	MN	Horismenus cupreus (Ashmead, 1894)*	2	CA07		Reared from Phyllocnistis sp. (Gracillariidae) on Annona montana (Annonaceae)*
1467	MT	Horismenus elachurusHansson, 2009*	1	CA06		Costa Rica (Noyes, 2021)
3831	SW	Horismenus eumantisHansson, 2009*	2	CA03		Costa Rica, Ecuador, Panama, Peru, Trinidad & Tobago (Noyes, 2021
1465	MT	Horismenus lacticoxaHansson, 2009*	1	CA06		Costa Rica (Noyes, 2021)
1466	MT	Horismenus nr. selvensisHansson, 2009	1	CA06
3828	SW, MT	Horismenus orbiculus Hansson, 2009	2	CA03, CA06
1196	SW	Horismenus striatusHansson, 2009*	2	CA03		Costa Rica, Ecuador, El Salvador; Honduras, Trinidad & Tobago (Noyes, 2021)
3829	MN	Horismenus sp.	1	CA06
5041	SW, MT	Phymasticus sp.	6	CA03, CA06
3469	MT	Tetrastichus sp.	1	CA06
		EUPELMIDAE	11
1192, 1360, 1821, 3778, 5016, 5554	MT, MN, SW	Anastatus sp.1-sp.6	6	CA03, CA04, CA06, CA07, PU09
1359	MT	Brasema sp.	1	CA03
1358	MT	Brasema sp.	1	CA06
2535	MT	Merostenus (Merostenus) sp.	1	CA06
3777	MN	Phlebopenes longicollis (Westwood, 1874)	1	PU05
3776	SW	Zaischnopsis sp.	1	CA03
		EURYTOMIDAE	45
1450	MT	Aximopsis sp.	1	CA06
1429-1431, 4090	SW, MN	Eurytoma sp.	18	CA01, CA07, CA10, PU07	sp.4: Reared from root galls on Ficus sp. associated with species of Eurytomidae, Braconidae and Ichneumonidae
5046	SW	Isosomodes monteria Hanson & Gates, 2013	1	PU09
3779	SW	Neorileya meridionalis Gahan, 1927*	1	PU03		Argentina, Costa Rica, Ecuador, El Salvador, Guatemala, Honduras, Mexico, Panama, Peru, Trinidad & Tobago (Noyes, 2021)
1432	MN	Noerileya flavipes Ashmead, 1904*	1	CA10	Reared from Ascomycota fungus on Zygia longifolia (Fabaceae). Note: The fungus supplies food resources to different parasitoids (Observed in field)	Argentina, Brazil, Costa Rica, El Salvador, Nicaragua, Panama, Peru, Venezuela (Noyes, 2021)
3824	MN	Phylloxeroxenus sp.	7	PU07
3825-3827, 5120	MT, MN, SW	Prodecatoma sp.1-sp.4	14	CA06, PU01, PU02
5047	SW	Rileya antennataGates, 2008*	2	CA04, PU06		Brazil, Ecuador, Honduras, Peru, Surinam, Trinidad & Tobago
		MYMARIDAE	20
1451-1455, 3841-3843	MN, MT, SW	Gonatocerus sp.1-sp.8	15	CA01, CA03, CA06, CA08
3415	SW	Neomymar sp.	1	CA03
3838-3840	MT	Polynema sp.1-sp.3	3	CA06
1471	MT	Stephanodes sp.	1	CA06
		PERILAMPIDAE	6
5562	SW	Perilampus nr. hyalinus Say, 1829	1	AM05
4128, 4129, 1361	MT, SW	Perilampus sp.1-sp.3	5	PU03, PU06, CA04, CA06
		PTEROMALIDAE	75
3463	SW	Anisopteromalus sp.	1	PU09
3464	SW	Bubekia tricarinata (Ashmead, 1888)**	1	PU09		Argentina, United States of America (Noyes, 2021)
3467	SW	Chrysoglyphe apicalis Ashmead, 1894**	1	CA03		Nicaragua, St. Vincent & Grenadines, Venezuela (Noyes, 2021)
5119	MT, SW	Critogaster sp.	4	CA04, PU09
1534	MT	Epistenia (Epistenia) sp.	2	CA04, CA06
