Distribution and biology of Phytomyza orobanchia (Kaltenbach, 1864) (Diptera, Agromyzidae) in Slovakia

Abstract

Phytomyza orobanchia Kaltenbach, 1964, a leaf miner fly of Orobanche spp. and Phelipanche ramosa (L.) Pomel, is reported as a species new to Slovakia based upon dates from 50 localities from lowlands after as much as alpine location.

Full text

ISSN 2336-3193 Acta Mus. Siles. Sci. Natur., 71: 263-284, 2022
DOI: 10.2478/cszma-2022-0015 Published: online February 2023, print February 2023
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Distribution and biology of Phytomyza orobanchia (Kaltenbach, 1864)
(Diptera, Agromyzidae) in Slovakia
Miloš Černý, Peter Tóth & Michael von Tschirnhaus
Distribution and biology of Phytomyza orobanchia (Kaltenbach, 1864) (Diptera, Agromyzidae) in Slo-
vakia. – Acta Mus. Siles. Sci. Natur., 71: 263-284, 2022.
Abstract: Phytomyza orobanchia Kaltenbach, 1964, a leaf miner fly of Orobanche spp. and
Phelipanche ramosa (L.) Pomel, is reported as a species new to Slovakia based upon dates from 50 lo-
calities from lowlands after as much as alpine location.
Key words: Diptera, Agromyzidae, Phytomyza orobanchia, Orobanche, Phelipanche ramosa, seed
feeder, Slovakia, biology, distribution, faunistics, Crete, Poland, Rhodes, Sardinia, The Alps.
Introduction
The Fly
Kaltenbach (1864) described Phytomyza orobanchia from flies bred from larvae on
Orobanche sp. in Germany. Brauer (1883: 91) was the first author to use the emendation
orobanchiae and Becker (1905: 258) followed him. At least 15 further authors between 1911
and 2007 used this unjustified spelling. The species was also repeatedly emended or misspelled
as orbobanchia, orobanchae or oronbachiae; those alterations being unjustified, too. Two
junior synomyms were not doubted by any author: Phytomyza simillima Strobl, 1893 and Ph.
longicornis Czerny in Czerny & Strobl, 1909. Both were described without mentioning a host
plant and both were synonymized with Kaltenbach’s species by Hendel (1920). All
identifications in the literature can be trusted as the species can easily be reared from stems and
flowers of Broomrape and because of its peculiar large and elongate third antennal segment (1st
flagellomere). M. von Tschirnhaus (MvT) observed in a Hungarian series (received from Zoltán
Horváth (leg. 10.vii.1986, 33♂♂, 30♀♀, Bácsalmás), that this often is slightly larger in females
than in males, quite opposite to the few world Agromyzidae species with such a sexual
dimorphism, in which the male has a larger one, e.g. Cerodontha (Dizygomyza) species,
Liriomyza commelinae (Frost, 1931), and L. robustae Spencer, 1985.
Ph. orobanchia together with the tropical Ophiomyia lantanae (Froggatt, 1919) are two
frequently cited and studied species which are used as biological agents against very harmful
plants, the prickly Lantana shrubs and the multitude of parasitic Broomrape species. Larvae of
both consume the fruits and seeds of their host plant, thus reducing the dissemination of those
pest species. A short overview on the harmfulness of its hosts and the biology of the Broomrape
fly (in Russian literature addressed as the „fitomiza“, in German as the „Kleeteufel“ or
„Sommerwurz-Fliege“) is compiled from the extensive literature, mainly published in
Bulgarian, Hungarian, Russian, Serbocroatian and Turkish languages. Ph. orobanchia feeds
exclusively on all species of Broomrapes (Orobanche and Phelipanche spp.) (Klein et al. 1999).
The preferred food of Ph. orobanchia are the Orobanche-seeds, but larvae also mine the
epidermis of the shoots. Damage to the shoots produces premature desiccation of the seed
capsules (Spencer 1973b). Development starts in spring, when temperature and photo-period
trigger the end of diapause of overwintering pupae. As Ph. orobanchia depends on its host, it is
adapted to the summer vegetation period. Depending on the specific climatic conditions there
are 1–6 generations per year (Klein & Kroschel 2002).

