Latvijas Entomologs, 2004, 41: 93-99. 93

The (Diptera) Feeding Particularities on Some Genera of

SAULIUS PAKALNIŠKIS

Institute of Ecology, Vilnius University, Akademijos 2, LT–08412, Vilnius, Lithuania; e–mail: [email protected]

PAKALNIŠKIS S. 2004. THE AGROMYZIDAE (DIPTERA) FEEDING PARTICULARITIES ON SOME GENERA OF RANUNCULACEAE. – Latv. entomol., 41: 93-99.

Abstract: There were the life stories of 47 Agromyzidae (Diptera) species on 11 genera of ranunculaceous plants studied, including their host specialization, feeding character and localization of mine as well as pupation particularities. The agromyzid larvae colonizing the assimilative, generative as well as support organs of certain host–plant show a high level of specialization. On the other hand, almost all the mining types may be characteristic to one species (e.g. clematidis on Ranunculus lingua). Further bionomic data on several poorly known species are provided in this report for the first time. Also some possible micro-evolutionary ways of the feeding behaviour are discussed in present paper.

Key words: Agromyzidae, Ranunculaceae, bionomics, feeding behaviour, Lithuania.

Introduction Ranunculaceae and form there rather all types of mines, represent in even narrow geographical The ranunculaceous plants form an old, rich areas. This species complex is a good model for in species as well as unique family of studies on evolution of the host specialization and Magnoliophyta, widespread in temperate to arctic larval feeding behaviour. This paper provides new areas over the Holarctic and partially in temperate biological data on some poorly known species areas of southern hemisphere. Because of the and discusses on particularities of feeding particular chemical stuffs there are almost no specialization. polyphagous Agromyzidae on Ranunculaceae. There are predominantly (more than 100) representatives of Phytomyza genus feeding on Methods Ranunculaceae. Some of them demonstrate certainly distinctive morphological characters and Author in Lithuania and contiguous were placed in the Napomyza up to 1994. Many districts of neighbouring countries collected early species groups of Phytomyza are represented on stages of Agromyzidae between 1980 and 2003, Ranunculaceae and species group limits are here with the consequent imago rearing in laboratory. almost invisible. These groups are descended on Material is deposited in the Institute of Ecology, this plant family more probably than reverberate a Vilnius. result of several colonisations. Thus K.A. Spencer The species are laid out in the list below, (1990) considered that Agromyzidae are on taking into account their morphological Ranunculaceae primary, not secondary, and that resemblance. The six species with note of means they are ‘inherited’. This proposition, interrogation marked need a formal confirmation being correct generally, cannot be aimed at all by rearing of imagines or even imago males (in Agromyzidae though. case of P. platonoffi). The agromyzid larvae (and Phytomyza particularly) attack all the plant–organs of 94 The Agromyzidae (Diptera) Feeding Particularities on Some Genera of Ranunculaceae

