VICTOR FURSOV

Originally published in: Bulletin of Irish Biogeographical Society, 1995, vol.18 p.2-12.

VICTOR FURSOV

Institute of Zoology of National Ukrainian Academy of Sciences, Kiev, Bogdan Khmelnitskiy Street, 15, 252601, UKRAINE.

A REVIEW OF EUROPEAN CHALCIDOIDEA (HYMENOPTERA) PARASITIZING THE EGGS OF AQUATIC INSECTS.

The Chalcid egg-parasitoids of aquatic insects in Europe are reviewed. At present 2 species of Trichogrammatidae, 5 species of Mymaridae and 9 species of Eulophidae have been recorded in this group - Prestwichia aquatica Lubb., P. solitaria Rusch., Anagrus incarnatus Hal., Caraphractus cinctus Walk., Patasson leptoceras Debauche, Litus cynipseus Hal., Anaphoidea conotrachelli Gir., Mestocharis maculata Forst., M. bimacularis Dalm., Aprostocetus natans Kost. et Furs., A. rimskykorsakovi Kost. et Furs., A. zerovae Kost. et Furs., A. citripes (Thomson), A. pantschenkoi Kost., A. pseudopodiellus Bakk. and A. rufus Bakk. The development of aquatic Chalcidoidea has been observed in the eggs of water-beetles (Coleoptera, Dytiscidae: Dytiscus L., Cybister Curt., Agabus Leach, Acilius Leach, Ilibius Er., Noterus Clairv., Colymbetes Clairv., Graphoderus Dej., Hygrobiidae: Hygrobia Latr.), water bugs (Hemiptera: Notonecta L., Naucoris F., Ranatra F., Aphelocheirus Westw., Gydrometra Latr., Nepa L.), dragonflies (Odonata: Aeshna F., Lestes Leach, Calopteryx Leach, Coenagrion Kirby). The aquatic plants which are mostly attractive for the hosts' oviposition and their parasitoids have been established (Alisma plantago L., Sagittaria sagittifolia L., Calla palustris L., Nymphaea L., Nuphar L., Potamogeton L., Hydrocharis L., Stratiotes L., Hippuris L., Juncus L.). The ability to swim under the water by means of its legs (Prestwichia Lubb., Patasson Walk.) and wings (Aprostocetus Westw., Caraphractus Walk.) have been observed.

Introduction.

Three families of chalcid wasps (Trichogrammatidae, Mymaridae, Eulophidae) are known as egg-parasitoids of many aquatic insects. The parasitoids follow their hosts into the water. The larvae and pupae of these Chalcidoidea live, strictly speaking, inside the egg of the hosts, and only the adults can live in the water. In the literature, these chalcid wasps are called aquatic chalcids or aquatic wasps. Actually, they are amphibiotic organisms because the adults can live directly in the water, run on the water surface and fly in the air. Some species (Prestwichia aquatica Lubb., P. solitaria Rusch.) are better adapted to the aquatic habitat of life and quickly die out of the water in the open air, but others (Mestocharis bimacularis Dalm.) live in the air for a long time. Some aquatic chalcids have the unique capability to swim under the water by means of their legs (Prestwichia Lubb.) and their wings (Caraphractus Walk., Aprostocetus Westw.). Moving in this way in the water or air, aquatic chalcids can successfully find and parasitize the eggs of their insects-hosts.

Material and methods.

Material was collected by the author from 1981 to 1994 in various localities in the European part of Russia (Voronezh, Belgorod, Saint-Petersburg and Krasnodar Kray Districts), the Far East of Russia (Vladivostok), Ukraine (Kiev, Kharkov, Khmelnitskiy, Kherson, Nikolaev, Cherkassy, Poltava Districts and the Crimea), Hungary, Ireland and England.