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The host plant
Several technical, vegetable and fodder crops are damaged by a harmful flowering parasite
– the Broomrape (Orobanche L., 1753, Orobanchaceae). Parasitic weeds of the genus
Orobanche pose a tremendous threat to European agriculture (Joel 2000). These weeds
considerably damage crop plants due to withdrawal of water, minerals and organic compounds.
The growth of the hosts is retarded and yield losses range from 5 to 100% depending on the
region and the crop (Sauerborn 1991). For example, Orobanche ramosa decreased tomato yield
in Slovakia by 43–53% (Cagáň & Tóth 2003). A detailed literature overview on Orobanche was
published by Pieterse (1979). This genus [sensu lato] includes 140–200 species worldwide of
which O. crenata, O. cumana, O. minor, and Phelipanche ramosa are the most noxious ones.
Certain Orobanche species are specific to one host plant species, whilst others attack a group
of hosts. Crops of Beans, Cabbage, Carrots, Chickpea, Cucumber, Hemp, Lentil, Honey- and
Water melon, Peas, Potato, Tobacco, Tomatoes, and Sunflowers belong to their parasitized
hosts. In heavily infested fields more than 200 shoots per m² may destroy the whole crop. In
Bulgaria, 100 flowering Broomrape sprouts produced 2,302 seed capsules, and in Egypt 1,168
seeds had been counted in one capsule; in other countings the result was 2,500 healthy seeds
per capsule and on an average 150,000 seeds per plant, partly even more than 1 million. The
minuscule wind-dispersed seeds (size 0.3mm) are germinable in the ground for 20 years. They
exclusively germinate up to only 1cm away from the roots of their host plant, influenced by
exudate root-substances (Antonova et al. 2015). Chlorophyll is completely absent in all total-
parasitic Orobanche species.
Only one leaf miner fly, the monophagous and polyvoltine Ph. orobanchia attacks
Broomrape. Altogether, 21 species of Orobanche are known as larval host plants. Bronštejn &
Kabulov (1961) recorded the genus Cistanche Hoffmannsegg & Link, 1809 as a further host
genus. Ph. orobanchia belongs to a phylogenetic clade of closely related Phytomyza species for
which in the past only hosts from the families Scrophulariaceae and Plantaginaceae were
recorded. Those semiparasitic genera of Scrophulariaceae actually are treated as
Orobanchaceae, too, e.g. the known semiparasitic host plant genera for Phytomyza species:
Euphrasia, Melampyrum, Odontites, Pedicularis, Rhinanthus; in modern taxonomy Chelone
and Veronica were transferred to the Plantaginaceae, a closely related family. Zlobin (1967:
106; 1999; 2008: 126) listed 26 and 14 Phytomyza spp., respectively, all being closely related
monophagous or oligophagous species from those host genera. He placed them as the clades
atomaria Zetterstedt group and plantaginis Robineau-Desvoidy group, neglecting the earlier
name affinis Fallén group which was already introduced by Hendel (1922: 67). It is of great
interest, that nine of Zlobin‘s listed species develop in seed capsules or additionally in stems.
Seeds are a rare larval substrate for Agromyzidae, e.g. in Europe for Melanagromyza albocilia
Hendel, 1931, M. cuscutae Hering, 1958, Liriomyza lutea (Meigen, 1830), L. wachtlii Hendel,
1920, Phytoliriomyza ornata (Meigen, 1830), Gymnophytomyza heteroneura (Hendel, 1920),
Napomyza scrophulariae Spencer, 1966, N. lateralis (Fallén, 1823), and Phytomyza krygeri
Hering, 1949.
The larvae of Ph. orobanchia mine Orobanche shoots and feed in seed capsules, thus
intervening at the sensitive reproductive stage of Orobanche (Figs 5-9). Hence, the reduction
of Orobanche seed production prevents supplementary infestation and dissemination. The
release of flies from a 3 m³ volume field cage with enclosed masses of withered Broomrape
plots, the so-called "phytomyzarium" (Kljueva et al. 1979; Kljueva & Pamukči 1982) (figs.
reproduced from Bondarenko by Klein & Kroschel 2002) are used for biological control with
the necessity to separate and destroy the emerging smaller parasitoids by a construction using
gauzes with two different mesh widths. By this technique the natural efficiency of the fly can
be increased considerably. In moderately infested fields, about 1,000 flies should be released

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per hectar. Klein & Kroschel (2002) in their detailed review calculated 49% of seed capsules
being infested in Morocco. Only about 5% of viable seeds have been produced in comparison
to 62% without fly releases (Klein et al. 2004). The developmental cycle lasts 25–30 days. Flies
emerge in a sex ratio of 1 : 1 (n = 313 puparia), in other trials females outnumber the males by
1.3 : 1. Copulation takes place one day after emergence and flies survive with food supply for
on an average 9 days. The eggs are deposited either on the stigma of the style, into petals, into
the immature seed capsules or under the epidermis of the stalks. Larvae feed on the seeds and
subepidermal tissue, sometimes penetrating into the stalks where they feed or only tunnel in
order to reach another seed capsule. Pupation takes place in the capsules but most frequently in
the stem near the ground or deeper in the hidden part of the stem. Up to 19–64 larvae and
puparia have been counted in one sprout (n = 40 sprouts) (Mihajlović 1986). In another
investigation 300–1,380 specimens had been found per one m². In Europe three or four
generations develop during the growing period, in warmer countries more.
The control of Broomrape
Rearing the fly larvae under a 12-hour photo-period favours the quantity of diapaused
pupae. Thus, for industrial purposes a shortened-day rearing should be preferred in order to
obtain as many imagines for release as possible. The high reproductive potential of the fly acts
as one of the main controls of Broomrape. Puparia spend up to three years in the hibernation
diapause stage and thus are able to survive temporary disappearances of their host plants. The
most suitable stage for introducing the insect is the imaginal stage when the danger of
introducing the associated 31 published Braconid and Chalcidoid parasitoids (Aphelinidae,
Braconidae, Eulophidae, Eupelmidae, Pteromalidae) is excluded. In one published trial 511
flies, 477 Chalcidoidea and 599 Braconidae emerged from puparia. Under free conditions the
Orobanche fly spreads rapidly. In low to medium infested fields, releases of Ph. orobanchia
alone are sufficient to reduce seed production to an acceptible level. Interestingly, the chloropid
Polyodaspis sulcicollis (Meigen, 1838) was repeatedly reared in numbers from Orobanche
stems together with Ph. orobanchia, identified also by MvT. Larvae in this 3-trophic system
may consume dead fly larvae. It is already known which volatile organic compounds are
responsibe for Phytomyza attraction. They may potentially improve biocontrol of Broomrapes,
stimulate artificial attraction to the host in order to carry out mass trapping for subsequent
redistribution or be used as vectors for specific fungal diseases of Orobanche (Peter Toth,
unpublished data).
Material and methods
The presence of Ph. orobanchia on ten confirmed host plants, namely Orobanche alba Willdenow, O. alsatica
Kirschleger, O. caryophyllacea Donnel Smith, O. elatior Sutton, O. flava F.W. Schultz, O. kochii F.W. Schultz,
O. lutea Baumgarten, O. pallidiflora Wimmer & Grabowsky, O. reticulata Wallroth and Phelipanche ramosa (L.)
Pomel was monitored in 50 locations from lowlands to high mountain locations in western, central and eastern
Slovakia during 2002–2015 (Figs 1, 2). During field trips, the occurrence of larvae, puparia, and adults on plants
was observed, and plants with puparia were sampled. The collected plants were stored in air-conditioned cabins,
the reared adults were determined according to the male genitalia. All material was collected by P. Tóth, the adults
obtained from collections in 2002–2004 were determined by M. Černý, and material from other collections had
been already determined by P. Tóth. M. von Tschirnhaus collected the species in Germany, Hungary, Bulgaria, on
the Greek islands of Rhodes and Crete and he possesses it from the Ethiopian studies by Elzein et al. (1999) and
Horváth (1981). Without doubt all flies belong to one species. In the forthcoming database „World Agromyzidae
online“ of MvT all 423 references found for Ph. orobanchia are included but only very few of those articles and
books contain exact collecting data. Thus, we add some in the Distribution section to the relevant country. Germany
is a special example: Since the original description, for the first time we record an exact locality. From an altitude
of 2,032m a.s.l. this is the highest elevation for this species ever published. Hering collected it in Nazareth, Ethiopia
(Spencer 1961: 429) which is situated at 1,712m a.s.l. Abbreviations used in text: CHKO = Protected Landscape
Area, NP = National Park, NPR – National Natural Reserve, Res. – reserve.

