Parasitoids (Hymenoptera) of Leaf-Spinning Moths (Lepidoptera) Feeding on Vaccinium Uliginosum L

Parasitoids (Hymenoptera) of leaf-spinning moths (Lepidoptera) feeding on Vaccinium uliginosum L. along an ecological gradient in central European peat bogs

Aurel I. Lozan, Karel Spitzer, Josef Jaros, Andrey Khalaim, Maria Concetta Rizzo, Emilio Guerrieri & Ales Bezdék

A. J M. E. & Lozan, 1., Spitzer, K., Jaros, ., Khalaim, A., Rizzo, C., Guerrieri, Bezdek, A. 2010: Parasitoids (Hymenoptera) of leaf-spinning moths (Lepidop- tera) feeding on Vaccinium uliginosum L. along an ecological gradient in central European peat bogs. — Entomol. Fennica 21: 243—253.

Parasitoids ofleaf-spinning Lepidoptera associated with two isolated central Eu- ropean peat bogs were investigated. Five families of parasitoid Hymenoptera (Braconidae, lchneumonidae, Eulophidae, Pteromalidae and Encyrtidae) were recorded. Three categories were recognised: (1) primary parasitoids, (2) faculta— tive hyperparasitoids and (3) obligatory hyperparasitoids. Ten species ofBraco- nidae, five species and seven marked morphospecies among lchneumonidae, and three species of Chalcidoidea were identified. Despite of some niche-specific (but less host-specific) parasitoids, all these hymenopterans are likely to be generalists and none of them were confirmed to be habitat and/or host specialists. Unlike their eurytopic (opportunistic tyrphoneutral) parasitoids, the Lepidoptera hosts associated with peat bogs are partially highly stenotopic (tyrphobionts and tyrphophiles). The occurrence of parasitoids compared to their potential hosts was structured along an ecological (mesoclimatic) gradient, so most parasitoids were recorded from margins while stenotopic (narrow habitat adaptation) moths were mostly distributed near the centre of the bog habitat.

A. I. Lozan, K. Spitzer, J. Jaros &A. Bezdek, Biology Centre, Institute ofEntomo— logy, Czech Academy of Sciences, Branisovska 31, 37005 Ceske' Budejovice, Czech Republic; E—mails.‘ [email protected], [email protected],jaros@entu. cas. cz, bezdek@entu. cas. cz A. Khalaim, Zoological Institute, Russian Academy of Sciences, Universitets— kaya nab. I, St. Petersburg I99034, Russia; E—mail.‘ [email protected] M. C. Rizzo, SENFIMIZO Department, Entomology, Acarology and Zoology Section, Faculty ofAgriculture, University ofPalermo, viale delle Scienze I3, Ed. 5, Palermo, Italy; E—mail.‘ [email protected] E. Guerrieri, Institutefor Plant Protection, the National Research Council ofIt— aly, Via Universita I33, 80055 Portici (NA), Italy; E—mail.‘ guerrieri@ipp. cnr. it

Received 26 January 2009, accepted 2 June 2010 244 Lozan et al. ° ENTOMOL. FENNICA Vol. 21