Collections were made in various aquatic habitats with a range of vegetation. They were mostly shallow, with slow flowing or mainly stagnant water. These included rivers and streams with slow current, large or small water ponds, temporary water-bodies like shallow water ponds, ditches for drainage and little ponds which dry out before the middle or end of the summer.

From a review of the present data and literature (asterisk *), the aquatic Chalcidoidea have been reared from the eggs of different aquatic insects: water-beetles (Coleoptera, Dytiscidae: Dytiscus L., Cybister Curt., Agabus Leach, Acilius Leach, Ilibius Er., Noterus Clairv., Colymbetes Clairv.*, Graphoderus Dej.*, Hygrobiidae: Hygrobia Latr.*), water bugs (Hemiptera: Notonecta L.*, Naucoris F., Ranatra F., Aphelocheirus Westw.*, Hydrometra Latr.*, Nepa L.*), dragonflies (Odonata: Aeshna, Lestes Leach*, Calopteryx Leach*, Coenagrion Kirby).

The most attractive aquatic plants for the hosts' oviposition are the following: Alisma plantago-aquatica L., Sagittaria sagittifolia L., Calla palustris l., Nymphaea L., Nuphar L., Potamogeton L., Hydrocharis L., Stratiotes L., Hippuris L., Juncus L.. The most productive plants for collecting from were Alisma L., Sagittaria L., Nuphar L., Nymphaea L. since they are common, very visible and most suitable.

The water bugs, water beetles and dragonflies frequently lay their eggs in the outer leaf stalks of Alisma and Sagittaria submerged under the water. In this position the eggs have the best conditions for development surrounded by air and moisture in the hollows of air-filled leaf stalks. The eggs are completely hidden but that affords no protection against egg-parasitoids. The females of aguatic chalcids have no difficulty in parasitizing the hosts' eggs laid in aquatic plants. They insert their ovipositors through the leaf tissue into the eggs beneath, or lay directly into the eggs at the side of the leaf scar.

The presence of the host eggs can be recognized by gashes and scars in the plant tissue which are making by the ovipositor of the host females when inserting the eggs.

The form, size and position of eggs in the tissue of the aquatic plants are specific and can be used for the identification of various species of water insects.

The injuries of the aquatic plants (scars, gashes, holes) made by the host females may be successfully used for finding the hidden eggs of aquatic insects. The females of Dytiscus L. make a long longitudional scar in the plant tissue of Alisma and insert their eggs inside. The eggs of Cybister Curt. and Acilius Leach. Are placed in groups on both sides of special gashes or holes in the plant tissue. The egg of Agabus Leach are laid separately in the plant tissue, and usually a small tongue of leaf tissue projects over the hole. The eggs of large dragonflies (Aeshna F.) are inserted in the plant tissue in a visible group, and frequently small apices of eggs project from the surface of a plant.

The eggs of aquatic insects-hosts were collected in the leaves and leaf stalks of various aquatic plants with different positions in the water and on the bottom. The plants were either submerged partially or completely under the water (Sagittaria L.), or growing over the water surface (Alisma L.), or floating on the water (Nuphar L.). Aquatic chalcids successfully find and parasitize the eggs of aquatic insects in the tissue of aquatic plants either submerged under the surface (Prestwichia Lubb.) or in the leaf stalks that appear over the surface of water (Mestocharis Forst.).

The parasitized eggs inserted in the plant tissue were kept in small glass tubes (size 15 mm x 40 mm) with a part of the leaf stalk and water. Some host eggs were separated from the plant tissue and simply kept under the water in the tubes. It was better to save the eggs of Dytiscidae and Odonata, parasitized by Eulophidae, with a small part of plant stalk in the tube. Such eggs were dark-brown, non-transparent and very with a fragile chorion. The eggs, parasitized by Trichogrammatidae and Mymaridae, were separated using pins from the plant tissue and submerged under the water in the tube. The chorion of such hosts' eggs remained transparent and the contents became bright yellow or white. The development of the larvae of the parasitoids was visible inside these eggs.