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Figs 1–2: Maps. 1 – Localities of Slovakia: 1– Martovce; 2 – Svätý Peter; 3 – Štúrovo 1; 4 – Štúrovo 2; 5 – Dubník;
6 – Branovo; 7 – Bešeňov; 8 – Santovka 1; 9 – Santovka 2; 10 – Plášťovce; 11 – Mochovce; 12 – Žibrica;
13 – Malé Kršteňany; 14 – Dolné Vestenice; 15 – Nitrica; 16 – Blatnica; 17 – Fačkov; 18 – Rajecká Lesná;
19 – Ľubochňa; 20 – Belá, Dolina Malá Bránica; 21 – Belá, Dolina Veľká Bránica; 22 – Zázrivá; 23 – Sedlo
Príslop; 24 – Oravská Polhora, dolina Polhoranky; 25 – Oravská Polhora, Slaná voda; 26 – Vitanová; 27 – Zuberec,
Roháčska dolina; 28 – Zuberec; 29 – Prosiek; 30 – Liptovská Sielnica; 31 – Demänovská dolina; 32 – Pusté;
33 – Svidovské sedlo; 34 – Ohniště; 35 – Kráľova Lehota; 36 – Malužiná; 37 – Tatranská Javorina; 38 – Ždiar,
Monkova dolina; 39 – Telgárt; 40 – Petrovce, field; 41 – Petrovce, hillside; 42 – Gemer, steep meadow;
43 – Gemer, old orchard; 44 – Kečovo; 45 – Turňa nad Bodvou, meadow; 46 – Turňa nad Bodvou, near castle;
47 – Zádiel, Zádielsky kameň; 48 – Zádiel, NPR Zádielska tiesňava; 49 – Zádiel, Zádielska dolina; 50 – Ladmovce;
2 – Location of Slovakia in Europe (red area). Map sources (Fig. 1) Mapy.cz; (Fig. 2) https://d-maps.com.
FAMILY: AGROMYZIDAE
Subfamily: Phytomyzinae
Phytomyza orobanchia Kaltenbach, 1864 (Figs 3, 4)
Phytomyza Orobanchia m. [= mea = sp. nov.]; Kaltenbach 1864: 265-266. (Descr., host plant, biology)
Phytomyza Orobanchia m.; Kaltenbach 1873: 457-458. (Repeated description)
Phytomyza Orobanchia m.; Kaltenbach 1874: 457-458. (Re-issued as hard cover edition)
Phytomyza orobanchiae Kltb.; Brauer 1883: 91. (First unjustified emendation, citing „Kltb.“ only)
Phytomyza simillima Strobl, 1893: 306; (Synonymised by Hendel 1920)
Phytomyza orobanchiae Kaltenb., 1872; Becker in Becker et al. 1905: 258. (2nd unjustified emendation)
Phytomyza longicornis Czerny in Czerny & Strobl, 1909: 265. (Synonymised by Hendel 1920)
Phytomyza Orobanchia Kalt.; Hendel 1920: 157, 174. (1st key; synonymy of simillima and longicornis)
Phytomyza orobanchia Kalt.; de Meijere 1926: 279-280. (Description of larva)
Phytomyza orobanchia Kaltenbach 1872; Hering in Dahl 1927: 107, 166. (2nd key, description)
Phytomyza orobanchia Kalt.; Speijer 1934: 52, 53, 56, 81-82, 93, 95. (1st fig. and descr. of male genitalia)
Phytomyza orobanchia Kaltenbach (1864); Hendel 1936 [in 1931-1936]: 8, 447-448, 502, 543, pl. xii
Phytomyza orobanchia Kaltenbach; de Meijere 1944: 72. (Correction of larval description 1926)
Phytomyza orobanchae; Čalakov 1973: 125-130. (Earliest error for orobanchia).
Phytomyza orobanchia Kaltenbach, 1864; Spencer 1973: 355, 358 364-367. (Figs of head, male genitalia)
Phytomyza orobanchiae Kalt.; Tawfik et al. 1976. (Detailed description of larval stages; biology)
Phytomyza orobanchia Kaltenbach, 1872; Klein & Kroschel 2002: 245-277. (Lit. review & orig. study)
Phytomyza orobanchia Kaltenbach, 1864; Sumner 2018. (First photographs of alife fly)