1. Introduction nopteran parasitoids (Braconidae), collected by light traps (Lozan 2002), were not restricted to the Parasitoids of an ecological guild of Lepidoptera bog as reported for stenotopic Coleoptera and feeding on relict boreo-montane plant Vaccinium Lepidoptera (cf. Bezdek et al. 2006). uliginosum L., a deciduous circumboreal shrub characteristic of peaty soils of coldlands, in two isolated central European peat bogs (Spitzer et al. 2. Material and methods 2003) were studied. The moths reared from leaf spinnings belong to four families (Tortricidae, 2.1. Sites of investigations Gelechiidae, Chimabachidae and Geometridae) and include both stenotopic (tyrphobiontic and Leaf spinnings on Vaccinium uligz'nosum were tyrphophilous taxa), closely associated with peat collected during June 1998—2001 from two bogs, and opportunistic (tyrphoneutral) species montane isolated peat bogs ofthe core zone ofthe not related to the bogs. gumava National Park, SW Bohemia, Czech Re- Peat bogs ofcentral Europe, which developed public; details are given by Spitzer et al. (2003): under isolation, are true habitat islands for a unique insect diversity of highly stenotopic taxa a) Mrtvy luh near Volary (740 m a.s.l., 310 ha) (”relicts”) among Lepidoptera and parasitoid Hy- represents a montane oligotrophic valley peat menoptera (Spitzer & Banks 2006, Lozan et al. bog more or less closed by the forest. Open 2010). The Lepidoptera community of central treeless areas are covered by V. uligz'nosum European peat bogs has been well studied under (and other Vaccinium spp.), Eriophorum va— the long-term monitoring programmes, but the ginatum and Calluna vulgaris with a gradual parasitoids have not been subject of such investi- transition to dwarfforest ofPinus mugo S. lat. gations. This paper is based on previous investi- around the bog. gations of Lepidoptera (Spitzer et al. 2003) and b) Chalupska slat’ bog near Borova Lada (900 m aims at assessing parasitoid diversity along an a.s.l., 1 16 ha) is a montane oligotrophic raised ecological (mesoclimatic) gradient in two differ- bog with a central bog-lake and mountain ent peat bog systems. This mesoclimatic gradient pine forest around, with large patches of V. is characterised by extreme temperatures and eX- uligz'nosum (including other Vaccinium spp.) pressed by local vegetation of “forest-tundra” and Betula pubescens (the gradient between formations between bog centres and bog margins the centre and margins is not gradual like in (including “lagg”, see Material and methods, and the Mrtvy luh bog). Bezdek et al. 2006). These two central European bogs are isolated ancient habitats of distinct climatic and edaphic conditions close to the forest- 2.2. Sampling tundra biome with a high proportion oflocal cold- adapted species. For collecting the hosts, leaf-spinnings were There is an identified distinct micro-climatic sampled along an ecological gradient between the gradient from lagg (the ecotone of outer parts of outer margins, lagg (inner margins) and the cen- the bog) to margins and centres of peatbogs, in- tres ofeach investigated bog system. The cover of cluding intermediate zones, where we collected V. uligz'nosum was higher near the treeless areas our field samples for ecological analysis. The bog of the bogs and the stenotopic host taxa (i.e. habitat affinity (association or relation to bog tyrphobionts+tyrphophiles) were most abundant habitat) of both moths and parasitoids from our in the centres (edaphic “tundra-like” formation) samples was correlated with available reliable re- when compared with the pine forested margins cords of levels of host specialisation in order to (including the lagg ecotone, which is an integral reveal the degree oftheir stenotopy and eurytopy. part ofthe bog) ofthe bogs. It was not possible to Previous preliminary investigations in one of the identify exactly which parasitoid species studied peat bogs under the same ecological gra- emerged from the particular host spinning. The dient (centre versus margins) showed that hyme- attempt for host larvae identification by head cap- ENTOMOL. FENNICA Vol. 21 ° Parasitoids ofleafspinning moths 245 sules was not successful and not sufficiently reli- Table 1. No. of reared specimens/species from the able. four families of leaf-spinning Lepidoptera (Chima- bachidae, Gelechiidae*, Tortricidae*, Geometridae*; include specialist/sten0t0pic taxa: tyrphobionts + tyrphophiles) in two peatbogs. 2.3. Lepidoptera Parasitoid family Specimens Species The complete list of moth species with quantita- reared reared tive data (species, reared specimens and leaf spinnings per site) is given by Spitzer et al. Ichneumonidae 26 12 Braconidae 56 1O (2003), here we supply only the list of species Eulophidae 4 1 where taxa are marked with an asterisk stenotopic Pteromalidae 4 1 and as follow: (tyrphobionts tyrphophiles), Encyrtidae 14 1 Diurnea lipsiella (Denis et Schiffermiiller) Unidentified (Chalcidoidea) 3 ? and Dasystoma salicella (Hiibner) (Chimabachi- dae); Athrz'pspruinosella (Lienig & Zeller)>’< (Ge- Total 107 25 lechiidae); Aclerz's laterana (Fabricius), Aclerz's maccana (Treitschke)*, Aclerz's lipsiana (Denis & Schiffermiiller)*, Cnephasia stephensiana All Braconidae and Chalcidoidea specimens (Doubleday), C. asseclana (Denis & Schiffer- were identified at the species level except for miiller), Argyrotaenia [jungiana (Thunberg), three damaged ones (presumably Chalcidoidea). Pandemis cinnamomeana (Treitschke), P. hepa— Most ofthe collected Ichneumonidae were identi- rana (Denis & Schiffermiiller), Clepsis senecio— fied at the species level, some only at the genus nana (Hubner), Adoxophyes orana (Fischer von level. Roslerstamm), Apotomis sauciana (Frolich)*, Celypha lacunana (Denis & Schiffermiiller), 2.5. Data analysis Phiaris bl'punctana (Fabricius)*, Rhopobota naevana (Hiibner) and Pammene luedersiana We used the same community data analysis (Sorhagen)>’< (Tortricidae); Rhinoprora (Pasiphi— scheme as in Spitzer et al. (2003). The Canonical la) debiliata (Hubner) (Geometridae). Correspondence Analysis (CCA; CANOCO ver- The rearing ofa total of 19 species (18 species sion 3.12 software) by Ter Braak (1987) was used of typical leaf-spinning microlepidopteran spe- to determine the habitat preferences ofparasitoids cies and one macrolepidopteran leaf-spinning in relations to the centers and the margins of the species) was conducted under laboratory condi- two investigated bogs. tions, where larvae were kept and fed on V. in boxes. uligz'nosum glass 3. Results