The non-parasitized newly laid eggs of water beetles and water bugs are transparent, usually cream-white and later grey segments of the larva are visible.

Results and discussion.

According to the present data and a literature review, 2 species of Trichogrammatidae, 5 species of Mymaridae and 9 species of Eulophidae have been recorded in the complex of aquatic chalcids viz. Prestwichia aquatica Lubb., P. solitaria Rusch., Anagrus incarnatus Hal., Caraphractus cinctus Walk., Patasson leptoceras Debauche, Litus cynipseus Hal., Anaphoidea conotrachelli Gir., Mestocharis maculata Forst., M. bimacularis Dalm., Aprostocetus natans Kost. et Furs., A. rimskykorsakovi Kost. et Furs., A. zerovae Kost. et Furs., A. citripes (Thomson), A. pantschenkoi Kost., A. pseudopodiellus Bakk. and A. rufus Bakk.

Trophic specializations were studied by the author and are shown in Table 1. The data from the literature are given in Table 2.

It was recorded that egg-parasitoids of water beetles develop in the eggs of different species during the annual season. In May-June the first generation of chalcids (Prestwichia Lubb., Patasson Walk., Mestocharis Forst., Aprostocetus Westw.) parasitizing the large eggs of Dytiscus L. and Cybister Curt.. The second, third and forth generations of these parasitoids appear in June-July, August and September approximately and develop in the small eggs of the water beetles (Agabus Leach, Acilius Leach, Ilibius Er., Noterus Clairv., etc.). Later the parasitoids in the stage of prepupa and pupa hibernate inside the eggs of their hosts under the water. In the Ukraine 4 generation of Prestwichia aquatica Lubb., 3 - Caraphractus cinctus Walk., 3-4 – Mestocharis bimacularis Dalm. were recorded. The size and number of individuals depend upon the size of the host's eggs. From a single egg of Dytiscus L., 178 individuals of P.aquatica Lubb. (usually 10-20), or 104 individuals of C.cinctus Walk. (commonly 25-35), or up 44 individuals of M. bimacularis Dalm. (usually 8-9) were reared. From one egg of Acilius Leach up to 45 individuals of P. aquatica Lubb. (usually 7-8) and up to 13 from one egg of Agabus (usually 4-5) were reared. The development of 2-6 individuals of C.cinctus in one egg of Agabus Leach, 3 individuals of M. bimacularis Dalm. in one egg of Acilius Leach was recorded.

Rimsky-Korsakov (1916) and Jackson (1956) observed that in P. aquatica Lubb. and C. cinctus Walk. arrhenotokous parthenogenesis occurs as in most parasitic Hymenoptera where unmated female will produce only male progeny and mated female can deposit both fertilized and unfertilized eggs.

Jackson (1956, 1959) observed that in C. cinctus Walk. the wing size usually varied in accordance with the size of insect and intermediates occured between the large specimens with long wings and the small specimens with short wings. There are often micropterous individuals of C. cinctus Walk. in the cases of superparasitization. Rimsky-Korsakov (1920) indicated two races of P. aquatica Lubb.: fully winged (macropterous females) and short winged (brachypterous females). He mentioned that these two forms did not integrate. But we have found intermediate forms of winged females with partially reduced ciliation of wings.

It was noted that the parasitoids lay their eggs in the host eggs of all stages of their development, but later stages are less attractive for the parasitoids. Parasitoids usually reject the host eggs that are already parasitized. According to Ivanova-Kazas (1950), twofold and multifold parasitizations often happen. Rimsky-Korsakov (1916, 1931) recorded that it is possible to find several larvae of P. aquatica Lubb. on different stages of development in a single host egg. In some cases of twofold parasitization there are two distinctive and separate age groups of larvae without intermediate stages.