Results Ranunculoideae: Ranunculeae. Upper–surface leaf mines in , R. lanuginosus There were 47 species of Agromyzidae and R. polyanthemos. Larva leaves the mine found feeding on 11 genera of Ranunculaceae through a lover leaf surface, pupation takes place during the investigation. These phytophagoes host in the opening, and the yellowish puparium specialization range varies here between the remains hung in the opening or falls down. monophagy and oligophagy and does not overstep Phytomyza linguae Lundquist, 1947 a plant genus limits mostly. Only 3 species Ranunculoideae: Ranunculeae. Upper–surface colonise plants of 2–3 relate genera, three species leaf mines in Ranunculus lingua. Larva leaves the feed on 2 most relate genera of different plant mine through an upper leaf surface, pupation tribes (Isopyreae and Thalictreae). But Phytomyza takes place on the leaf blade, puparium is black clematidis colonize only selective plant species, and stuck to the leaf in some centimetres from the which represent 2 genera of different tribes opening away. (Anemoneae and Ranunculeae), choosing even Not a synonym of P. ranunculivora (cf. different organs of each host. And Phytomyza Pakalniškis, 1996b). actaeae can feed on selective plant species of 2 Phytomyza pulsatillicola Hering, 1962 genera from different subfamilies (Helleboroideae Ranunculoideae: Anemoneae. Upper–surface leaf and Ranunculoideae). mines in Pulsatilla patens and P. pratensis. Larva Two last phenomena are most interesting leaves the mine through an upper leaf surface, since analysing the evolution of feeding pupating in the ground. behaviour and host specialization in Agromyzidae Phytomyza anemonantheae Spencer, 1969 and may be considered to be a kind of ‘selective Ranunculoideae: Anemoneae. Upper–surface leaf oligophagy’ rather confirmable with the mines in Anemone sylvestris. Pupation takes place xenophagy (cf. Spencer 1999). inside. Phytomyza ? aconiti Hendel, 1920 Helleboroideae: Delphineae. Upper–surface leaf List of species mines in Aconitum napellus. Several larvae feed together, leaving the mine through an upper leaf surface and pupating in the ground. The species Phytomyza ? albimargo Hering, 1925 can feed on Delphinium spp. as well (Spencer, Ranunculoideae: Anemoneae. Upper–surface leaf 1996, 1999). mines in Anemone nemorosa. Larva leaves the Lithuania: Šilainiai, 54º56'N, 23º52'E, mines and mine through an upper leaf surface, pupating in puparia collected only. An introduced species, the ground. doubtless. Lithuania: Spalviškiai environs, 56º16'N, 24º58'E, Phytomyza aconitophila Hendel, 1927 mines and puparia collected only. Helleboroideae: Delphineae. Upper–surface leaf Phytomyza pulsatillae Hering, 1924 mines in Aconitum septentrionale. Larva leaves Ranunculoideae: Anemoneae. Upper–surface leaf the mine through an upper leaf surface, pupating mines in Pulsatilla patens and P. pratensis. Larva in the ground. Introduced species. leaves the mine through an upper leaf surface, Phytomyza actaeae Hendel, 1922 pupating in the ground. Helleboroideae: Cimicifugeae. Upper–surface leaf Phytomyza hendeli Hering, 1923 mines in Actaea spicata. Pupation takes place Ranunculoideae: Anemoneae. Upper–surface leaf internally. M. Beiger recorded (1980) in Poland mines in Anemone nemorosa. Larva leaves the Clematis alpina (Ranunculoideae: Anemoneae) to mine through an upper leaf surface, pupating in be next host plant. the ground. Phytomyza rydeni Hering, 1934 Phytomyza ranunculivora Hering, 1934 Ranunculoideae: Ranunculeae. Upper–surface Latvijas Entomologs, 2004, 41: 93-99. 95 leaf mines in Ranunculus acris. Some larvae are Helleboroideae: Trollieae. Upper–surface leaf feeding together usually, and pupation takes place mines in Caltha palustris. Larva leaves the mine in the mine. through a lower leaf surface, puparium remains Phytomyza trollii Hering, 1930Helleboroideae: hung in the opening. Trollieae. Upper–surface leaf mines in Trollius Lithuania: Marcinkonys environs, 54º05'N, europaeus. Larva leaves the mine through an 24º27'E, mines and puparia collected only. upper leaf surface, pupating in the ground. Phytomyza ?soenderupi Hering, 1941 Phytomyza ignota Pakalniškis, 1994 Helleboroideae: