Hymenoptera associated with conilon coffee crops in Espírito Santo state, Brazil, with emphasis on the families Diapriidae, Platygastridae and Scelionidae

Information about parasitoid wasp fauna can help determine the most appropriate methods for maintaining the ecological balance in agroecosystems, as these organisms are efficient natural enemies of various agricultural pests. The aim of this study was to survey the Hymenoptera families in conilon coffee plantations intercropped with other crops, focusing on the Diapriidae, Platygastridae and Scelionidae families, in order to determine wasps that could possibly act as biological controls. The study was carried out in eight conilon coffee farms located in three municipalities (Linhares, Marilândia and Sooretama) in Espírito Santo state, Brazil, with field samples collected in May (dry season) and December (rainy season) 2014. Were collected 1084 Hymenoptera specimens distributed in 10 superfamilies and 25 families. Fourteen genera of Scelionidae were collected, with Telenomus (34%), Idris (15%), Trissolcus (14%) and Ceratobaeus (10%) as the most abundant genera; seven genera of Diapriidae were collected with Doliopria (41%), Basalys (22%) and Trichopria (20%) as the most abundant; and two genera of Platygastridae were collected: Leptacis (52%) and Synopeas (14%). The highest abundance of wasp individuals was found in coffee intercropped with rubber trees. Intercropped coffee cultivation could potentially attract more natural enemies, as well as egg parasitoids that are promising biological controls.


INTRODUCTION
Coffee makes up a huge portion of the Brazilian economy. From January to July 2020, Brazil exported about 23 million bags of coffee to 118 countries around the globe, generating an exchange revenue of US$ 3 billion (Conselho dos Exportadores de Café do Brasil, CECAFE, 2020). The two species of planted coffee are arabica (Coffea arabica L.) and conilon (Coffea canephora Pierre ex A. Froehner). Espírito Santo state produces 63% of the total conilon coffee from Southeastern Brazil, containing about 266 thousand hectares of plantations (Companhia Nacional de Abastecimento, CONAB, 2017). Conilon coffee crops present remarkable advantages as adaptation to higher average temperatures (23±3 °C) and stronger disease resistance (Souza et al., 2004).
Coffee crops intercropped with trees (e.g., rubber trees) are associated with less extreme weather conditions such as lower incidence of solar radiation (Partelli et al., 2014). Additionally, these species can provide extra income sources of farmers by providing products such as food, firewood or fibers (Salgado et al., 2004;Nicoleli;Moller, 2006;Silva et al., 2012). These associations improve ecosystem functioning, aid in natural soil fertilization processes without additional chemical mixtures and enrich the fauna and flora diversity. This increase in flora diversity also favors the presence of pollinators and natural enemies that help control pests; thus, resulting in fewer chemical interventions to control them (Schroth et al., 2004).
In this context, Hymenoptera is an essential component of agroecosystems. This order contains families that act in two key niches: bee pollination and biological control of predator groups such as wasps, ants and parasitoids, which control and reduce pests at all developmental stages -egg, larva, pupa and adult (Gauld;Bolton, 1988;La Salle, 1993;Parra et al., 2002).
Egg parasitoids are one of the effective natural enemies of agricultural pests and have been successfully used for many decades as biological controls (Mills, 2010;Ballal, 2013). According to Mills (2010), six families of parasitic Hymenoptera have been used as classical biological controls of agricultural insect pests: families with exclusively egg parasitoids (Mymaridae, Scelionidae, and Trichogrammatidae); and families with some species of egg parasitoids (Elasmidae, Encyrtidae, Eulophidae and Platygastridae).
Research about egg parasitoids has received a lot of attention for two reasons: a) the relative ease in which they can be mass reared; and b) the fact that they not only attack host eggs, but also kill hosts in the egg stage, preventing damage to crops (Hassan, 1993;Parra;Zucchi, 2004). These parasitoids have been used to control many insect pests that infest crops such as cotton, grape, sorghum, soybean, sugar cane and tomato (summarized in Lenteren;Bueno, 2003).
Additionally, information about the Hymenoptera present in coffee crops is important, for developing biological control programs, to the extent as it is known which families are present at the crop. Thus, the objective of this work was to survey the Hymenoptera families in conilon coffee plantations intercropped with other crops, focusing on the families that have been poorly explored in agroecosystem studies: Diapriidae, Platygastridae and Scelionidae, in order to determine which wasps could potentially be used as biological controls, particularly parasitoids of Scelionidae eggs (Gauld;Bolton, 1988).

MATERIAL AND METHODS
The study was carried out in Espírito Santo state (Brazil), in three municipalities (Linhares, Marilândia and Sooretama) and eight conilon coffee farms. Among these coffee farms, coffee plants were intercropped with different associated crops (Figures 1-4), with different spacing between plants and associated crops ( Table 1). The weather in the region is dry in the winter and rainy in the summer season, and classified as tropical, with average annual precipitation of 151-250 mm, 24-27°C average temperature and 74% relative humidity  A 14-inch sweep net made of canvas or other linenlike fabric with a metallic structure reinforcing at the end was used to collect samples. Five blocks of 10 plants were sampled from each farm and the upper third portion of the coffee plant was swept. Sweeping time on each plant was not timed. The contents of the net were deposited in a plastic bag with paper strips and a modified lethal chamber (glass container with a cotton wick soaked in ethyl acetate). The insects were kept in the bags for two hours. The material was sorted at the entomology laboratory of the Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural (INCAPER), in Linhares (Espírito Santo state). Then, they were transported in entomological blankets with the field information (date, type of agroecosystem, collector, location and geo-references), and stored in alcohol containers that were sent to the Instituto Nacional de Pesquisas da Amazônia (INPA), in Manaus (Amazonas state) for identification. Hymenoptera were identified under a stereomicroscope (model Nikon SMZ645) with a 2x magnifying glass (model Nikon G-AL). To identify the families, the taxonomical keys proposed by Goulet and Huber (1993) were used, and to identify the genera of Diapriidae, Platygastridae and Scelionidae families, the keys proposed by Masner and Garcia (2002), Masner and Huggert (1989) and Masner (1976) were used respectively. The generic identifications of some Platygastridae specimens were not possible because they were destroyed during the sweep sampling process.