A total of 107 specimens ofparasitoids (Table 1) 2.4. Hymenoptera were reared under laboratory conditions from 19 species of leaf-spinning Lepidoptera feeding on All reared hymenopterans were initially pre- typical bog plant V. uliginosum in two central- served in 80% ethanol, then dried up with the help European peat bogs of the 8umava Mountains. offilter paper and mounted into collections. Tax- All identified parasitoid species can be classified onomic analysis was done by using the most re- as tyrphoneutral taxa, being generalists and more cent keys (e.g., Graham 1959, Askew 1968, or less polyphagous parasitoids ofLepidoptera or Huddleston 1980, 1984, Boucek & Rasplus 1991, oligophagous species associated with smaller Belokobylskij & Tobias 1998, 2000, Guerrieri & numbers of biologically similar Lepidoptera Noyes 2005), and by comparing the specimens (Table 2). None of them was confirmed to be a with authoritatively identified specimens and habitat and/or host specialist, despite that some of with other material deposited in institutional col- their leaf-spinning Lepidoptera hosts were bog lections. specialists. 246 Lozan et al. ° ENTOMOL. FENNICA Vol. 21

Table 2. Known geographic range and host range for parasitoid Hymenoptera (lchneumonoidea, Chalcicoidea) reared from leaf-spinning Lepidoptera feeding on Vaccinium uliginosum L. in two central European peat bogs (Sumava Mts.).

Number of Lepidoptera recorded in literature per: Taxa Geographic range Families Species lchneumonoidea: Braconidae Hormius moniliatus Holarctic, Oriental 5 at least 17 Hormius similis Transpalaearctic, Oriental Probably as H. moniliatus Oncophanes minutus Transpalaearctic 10 >50 Bracon erraticus Transpalearctic 4 5 Charmon extensor almost Cosmopolitan 13 >75 Meteorus ictericus Palaearctic, Australian 13 >90 Meteorus colon Transpalaearctic 1O 25 Earinus gloriatorius West Palaearctic 6 12 Orgilus pimpinellae Transpalaearctic 9 25 Ascogaster bidentula Transpalaearctic 2 2 lchneumonoidea: lcnheumonidae ltoplectis tunetana* Transpalearctic 6 13 Glypta ceratites Europe, Mongolia 6 183 Tranosema carbonellum Holarctic First record on Lepidoptera Chorinaeus funebris Holarctic 7 17 Exochus tardigradus Palaearctic Unknown Unknown Chalcidoidea: Eulophidae Elachertus artaeus Palaearctic, Nearctic 5 11

Chalcidoidea: Pteromalidae Termolampa pinicola Transpalaearctic 1 2 Chalcidoidea: Encyrtidae Copidosoma filicorne Holarctic 2 17

* Facultative hyperparasitoid.

