Research Article |
Corresponding author: Gustavo Moya-Raygoza ( moyaraygoza@gmail.com ) Academic editor: Jack Neff
© 2017 Iskra M. Becerra-Chiron, Gustavo Moya-Raygoza, Alejandro Muñoz-Urias.
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:
Becerra-Chiron IM, Moya-Raygoza G, Muñoz-Urias A (2017) Host-Dryinidae (Hymenoptera) interactions on edge grasses of maize agroecosystem throughout winter in Mexico. Journal of Hymenoptera Research 57: 155-166. https://doi.org/10.3897/jhr.57.12990
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Little is known about the host-parasitoid interactions on the edges of crops during winter. Our objective was to determine the parasitoid species that attack nymphs and adults of leafhoppers and planthoppers, and evaluate the interactions that occur during winter on maize edges. Between January and June of 2014 and 2015 leafhoppers and planthoppers with evidence of parasitism by Dryinidae (Hymenoptera) were collected on grasses that grow in maize fields margins in Mexico and were maintained alive until parasitoid adult emergence. Dryinids such as Gonatopus huggerti (Olmi), Gonatopus mimoides (Perkins), Gonatopus breviforceps (Kieffer), and Gonatopus caraibicus (Olmi) were the most common parasitoids. They attacked several leafhopper species such as Dalbulus maidis (DeLong), Balclutha incisa (Matsumura), Exitianus picatus (Gibson), and Stirellus bicolor (Van Duzee). The connection of the net was of 31%. The presence of parasitoids in winter margins highlights the importance of conserving maize edges for biological control.
Chrysidoidea , Auchenorrhyncha , Cicadellidae , biological control, Host-parasitoid interactions
Edges in agroecosystems form a habitat hosting herbivore insects and their predators and parasitoids (
Many leafhopper species are efficient vectors of viruses and bacteria to plants (
On the other hand, leafhoppers that inhabit edge grasses of maize fields were parasitized by dryinids and strepsipterans during the dry season (
The study was conducted in the region of Zapopan, state of Jalisco, Mexico 20°44'49"N, 103°30'48"W; 1,662 m above sea level. This region was selected because it represents the environmental condition in which maize is cultivated in most of the tropics. Maize is seeded there in June, when the wet season starts. Maize plants dry out in November and are harvested in December. From December to May grasses grow and have green foliage in the maize edges. This study was conducted during two consecutive winter seasons in 2014 and 2015, starting in January and ending in May. Sampling was done three times per week, using a sweep net for one hour between 11 am. and noon and performing 1,200 sweeps per sampling.
The collected hopper (leafhoppers or planthoppers) nymphs or adults with evidence of parasitism were maintained alive. Parasitized hoppers show on the thorax or abdomen a black sac hosting a larva of a parasitoid (
Network size, link density, dependence, and connectance were performed with Package bipartite (
The grasses found bordering the harvested maize fields during the 2014 and 2015 winter season were the following Cyperales-Poaceae: Brachiaria plantaginea , Rhynchelytrum repens (Willd), Cynodon plectostachyus (Schum.), Sorgum vulgare (Pers), and Digitaria ciliaris. They showed green foliage throughout the winter-dry season from January to May. Hoppers without and with parasitism evidence were found on these grasses.
Leafhopper (Hemiptera: Cicadellidae) nymphs and adults of the subfamily Deltocephalinae were parasitized mainly by wasps (Hymenoptera: Dryinidae) of the subfamily Gonatopodinae during two consecutive winter seasons of 2014 and 2015. Most of the leafhoppers with evidence of parasitism were collected in March, April, and May, when compared with those collected in January and February (χ² = 65.15, P < 0.05). Nymphs of Exitianus sp. and adults of E. picatus were parasitized in January and February by the following Dryinidae species: Gonatopus huggerti (Olmi), Gonatopus mimoides (Perkins) and Gonatopus sp. In addition, an undetermined species of Delphacidae was parasitized by an undetermined strepsipteran of the genus Elenchus (Strepsiptera: Elenchidae). In March, April, and May, more species of leafhoppers were parasitized. Nymphs and adults of B. incisa, E. picatus, Amblysellus sp., D. maidis, and S. bicolor were parasitized by the following Dryinidae: G. huggerti, G. mimoides, Gonatopus breviforceps (Kieffer), Gonatopus caraibicus (Olmi), and Gonatopus sp. (Table
Adult parasitoids emerged (♀ or ♂) from the hopper in nymphal (N) or adult (A) stage collected on grasses during the winter seasons (January to May) of 2014 and 2015.