Trollieae, Internal petiole mines Ranunculoideae: Anemoneae. Upper–surface leaf in Caltha palustris, sometimes (if some larvae are mines in Pulsatilla pratensis. Pupation takes feeding together) appearing in the surface place inside (under the upper epidermis) or rarely irregularly and even in basal part of leaf blade larva leaves the mine through an upper leaf (just as P. stolonigena), pupation takes place surface, pupating in the ground. inside. Phytomyza ? kaltenbachi Hendel, 1922 Latvia: Rucava environs, 56º10'N, 21º08'E, Ranunculoideae: Anemoneae. Upper–surface leaf puparia collected 28.08.2003, 2 females and 3 males mines in Clematis vitalba and relate spp. Larva emerged. leaves the mine through an upper leaf surface, Phytomyza socia Brischke, 1881 pupating in the ground. Ranunculoideae: Anemoneae. Upper–surface leaf Lithuania: Kryžiokai, 54º48'N, 25º21'E; Merkinė, mines in Hepatica nobilis and Pulsatilla 54º10'N, 24º11'E; Šilainiai, 54º56'N, 23º52'E; pratensis. Larva leaves the mine through an upper Tamošava, 54º36'N, 24º34'E. Mines and puparia leaf surface, pupating in the ground. collected only. An introduced species, doubtless. Phytomyza abdominalis Zetterstedt, 1848 Phytomyza palionisi Pakalniškis, 1998 Ranunculoideae: Anemoneae. Upper–surface Ranunculoideae: Ranunculeae. Upper–surface mines in over-wintered leaves of Hepatica leaf mines in Ranunculus cassubicus. Pupation nobilis. Larva leaves the mine through an upper takes place inside, under the lower epidermis. leaf surface, pupating in the ground. Phytomyza anemones Hering, 1925 Phytomyza ranunculicola Hering, 1949 Ranunculoideae: Anemoneae. Upper–surface leaf Ranunculoideae: Ranunculeae. Upper–surface mines in Anemone nemorosa. Pupation takes leaf mines in Ranunculus acris and R. bulbosus. place inside, under the upper epidermis. Pupation takes place inside, under the upper Phytomyza fallaciosa Brischke, 1881 epidermis. Ranunculoideae: Ranunculeae. Upper–surface Phytomyza albifrons Groschke, 1957 leaf mines in Ranunculus acris, R. lanuginosus Isopyroideae: Thalictreae. Upper–surface leaf and R. lingua, with some larvae feeding together. mines in Thalictrum aquilegifolium. Larva leaves Pupation takes place inside, under the lower the mine through an upper leaf surface, pupating epidermis. in the ground. Phytomyza trolliivora Hering, 1935 Phytomyza thalictricola Hendel, 1925 Helleboroideae: Trollieae. Upper–surface leaf Isopyroideae: Thalictreae. Upper–surface leaf mines in Trollius europaeus. Larva leaves the mines in Thalictrum flavum. Larva leaves the mine through an upper leaf surface, pupating in mine through an upper leaf surface, pupating in the ground. the ground. New to Belarus: Ritshany environs, Phytomyza calthophila Hering, 1931 55º41'N, 26º41'E, 25.06.1985, larvae in T. flavum, Helleboroideae: Trollieae. Upper–surface leaf 2 females emerged. mines in Caltha palustris. Larva leaves the mine Phytomyza aquilegiae Hardy, 1849 through an upper leaf surface, pupating in the Isopyroideae: Isopyreae and Thalictreae. Upper– ground. surface leaf mines in Aquilegia vulgaris, Phytomyza ? calthivora Hendel, 1934 Thalictrum aquilegifolium, T. flavum, T. lucidum 96 The Agromyzidae (Diptera) Feeding Particularities on Some Genera of Ranunculaceae and T. minus. Larva leaves the mine through an and R. lanuginosus, than mines it internally, upper leaf surface, pupating in the ground. pupating in stem hole. Phytomyza subrostrata Frey, 1946 Phytomyza nigritula Zetterstedt, 1838 Helleboroideae: Trollieae. Larvae feed in flower Ranunculoideae: Ranunculeae. Larva forms heads and peduncles of Trollius europaeus as primary surface stem mine in Ranunculus acris, well as mine a stem or