According to their known foraging activity, bog was almost equal in both parts, i.e. 15 speci- they are either primary parasitoids (Braconidae mens and seven species in centre and 16 speci- and Chalcidoidea, partially Ichneurnonidae) of mens and siX species in margins (Table 4). Lepidoptera and rarely of other insect groups, or and facultative obligatory hyperparasitoids Table 3. No. of reared specimens and species per (among Ichneurnonidae) (see Table 3). parasitoid category from the four families of leaf-spin- Being widely distributed with a wide host ning Lepidoptera (Chimabachidae, Gelechiidae*, * range (Ichneumonoidea) or partially with a nar- Tortricidae*, Geometridae; include specialist/steno- taxa: + in two rower host spectrum among Lepidoptera only topic tyrphobionts tyrphophiles) peat (Chalcidoidea), they have comparatively low bogs. host specificity and a wide coverage of various Parasitoid category Specimens Species not restricted to the habitat at habitats, being bog reared reared all. Quantitatively, most parasitoids were re- Primary 95 22 corded from margins in the Mrtvy Luh bog, i.e. Facultative hyperparasitoids 1 1 8 2 55 specimens belonging to twelve species versus Obligatory hyperparasitoids Unidentified (Chalcidoidea) 3 ? only 21 specimens and nine species from the The number of centre+intermediary parts. para- Total 107 25 sitoids reared from hosts of the Chalupska slat’ ENTOMOL. FENNICA Vol. 21 ° Parasitoids ofleafspinning moths 247

Table 4. Number of reared parasitoids (Hymenoptera: Ichneumonoidea, Chalcicoidea) from leaf-spinning moths (Lepidoptera) on Vaccinium uliginosum L. per each investigated bog site (éumava Mts.).

Position along the gradient#

Mrtvy luh Chalupska slat’

Taxa Cntr Inter Marg Lagg Cntr Marg+Lagg

Ichneumonoidea: Braconidae Hormius moniliatus Hormius similis Oncophanes minutus Bracon erraticus Charmon extensor Meteorus ictericus Meteorus colon Earinus gloriatorius Orgilus pimpinellae Ascogaster bidentula A Ichneumonoidea: lcnheumonidae 0—\00000—\—\OO 0000000000 (00000000000 _\00l\)—\—\O‘ll\)00 00040400000 0000000000 ltoplectis tunetana* Glypta ceratites Glypta sp. Campoplex sp. 1 Campoplex sp. 2 Campoplex sp. 3 Campoletis sp. Tranosema carbonellum Chorinaeus funebris Exochus tardigradus Mesochorus sp. 1** Mesochorus sp. 2** Chalcidoidea: Eulophidae 000000000000 00—\—\00000000 0000000004404 400000N0000—\00 0—\00—\0000000 000000N—\00000 Elachertus artaeus 3 O

Chalcidoidea: Pteromalidae Termolampa pinicola OO Chalcidoidea: Encyrtidae Copidosoma filicorne 7 O Other Chalcidoidea (damaged) 3 0

Total 1 9 2 23 32 15 16

* Facultative hyperparasitoid. ** Obligatory hyperparasitoid. # Abbreviations: Cntr — centre, Marg — margins, Inter — intermediate zone, Marg+Lagg — margins and Iagg ecotone.

The stenotopic tyrphobiontic species of leaf microclimatic gradient. On the contrary, the spinning Lepidoptera were mostly associated stenotopic species spectra ofLepidoptera ofboth with shrubs of V. uliginosum near the centre ofthe bog centres were very similar, but very different investigated bogs, while tyrphoneutral taxa were in bog margins (Fig. lb). The gradient is charac- distributed in the margins ofthe bog habitat. Spe- terised by the near ground temperatures which cies spectra ofparasitoids recorded from bog cen- were extremely low near the bog centres and tres and bog margins were irregularly dispersed gradually increasing to the bog margins, e. g. the (Fig. la), so that only few species were present in minimum temperatures in July—August reach of- two or more investigated habitats along the ten —4°C near the centres (margins —2°C at the 248 Logan er of. a ENTOMOL.

ML centre

CS centre

ML intermediate

ML margin

ML lagg

CS margin + lagg

1.8 1.8 2.0 2.2 2.4 2.8 2.8

ML centre . Fig. ’l. Similarities (pres- enceuabsence data, sin- CS centre . gle linkage, Euclidean dis" tance) of different parts, Ml. intermediate . from centres to margins (including inner mar- of luh Ml... margin ginsxlagg), Mrtvy (Ml...) and Chalupska slat’ (CS) peat bogs. m a. Para" CS margin + lagg sitoids (number of species and morphospecies) of Ml. lagg leaf-spinning moths. m b. Leaf spinning moth com munities; data from 1.6 1.8 2.0 2.2 2.4 2.8 2.8 Spltzer et ai. (2003). same time period) (for basic temperature data of Teophoridae, Tortricidae. Pyrahdae) (Belokobyi- the bog sites see Spitzer er al. 2003). ski]? & Tobias 1998).