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Material examined
WESTERN SLOVAKIA: [1] – Martovce, field with tobacco, 47°52'09"N, 18°08'09"E, 112m a.s.l., 3.ix.2004,
the larvae, puparia and adults were present in large numbers on P. ramosa. [2] – Svätý Peter, field with tobacco,
47°50'26"N, 18°17'24"E, 168m a.s.l., 17.viii.2004, 3.ix.2004, the puparia were present in large numbers on
P. ramosa. [3] – Štúrovo 1, Vŕšok, a hill with rare phytogeographic elements, thermophilic vegetation, 47°49'08"N,
18°38'36"E, 221m a.s.l., 4.vi.2009, puparia and adults on O. alsatica (Figs 16, 17). [4] – Štúrovo 2, Vŕšok, meadow
with thermophilic vegetation, 47°49'09"N, 18°38'42"E, 221m a.s.l., 21.vi.2009, adults on O. kochii (Figs 18, 19).
[5] – Dubník - Dvor Mikuláš, tomato fields, 47°56'48"N, 18°19'11"E, 132m a.s.l., 12.viii.2003, 31.vii.2013 puparia
on P. ramosa; 2.viii.2013, puparia and adults on P. ramosa. [6] – Branovo, tomato fields, 48°00'22"N, 18°16'58"E,
125m a.s.l., 5.viii.2011, 12.vii.2012, 2.viii.2012, larvae, puparia and adults on P. ramosa (Figs 10, 11).
[7] – Bešeňov, field with tobacco, 48°03'09"N, 18°15'52"E, 130m a.s.l., 30.vii–3.ix.2004, the larvae and puparia
were present in large numbers on P. ramosa. [8] – Santovka 1, field with tobacco, 48°09'08"N, 18°45'06"E,
200 m a.s.l., 2.ix.2004, the larvae, puparia and adults were present in large numbers on P. ramosa. [9] – Santovka
2, ditch above the road opposite the swimming pool, 48°09'18"N, 18°46'14"E, 162m a.s.l., 31.v.2014, puparia and
adults on O. pallidiflora (Figs 14, 15). [10] – Plášťovce, hill Konerád, light forest in the upper part and grassy
slopes below, 48°08'53"N, 18°58'17"E, 242m a.s.l., 1.vi.2013, larvae and puparia on O. caryophyllacea (Figs 20,
21). [11] – Mochovce, hill Dobrica, 326 m, in the volcanic mountain range of Kozmálové vršky, opposite
the Mochovce nuclear power plant, xerothermic slope, 48°16'33"N, 18°26'43"E, 320m a.s.l., 30.v.2022, puparia
on O. alba (Figs 12, 13). [12] – Tribeč Mts, Žibrica, Vápeník, limestone hill, grass ridge, 48°21'51"N, 18°09'36"E,
531m a.s.l., 9.vii.2003, puparia on O. alba and O. caryophyllacea. [13] – Malé Kršteňany, Veľký vrch, slope at
the edge of the quarry, 48°38'35"N, 18°27'01"E, 320m a.s.l., 5,vi.2003, larvae and puparia on O. alba. [14] – Dolné
Vestenice, rocky slopes with low vegetation, 48°42'13"N, 18°23'25"E, 237m a.s.l., 12.vi.2013, puparia and adults
on O. alba. [15] – Nitrica, Račice, uncultivated rocky island in the middle of fields, 48°41'55"N, 18°26'01"E, 250m
a.s.l., 12.vii.2004, puparia on O. alba.
CENTRAL SLOVAKIA: [16] – Blatnica, Blatnicka dolina, meadows in the valley along the stream Balatnický
potok, 48°55'19"N, 18°56'34"E, 680m a.s.l., 27.vi.2009, 13.–17.vii.2010, 2.vii.2015, the adults were present in
large numbers on O. flava (Figs 22, 23). [17] – Fačkov, Rajecká dolina, butterbur vegetation by the main road,
49°00'01"N, 18°35'46"E, 537m a.s.l., 2.vii.2002, larvae on O. flava. [18] – Rajecká Lesná, Lesná dolina, wooded
valley, bright spots by the Rybná stream, 49°01'48"N, 18°37'51"E, 530m a.s.l., 15.viii.2004, the puparia and adults
were present in large numbers on O. flava. [19] – NP Veľká Fatra, Ľubochňa, Ľubochnianska valley, moist, sunny
meadow, 49°05'46"N, 19°08'47"E, 460m a.s.l., 24.vi.2012, puparia and adults on O. flava. [20] – NP Malá Fatra,
Belá, Dolina Malá Bránica, meadows along the forest road and stream Malá Bránica, 49°13'37"N, 18°58'34"E,
560m a.s.l., 14.viii.2004, the puparia were present in large numbers on O. flava. [21] – NP Malá Fatra, Belá, valley
Veľká bránica, meadows along the forest road and stream Veľká bránica, 49°13'49"N, 18°58'54"E, 582m a.s.l.,
12.vi.2004, adults on O. caryophyllacea; 2.vii.2002, 3.ix.2004, 26.vi.2009, the larvae, puparia and adults were
present in large numbers on O. flava. [22] – Zázrivá, damp meadow near road, 49°15'56"N, 19°08'48"E, 612m
a.s.l., 2.vii.2002, larvae on O. flava. [23] – NP Malá Fatra, Sedlo Príslop, Pod Sokolím, 49°13'52"N, 19°00'38"E,
916m a.s.l., 13.vi.2004, rocky, limestone saddle, adults on O. caryophyllacea. [24] – CHKO Horná Orava, Oravská
Polhora, Polhoranka valley, around the stream in the whole valley around the stream Kalužovka, 49°33'44"N,
19°24'28"E, 733m a.s.l., 20.–21.vii.2010, puparia and adults on O. flava. [25] – CHKO Horná Orava, Oravská
Polhora, near Slaná Voda, moist sunny meadows around the spring, 49°31'59"N, 19°28'23"E, 783m a.s.l.,
23.viii.2004, 20.vii.2010, larvae, puparia and adults on O. flava. [26] – Vitanová, by the road in the direction of
Oravice, next to the stream, 49°19'44"N, 19°44'10"E, 737m a.s.l., 2.vii.2002, larvae on O. flava. [27] – Vysoké
Tatry Mts, Zuberec, Roháčska dolina, near cottage Primula, a meadow by the cottage and a butterbur by the stream
Roháčsky potok, 49°15'04"N, 19°42'13"E, 1,001m a.s.l., 22.vii.2009, 23.vii.2013, 5.viii.2013, puparia and adults
on O. flava (Figs 24, 25). [28] – Vysoké Tatry Mts, Zuberec, wet meadows by the side of the road, 49°14'53"N,
19°36'43"E, 767m a.s.l., 2.vii.2002, 5.viii.2002, 23.viii.2004, the puparia was present in large numbers on O. flava.
[29] – Chočské vrchy Mts, Prosiek, NPR Prosiecka dolina, 49°09'29"N, 19°29'52"E, 622m a.s.l., 27.vi.2003,
puparia on O. elatior. [30] – Liptovská Sielnica, butterbur vegetation by the main road, 49°08'07"N, 19°30'56"E,
562m a.s.l., 5.viii.2002, puparia on O. flava. [31] – NP Nízke Tatry, Demänovská dolina, Demänovská valley,
meadows along the stream Demänovka, 49°00'11"N, 19°34'56"E, 810m a.s.l., 30.vi.2012, 5.vii.2012, 8.vii.2013,
puparia and adults on O. flava. [32] – NP Nízke Tatry, Pusté, above Demänovská valley, rocky/limestone meadow
ridge, 48°59'52"N, 19°36'43"E, 1,500m a.s.l., 30.vi.2004, 25.vii.2009, 28.vii.2013, puparia and adults on
O. reticulata (Figs 32, 33). [33] – NP Nízke Tatry, Svidovské sedlo, above the grass pass, 48°58'51"N, 19°43'48"E,
1,438m a.s.l., 5.viii.2003, puparia on O. caryophyllacea. [34] – NP Nízke Tatry, Ohnište, the vicinity of the rocky
hill, 48°59'09"N, 19°44'01"E, 1,290m a.s.l., 4.vii.2012, adults on O. reticulata. [35] – NP Nízke Tatry, Kráľova
Lehota, Svarín, Čierny Váh valley, butterbur vegetation along the stream, 49˚00'N, 19˚52'E, 721m a.s.l.,
23.vii.2009, larvae and puparia on O. flava. [36] – NP Nízke Tatry, Malužiná, Dolina Svidovo, 48˚58'N, 19˚43'E,
23.vii.2009, 1,100m a.s.l., butterbur vegetation along the stream Svidovský potok, puparia on O. flava (Fig. 30,
31). [39] – Telgárt, grass pass Besník, under hill Kráľová hoľa, 48°51'43"N, 20°13'35"E, 994m a.s.l., 25.vi.2009,