petiole internally (cf. R. cassubicus and R. lanuginosus, than mines it Pakalniškis, 1998b), pupating in stem (petiole) internally, pupating in stem hole. hole. Phytomyza notata Meigen, 1830 Phytomyza ? platonoffi Spencer, 1976 Ranunculoideae: Ranunculeae. Upper–surface Helleboroideae: Trollieae. Upper–surface mines leaf mines in Ranunculus repens. Pupation takes in lower parts of stem and petiole of Trollius place in the ground. Also 3 further Ranunculus europaeus. Pupation takes place in the ground. species are known (Spencer, 1976) being hosts of Lithuania: Agailės, 56º06'N, 22º54'E. A male is this species. lacking for confirmation. Phytomyza stolonigena Hering, 1949 Phytomyza soenderupiella Spencer, 1976 Ranunculoideae: Ranunculeae. Upper–surface Ranunculoideae: Anemoneae. Larva feeds in a mines in leaves and petioles of Ranunculus stem of Pulsatilla pratensis, no more lanuginosus and R. repens. No specimens were particularities are known. Only imagines have reared after description. Only mines have been been found in Lithuania (Pakalniškis 1998c). found in Lithuania (Ostrauskas et all., 2003) as Phytomyza clematidis Kaltenbach, 1859 well. Ranunculoideae: Anemoneae and Ranunculeae. Phytomyza ranunculi (Schrank, 1803) The species was described from flower heads and Ranunculoideae: Ranunculeae. Upper–surface peduncles of Clematis vitalba, and further found leaf mines in Ficaria verna (new host plant (Pakalniškis 1995) feeding on Ranunculus acris, established), common on Ranunculus acris, R. R. auricomus, R. lanuginosus and in all over- auricomus, R. bulbosus, R. flammula, R. ground organs of R. lingua. Pupation takes place lanuginosus, R. lingua, R. repens and R. in mine, in stem hole (most usually) or in the sceleratus. Larva leaves the mine through an ground (rarely). upper leaf surface, pupating in the ground. The Phytomyza murina Hendel, 1935 species feeds also on Myosurus occasionally Isopyroideae: Thalictreae. Larva feeds in a seed (Spencer, 1999). capsule of Thalictrum minus, pupating internally, Phytomyza caulinaris Hering, 1949 and P. fennoscandiae Spencer, 1976 is a junior Ranunculoideae: Ranunculeae. Upper–surface synonym of this species very likely (Pakalniškis stem mines in Ranunculus acris. Pupation takes 2000). place in the ground. Phytomyza enigmoides Hering, 1937 Phytomyza jonaitisi Pakalniškis, 1996 Ranunculoideae: Ranunculeae. Larva forms Isopyroideae: Thalictreae. Internal mines in primary surface stems mine in Ranunculus petiole of Thalictrum aquilegifolium. Pupation cassubicus, than mines it internally, pupating in takes place in the stem hole (Pakalniškis, 1998b). stem hole (Pakalniškis, 1998b). Phytomyza minuscula Goureau, 1851 Phytomyza albipennis Fallén, 1823 Isopyroideae: Isopyreae and Thalictreae. Upper– Ranunculoideae: Ranunculeae. The first host surface leaf mines in Aquilegia vulgaris, plant established. Larva forms primary surface Thalictrum aquilegifolium, T. flavum, T. lucidum stem mine in Ranunculus acris, than mines it and T. minus. Larva leaves the mine through an internally, pupating in stem hole. upper leaf surface, pupating in the ground. Phytomyza evanescens Hendel, 1920 subapproximata (Sasakawa, 1955) Ranunculoideae: Ranunculeae. Larva forms Isopyroideae: Thalictreae. Internal stem mines in primary surface stem mine in Ranunculus acris Thalictrum flavum, T. lucidum and T. minus. Latvijas Entomologs, 2004, 41: 93-99. 97