Hormius Simflis Széphgefi, 1896 Tdiobiont ectoparasitoid, very close to previous The data below have been summarized in Table 2, species sharing, probably, same habitat require- accompanied by the geographic ranges of the ments and host range (Belokobyiskij & Tobias parasitoid species. 1998)

Oncophanes minums (Wesmael. 1838) 4.1.. Pfil ary parasi‘mids idiobiont ectoparasitoid of Lepidoptera. The pan- rasitism on Bostri— 41.]. [Chneumonoidea Coieoptera (Cerambycidae, chidae) and. Hymenoptera, Symphyta (Tenthredim Braconidae nidae) is not counted and require continuation (Belokobyiskij & Tobias 1998,, Diaconu & Lozan Hormius monflmms (Nees, 1811) 2000) Tdiobiont ectoparasitoid of Lepidoptera (cg. Com ENTOMOL. FENNICA Vol. 21 ° Parasitoids ofleafspinning moths 249

Bracon erraticus (Wesmael, 1838) a wide spectrum of only Lepidoptera (Aeschli- Idiobiont ectoparasitoid covering a wide spec- mann 1975). trum ofhosts, mainly among Lepidoptera (Tortri- cidae, Geometridae, Gelechiidae etc.) (Tobias Glypta ceratites Gravenhorst, 1829 1986). The species is both morphologically and Solitary koinobiont endoparasitoid of a wide ecologically very variable (or there are several spectrum of Lepidoptera (Aubert 1978). species in fact), so parasitism on Coleoptera (Chrysomelidae), Diptera (Tephritidae) and Hy- Glypta sp. menoptera (phytophagous taxa of Eurytomidae) Members of the genus Glypta are koinobiont en- is not excluded. doparasitoids covering a wide spectrum ofmicro- lepidopteran hosts living in concealment (Tortri- Charmon extensor (Linnaeus, 1758) cidae, Gelechiidae, Geometridae etc.) or other Larval koinobiont endoparasitoid covering a wi- Lepidoptera (Lasiocampidae, Lymantriidae, Ly- de spectrum ofLepidoptera hosts (typically from caenidae etc.). There are records of their parasi- families Gelechiidae, Geometridae, Tortricidae, tism on other insect orders as Hymenoptera- Yponomeutidae etc.) (Billups 1897, Achterberg Symphyta (Cephidae, Diprionidae) and Coleop- 1979, Belokobylskij & Tobias 1998). Parasitism tera (Cerambycidae, Scarabaeidae, Curculioni- on Coleoptera (Cerambycidae, Bostrichidae) dae) (Dasch 1988), however these require confir- and/or Hymenoptera, Symphyta (Tenthredini- mation. dae) require confirmation. Exochus tardigradus Gravenhorst, 1829 Meteorus ictericus (Nees, 181 1) Host unknown. Members ofthe metopiine genus Solitary koinobiont larval endoparasitoid cove- Exochus are primary koinobiont larval-pupal en- ring a wide spectrum ofLepidoptera (Huddleston doparasitoids of a wide range of microlepidopte— 1980, Tobias 1986). A record on a diprionid saw- rous larvae in leaf rolls or similar situations (Ge- fly requires confirmation. lechiidae, Tortricidae, Geometridae, Yponomeu- tidae etc.) (Gauld 2002, Tolkanitz 2007). Records Meteorus colon (Haliday, 1835) on Coleoptera and Hymenoptera—Symphyta Solitary koinobiont larval endoparasitoid of Le- (Tenthredinidae) are probably erroneous. pidoptera (Huddleston 1980, Tobias 1986). Tranosema carbonellum (Thomson, 1887). Earinus gloriatorius (Panzer, 1809) Mentioned as koinobiont endoparasitoid of saw- Solitary koinobiont endoparasitoid of Lepidop- fly Arge pagana Panzer (Argidae) by Hedwig tera (Nixon 1986). (1939). This is the first record ofthis species from Lepidoptera. Members ofthe genus are generally Orgilus pimpinellae Niezabitowski, 1910 known as endoparasitoids ofvarious small Lepi- Solitary koinobiont larval endoparasitoid of ma- doptera, especially the family Tortricidae. ny Lepidoptera (Taeger 1988, Belokobylskij & Tobias 1998). Campoletis sp. and Campoplex spp. (three unidentified species). Ascogaster bidentula Wesmael, 1835 Members of these Campopleginae genera are Solitary koinobiont egg-larval endoparasitoid of known as primary koinobiont larval (rarely lar- only Lepidoptera (typically families Geometri- val-pupal) parasitoids ofsmall and medium-sized dae and Tortricidae) (Huddleston 1984, Tobias Lepidoptera of various families (Townes 1969, 1986) Kasparyan 1981, Gauld 1991, Shaw & Aeschli- mann 1994, Wagener et al. 2006). Records of Ichneumonidae their parasitism on other insect groups (Coleop- tera) and/or their hyperparasitism on other Ich- Chorinaeusfunebris (Gravenhorst, 1829) neumonidae require confirmation (Townes Larval-pupal koinobiont endoparasitoid covering 1945) 250 Lozan et al. ° ENTOMOL. FENNICA Vol. 21