Parasitoid species | January | February | March | April | May |
---|---|---|---|---|---|
Gonatopus huggerti ♀ | Exitianus sp. (N) Exitianus picatus (A) | Balclutha incisa (N) | |||
Gonatopus mimoides ♂ ♀ | Exitianus picatus (A) | Balclutha incisa (A) Exitianus picatus (N) |
Exitianus picatus (N) Amblysellus sp. (N) Exitianus picatus (A) |
Exitianus picatus (A) Exitianus picatus (N) Balclutha incisa (A) Dalbulus maidis (A) | |
Gonatopus breviforceps ♀ | Balclutha incisa (A) | Balclutha incisa (A) | |||
Gonatopus caraibicus ♀ | Stirellus bicolor (A) Amblysellus sp. (N) Stirellus bicolor (A) | Stirellus bicolor (A) Amblysellus sp. (A) | |||
Gonatopus sp.♂ | Exitianus sp. (N) | Amblysellus sp. (N) | Amblysellus sp. (A) | ||
Elenchus sp. | Planthopper (A) | ||||
Total with evidence of parasitism | 5 | 2 | 29 | 27 | 28 |
Dryinids of the genus Gonatopus attacked leafhoppers belonging to different tribes throughout the 2014 and 2015 winter seasons. For example, G. mimoides attacked leafhoppers of different tribes almost the whole winter season, parasitizing D. maidis and B. incisa (Macrostelini), E. picatus (Chiasmini), and Amblysellus sp. (Deltocephalini), whereas species such as G. caraibicus parasitized Amblysellus sp. (Deltocephalini) and S. bicolor (Stenometopiini) (Fig.
Host (hopper)-parasitoid interactions are indicated by a qualitative network of species that occur on winter perennial grasses bordering harvested fields of maize. The network comprises 13 species (six parasitoid species and seven hopper host taxa) (Fig.
The present study is a report on the grass species (first trophic level), the herbivore hoppers and their nymphs (second trophic level), and adult parasitoids (third trophic level), that live during the winter-dry season on the edges of maize fields once the crop is harvested. Our results agree with those of
Little is known about herbivore leafhopper vectors during winter season on the edges when the crop is absent. In maize, edge grasses host high diversity of leafhoppers, among which Exitianus sp. B. incisa, S. bicolor, G. sonora, Amblysellus sp., E. picatus and D. elimatus are the most abundant species (
Six parasitoids species develop and emerge from nymph or adult hoppers. The most abundant leafhopper species were attacked by dryinids, among which most species are reported for first time on edge grasses. Previously, G. caraibicus was reported as a parasitoid of the leafhoppers Amplicephalus simpliciusculus (Linnavuori), Haldorus sexpunctatus (Berg), Chlorotettix sp., Planicephalus flavicosta (Stål), Exitianus obscurinervis (Stål) and Graminella stelliger (Berg) (
Parasitoids attacked, developed and emerged from nymphs and adult leafhoppers belonging to different tribes. This report indicates that most parasitoids that live on the edge grasses during winter are generalists. Egg parasitoids, i.e Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Paracentrobia sp. and Pseudoligosita sp. (Hymenoptera: Trichogrammatidae), also were generalists. They are the most common parasitoids attacking the eggs of D. maidis during the maize growing season in Mexico (
Generalist parasitoids are important because a wide host range is a vital parameter with regard to a natural enemy´s quality as a control agent (
Edges with reduced management intensity show an increase in immigration of insects, particularly natural enemies (
In conclusion, edges that surround maize agroecosystem during winter hold leafhoppers from different tribes, which are attacked by generalist parasitoids. A food web of leafhoppers-parasitoids is presented for the first time for maize field edges formed by grasses. It is important to conserve this biodiversity of parasitoids for the conservation of natural biological control in maize edges.
We thanks Massimo Olmi (Tropical Entomology Research Center) for the identification of dryinids, Jeyaraney Kathirithamby (University of Oxford) for the identification of the Strepsipteran taxon, Christopher Dietrich (Illinois National History Survey Museum) and Adilson Pinedo-Escatel (CUCBA, Universidad de Guadalajara) for the identification of leafhoppers. Also we thank Liberato Portillo (CUCBA, Universidad de Guadalajara) for the suggestions during the study and Jose Luis Villalpando Prieto (SAGARPA) for the grasses determination.