661	MT	Erotolepsia sp.**	1	CA06		Brazil, Grenada, St. Vincent & Grenadines
3844	SW	Gbelcia sp.**	1	PU07		Canada, Czechoslovakia, Hungary, Kazakhstan, Moldova, Romania, Sweden, Kazakhstan, United Kingdom, United States of America (Noyes, 2021)
3459	MT	Hadroepistenia erwini Gibson, 2003	1	CA06
5207	MN, SW	Halticopteroides exemaeBouček, 1993**	1	AM03, CA04		Canada, United States of America, Argentina, Paraguay
1437	MN	Heteroschema rugosopunctata (Ashmead, 1894)	42	CA03, PU06	Reared from Melanagromyza obtusa (Agromyzidae) in pods of Flemingia macrophylla (Fabaceae)
1347, 4134	MT, SW	Heteroschema sp.1-sp.2	5	CA03, CA06, CA09
659	MT	Lelaps aeneiceps Ashmead, 1904*	1	CA07		Brazil (Noyes, 2021)
658	MN	Lelaps affinis Ashmead, 1904*	1	CA07		Brazil (Noyes, 2021)
3461	SW	Lelaps bimaculata Ashmead, 1904*	1	PU05		Argentina, Brazil (Noyes, 2021)
3462	MN, SW	Lelaps nr. striaticepsStrand, 1911	4	AM02, CA06, PU08, PU09
5205	MN, SW	Lelaps setifronsStrand, 1911*	2	CA04		Peru (Noyes, 2021)
3466	SW	Neocatolaccus sp.**	1	PU01		Australasia, Africa, Nearctic, Neotropics (Noyes, 2021)
660	SW	Netomocera sp.**	1	CA09		Australasia, Africa, Asia, Neotropical, Nearctic, Palearctic (Noyes, 2021)
3468	SW	Propodeia complexaBouček, 1993**	1	CA03		United States of America, Trinidad & Tobago (Noyes, 2021)
3460	MT	Proshizonotus sp.	1	CA03
5122	MT	Psilocera sp.	1	CA04
5121	MT	Tomocerodes sp.**	1	CA06		United States of America, Mexico (Noyes, 2021)
		SIGNIPHORIDAE	3
4132	MN	Signiphora merceti Malenotti, 1917	1	CA05
1434	MT	Signiphora sp.	2	CA06
		TORYMIDAE	1
1425	MT	Podagrion sp.	1	CA06
		CYNIPOIDEA
		FIGITIDAE	39
4095	MT, SW	Acantheucoela sp.**	2	CA03, PU05		Belize
1464, 4111-4115	MT, SW	Aganaspis sp.1-sp.6	8	CA03, CA06, PU08
1424	SW	Agrostocynips sp.**	1	CA03		Argentina, Canada, Chile, Mexico, United States of America (Buffington & Scheffer, 2008)
4094	MN	Caleucoela sp.	1	PU08
4102	SW	Dieucoila sp.	1	CA03
1426-1428, 4105-4110	MT, SW	Ganaspis sp.1-sp-9	11	CA03, CA06, CA08, PU09
4100, 4101	SW	Hexacola sp.1-sp.2	2	CA07, PU09
4116-4118	MT	Leptopilina sp.1-sp.3	3	CA06
4096	SW	Neralsia sp.	1	PU04
4104	SW	Odonteucoila sp.	1	PU07
1423	SW	Trichoplasta sp.	1	CA03
1422	SW, MT	Tropideucoila sp.	3	CA03, CA06, CA07
2533, 2534, 4103	SW	Trybliographa sp.	3	CA03
3784	SW	Zaeucoila sp.	1	PU01
		DIAPRIOIDEA
		DIAPRIIDAE	22
3452	SW	Acanthropia sp.	1	CA03
3447, 3448	MT	Aclista sp.1-sp.2	3	CA06
1198-1201	MN, SW	Basalys sp.1-sp.4	9	CA03, CA07
3446	SW	Doliopria sp.	1	CA03
3449	SW	Hansona sp.**	1	PU09		Brazil, Costa Rica, Ecuador, Panama, Trinidad, Venezuela (Masner & García, 2002)
3453	SW	Idiotypa sp.**	1	CA03		Australia, Belize, Brazil, Canada, Jamaica, Mexico, United State of America, Venezuela (Masner & García, 2002)