4.1.2. Chalcidoidea 4.3. Obligatory hyperparasitoids

Eulophidae Ichneumonoidea: lchneumonidae Mesochorus spp. (two unidentified species). Elachertus artaeus (Walker, 1839) Members ofthis large genus are endoparasitic hy- Gregarious ectoparasitoid ofvarious Lepidoptera perparasitoids of either Hymenoptera (e. g. para- (Gelechiidae, Gracillariidae, Noctuidae, Noto- sitoids of the families Braconidae, lchneumoni- dontidae, Tortricidae), attacking larvae of free- dae) or tachinid parasitoids (Diptera: Tachinidae) moving leafspinning/rollers, or larvae ofleaf-mi- (Wahl 1993, Schwenke 1999). ners which spin cocoons in their last stage often by rolling the edge of the leaf (Boucek & Askew 1968, Noyes 2003). 5. Discussion

Pteromalidae 5.1. Parasitoid diversity

Termolampa pinicola Boucek, 1961 Parasitoids in our samples can be classified as Known as a primary parasitoid ofRetinia resinel— shown in Table 3. The members of the family la (L.) (Lepidoptera, Tortricidae) on Pinus thun— Braconidae were the most numerous and they bergz'z' (Parl.) and Pinus sp. (Noyes 2003). Our re- were only primary parasitoids. The lchneumo- sults show this species is probably associated nidae were twice less numerous than the Braco- with a tortricid or gelechiid moth other than the nidae and were more diversified, e.g. primary and only known host, which can be considered a new secondary (obligatory and facultative) parasi- host record. The species is therefore likely to be at toids. Identified species of Chalcidoidea (Ptero- least oligophagous. malidae, Encyrtidae and Eulophidae) were all reported as primary parasitoids. For the list of spe- Encyrtidae cies see Table 2. Primary parasitoids of families Braconidae Copidosomafilicome (Dalman, 1820) and lchneumonidae can be classified as poly- Egg-larval endoparasitoid, one of the most com- phagous species associated with various Lepi- mon species of the genus in Europe with a relati- doptera (except probably Bracon erraticus, vely narrow host spectrum, limited to the families which in literature is also recorded from other in- Gelechiidae and Tortricidae (Lepidoptera) (Gu- sect orders (see below)). Primary parasitoids of errieri & Noyes 2005). family Chalcidoidea are often more niche-specific than taxon-specific, with a moderate host range of biologically similar host taxa belonging 4.2. Facultative hyperparasitoids to a more or less large taxonomic range (Askew & Shaw 1986, Lawton 1986). Ichneumonoidea: lchneumonidae The only one facultative hyperparasitoid species (Itoplectis tunetana, lchneumonidae) is not Itoplectis tunetana (Schmiedeknecht, 1914) very habitat selective and generally polyphagous, Primary parasitoids of various Lepidoptera with wide geographic range. The obligatory (Acrolepiidae, Choreutidae, Gelechiidae, Plutel- ichneumonid hyperparasitoids of the genus Me— lidae, Tortricidae, Yponomeutidae) and hyperpa- sochorus attack probably a series of other pri- rasitoids of other parasitoid Hymenoptera (Bra- mary parasitoids, e.g. among parasitoid Hyme- conidae: Aleiodes rossz'cus) (Kasparyan 1981). noptera and Diptera (Wahl 1993). Although hyperparasitic intraguild strategy frequently oc- curs in parasitoid Hymenoptera, it is difficult to reveal and detect such connections in the field samples. The multitrophic parasitism in our samples is undoubtedly only a small part of the ENTOMOL. FENNICA Vol. 21 ° Parasitoids ofleafspinning moths 251 intrinsic and almost unknown parasitoid food (Taeger 1988), consistently with our samples. All web of peat bogs. these species of Lepidoptera and Hymenoptera Most parasitoid species recorded in this study (Braconidae) were represented in our samples are considered to be widely distributed in the Pa- and were also encountered during our previous laearctic (except Earz'nus gloriatorius, recorded studies in the investigated bog sites (e.g. Lozan recently only from Europe) and several species 2002, Spitzer et al. 2003, Bezdek et al. 2006). with almost cosmopolitan range (some taxa intro- Many of the obtained parasitoids are known duced). All such species seem to be characteristic also as true bioregulators operating in orchards in various biotopes, including peatlands, but hav- and forests (Oncophanes minutus, Charmon ing no specific requirements to bog habitats. extensor, genus Meteorus etc.), and some oftheir A huge amount ofhost records has thoroughly potential tyrphoneutral