Cases of combined parasitization were also observed. The larvae of P. aquatica Lubb. may be found simultaneously with larvae of C. cinctus walk. and M. bimacularis Dalm. inside one host egg. The larvae of P. aquatica Lubb. are sack-formed and successfully develop together with larvae of C. cinctus Walk.. The gregarous larvae of P. aquatica Lubb. and C. cinctus Walk. do not attack each other. The larvae of Mestocharis Forst. have sharp mandibules and may actively kill other larvae of parasitoids including those of the same species. Occasional superparasitism was observed when a female of P. aquatica Lubb. laid its eggs inside the later stages of larvae of C. cinctus (Rimsky-Korsakov, 1920, 1931, Ivanova-Kazas, 1950).

The ability to swim under the water is specific for P. aquatica Lubb. and C. cinctus Walk.. The females and males of P. aquatica dive beneath the water surface and swim by means of rapid movement of their legs and keep their wings folded over the back of body. The imago of C. cinctus Walk. swims by use of their wings, intensively paddling under the water. The swimming of Aprostocetus natans Kost. et Furs. under the water was first described by the author ( Fursov and Kostyukov, 1987).

C. cinctus can also quicky move on the water's surface and fly freely in the air. The females of P. aquatica Lubb. are poor fliers, but can still jump and open the wings. According to Rimsky-Korsakov (1916) and Jackson (1961), the mating of the adults of P. aquatica Lubb. and C. cinctus Walk. has been observed within a submerged host eggs. The imago of P. aquatica Lubb. can remain under the water up to five days (Heymons, 1909). Such species as P. leptoceras Debauche and A. incarnatus Hal. can not swim but only slowly move under the water with opened wings. M. bimacularis Dalm. and M. maculata Forst. do not like to go under the water and do not swim (Jackson, 1958, 1964). Usually these species prefer to parasitize the eggs of Dytiscidae in the plant tissue over the water.

L I T E R A T U R E

Bakkendorf O. Biological investigations on some Danish hymenopterous egg-parasites especially in Homopterous and Heteropterous eggs, with taxonomic remarks and descriptions of new species // Ent.Medd. - 1934. - Vol.19. - P.1-134.

Bakkendorf O. Description of three species of Tetrastichus Haliday (MicroHym.) with a host list // Ent.Medd. - 1953. - Vol.26,N 7. - P.549-576.

Boucek Z., M.W.R.de Graham, Kerrich G.J. A revision of the European species of the genus Mestocharis Forster (Hymenoptera, Chalcidoidea, Eulophidae) // Entomologist. - 1963. - Vol.96. - P.4-9.

Brocher F. Observations biologiques sur quelques Dipteres et Hymenopteres dits "aquatiques" // Ann.Biol.Lacustre. - 1910. - Vol.4. - P.170-186.

Enock F. Notes on aquatic Hymenoptera and rediscovery of Prestwichia aquatica (Lubbock) // Journ.Quekett Mic.Club. - 1896. - Vol.6,N 2. - P.275-277.

Enock F. // Ent.Mon.Mag. - 1899. - Vol.35,N 10. - P.167-168.

Fursov V.N., Kostyukov V.V. New species of the genus Tetrastichus (Hymenopera, Eulophidae), egg-parasites of damselflies and dragonflies and of predaceous diving beetles. Zoologicheskii Zhurnal, 1987, N 2, p.217-228.

Graham M.W.R de V. A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. - Bull.Brit.Mus.(Nat.Hist.). - 1987.- Vol.55(1). - P.1-392.

Graham M.W.R. de V., J.LaSalle New synonymy in European Tetrastichinae (Hymenoptera: Eulophidae) including designation of some neotypes, lectotypes and new combinations. - Entomologist's Gazette. - 1991. - Vol.42. - P.89-96.

Henriksen K.L. De europaeiske vandsnyltehvepse og deres Biologi (The aquatic Hymenoptera of Europe and their biology) // Ent.Medd. - 1919. - Bd.12, Hf.2. - S.137-251.

