JOURNAL OF FOREST SCIENCE, 55, 2009 (12): 578–590

How do lepidopteran seasonal guilds differ on some (Quercus spp.) – A case study

† M. Turčáni1, J. Patočka1 , M. Kulfan2

1 Faculty of Forestry and Wood Sciences, Czech University of Life Sciences in Prague, Prague, Czech Republic 2Department of Zoology, Comenius University, Mlynská dolina, Bratislava, Slovakia

Abstract: The differences between lepidopteran communities were studied in Slovakia in 1993 and 1994. Sampling was undertaken between April and October on 3 oak species (Quercus robur, Q. petraea, Q. rubra). Biologi- cal traits of larvae were examined in order to explain differences in seasonal guilds among oaks. Communities varied in structure and abundance. Species richness in four seasonal guilds (flush, late spring, summer and autumn feeders) had a similar pattern on each of the studied oak species. The guild of flush feeders had the richest species assemblage, followed by the late spring feeder guild and both guilds were significantly richer than the summer feeder guild and autumn feeder guild.

Keywords: lepidopteran larvae communities; Slovakia; oaks; seasonal guilds

Oaks (Quercus spp.) are represented in Slovakia dant defoliators: Lymantria dispar, Operophtera (Central Europe) by eight native and one introduced brumata, Erannis defoliaria, Tortrix viridana, Aleim- species; they are distributed in the warmest part ma loeflingiana, Archips xylosteana and several of the country from an altitude of about 100 m up others. The occurrence of outbreaks was used as an to 1,000 m a.s.l. More than 250 lepidopteran spe- indicator of habitat preference (the outbreak is de- cies have been recorded feeding on Quercus spp. fined as an increase in abundance to an extent where (Patočka 1980; Patočka et al. 1999). feeding causes visible defoliation, usually heavier The life history traits of in Central than 30–40%). The role of other species as elements Europe and basic information about the species in forest ecosystems, the relationships among spe- habitat preferences are relatively well known. Habitat cies, and their formation into guilds on various oak preferences and community structure of Lepidoptera species have remained speculative. in Slovakia were studied earlier by Patočka (1980) Patočka (1954) divided the lepidopteran species and Patočka et al. (1962, 1999) and Stolina et al. on oaks in Slovakia into four seasonal guilds. The (1985), but their assessment relied mainly on direct first was from budburst till the beginning/middle observations and qualitative characteristics rather of June. It is estimated that 80–90% of the total than on quantitative statistical analyses. Habitat number of caterpillar species recorded on oaks is preference was simplified and expressed by “forest present at that time. The caterpillars in this guild types” (units of forest ) – areas where the overwinter as larvae or eggs or hatch from those laid ecological optima of these species were found. These in early spring. The second guild mainly consists of studies showed habitat preferences of the most abun- leaf miners (Stigmella spp., Phyllonorycter spp. and

Supported by the Ministry of Agriculture of the Czech Republic, project No. QH 71094 The use of dendrochronology in the reconstruction of fluctuation cycles of nun and gypsy in Central Europe.

578 J. FOR. SCI., 55, 2009 (12): 578–590 Table 1. Number of species, number of specimens and seasonal diversity and evenness of Lepidoptera collected at four sites in 1993 and 1994

Site 4 Site 1 Site 2 Site 3 Site/host tree (Q. rubra) (Q. petraea) (Q. robur 1) (Q. robur 2) Year of study 1993 1994 1993 1994 1993 1994 1993 1994 Number of species 15 25 29 43 46 57 56 67 Number of specimens 23 44 87 139 216 372 264 347 Maximum seasonal diversity 1.9 2.4 1.7 2.2 2.2 2.7 2.6 2.9 (Shannon-Weaver index) Maximum seasonal evenness 1.00 1.00 0.96 0.97 0.97 0.98 0.97 0.98 (Pielou’s index)

