Association of Anagrus amazonensis Triapitsyn, Querino & Feitosa (Hymenoptera, Mymaridae) with aquatic insects in upland streams and floodplain lakes in central Amazonia, Brazil

ABSTRACT

Anagrus amazonensis Triapitsyn, Querino & Feitosa (Hymenoptera, Mymaridae) is a parasitoid that uses aquatic insect eggs as a host for the development of its immature stages. The objectives of this study are to record the interaction between A. amazonensis and its hosts and the aquatic plants used by these hosts to lay their eggs. Field work was conducted in floodplain lakes and upland (terra firme) streams, in four municipalities in Amazonas State, Brazil, where aquatic plants were scanned for the presence of aquatic insect eggs. In the laboratory, eggs were maintained in plastic containers with water until the emergence of the parasitoid or of the first instar insect. A total of 1223 adults of A. amazonensis emerged from eggs of Hemiptera, Lepidoptera and Odonata; these eggs were collected on 12 species of aquatic plants.

Keywords:
Amazonia; Aquatic Hymenoptera; Macrophyte; Trophic interaction

Among parasitoid hymenopterans, a small group has one or more life stages associated with aquatic environments (Bennett, 2008) where they oviposit on the eggs, larvae or pupae of a large range of host insects (Williams and Feltmate, 1992). Most are endoparasitoids of immature insects that are actually embedded partly or almost completely inside the host plant tissue or other submersed substrates or on floating substrates (Querino, 2012). In Brazil there are currently seven families (Braconidae, Diapriidae, Eulophidae, Figitidae, Mymaridae, Platygastridae, and Trichogrammatidae) and eight genera of Hymenoptera known to be associated with aquatic hosts (Querino and Hamada, 2014). In Central Amazonia, the riparian vegetation and aquatic macrophytes in streams and floodplain lakes are the preferred substrates for aquatic insects to oviposit (Bentes et al., 2014) but few records exist of the interaction between parasitoid, aquatic host, and plant used for oviposition by the insect host. Hydrophylita neusae Querino and Pinto (Hymenoptera: Trichogrammatidae) was found associated to Odonata eggs deposited on leaves of Thurnia sphaerocephala Hook. (Thurniaceae) (Querino and Pinto, 2007). Pseudoligosita longifrangiata (Viggiani) (Hymenoptera, Trichogrammatidae) was recorded for the first time in Brazil parasitizing eggs of Argia insipida Hagen in Selys (Odonata, Coenagrionidae) deposited on Tonina fluviatilis Aublet (Eriocaulacea) (Querino and Hamada, 2009). Anagrus amazonensis Triapitsyn, Querino and Feitosa (Hymenoptera, Mymaridae) was observed parasitizing Odonata (Zygoptera) eggs deposited on Rhynchospora pubera (Vahl) Bockeler (Cyperaceae) (Triapitsyn et al., 2008).

Knowledge of the parasitoid host fauna and their habitats is important for studies of population dynamics because these organisms act as a natural population control of their hosts. The aim of the present study is to document the aquatic insect hosts of A. amazonensis and the plants on which host eggs are laid in Central Amazonia. Eggs were randomly collected in 2004, 2005, and 2006 in three floodplain lakes (lentic environments) and eight upland (terra firme) forest streams (lotic environments) in four municipalities (Iranduba, Manaus, Presidente Figueiredo, and Rio Preto da Eva) in Amazonas State, Brazil (Fig. 1). Aquatic plants and vegetation trailing from stream banks were scanned for aquatic insect eggs, and, when present, eggs were collected and placed in plastic bags to be transported to the laboratory in Styrofoam boxes. In the laboratory, each aquatic insect egg batch was placed in a plastic container with water treated with fungicide in order to inhibit fungal growth, and was inspected daily until the emergence of parasitoids or immature insect hosts. Identification of aquatic insect egg was based on Bentes et al. (2014) and of A. amazonensis was based on the original description (Triapitsyn et al., 2008). Specimens obtained in this study are deposited in the Invertebrate Collection of the National Institute of Amazonian Research, Manaus, Brazil.

Fig. 1
Sites where Anagrus amazonensis (Hymenoptera, Mymaridae), its hosts, and their associated plants were collected in Amazonas State, Brazil.

A total of 1223 individuals of A. amazonensis were obtained, of which 1128 were female and 95 were male. Many factors can be influencing the sex ratio and result in a higher prevalence of females in the samples, such as reproduction habits and host characteristics. These factors may be explored in future studies.

A. amazonensis emerged from eggs of Hemiptera, Lepidoptera, and Odonata. A. amazonensis parasitized eggs placed on the underside of the macrophyte's leaves, with the exception of lepidopteran eggs, which were placed on the upper surfaces of the leaves. The higher rate of parasitism in Odonata eggs is most likely due to the fact that they are more easily found in the sampled locations. The host range of A. amazonensis appears to be exceptionally wide (encompassing three insect orders) even for a taxon (Mymaridae) where there seems to be a tendency for species not to be host-species specific; many mymarid species present host specificity at the genus level, while others are known to parasitize hosts of a wide range of families in a single insect order (Huber, 1997). The habitat range also appeared to be exceptionally wide. Although most aquatic Hymenoptera are recorded in lentic environments, at least 1/3 of the species are associated with lotic environments (Bennett, 2008). A. amazonensis did not show any preference, occurring in both lotic (upland streams) and lentic (floodplain lakes) environments (Fig. 1).