hosts were abundant in been analysed (for example, Taxapad) in order to the investigated peat bogs. be able to assess the real host range and distribution of each parasitoid species we managed to identify in our samples. However, many pub- 6. Conclusions lished records of parasitism on a large spectrum of lepidopteran families and/or on other insects In the two isolated central European peat bogs than Lepidoptera (such as Hymenoptera-Sym- studied here, the diversity of parasitoids (super- phyta (Tenthredinidae, Cephidae, Diprionidae) families Ichneumonoidea and Chalcidoidea) is and Coleoptera (Cerambycidae, Scarabaeidae, slightly higher compared with their lepidopteran Curculionidae etc.)) might be wrong and, at mini- hosts. The overall “tyrpho-association” of both mum, all these published connections would re- leaf-spinning Lepidoptera and their potential quire confirmation. Ultimately, only a number of parasitoids (Ichneumonoidea + Chalcidoidea) more limited and more reliable sources were con- represents: sidered, by judging the host ranges as a context that has reasonable boundaries (e.g. ‘generalist’ a) 19 species of Lepidoptera, of which seven versus ‘specialist’ parasitoid, see Shaw 1994) and stenotopic taxa (tyrphobionts+tyrphophiles) by using data from taxonomic collections that we and 12 tyrphoneutrals (cf. Spitzer et al. 2003, managed to examine elsewhere (see also Ac- Spitzer & Danks 2006); knowledgements). b) 25 species ofmultitrophic parasitoids; none of the identified species was a bog stenotopic taxon, therefore, all of them are tyrpho- 5.2. Association with bog Lepidoptera neutrals (eurytopic components of various ecosystems). It was really difficult to reveal the precise relationships of emerged parasitoids to the reared Associated with peat bogs, there are a few known host(s) in our leaf spinning samples. The braco- stenotopic taxa among Braconidae (Lozan & nid endoparasitoid Charmon extensor, which at- Tobias 2002, Lozan et al. in press) and Ichneu- tacks a large spectrum of insects throughout the monidae (Tereshkin 1996) so far. However, none world, is known from a strictly tyrphophilous of them matched our data of rearings from leaf tortricid moth Aclerl's maccana (Billups 1897). spinnings. Investigations of parasitoid Hyme- The same host species is recorded for a poly- noptera associated only with peat bogs were gen- phagous endoparasitoid braconid, Meteorus erally neglected and not many data are available ictericus, which is a widely distributed species (cf. Krogerus 1960, Spitzer & Danks 2006). not only in the Palaearctic region. Another braco- The ability of parasitoids (including multi- nid endoparasitoid, Orgiluspimpinellae, which is trophic levels) to populate a wide range of habi- Lepidoptera host oriented and widely distributed tats and hosts (i.e. eurytopy) contrasts with that of in the Palaearctic, has been recorded from the stenotopic leaf-spinning Lepidoptera species. tyrphobiontic gelechiid moth Athripspruinosella The historical patterns ofevolution ofparasitoids associated with the host plant V. ulz'ginosum are more important determinants than current 252 Lozan et al. ° ENTOMOL. FENNICA Vol. 21 ecological characteristics in an ‘isolated habitat’, Askew, R. R. & Shaw, M. 1986: Parasitoid communities: their size, structure and development. 7 In: Waage, J. which reflects a certain degree of environmental & Greathead, D. (eds), Insect Parasitoids: 2257264. tolerance (cf Hawkins 1994, Hawkins & Mills Academic Press, San Diego. 389 pp. 1996, Tschamtke et al. 2002). It may also suggest Aubert, J. F. 1978: Les Ichneumonides ouest—palearctiques that any single perturbation in the peat bog envi- et leurs hotes 2. Banchinae et Suppl. aux Pimplinae. 7 ronment might shift the host-parasitoid evolu- Laboratoire d’Evolution des Etres Organises, Paris & Echauffour. 318 tionary relationships not in favour ofLepidoptera EDIFAT-OPIDA, pp. Belokobylskij, S. A. & Tobias, V. I. 1998: Family Braconi— hosts which seem to be much more habitat de- dae. 7 In: Lehr, P. A. (ed.), Key ofthe Insect ofRussi— “relict” than pendent (often cold—adapted taxa) an Far East (Neuropteroidea, Mecoptera, Hymenopte— their opportunistic parasitoids (Spitzer & Danks ra) 4(3). Dal’nauka, Vladivostok. 708 pp. [In Rus— 2006). All parasitoids are therefore only eury- sian.] S. A. & Tobias V. I. 2000: Braconi— taxa when with the steno- Belokobylskij Family