Henriksen K. Notes upon some aquatic Hymenoptera // Ann.Biol.Lacustre. - 1922. - Vol.11.- P.11-37.

Heymons R., Heymons H. Hymenoptera. In: Brauer A. (Ed.) Die susswasserfauna Deutschland - 1909. - Hf.7. - P.27-36.

Hinks W.D. Some additions to the British Mymaridae (Hym., Chalcidoidea) // Ent.Month.Mag. - 1959. - Vol.95. - P.210-216.

Ivanova-Kazas O.M. Adaptations to parasitism in embryonal development of Prestwichia aquatica // Zoologicheskij Zhurnal. - 1950. - Vol.29, Ser.6. - P.530-544.

Jackson D.J. Notes on Hymenopterous parasitoids bred from the eggs of Dytiscidae in Fife // J.Soc.Brit.Entomol. - 1956. - Vol.5, Pt.5. - P.144-149.

Jackson D.J. A further note on a Chrysocharis (Hymenoptera, Eulophidae) parasitizing the eggs of Dytiscus marginalis L., and a comparison of its larva with that of Caraphractus cinctus Walk. (Hym., Mymaridae) // J.Soc.Brit.Entomol. - 1958. - Vol.6. - P.15-22.

Jackson D.J. Observations on three gynandromorphs of Caraphractus cinctus Walker (Hym., Mymaridae), and notes on antennal variation in this species // Entomol.Month.Mag. - 1959. - Vol.95, N 1144. - P.198-203.

Jackson D.J. Observations on the biology of Caraphractus cinctus Walker (Hymenoptera, Mymaridae), a parasitoid of the eggs of Dytiscidae. II. Immature stages and seasonal history with a review of mymarid larvae // Parasitology. - 1961. - Vol.51. - P.269-294.

Jackson D.J. Observations on the life-history of Mestocharis bimacularis (Dalman) (Hym., Eulophidae), a parasitoid of the eggs of Dytiscidae // Opusc.Ent. - 1964. - Vol.29. - P.81-97.

Matheson R., Crosby C.R. Aquatic Hymenoptera in America // Ann.Ent.Soc.Amer. - 1912. - Vol.5. - P.65-71.

Rimsky-Korsakov M.N. Biological observations on aquatic Hymenoptera // Russ.Entomol.Review. - 1916. - Vol.16, N3-4. - P.209-225.

Rimsky-Korsakov M.N. Observations on variation and heredity of parasitic wasps // Proceedings of Petrograd Society of Natur.History / Trudy Petrogradskogo Obzhestva Estestvoispytatelej. - 1920. - Vol.51, Ser.1, N 5-6. - P.89-111.

Rimsky-Korsakov M.N. Methoden zur untersuchung von wasserhymenopteren // Handbuch der biologischen Arbeitsmethoden. - Berlin, Wien, Urban, Schwarzenberg, 1931. - Bd.7, Hf.1. - S.227-258.

TABLE 1.

LIST OF EUROPEAN CHALCIDOIDEA, PARASITIZING IN THE EGGS OF AQUATIC INSECTS.

Parasitoid

Hosts

Literature

Order

Genus/Species

Prestwichia aquatica Lubb.

Hemiptera

Coleoptera

Ranatra linearis L.

Nepa L., Notonecta L., Apheloheirus Westw.

Dytiscus L., Cybister Curt.,

Acilius Leach,

Agabus Leach

Colymbetes Clairv.

Hygrobia Latr.

Heymons, 1909

Rimsky-Korsakov, 1931

Rimsky-Korsakov, 1916

Enock, 1899

Enock, 1896

P. solitaria Rusch.

Coleoptera

Odonata

Graphoderus Dej.,

Agabus Leach

Aeshna F.,

Lestes Leach

Erythromma najas Hans.

Henriksen, 1919

Rimsky-Korsakov, 1916

Henriksen, 1919

Caraphractus cinctus Walk.