A. amazonensis emerged from aquatic insect eggs laid on 12 species of aquatic plants (Table 1). Of these, only Eichhornia crassipes (Mart.) Solms., Salvinia sp., Pistia stratiotes L., T. fluviatilis Aublet, Thurnia sp., and Ciperaceae had been previously associated with oviposition of aquatic insect eggs in the Amazon region (Bentes et al., 2014).

Table 1
Anagrus amazonensis Triapitsyn, Querino & Feitosa (Hymenoptera, Mymaridae) associations with aquatic plants and aquatic insect hosts sampled from upland streams and floodplain lakes during the years 2004, 2005, and 2006 in Amazonas State.

Aquatic plants		Insect hosts	Anagrus amazonensis
Family	Species		♀	♂	Subtotal
Thurniaceaea	Thurnia sphaerocephala (Rudge) Hook.	Odonata	645	3	648
Araceaea	Philodendron sp.	Odonata	92	1	93
	Urospatha sagittifolia (Rudge) Schott	Lepidoptera	51	1	52
		Odonata	42	0	42
	Spathiphyllum maguirei Bunting	Odonata	16	0	16
Cyperaceae a	Rhynchospora pubera (Vahl) Boeck.	Odonata	83	23	106
Eriocaulaceae a	Tonina fluviatilis Aublet	Odonata	25	0	25
Parkeriaceaeb	Ceratopteris pteridoides (Hook.) Hieron	Odonata	14	1	15
Poaceae a	Panicum laxum Sw.	Odonata	45	0	45
	Poaceae not identified	Odonata	4	0	4
Pontederiaceaeb	Eichhornia crassipes (Mart.) Solms.	Hemiptera	52	39	91
		Odonata	15	6	21
	Pontederia rotundifolia L.f.	Hemiptera	28	21	49
Xyridaceae a	Xyris caroliniana Walt.	Odonata	25	2	27
Total			1137	97	1234

• ^a
  Upland stream plants.
• ^b
  Floodplain lake plants.

Huber (1986) reported Anagrus as one of the three most-abundant genera of Mymaridae in faunal surveys. However, of the eight species of Anagrus recorded in Brazil, as far as it is known, only A. amazonensis is associated with aquatic environments (Triapitsyn et al., 2008). Host records are only known for 7 of these 8 species; only A. brasiliensis Triapitsyn does not have a confirmed host.

The results of this study therefore contribute to current understanding of this parasitoid, including its natural history, host interactions, and geographic distribution, especially for aquatic environments.

Acknowledgements

We thank the staff of the Instituto Nacional de Pesquisas da Amazônia (INPA) Herbarium (Gleison Viana and José Ferreira Ramos) for identifying the plants and Vivian C. de Oliveira for generating the map. The INPA/PIBIC program provided a fellowship for Malu Feitosa and CNPq provided a research fellowship for N. Hamada. We also thank Natsumi H. Fearnside and Philip M. Fearnside for the English translation and we are grateful for valuable comments on the manuscript from anonymous reviewers.

References

• Bennett, A.M.R., 2008. Global diversity of hymenopterans (Hymenoptera; Insecta) in freshwater. Hydrobiologia 595, 529-534.
• Bentes, S.P.C., Hamada, N., Ferreira-Keppler, R.L., 2014. Caracterização morfológica de ovos de insetos aquáticos e seus habitats na Amazônia Central, Brasil. In: Hamada, N., Nessimian, J.L., Querino, R.B. (Eds.), Insetos aquáticos na Amazônia Brasileira: taxonomia, biologia e ecologiaE., 1st ed. Editora do INPA, Manaus, pp. 51–68.
• Huber, J.T., 1986. Systematics, biology, and hosts of the Mymaridae and Mymarommatidae (Insecta: Hymenoptera). Entomography 4, 185-243.
• Huber, J.T., 1997. Mymaridae. In: Gibson, G.A.P., Huber, J.T., Woolley, J.B. (Eds.), Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). NRC Research Press, Ottawa, pp. 499–530.
• Querino, R.B., Pinto, J.D., 2007. A new Hydrophylita (Hymenoptera: Trichogrammatidae) from the Neotropics, with a key to species. Zootaxa 1437, 47-54.
• Querino, R.B., Hamada, N., 2009. An aquatic microhymenopterous egg-parasitoid of Argia insipida Hagen in Selys (Odonata, Coenagrionidae) and biological observations in the central Amazon, Brazil. Neotrop. Entomol. 38, 346-351.
• Querino, R.B., 2012. Hymenoptera. In: Hamada, N., Ferreira-Keppler, R.L. (Eds.), Guia ilustrado de insetos aquáticos e semiaquáticos da Reserva Florestal Ducke, Manaus, Amazonas, Brasil. Editora da Universidade Federal do Amazonas, Manaus.
• Querino, R.B., Hamada, N., 2014. Ordem Hymenoptera. In: Hamada, N., Nessimian, J.L., Querino, R.B. (Eds.), Insetos aquáticos na Amazônia Brasileira: taxonomia, biologia e ecologia., 1st ed. Editora do INPA, Manaus, pp. 377–390.
• Triapitsyn, S.V., Querino, R.B., Feitosa, M.C.B., 2008. A new species of Anagrus (Hymenoptera, Mymaridae) from Amazonas, Brazil. Neotrop. Entomol. 37, 681-684.
• Williams, D.D., Feltmate, B.W., 1992. Aquatic Insects. C.A.B. International, Wallingford.

Publication Dates

• Publication in this collection
  Jul-Sep 2016

History

• Received
  18 Jan 2016
• Accepted
  28 Apr 2016