Pupation takes place in stem hole (Pakalniškis, species of genus with known biology are leaf 1998b). miners on Asteraceae predominantly. The phylogeny of genus stays indefinite. Agromyzinae Majority of species groups of Ophiomyia have Ophiomyia ranunculicaulis Hering, 1949 representatives on Fabaceae, also species most Ranunculoideae: Ranunculeae. Upper–surface resembling other genera are known there. That stem mines in Ranunculus acris and R. shows a later origin of this ‘supergenus’, thus lanuginosus. Pupation takes place in mine, under Ophiomyia miners are secondary on epidermis. Ranunculaceae, and no pair of species is truly Ophiomyia aquilegiana Lundquist, 1947 monophyletic here. Isopyroideae: Isopyreae and Thalictreae. Upper– Inside the rather archaic Magnoliopsida class only surface stem mines in Aquilegia vulgaris, Ranunculidae (and Ranunculaceae namely) are Thalictrum aquilegifolium, T. flavum and T. colonised by numerous Phytomyza species. There minus. Several petiole mines were detected, too. are known by one Phytomyza species feeding on Pupation takes place in mine, under epidermis. relate subclasses Magnoliidae and Ophiomyia definita Spencer, 1971 Hamamellididae, and no species on most relate Isopyroideae: Thalictreae. The first host plant Caryophyllidae (cf. Spencer, 1999). established. Larvae form inconspicuous surface Thus the only probable candidates to be primary stem mines in the finest upper branches of Ranunculaceae miners are Phytomyza species (no Thalictrum minus, pupating in mine, under Napomyza feed on this family plants). Trying to epidermis. Puparium is pale brown to shiny– reconstruct a phylogeny of feeding behaviour of black¸ with 4 (rarely 3 to 7) bulbs on each these species, such tendencies or stages manifest posterior spiracle. O. sueciae Spencer, 1976 is a them self: junior synonym of this species (Scheirs et all., 1) larva mines the leaf blade pupating in the 2000).New to Lithuania: Gerdašiai, 53°58'N, ground (as a rule) or internally (P. 23°53'E, puparia collected 05.08.1997, and 1 male anemonantheae, P. actaeae, P. anemones, P. emerged; puparia 18.05.1998, 1 female emerged; clematidis (in a leaf of Ranunculus lingua), P. puparia 20–28.08.1998, 3 females and 3 males fallaciosa, P. ignota (occasionally), P. palionisi, emerged. Kalviai, 55°05'N, 23°21'E, 1 male swept P. ranunculicola, P. rydeni); 28.05.1992; puparia 20.06.1999, 1 female 2) puparium has posterior spiracles widely emerged. Merkinė, 54°10'N, 24°11'E, puparia protuberant and stays to hang in the exit hole (P. 04.04.1999, 1 male emerged. Ražiškiai, 54°48'N, ranunculivora), that is characteristic for some non 23°54'E, puparia 28.06.1999, 1 female and 1 male related species of aquatic environment (Spencer, emerged. 1990); another way is to adhere puparium to the Ophiomyia ivinskisi Pakalniškis, 1996 leaf blade as it does P. linguae; Isopyroideae: Thalictreae. Upper–surface stem 3) larva mines the leaf blade and petiole (leaf– mines in Thalictrum flavum, T. lucidum T. minus, stalk) like P. stolonigena; usually hidden under a leaf stalk base. Pupation 4) larva mines the petiole internally, pupating takes place in mine, under epidermis. therewith (P. subrostrata) or in the stem hole (P. jonaitisi); 5) larva mines the stem surface, pupating in the Discussion ground (P. caulinaris); 6) larva forms up to 10 cm long linear, down Calycomyza subapproximata represents a poorly stretching surface mine in the upper part of stem, investigated species group characteristic by which usually has a spiral shape, later mines the darker coloration and was confirmed (Pakalniškis, stem internally and pupates therewith (P. 1998b) to mine stems internally, whereas the rest albipennis, P. enigmoides, P. evanescens, P. 98 The Agromyzidae (Diptera) Feeding Particularities on Some Genera of Ranunculaceae nigritula); consequently (P. stolonigena) or stems only (P. 7) larva eats the seed–buds (P. murina, P. caulinaris). subrostrata) and