3456	SW	Megalastopria sp.**	1	CA03		Antilles, Brazil, Mexico (Masner & García, 2002)
1459	MN	Monelata sp.	1	CA07
1194	SW	Paramesius sp.**	1	CA03		Australia, Brazil, Brunei, India, Jamaica, Mexico, Pakistan, United States of America, Venezuela (Masner & García, 2002)
1816	SW	Spilomicrus integer Thomson, 1858**	1	PU01		Australia, Belize, Brazil, British Virgin Islands, Brunei, Costa Rica, Dominican Republic, Guatemala, India, Jamaica, Japan, New Caledonia, Mexico, Trinidad & Tobago, Venezuela (Masner & García, 2002)
3450	SW	Spilomicrus sp.	1	CA03
1357	MT	Trichopria sp.	1	CA06
		EVANIOIDEA
		EVANIIDAE	19
4125	SW	Evania sp.	1	PU09
4121, 4126-4127	MN	Evaniella sp.1-sp.3	10	CA04, PU03, PU05, PU06, PU07, PU09
4124	SW	Hyptia sp.	1	PU06
3780-3782, 4122-4123	MT	Semaeomyia sp.1-sp.5	7	CA06, PU01, PU05, PU07, PU08
		PLATYGASTROIDEA
		PLATYGASTRIDAE	24
1435	SW	Inostemma sp.	1	CA07
3457, 3767-3769, 4130	MN, MT, SW	Leptacis sp.1-sp.5	11	CA03, CA05, CA06, CA07	sp.5: Reared from galls of Cecidomyiidae
1469	MT	Leptoteleia sp.	1	CA06
3773-3775	MN, SW	Platygaster sp.	3	CA03, CA08, PU09
3458, 3770-3772, 4131, 5015	MN, MT, SW	Synopeas sp.1-sp.6	8	CA01, CA03, CA05, CA06, PU09	sp.5: Reared from galls of Cecidomyiidae
		SCELIONIDAE	148
5117	MT	Acanthoscelio acutus Dotseth & Johnson, 2001	1	CA04
1445	SW	Apegus sp.	1	CA03
3756-5118	MT, PT	Baeus sp.	2	CA04, CA06
3761-3762	SW, MT	Baryconus sp.	6	CA03, CA04, CA06
1439-1440	MT, SW	Calliscelio sp.	2	CA03, CA06
1441	MT	Calliscelio suni Chen & Johnson, 2017	1	AM02
1472, 1446-1447, 3454-3455	MT, SW	Ceratobaeus sp.1-sp.5	8	CA03, CA04, CA06
5114	MT	Chromoteleia copiosaChen & Johnson, 2018*	3	CA06		Belize, Brazil, Costa Rica, Guatemala, Honduras, Mexico, Panama, Trinidad & Tobago, Venezuela (MBD, 2021)
5116	MT	Chromoteleia cuneusChen & Johnson, 2018*	4	AM02		Costa Rica, Ecuador, Panama (MBD, 2021)
5115	MT	Chromoteleia fuscicornis Kieffer, 1910	2	CA04, CA06
1470	SW	Duta sp.	1	CA07
1442, 3816	MT, SW	Gryon sp.1-sp.2	6	CA03, CA06
1475	MT	Macroteleia sp.	1	CA06
3760	SW	Opisthacantha sp.	1	PU09
3766	MT	Probaryconus sp.	1	CA06
3815	SW, PT	Scelio luteus (Cameron, 1888)	2	CA02, CA06
1438, 3757-3759	MT	Scelio sp.1-sp.5	9	CA06, PU09
1456-1458, 3804-3813	MN, MT, SW	Telenomus sp.1-sp.13	74	AM04, CA01, CA03, CA04, CA06, CA07, CA09, PU02, PU07, PU08
3765	SW	Thoron sp.	1	CA06		Azerbaijan, Brazil, Mexico, Sweden, Paraguay, United States, Ukraine (MBD, 2021)
1195, 1462	MN	Trissolcus sp.1-sp.2	18	CA03, CA09	sp.1: Reared from eggs of Antiteuchus sp. (Pentatomidae) on leaves of Theobroma cacao
3763-3764, 1468	MN, MT, SW	Triteleia sp.1-sp.3	3	CA06, CA07, CA09
1443	SW	Xenomerus sp.	1	CA03