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adults on O. caryophyllacea. [40] – Petrovce, field with tobacco, 48°11'08"N, 20°00'32"E, 240m a.s.l., 22.vi.2004,
30.viii.2004, the larvae and puparia was present in large numbers on P. ramosa. [41] – Petrovce, hillside above
village, 48°10'59"N, 20°01'27"E, 250m a.s.l., 17.vii.2003, the puparia was present in large numbers on O. alba.
[42] – Gemer, steep meadow near the castle, 48°27'22"N, 20°18'56"E, 247m a.s.l., 7.vi.2022, puparia on O. alsa-
tica (Figs 28, 29). [43] – Gemer, ridge above the castle, old orchard, 48°27'31"N, 20°18'55"E, 270m a.s.l.,
13.vi.2012, the puparia and adults were present in large numbers on O. lutea (Figs 26, 27).
EASTERN SLOVAKIA: [37] – Vysoké Tatry Mts, Tatranská Javorina, NPR Javorová dolina, near Javorinka
river, 49°15'23"N, 20°08'53"E, 1,076m a.s.l., 21.vii.2010, puparia and adults on O. flava (Figs 34, 35). [38] – NPR
Belianske Tatry, Ždiar, Monkova dolina, wide sunny meadows and stands of butterbur by the stream Biela
49°16'04"N, 20°14'53"E, 910m a.s.l., 21.vii.2010, puparia and adults on O. flava. [44] – NP Slovenský kras,
Kečovo, Kečovské škrapy, 48°29'39"N, 20°29'12"E, 370m a.s.l., 31.viii.2004, puparia on O. alba. [45] – Turňa
nad Bodvou, mowed meadow under castle, 48°36'42"N, 20°51'47"E, 200m a.s.l., 17.viii.2005 and 8.vi.2013, adults
on O. alsatica. [46] – Turňa nad Bodvou, a castle on a limestone hill with drought-loving vegetation, 48°36'40"N,
20°52'28"E, 295m a.s.l., 22.v.2009, puparia on O. alba and O. caryophyllacea. [47] – NP Slovenský kras, Zádiel,
Zádielsky kameň, karst, scrap habitats, 48°37'27"N, 20°50'02"E, 610m a.s.l., 22.vi.2004, the puparia and adults
was present in large numbers on O. alba and O. caryophyllacea. [48] – NP Slovenský kras, Zádiel, NPR Zádielska
tiesňava, Zádielska dolina, closed wet and cool valley with dense vegetation near the stream Blatný potok,
48°37'55"N, 20°49'45"E, 435m a.s.l., 6.vii.2011, larvae, puparia and adults on O. pallidiflora (Figs 38, 39);
2.vii.2012, puparia and adults on O. pallidoflora. [49] – NP Slovenský kras, Zádiel, Zádielska dolina, site Nad
kaňonom, limestone karst 48°38'08"N, 20°49'37"E, 570m a.s.l., 29.vi.2004, puparia and adults on O. alba.
[50] – Ladmovce, Kašvár Res., hill Šomoš, limestone hill with low xerothermic vegetation, 48°25'08"N,
21°46'33"E, 190m a.s.l., 20.v.2009, puparia and adults on O. alba; 29.v.2010, adults on O. alba (Figs 36, 37).
Distribution
Ph. orobanchia Kaltenbach is widespread mainly in southern Europe, Near and Middle
East and northern and eastern Africa. In Chile the species was introduced as an beneficial agent
against its host plants. Table 1 presents all confirmed countries for which the species is recorded,
but predominantly without detailed collection data. Secondary records like checklists and
mentions based on earlier publications are not cited. Only the earliest confirmations are listed,
constricted to four.
Tab 1: Distribution of Phytomyza orobanchia. Only references for the earliest original records are listed. Notes
1–10 apply to samples with first detections on three major islands or first exact collection data for already known
countries.
Austria (Strobl 1893 as simillima; Werneck 1936; Watzl 1936).
Algeria (Ait Abdallah et al. 1999; Zermane et al. 1999).
Bulgaria (Čalakov & Šabanov 1970; Čalakov 1973; Trenčev 1981: 112; leg. von Tschirnhaus X1473, X1476,
Notes 7-8).
Chile the species was introduced as an agent against its host plants (Norambuena et al. 1999; Norambuena et
al. 2001).
Cyprus (Černý & Vála 2006).
Egypt (Hammad et al. 1967; Subba Rao 1973; Tawfik et al. 1976; Hegazi et al. 1981; Kolaib et al. 1986).
Ethiopia (Spencer 1961: 429; Elzein et al. 1999; von Tschirnhaus collection P140, Note 2).
France (Séguy 1934; Buhr 1954: 261; Service d’Identification des Entomophages 1963 and 1965).
Georgia (Japoshvili & Kostjukov 2016).
Germany (Kaltenbach 1864; Rühl 1914: 39; 3rd record and 1st record for The Alps: leg. von Tschirnhaus
sample 569, Note 1).
Great Britain (Spencer 1960: 170; Spencer 1972a; Chandler 1975; Sumner 2018).
Greece, mainland (Černý 2011).
Greece, isles of Crete and Rhodes (first records, leg. von Tschirnhaus X530, X533, X542, Note 3-6).
Hungary (Ubrizsy & Reichart 1958; Szökö 1968; Horváth 1981). See also Introduction!
India - transfer of 2,000 puparia in 1982 (Manjunath & Nagarkatti 1977; Mihajlović 1986).
Iran (Vidal 1997: 17, 48; Jafarzadeh & Pourmirza, 1999; Movahedi-Fazel et al. 1998).