later mines peduncle (flower- Closely related species feed on comparatively stalk) and a part of stem internally (P. clematidis, remote hosts or different plant organs often. Any P. subrostrata). competition for food resources is practically The stem mining in Phytomyza on Ranunculaceae unlikely possible among the leaf miners; it comes is secondary most probably, because the oldest out through the highest trophic chain – the forms of this family, very scantly represent in parasitoids (Jonaitis, Pakalniškis, tropics, are shrubs and lianas, and the leaf–blade, 2000). A change of host plant usually means an leaf–midrib or petiole mining could be modified accidental change of biotope and some possibility to the stem–rind mining and to the internal stem– to escape the specific parasitoids. Some effect pith mining consequently in further herbaceous also cold result a cardinal change of the feeding forms only. behaviour on the same host plant. The feeding behaviour of many Phytomyza species is definite, but P. subrostrata can mine generative organs as well as petiole and stem References internally (Pakalniškis, 2000). P. clematidis feeds in flower–buds, blossoms and mines internally the Beiger M. 1980. Studies on mining of the stem of Clematis vitalba (cf. Kaltenbach, 1859), Tatry National Park. 11. Materials Ranunculus acris, R. lanuginosus and R. lingua concerning the morphology, and (cf. Pakalniškis, 1995). On the next host it mines systematics of some Phytomyza Fallén leaf blades as well. If larva finds the leaf axle in species (Diptera, Agromyzidae). – Bull. its way, it moves along the petiole internally to Soc. Amis Sci. et lettres Poznań. Ser. D, 20: reach a bud. 135–143. Some competition exists among the blossom Hering E.M. 1949. Neue palaearktische miners, and species colonize different plants. So Agromyziden. – Notul. ent., 29: 18–32. Phytomyza murina is closely relate to further Jonaitis V., Pakalniškis S. 2000. Long–term European species confirmed to feed (Rougemont, dynamics of biocenotic relations of insects. 1912; Hering, 1949) within the blossoms and seed In: Jonaitis V. (ed.) The Inter– capsules of Anemone (P. franzi Hering, 1944), Ecosystematic Relationships of Insects and Aquilegia (P. krygeri Hering, 1949) and Their Dynamics. Institute of Ecology. Thalictrum aquilegifolium (P. thalictri Escher– Vilnius: 227–238. Kündig in Rougemont, 1912). Kaltenbach J.H. 1859. Die deutschen Hosts of four further relate species are as follows: Phytophagen aus der Klasse der Insecten Ranunculus acris (Phytomyza albipennis, P. (C). – Verh. natur. Ver. preuss. Rheinl., 16: evanescens), R. cassubicus (P. enigmoides), R. 216–299. lanuginosus (P. evanescens). But P. nigritula was Ostrauskas H., Pakalniškis S., Taluntytė L. 2003. found in stems of all three Ranunculus species. The species composition of plant mining The Ophiomyia species mine different parts of dipterans (Insecta: Diptera) of greenhouse stem of Thalictrum minus. Blossom mines of O. surroundings in Lithuania. Ekologija, 3: 3- ivinskisi are findable in the lower parts, O. 11. aquilegiana mines the upper part (and leaf stalks Pakalniškis S. 1994. The Lithuanian occasionally), and larvae of O. definita mine the Agromyzidae (Diptera). Descriptions of 6 thinnest branches. new species and other notes. – Acta The species of the same Phytomyza ranunculi entomologica Lituanica, 12: 5–34. species group mine leaves of Ranunculus spp. (P. Pakalniškis S. 1995. Addition to the fauna list of notata, P. ranunculi), leaves and petioles Lithuanian Agromyzidae (Diptera). - In: Latvijas Entomologs, 2004, 41: 93-99. 99

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Received: October 31, 2003.