RESULTS AND DISCUSSION
A total of 1084 Hymenoptera specimens distributed in ten superfamilies and 25 families were collected ( Table 2). The most abundant families were Trichogrammatidae (14%), Eulophidae (13%), Braconidae (10%) and Scelionidae (10%). The coffee intercropped with rubber trees presented the highest abundance of Hymenoptera (32%), followed by coffee with coconut trees (22%) and coffee with cedar trees (21%) ( Figure 5). Likewise, family richness was also higher in coffee with rubber trees (19 families), followed by coffee with coconut (18) and monoculture coffee (16). Intercropping other plants with coffee could increase arthropod diversity in the local environment due to microhabitat variety. For example, Perdoná, Cruz and Fischer (2013) have reported that the shading of coffee crops associated with macadamia (Macadamia intergrifolia Maiden & Betche) reduced scalding (Rhynchosporium secalis (Oudem) J.J. Davis) and freezing, the incidence of harm by winds, defoliation, with fewer attacks by the coffee leaf miner (Leucoptera coffeella (Guérin-Mèneville & Perrottet)), weeds, and increased nutrient cycling and the presence of natural pests and disease controllers.
Compared to the survey of parasitoid fauna in arabica coffee crops (Coffea arabica L.), which was collected using Moericke traps in inland São Paulo, the families Encyrtidae, Scelionidae, Ichneumonidae, Mymaridae and Braconidae were the most abundant, respectively (Perioto et al., 2004). Using Malaise traps in Chapada Diamantina (Bahia state), Ichneumonidae, Braconidae, Eulophidae, Mymaridae and Pteromalidade were the most abundant families, respectively (Palma-Santos; Pérez-Maluf, 2010). Additionally, Encyrtidae, Diapriidae, Ceraphronidae, Platygastridae and Braconidae were the most abundant families, respectively, in Moerecke traps used in organic coffee crops from Minas Gerais (Ferreira;Silveira;Haro, 2013). Therefore, the differences in the trap type, regions, and the presence or absence of associated crops could affect the abundance of Hymenoptera fauna diversity.
In this study, Trichogrammatidae was most abundant in coffee monoculture and coffee associated with coconut (Table 2). Such abundance is related to the egg mass collected from individuals of the same morphospecies. This occurs in polyembryonic parasitoids such as Trichogrammatidae and Encyrtidae, in which more than 10 parasitoid wasps can emerge from one single host egg (Strand, 2009;Segoli et al., 2010). Natural enemies with this habit are very efficient biological controls, as they directly attack eggs and eliminate pests before they cause any losses to farmers/growers.
In coffee intercropped with cocoa, Scelionidae was the most abundant family (Table 2). Similarly, the genera Telenomus (Scelionidae) was the most abundant in a survey performed on cocoa crops located in Aragua state (Venezuela), and its species are associated with Hemiptera and Lepidoptera eggs (Rodríguez;Montilla, 2005). For coffee intercropped with black pepper, the Encyrtidae family was most abundant (Table 2), which is an important parasitoid of mealybug (Noyes, 2017).
Idris and Ceratobaeus are parasitoids of Araneae oothecas that are commonly found in studies about Hymenoptera, especially in Neotropical regions (Arias-Penna, 2002;Azevedo et al., 2015).
Doliopria is a poorly studied genus, with few species in the Nearctic region and a high number of undescribed species in the tropical regions of the Americas (Masner;García, 2002). This genus presents parasitic relationships with ants from Ecitonini and Attini tribes (Masner;García, 2002). In general, Basalys and Trichopria are parasitoids of dipteran pupae (Notton, 1990;Neutzling;Garcia, 2011), however, there are some reports of Basalys parasitizing pupae of Psila rosae F., a carrot pest (Estrada, 2008).
Among the Diapriidae collected, Trichopria is the genus with the most potential for pest control, as it is associated with Anastrepha (Wollmann et al., 2016) that attack coffee fruits and can cause considerable losses for farmers (Montes et al., 2012;Camargos et al., 2015).
The presence of diverse Hymenoptera parasitoid groups is a good indication that coffee intercropped with other crops could be promising for biological control of coffee pests. Considering the sampling method, this could be due to the diversity of Scelionidae and Diapriidae.

CONCLUSIONS
Intercropped coffee could potentially attract more natural enemies, as well as egg parasitoids that are promising for biological control. Herein, several genera of Platygastridae, Scelionidae and Diapriidae were recorded in this agroecosystem and their potential as biological controls is reported for the first time.

ACKNOWLEDGMENTS
We thank reviewers for their critical reviews and suggestions on this manuscript. We also thank to owners of the farms where the collections were made, and to all people of the Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural (INCAPER) for contributing to logistics and human resources. Thanks to Karine Schoeninger who identified the Chalcidoidea wasps. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES), Finance Code 001 (D.G. Pádua).