Ants establish mutualistic interactions with hemipteran insects belonging to 2 suborders: Auchenorrhyncha, which includes the Cicadellidae (leafhoppers) and Membracidae (treehoppers); and Sternorrhyncha, which includes the Aphididae (aphids), Coccidae (soft scales), and Pseudococcidae (mealybugs) (Delabie 2001; Styrsky & Eubanks 2007). These interactions are widespread in insects, and most of the ant-tended Hemiptera share several characteristics: nymphs and adults are gregarious, they produce honeydew, and they feed on plant phloem. Nymphs and adults of the leafhopper Dalbulus quinquenotatus DeLong & Nault (Hemiptera: Cicadellidae) aggregate within partially unfolded leaves at the base of their gamagrass host plants Tripsacum (Poaceae) (Nault et al. 1983), which is a relative of maize (Zea mays subsp. mays L.; Poaceae) (Wilkes 1972). There, they produce large amounts of honeydew, which attracts certain ant species, resulting in an obligatory mutualistic association with the leafhopper (Moya-Raygoza & Nault 2000).

The nymphs of D. quinquenotatus are parasitized by the dryinid wasp Anteon ciudadi Olmi (Hymenoptera: Dryinidae) (Moya-Raygoza 1995). Using baited gamagrass plants, it was determined that D. quinquenotatus eggs are parasitized by Anagrus naulti Triapitsyn & Moya-Raygoza (Hymenoptera: Mymaridae), Paracentrobia sp. near subflava (Girault), and Pseudoligosita sp. near longifrangiata (Viggiani) (both Hymenoptera: Trichogrammatidae) (Moya-Raygoza & Triapitsyn 2015). The canopy leaves of the gamagrass plants are inhabited by Dalbulus maidis (DeLong) and Dalbulus gelbus DeLong (both Hemiptera: Cicadellidae) adults, but they have not been observed to be attended by ants (Larsen et al. 1992). To our knowledge, little is known about the community of egg parasitoids that attack Hemiptera tended by ants in the habitat where they have established this mutualistic interaction. The objective of the present study was to evaluate the abundance of D. quinquenotatus and its congeners, and the abundance of the egg parasitoid species living in the Tripsacum dactyloides (L.) L. (Poaceae) habitat. It was demonstrated recently that egg parasitoids living in the Tripsacum habitat parasitize, develop, and emerge from D. maidis eggs, reaching high rates of parasitism (Moya-Raygoza 2021). The corn leafhopper, D. maidis, is one of the most important maize pests in Latin America (Nault 1990), and parasitoids found in the wild Tripsacum habitat could be a biological control agent for control of D. maidis.

Materials and Methods

This study was conducted in a natural field population of T. dactyloides. This is a large population located at 20.5202778°N, 103.4822222°W; 1,621 masl, near the town of San Agustin, Jalisco State, in western central Mexico. This site was selected because the ant Brachymyrmex obscurior (Forel) (Hymenoptera: Formicidae) tends nymphs and adults of D. quinquenotatus on the basal leaves of Tripsacum. The presence and abundance of adult Dalbulus leafhoppers and adult egg parasitoids was monitored at the end of the wet season of 2018. Both leafhoppers and parasitic wasps (parasitoids of nymphs and eggs) were surveyed using double-sided yellow sticky card traps (AlphaScents, Bridgeport, New York, USA). Each trap was set 1 m from Tripsacum patches colonized by B. obscurior ants and D. quinquenotatus. In total, 14 traps, each 14 × 20 cm in size, were set for each sampling period. The traps were changed every 7 d from 11 Oct to 30 Nov, a seasonal period when leafhoppers and parasitic wasps are abundant on gamagrass (Larsen et al. 1992; Moya-Raygoza 1995). The traps were changed 7 times. Adult Dalbulus leafhoppers collected in the traps were identified using the keys developed by Triplehorn and Nault (1985), and adult egg parasitoids were identified with the keys of Moya-Raygoza and Triapitsyn (2015). Abundance of each of the adult Dalbulus species was compared using the Kruskal-Wallis test, and the same test was applied to compare the abundance of the adult egg parasitoid species. Statistical analyses were conducted in R (R Core Team 2018).