• *Record for species, ** Record for genus, SW = Sweep net, MT = Malaise trap, MN = Manually, PT = Pitfall.

Figure 2
Bar charts of parasitoid wasp families and genera of collected individuals inhabiting agroforestry systems of cacao (Theobroma cacao) and copoazu (T. grandiflorum) from the Colombian Amazon basin. (A) number of individuals per family, (B) number of genera and species per family.

Figure 3
Habitus of parasitoid wasps collected in agroforestry systems of cacao (Theobroma cacao) and copoazu (T. grandiflorum). (A) Aclista sp. (Diapriidae) [UNAB 3747], (B) Basalys sp. (Diapriidae) [UNAB 1198], (C) Paramesius sp. (Diapriidae) [UNAB 1194], (D) Trichoplasta sp. (Figitidae) [UNAB 1423], (E) Aganaspis sp. (Figitidae) [UNAB 1464], (F) Tropideucoila sp. (Figitidae) [UNAB 1422].

Figure 4
Habitus of Chalcidoidea collected in agroforestry systems of cacao (Theobroma cacao) and copoazu (T. grandiflorum). (A) Haltichella hydara (Walker, 1842) [UNAB 1190], (B) Stypiura sp. [UNAB 1356], (C) Aenasius sp. (Encyrtidae) [UNAB 663], (D) Coelopencyrtus sp. [UNAB 2538], (E) Horismenus striatusHansson, 2009 (Eulophidae) [UNAB 1196], (F) Brasema sp. (Eupelmidae) [UNAB 1358], (G) Anastatus sp. (Eupelmidae) [UNAB 1192], (H) Neorileya flavipes Ashmead, 1904 (Eurytomidae) [UNAB 1432], (I) Perilampus sp. (Perilampidae) [UNAB 1361], (J) Erotolepsia sp. (Pteromalidae) [UNAB 661], (K) Bubekia tricarinata (Ashmead, 1888) (Pteromalidae) [UNAB 3464], (L) Lelaps affinis Ashmead, 1904 (Pteromalidae) [UNAB 658].

Figure 5
Habitus of Platygastroidea (Scelionidae) collected in agroforestry systems of cacao (Theobroma cacao) and copoazu (T. grandiflorum). (A) Apegus sp. [UNAB 1445], (B) Calliscelio sp. [UNAB 1439], (C) Gryon sp. [UNAB 1442], (D) Scelio sp. [UNAB 1438], (E) Xenomerus sp. [UNAB 1443], (F) Thoron sp. [UNAB 3765].

A total of 20 genera and 23 species are new records for Colombia (Table 2). These belong to the families Braconidae, Bethylidae, Diapriidae, Figitidae, Encyrtidae, Eucharitidae, Eulophidae, Eurytomidae, Pteromalidae, and Scelionidae.

New ecological observations

From the insect-rearing boxes, we obtained several individuals of Horismenus cupreus (Eulophidae) emerging from larvae of Phyllocnistis sp. (Gracillariidae), which in turn were feeding on leaves of Annona montana (Annonaceae) (Table 2). We also observed Elachertus sp. (Eulophidae) emerging from larvae of Gracillariinae (Lepidoptera: Gracillariidae), which were feeding on leaves of Chrysophyllum cainito Griseb. ex Pierre (Sapotaceae). Lastly, we obtained Brachymeria mnestor Walker, 1841 (Chalcididae), parasitoids of a pupa of Pieridae (Lepidoptera) found on leaves of Duranta sp. (Verbenaceae).

DISCUSSION

Our results provide the first taxonomic list of parasitoid wasps from the Colombian Amazon region inhabiting agroecosystems of cacao and copoazu identified to genus and species levels. In addition, the list includes an important number of new records for the country. These findings supplement relevant information provided in different datasets such as those in Noyes (2021) (Chalcidoidea), Biological Diversity database (MBD) of Ohio State University (Platygastroidea), Biological information system (SiB) of Colombia, and the study of Fernandez (1995).