topic compared 7 dae. In: Lehr P. A. (ed.), Key ofthe Insect ofRussi— combination of topic+eurytopic leaf-spinning an Far East (Neuropteroidea, Mecoptera, Hymenopte— hosts. From the conservation Lepidoptera point ra) 4(4). Dal’nauka, Vladivostok. 651 pp. [In Rus— ofview, the complex ofthe isolated peat bog hab- sian.] J. & K. 2006: distribu— itats, hydrological conditions and the very spe- Bezdék, A., Jaros, Spitzer, Spatial tion of ground beetles (Coleoptera: Carabidae) and cific local micro- and mesoclimate might prevent moths (Lepidoptera) in the Mrtvy luh bog, Sumava the potential impact of the population outbreak Mts (Central Europe): a test ofhabitat island commu- or/and invasion of common opportunistic nity. 7 Biodiversity and Conservation 15: 3957109. parasitoids unless human and climatic impacts Billups, T. R. 1897: Additional notes on the hymenopte- are excluded. rous and dipterous parasites, bred by members of the South London Entomological and Natural History So- ciety during the years 1891 and 1892. 7 Proceedings Acknowledgements. Field and laboratory studies (rearing, of the South London Entomological and Natural His- identification, habitat comparative analysis) were sup— tory Society 1896: 80787. ported by the Czech Academy of Sciences (Grant Boucek, Z. & Askew, R. R. 1968: Palaearctic Eulophidae 1QS500070505) and partially by the EU Synthesys (grant sine Tetrastichinae. Index of Entomophagous Insects. GB-TAF-4159) and European Science Foundation 7 In: Delucchi, V. & Remaudicre, G. (eds), Index of (BEPAR Grant Nr. 1667). We thank D. R. Kasparyan, V. I. Entomophagous Insects 3. Le Francois, Paris. 254 pp. Tobias and S. A. Belokobylskij (Zoological Institute, Saint Boucek, Z. & Rasplus J. Y. 1991: Illustrated Key to West— Petersburg) for identification of some Ichneumonidae and Palaearctic Genera of Pteromalidae, Hymenoptera allowance of Braconidae collection; G. Broad (Natural Chalcidoidea. 7 INRA Editions, Paris. 140 pp. History Museum, London) and C. van Achterberg (Natio— Dasch, C. E. 1988: Ichneumon—flies of America north of naal Natuurhistorisch Museum, Leiden) for the access to Mexico: 10. Subfamily Banchinae, tribe Glyptini. 7 the Braconidae collections; our technical assistant H. Memoirs ofthe American Entomological Institute 43: Zikmundova (Biology Centre, Ceske’ Budéj ovice) who 17644. helped us with laboratory rearing ofboth Lepidoptera and Diaconu, A. & Lozan, A. 2000: Ectoparasitoid braconids Hymenoptera. We are thankful to Mark Shaw for his help- (Hym.: Braconidae) of certain species of leafrollers fill comments and valuable suggestions on early draft of (Lep.: Tortricidae) of fruit trees. 7 Mitteilungen der the MS. Last but not least we are grateful to the two anony- Schweizerischen Entomologischen Gesellschaft 73: mous reviewers for their useful comments. 571 1.

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