269
Iraq (Al Khesraji et al.1987; Al Khesraji & Abdel Wahid 1988).
Israel (Joel 2002).
Italy: Sardinia (first record, leg. M. von Tschirnhaus It 2016, Note 9).
Italy incl. Sicily (Martelli 1933a and 1933b; Puzilli 1983; Cubero & Moreno 1979).
Kazakhstan (Bondarenko & Prokofiev 1971).
Kyrgyzstan (Moiseeva & Mamraliev 1969; Moiseeva 1975).
Macedonia (Todorovski & Vasilev 1976).
Maltese Islands (Spencer 1973a).
Moldova (Kljueva et al. 1972; Kljueva & Ursake 1974; Kljueva & Pamukči 1980).
Morocco (Schmitt 1981; Geipert et al. 1994; Tihr 1997).
Netherlands (van der Wulp & de Meijere 1898; de Meijere 1924).
[Pakistan (Baloch et al. 1980: 8, 10; Klein & Kroschel 2002; both assumptions are not confirmed)].
Poland (Piwowarczyk et al. 2018; second record, leg. P. Tóth, Note 10).
Russia (Podjapoľskij 1911; Kurdjumov 1912; Mamonov 1929: 12, 17).
Serbia -Vojvodina in northern Serbia (Lekić 1971; Mihajlović 1986).
Slovakia (Tóth & Cagáň 2002); this article
Spain (Czerny & Strobl 1909, as longicornis; Hering 1943; Spencer 1961: 429; Spencer 1972b: 101).
Syria (Hendel 1920; Linke et al. 1990; Pieterse et al. 1994).
Tajikistan (Bronštejn & Kabulov 1961; Bronštejn 1972).
Tunisia (Zermane et al. 2002 and 2004).
Turkey (Giray & Nemli 1982; Nemli & Giray 1983; Petzold et al. 1994).
Turkmenistan (Nazarov & Setdarov 1980; Krivosheina 2012: 255).
Ukraine incl. Crimea (Kurdjumov 1912; Zatirka & Ilľin 1973; Okazova 1973; Kara & Lizenko 1976).
Uzbekistan (Bronštejn & Kabulov 1961; Chalimov 1970; Bronštejn 1972).
Yemen (Deeming 2006).
Notes: Original first records with exact collecting data:
Note 1: Germany, Bavaria, Alps, Karwendel mountain, 2,262m a.s.l.,
47°25'40''N, 11°17'49''E, 5.vii.2011, leg. M. von Tschirnhaus.
Note 2: Ethiopia, Malima, 1,620m a.s.l., xii.1994, puparia in O. cernua, 1♂ 1♀ emerged ix.1995,
coll. MvT, leg. A. Elzein.
Note 3: Greece, Isle of Crete, south coast, W' Kalo Nero, 35°01'05''N, 26°01'26''E, 15.iii.1987, 1♂1♀,
leg. MvT.
Note 4: Greece, Isle of Crete, south coast, Koutsounari, 35°00'26''N 25°49'05"E, 18.iii.1987, 1♂1♀, leg. MvT.
Note 5: Greece, Isle of Crete, east, road between Zákros and Xerócampos, 35°05'00''N, 26°13'30'', 23.iii.1987,
2♀♀, leg. MvT.
Note 6: Greece, isle of Rhodes, east coast, river mouth of Gaidouras, 36°08'56''N, 28°04'38''E, 29.iii.1997, 1♀,
leg. MvT.
Note 7: Bulgaria, coast of Black Sea, southern end of Bolata gorge, 43°23'00''N, 28°28'15''E, 1.vi.2002, 1♀,
leg. MvT.
Note 8: Bulgaria, Tutracan at river Danube, 44°03'02''N, 26°36'24''E, 3.vi.2002, 1♂, leg. MvT.
Note 9: Italy, Sardinia, Monte Zaparedda plateau, Tulli Nuraghe Tutturuddu, 39°44'13''N, 8°57'56''E, 4.v.2011,
1♀, leg. MvT.
Note 10: Poland, Podzamcze, Poland, Castle Ogrodzieniec, limestone rocks and meadows, 50°27'11.4"N,
19°33'04.3"E, 500m a.s.l., 16.vi.2012, many adults on Orobanche bartlingii, leg. P. Tóth.
Discussion
Despite the fact that the Slovak fauna of Diptera is rather well known and relatively
intensively studied, the family Agromyzidae with 379 species confirmed from the territory of
Slovakia is still one of the groups where discoveries of other new species for the fauna of this