Parasitoid wasps in cacao agroecosystems

We recorded here 20 parasitoid wasp families. This number is similar to that observed in cacao agroecosystems areas in Brazil, where 31 families were reported from Bahia (Sperber et al., 2004), then 30 from Itabuna (Nakayama et al., 2008), and 30 from Ilhéus (Sperber et al., 2012). The taxonomic composition of the families was almost the same in these studies and in ours. When we compare the taxa recorded from Bahia with those from the Colombian Amazon region, they are the same, except for Liopteridae, Megaspilidae, Agaonidae, Aphelinidae, Sclerogibbidae, Gasteruptiidae, Ichneumonidae, Monomachidae, and Proctotrupidae. The above-mentioned results of Sperber et al. (2004, 2012) and Nakayama et al. (2008) showed a high occurrence of Scelionidae and Braconidae. This is similar to our results, in which these families were mainly represented by the genera Telenomus and Lysiphlebus, respectively.

In cacao agroecosystems from Merida (Venezuela), Mazón (2015) and Mazón et al. (2018) reported 33 and 23 families of parasitoid wasps, respectively. Again, the richest families were similar to what we obtained in this study: Braconidae, Ichneumonidae, Scelionidae, Pteromalidae, Figitidae, Encyrtidae, and Mymaridae. However, our results for Chalcidoidea showed a higher richest of Chalcididae, Pteromalidae, and Eulophidae. Taxonomic identifications of the parasitoids in those investigations were carried out to the family level, whereas we achieved genus and species level identifications, which offer far greater information about the biology (Lenat & Resh, 2001). This is particularly true for parasitoid wasps, where the biology varies widely between species (Branca et al., 2019). For example, many of the hymenopteran genera we found in the current survey, such as Telenomus (Eberhard, 1975; Pardede, 1986), Brachymeria (Entwistle, 1963), Conura (García & Montilla, 2010), Aenasius, Anagyrus (Ackonor, 2002), Aprostocetus (Kerrich, 1963; LaSalle, 1994), Perilampus, and Heterospilus (García & Montilla, 2010), have been previously recorded as parasitoids of phytophagous species that feed on cacao.

Richness and number of curated parasitoids

Chalcididae accounted for 50 identified species and five genera, which makes it the richest family within the cacao and copoazu agroecosystems. Despite the lack of studies investigating the diversity of Chalcididae in cacao or copoazu, members of this family have been reported as parasitoids in pupae of phytophagous species such as Carmenta sp. (Sesiidae), an insect that feeds on cacao pods (García & Montilla, 2010). Chalcidid wasps have a cosmopolitan distribution, with a greater diversity in the Neotropical lowlands (Delvare, 1995). In Colombia, 17 genera and 115 species have been reported, many of them occurring in the Amazon basin (Pérez-Benavides & Serna, 2019).

Scelionidae constituted the second richest family we found in the cacao and copoazu agroforestry systems. Comparable results were found by García & Montilla (2005) in cacao, who reported 33 genera with the genera Idris, Trimorus, and Gryon as the most diverse. Although we recovered a lower number of genera, Apegus, Ceratobaeus, Thoron, and Xenomerus constitute additional reports observed for the family in these agroecosystems. Scelionidae is a highly diverse family in tropical forests, with 57 genera and 342 species reported from the Neotropics (Arias-Penna, 2002), out of 176 genera (extant and fossil) (Chen et al., 2021) and approximately 3,000 described species worldwide. According to Masner & Arias-Penna (2006), mixed agroecosystems can have a source-sink dynamics between forest and crop areas, where adults of Scelionidae are abundant in the surrounding forest, especially in the forest canopy where many of them search for hosts, which could also explain in part its high diversity in our work.