Results

During the survey, 723 adult Dalbulus leafhoppers belonging to 3 species were collected using yellow sticky card traps during the last mo of the wet season, between Oct and Nov (Table 1). The species found in the Tripsacum habitat were D. quinquenotatus, D. maidis, and D. gelbus. The abundance of the 3 species was significantly different (H = 145.86; df = 2; P = 0.0001) (Fig. 1). The most abundant leafhopper species was D. quinquenotatus (73.31%), whereas D. maidis was the least abundant (1.24%) (Table 1).

In total, 1,551 adult egg parasitoids were collected on the same yellow sticky cards (Table 1). The collected species were A. naulti, Paracentrobia sp., and Pseudoligosita sp. The abundance differed significantly among the 3 species (H = 21.86; df = 2; P = 0.0001; Fig. 2). Anagrus naulti was most abundant (42.74%), followed by Paracentrobia sp. and Pseudoligosita sp. (22.37 % and 34.89 %, respectively; Table 1). No A. ciudadi adults, which parasitize nymphs of D. quinquenotatus, were found on any of the yellow sticky cards.

Table 1.

Total number of Dalbulus and parasitic wasp species captured by yellow sticky traps, with percentage of abundance in parentheses for each species. All sampling from the Tripsacum dactyloides habitat was conducted during 2018, at the end of the wet season, in Jalisco, Mexico.

Fig. 1.

Average number of adult Dalbulus leafhoppers trapped by yellow sticky traps within the Tripsacum dactyloides habitat during the end of the wet season of 2018, in Jalisco, Mexico. Different letters (a, b, c) indicate statistical significance.

Discussion

Little is known about the interactions between the Hemipterans tended by ants and the parasitoid community living in the field habitat where this mutualism occurs. In the present study, we found both tended and non-tended Dalbulus leafhoppers and 3 egg parasitoid species inhabiting the Tripsacum field habitat. Dalbulus leafhoppers and egg parasitoids were collected using yellow sticky card traps. Previously, Larsen et al. (1992) surveyed adult Dalbulus leafhoppers on gamagrass using this type of trap. They found D. quinquenotatus, D. gelbus, and D. maidis within the Tripsacum habitat during the wet season (Oct and Nov). In the present study, we found that D. quinquenotatus, a species tended by ants, was more abundant than D. gelbus and D. maidis. The sheer number of D. quinquenotatus adults trapped using the yellow card method suggests a great dispersal by these adults within the Tripsacum habitat. Likely, D. quinquenotatus reached these high numbers in this Tripsacum habitat because it is tended by B. obscurior. A recent study found that the tending ant Solenopsis invicta Buren (Hymenoptera: Formicidae) produces a trail pheromone containing (Z, E)-α farnesene as its major component, and that this pheromone benefits population growth of the tended aphid Aphis gossypii Glover (Hemiptera: Aphididae) (Xu et al. 2021).

Fig. 2.

Average number of adult egg parasitoids trapped by yellow sticky traps within the Tripsacum dactyloides habitat during the end of the wet season of 2018, in Jalisco, Mexico. Different letters (a, b) indicate statistical significance.

Within the Tripsacum habitat, the adult egg parasitoids A. naulti, Paracentrobia sp., and Pseudoligosita sp. also were trapped, with A. naulti being the most abundant. The same 3 parasitoid species were trapped using baited Tripsacum plants, but in this case, Paracentrobia sp. was the most abundant, even though A. naulti adults emerge earlier than Paracentrobia sp. adults (Moya-Raygoza & Triapitsyn 2015). These egg parasitoids are generalists and are known to parasitize eggs of D. quinquenotatus and D. maidis in the gamagrass habitat (Moya-Raygoza 2021). Parasitoid emergence and efficacy was similar in D. maidis eggs laid on landrace and hybrid maize tested within the Tripsacum wild habitat, and egg parasitoids found in maize relatives such as Tripsacum could be an important resource to control hopper pests in maize agroecosystems (Moya-Raygoza 2021). However, Tripsacum populations have disappeared in Jalisco, Mexico, during the past 20 yr, affecting leafhopper and parasitoid presence. In 1998, 13 sites with Tripsacum populations bearing the D. quinquenotatus-ant mutualistic association were reported in central Jalisco (Moya-Raygoza & Larsen 2001). Only 3 of the 13 Tripsacum populations observed in 1998 were found in 2020, which disappeared due to anthropogenic perturbation (G. M. R., personal observation). The conservation of Tripsacum populations is important for maintaining egg parasitoids, which could be used as biological control agents in maize fields throughout Latin America.