270
country can still be expected. The findings presented above represent the first reliably
documented data on the occurrence of Ph. orobanchia in Slovakia. In the period 2002–2015,
the presence of this species, its reproduction and development on host plants of the genus
Orobanche and Phelipanche ramosa were monitored at 50 locations in western, central and
eastern Slovakia, from the lowlands to the highlands. A total of 10 parasitic plants with larvae,
puparia and adults of Ph. orobanchia were confirmed. The most widespread host plant for Ph.
orobanchia in Slovakia is Orobanche flava, which is confirmed in 17 localities in central and
eastern Slovakia at 500–1,100m a.s.l., the species parasitizes Petasites albus, P. kablikianus,
less often P. hybridus. Orobanche alba was found in 12 localities in low to medium locations
at an altitude of 190–767m a.s.l., the species parasitizes almost exclusively on species of the
genus Thymus, more rarely also on Clinopodium vulgare. Orobanche alsatica was found only
in 3 lowland locations with thermophilic vegetation one location in western, one in central and
one in eastern Slovakia, the species parasitises most often on Peucedanum cervaria and
Libanotis pyrenaica, rarely also on Seseli osseum. In Slovakia, O. alsatica is a vulnerable and
legally protected species (Eliáš et al. 2015). Orobanche caryophyllacea is confirmed at 8
localities from the lowlands to higher locations with the highest confirmed record at 1,438m
a.s.l., at the Svidovské sedlo locality in the NP Nízke Tatry. The species is parasitic on various
representatives of the Rubiaceae family, especially on species of the genus Galium. Orobanche
elatior is confirmed from only one locality in central Slovakia in the NPR Prosiecka dolina, the
species parasitizes mainly on Centaurea scabiosa. In Slovakia, O. elatior is relatively rare and
potentially endangered species (Eliáš et al. 2015). Orobanche kochii is found only in one heat-
loving locality, Vŕšok near Štúrovo, the species parasitizes on Centaurea scabiosa, much more
rarely on other Centaurea species. In Slovakia, O. kochii is classified as a potentially
endangered species (Eliáš et al. 2015). Orobanche lutea is confirmed from only one locality in
central Slovakia near the village of Gemer, the species parasitizes mainly on Medicago falcata,
less often on M. sativa. In Slovakia, O. lutea is a potentially endangered species (Eliáš et al.
2015). Orobanche pallidiflora is found in western Slovakia in the lowland area of Santovka and
in eastern Slovakia in the Zádielska dolina, the species is parasitic most often on species of the
genera Carduus and Cirsium. Orobanche reticulata is confirmed only from the NP Nízke Tatry
at two locations at an altitude of 1,290–1,500m a.s.l., the species parasitized mostlly on Carduus
glaucinus during our survey, but potentially also C. collinus, C. acanthoides, Carlina acaulis,
Cirsium erisithales and Knautia sp. Species Phelipanche ramosa was confirmed in
thermophilic locations of southwestern and central Slovakia in fields with tobacco and
tomatoes. The species mainly parasitizes on cultivated crops such as Tobacco (Nicotiana
tabacum), Hemp (Cannabis sativa) and Tomatoes (Solanum lycopersicum), rarely Pepper
(Capsicum annuum) and Potatoes (Solanum tuberosum). In Slovakia, P. ramosa is assessed as
a potentially vulnerable species in terms of threats (Eliáš et al. 2015). Host plants of
Broomrapes (Phelipanche and Orobanche spp.) in Slovakia are listed in detail by Zázvorka
(1997). The appearance and mating of Ph. orobanchia is linked to the period of full flowering
of the plants in the given habitat, which is usually one to one and a half weeks. The first
flowering Broomrape in Slovakia is O. alba from the end of May to the beginning of June, and
the last are O. flava and P. ramosa from mid-July to mid-August.
Ph. orobanchia is not yet used in Slovakia to control Orobanche attacking various
agricultural crops.
Acknowledgements: We express our sincerest thanks to Hans Smid (Laboratory of Entomology, Wageningen
University, Netherlands) for providing photos with imago of Phytomyza orobanchia, Jindřich Roháček (Opava,
Czech Republic) for valuable comments and assistance with the early draft of the manuscript and Barry
P. Warrington (Hessle, East Yorkshire, Great Britain) for the language revision of the manuscript.