A high number of individuals of Braconidae (the third richest family within the agroecosystems) was chiefly reached due to Hypomicrogaster sp., reared from larvae of Sphingidae on Ludwigia hyssopifolia (G. Don) Exell (Onagraceae), as well as by the species Lysiphlebus testaceipes (Cresson) reared from Aphis sp. on Citrus sp. (Rutaceae). Hypomicrogaster is a large genus, mainly distributed in the Neotropical region, with 45 described species, nine of which have been recorded from Colombia and the Amazon basin (Fernandez, 2000). Species of Hypomicrogaster act as parasitoids of microlepidopteran leaf-mining and other cryptic or endophytic hosts (Valerio & Whitfield, 2015). Lysiphlebus testaceipes is widely distributed in the Nearctic region, and to a lesser degree in the Neotropics (Stary, 1976). It has also been reported from the Palearctic region as an introduced species. Lysiphlebus testaceipes attacks more than 100 aphid species, often suppressing their populations below economic injury levels (Jones et al., 2007).

New taxa and occurrence records

Even though most of our new records of genera and species have a Neotropical distribution, one of those found in our study, Gbelcia (Pteromalidae), has an atypical occurrence, given that its natural distribution is Holartic (Noyes, 2021). Gbelcia is recognized by the following combination of diagnostic features, observed in the specimens examined in this study: transverse and stout head, depressed thoracic dorsum, rugose-reticulate propodeum with distinct though slightly irregular median carina and plicae, pronotal collar with a high carina, and forewings with 1 to 6 hairs on the basal fold (Bouček, 1993; Gibson et al., 1997). Gbelcia comprises two described species: G. cordilurae Bouček, whose adults are parasitoids of the pupae of Cordilura varipes (Walker) and C. praeusta Loew (Diptera: Scathophagidae: Scathophaginae) (Bouček, 1993); and G. crassiceps Bouček, which are associated with Phragmites sp. (Poaceae) (Mitroiu, 2013).

New host records

Our new record of Phyllocnistis sp. (Gracillariidae) as a host of Horismenus cupreus is congruent with previous observations by Hansson (2009), who reported H. cupreus as a species that primarily attacks leaf-miners, mainly from the families Buprestidae, Curculionidae, Agromyzidae, Tischeriidae, and several unidentified microlepidopterans, as well as two records from spider eggs, probably as primary parasitoids (Hansson, 2009).

CONCLUSION

The collection of wasp parasitoids obtained in the present work constitutes an important contribution to our knowledge of natural biological controllers in agroforestry systems of the Colombian Amazon basin. It also provides a basic alpha taxonomic input for new studies. Agroforestry systems of cacao and copoazu provide a refuge for a high number of parasitoid wasps and allow multiple ecological interactions with their hosts. The life histories of most of the taxa found here remain unknown, as well as their functional role in agricultural ecosystems as potential natural enemies of phytophagous insects. Therefore, much work remains to be done on this topic. We also accumulated the first cataloged voucher collection of parasitoid wasps in Colombia, which in times of the Anthropocene insect decline, will be a continuing source of data and information to be used by future scientists, especially applied entomologists.

ACKNOWLEDGMENTS

The authors want to thank Valentina Vergara (CTNI - Agrosavia) for her constant support and orientation in the curatorial process at the UNAB museum; to Helber Arevalo and Javier Martinez for identifications of Lepidoptera (Gracillariidae) and Diptera specimens. To the UNAB museum, Facultad de Ciencias Agrarias, for supplying materials and facilities to carry out this work and the Entomology Laboratory of the Universidad de la Amazonia, LEUA; and Jean Alexander Gamboa for coordinating field trips and providing workspace and equipment at LEUA.

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• FUNDING INFORMATION: The first author is grateful to Minciencias and the Facultad de Ciencias Agrarias (Universidad Nacional de Colombia) which funded this work through the “Jovenes Investigadores e Innovadores por la Paz 2017” Program, code 205010028525. We are grateful to the cacao project “Reconocimiento de insectos de importancia agronomica asociados al agroecosistema Cacaotero de la Amazonia Colombiana” code 110171250625 CT FP44842-128-2016 for supporting this study.
• Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP".

Edited by

Edited by: Helena Carolina Onody.

Publication Dates

• Publication in this collection
  03 Oct 2022
• Date of issue
  2022

History

• Received
  11 May 2021
• Accepted
  11 Mar 2022
• Published
  27 May 2022