Coleoptera

Hemiptera

Ilibius Er.,

Dytiscus L.

Acilius Leach, Graphoderus

bilineatus Degeer

Ilibius ater Degeer,

I. fuliginosus F.,

Hydroporus planus F., Agabus bipustulatus Gyllenh.,

A. labiatus Brahm.,

A. sturmii Gyllenh.,

A. nebulosus Forst.,

A. chalconatus Panz.,

D. semisulcatus Mull.

Notonecta glauca L.

Rimsky-Korsakov, 1920

Ivanova-Kazas, 1950

Jackson, 1958

Matheson, Crosby, 1912

Anagrus incarnatus Hal.

Odonata

Coenagrion Kirby,

Lestes Leach,

Calopteryx virgo L.

Erythromma Charp.

Agrion pulchellum Lind.

Rimsky-Korsakov, 1916

Rimsky-Korsakov, 1931

Henriksen, 1922

Patasson leptoceras

Debauche

Coleoptera

Ilibius fuliginosus F.

Hinks, 1959

Litus

cynipseus Hal.

Hemiptera

Hydrometra Latr.

Brocher, 1910

Anaphoidea

conotrachelli Gir.

Coleoptera

Agabus Leach

Bakkendorf, 1934

Aprostocetus

pseudopodiellus

Bakk.

Odonata

Lestes Leach

Bakkendorf, 1953

A. rimsky-korsakovi

Kost. et Furs.

Odonata

Aeshnidae

Fursov, Kostyukov, 1987

A. rufus Bakk.

Coleoptera

Dytiscus L.

Bakkendorf, 1953

A. citripes

(Thoms.)

Coleoptera

Agabus Leach, Ilibius Er.

Fursov, Kostyukov, 1987

A. zerovae

Kost. et Furs.

Coleoptera

Aeshnidae

Fursov, Kostyukov, 1987

A. natans

Kost. et Furs.

Coleoptera

Agabus Leach,

Ilibius Er.

Fursov, Kostyukov, 1987

A. pantschenkoi

Kost.

Coleoptera

Dytiscus L.,

Agabus Leach,

Cybister Curt.,

Acilius Leach

Fursov, Kostyukov, 1987

Mestocharis

bimacularis Dalm.

Coleoptera

D.marginalis L.,

D.circumflexus F.,

D.semisulcatus Mull.,

Graphoderus Dej.,

Acilius Leach,

Agabus Leach

Jackson, 1964

Ivanova-Kazas, 1961

M. maculata

Forst.

Coleoptera

Dytiscus sp.

Boucek et al., 1963

TABLE 2.

TROPHIC CONNECTIONS OF AQUATIC CHALCIDOIDEA, PARASITIZING

IN THE EGGS OF AQUATIC INSECTS IN UKRAINE AND RUSSIA.

PARASITE TAXA HOST TAXA

1 - Dytiscus L. 6 - Noterus Clairv.

2 - Cybister Curt. 7 - Naucoris F.

3 - Acilius Leach 8 - Ranatra F.

4 - Agabus Leach 9 - Aeshna F.

5 - Ilibius Er. 10 - Coenagrion Kirb

Parasitoid	Hosts
Parasitoid	1	2	3	4	5	6	7	8	9	10
Prestwichia aquatic Lubb.	X	X	X	X	X	X	X	X
P. solitaria Rusch.				X					X	X
Caraphractus cinctus Walk.	X			X	X
Anagrus incarnatus Hal.										X
Patasson leptoceras Debauche				X	X
Aprostocetus rimskykorsakovi Kost. et Furs.									X
A. citripes (Thomson)				X	X
A. zerovae Kost. et Furs.									X
A. pantschenkoi Kost.	X	X		X	X
A. natans Kost. et Furs.				X	X
Mestocharis bimacularis Dalm.	X	X	X	X	X
M. maculata Forst.			X	X

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