271
Figs 3–9: Phytomyza orobanchia Kaltenbach and its larva, puparium and mine. 3 – Ph. orobanchia, female on
Phelipanche ramosa; 4 – Mating on Orobanche flava Northwestern Slovakia, Oravska Polhora; 5 – Larva in shoot
of Phelipanche ramosa; 6 – Puparia in shoot of Orobanche flava; 7 – Larva in seed capsule of Orobanche flava;
8 – Puparium in seed capsule of Orobanche flava; 9 – Bunch of host plant Phelipanche ramosa with mine. Photo
by Hans Smid (3); Photo by Peter Tóth (4-9).

272
Figs 10–13: 10 – Western Slovakia, Dubník – Dvor Mikuláš, tomato fields, 5. August 2011. 11 – Host plant
Phelipanche ramosa; 12 – Western Slovakia, Mochovce, hill Dobrica in Kozmálovské vŕšky, xerothermic slope,
30. May 2022; 13 – Host plant Orobanche alba. Photo by P. Tóth.

273
Figs 14–17: 14 – Western Slovakia, Santovka, ditch above the road, 31. May 2014; 15 – Host plant Orobanche
pallidiflora; 16 – Western Slovakia, Štúrovo, hill with rare phytogeographic elements, thermophilic vegetation,
21. June 2009; 17 – Host plant Orobanche alsatica. Photo by P. Tóth.

274
Figs 18–21: 18 – Western Slovakia, Štúrovo, meadow with thermophilic vegetation, biotop with host plant
Orobanche kochii, 21. June 2009; 19 – Host plant Orobanche kochii; 20 – Western Slovakia, Plášťovce, hill
Konerád, light forest in the upper part and grassy slopes below 11. June 2022; 21 – Host plant Orobanche
caryophyllacea. Photo by P. Tóth.

275
Figs 22–27: 22 – Central Slovakia, Blatnická dolina, meadows in the valley along the stream Balatnický potok, 2.
July 2013; 23 – host plant Orobanche flava; 24 – Central Slovakia, Zuberec, Roháčska dolina, vegetetion of the
butterbur along stream Roháčsky potok, 22. July 2009; 25 – host plant Orobanche flava; 26 – Central Slovakia,
Gemer, ridge above the castle, old orchard, 7. June 2022; 27 – host plant Orobanche lutea. Photo by P. Tóth.

276
Figs 28–31: 28– Central Slovakia, Gemer, steep meadow near the castle, 7. June 2022; 29 – Host plant Orobanche
alsatica; 30 – Central Slovakia, Malužiná, Dolina Svidovo, vegetation along the stream Svidovský potok, 23. July
2009; 31 – host plant Orobanche flava. Photo by P. Tóth.

277
Figs 32–35: 32 – Central Slovakia, Pusté, above Demänovská valley, rocky/limestone meadow ridge, 28. July
2013; 33 – Host plant Orobanche reticulata; 34 – Eastern Slovakia, Javorová dolina, near Javorinka river, 21.
Maly 2010; 35 – Host plant Orobanche flava. Photo by P. Tóth.

278
Figs 36–39: 36 – Eastern Slovakia, Ladmovce, Šomoš hill in Kašvár Res., limestone hill with xerothermic
vegetation, 21. May 2009; 37 – Host plant Orobanche alba; 38 – Eastern Slovakia, Zádielska dolina, hydrophilic
vegetation near the stream Blatný potok, 6. July 2011; 39 – Host plant Orobanche pallidiflora. Photo by P. Tóth.

279
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Authorsʼ addresses: Miloš Če r ný, CZ-763 63 Halenkovice 1, Czech Republic.
E-mail: cerny.milos@centrum.cz
Peter Tó t h , Slovak University of Agriculture in Nitra, Institute of Agronomic
Sciences, Slovak Republic, A. Hlinku 2, 949 76 Nitra, Slovakia.
E-mail: petery@nextra.sk
Michael von Tsch i rnha u s, Fakultät Biologie, Universität Bielefeld,
Postfach 100131, 33501 Bielefeld, Germany.
E-mail: m.tschirnhaus@uni-bielefeld.de