Tischeria spp. and also some smaller free feeders like (2) To analyze the similarity of seasonal guilds at Cyclophora spp.). Some larger species from the first various sites represented by different oaks. guild like L. dispar, Orthosia spp. or Biston stratarius often complete their development at this time. The Study sites and methods third guild occurs in August–September. It consists partially of the second generation of the first guild A dataset was collected during May to Octo- for example Pandemis spp., Cyclophora spp. and ber in 1993 and 1994. Samples were taken every Pseudoips prasinanus. Finally, the fourth guild (Oc- 20 days (nine times per season, the last sampling tober–November) consists of the second flight pe- was excluded from statistical assessment due to riod of leaf miners in the genera Stigmella, Tischeria the zero number of larvae in almost all samples) and Phyllonorycter and the mostly univoltine genus using a beating tray (25 beatings per sample). There Ectoedemia. Recent studies of Kulfan et al. (1997) were nine sample intervals each year. Sampling and Kulfan and Degma (1999) showed that species started on 30 April, 7–10 days after budburst, and diversity and evenness differed significantly between finished on 7 October in both years. Branches at oak species and time of the year. eye height, about 1 m in length, were beaten dur- Our effort was focused on understanding the ing each sampling period. Approximately 99.5% of mechanisms that explain variance in lepidopteran 1,518 collected larvae were identified in situ to the communities in various seasonal guilds on different species level; others were identified after rearing in oaks. The main study goals were: a laboratory to the adult stage. Gerasimov (1952) (1) To investigate patterns of lepidopteran commu- and Patočka (1954, 1980) were used as identifica- nities on three oak species across a year; tion references. A systematic list of species includ-

Miles km

Fig. 1. Location of the forest complex and individual study sites

J. FOR. SCI., 55, 2009 (12): 578–590 579 ing selected life history traits can be found in the The species were divided into seasonal guilds by Appendix (Table 1A). determining when they were most abundant. Poly- The study area in Western Slovakia was between voltine species were sorted into seasonal groups 48°25' and 48°30'N and 17°09' and 17°11'E (Fig. 1). based on the time when the most abundant genera- Four sites were selected representing two stands of tion was found. For example a bivoltine species was Q. robur, one stand of Q. petraea and one of Q. rubra, treated as a summer feeder if its individuals were all plots were in the same vicinity. The maximum found only in the summer generation during our distance between any two sites was about 2 km. study. Seasonal guilds were usually well defined. Site 1 (Q. petraea): A 25 years old artificially Only in the case of late spring feeders (LSF) there planted stand of Q. petraea. Planted in dense rows were two subgroups: and surrounded by Scotch pine (Pinus sylvestris). (a) Flush feeders (FlF) that continued feeding in Sparse understorey. Site elevation about 160 m. The June; site represents the plant association Querco-Pinetum (b) species that started feeding in June. Kripel 1965. The former subgroup was included in the group Site 2 (Q. robur 1): A natural close growing of late spring feeders because they feed mainly on hardwood plain forest with the dominant species developed and mature leaves. Q. robur. The site was located in the vicinity of the The classification of the species was as follows: Moravia River. The age of trees was estimated to FlF – species present as larvae that overwintered or be about 100 years. Site elevation 150 m. The stand just hatched. These species were in synchrony with represents the plant association Fraxino-Ulmetum- budburst and were feeding almost exclusively on Quercetosum Somsak 1959. new foliage from the end of April to the end of May Site 3 (Q. robur 2): Similar to the previous site and and the beginning of June; LSF – species feeding forming a fringe of Q. robur stands along a culti- mainly on developed and recently matured foliage vated area. The age of the trees was estimated to be (usually the end of May up to the end of June and 120 years. Site elevation 160 m. The site represents the beginning of July); summer feeders (SF) – feed- the plant association Frangulo-alni-Quercetum ing on mature leaves at the beginning of July to the Michalko 1989. Both Q. robur stands had rich un- beginning of August; and autumn feeders (AF) – this derstorey vegetation. group hatched in the second half of August and the Site 4 (Q. rubra): The introducedQ. rubra is plant- beginning of September and was feeding on the ed among stands of Scotch pine. The site represents toughest leaves. the plant association Querco-Pinetum Kripel 1965. Leaf-mining Lepidoptera were excluded from this Results study as only free-living species sensitive to sampling using a beating tray were collected. The number of species and individuals varied In statistical analyses we summarized the number considerably between sites and years. Quercus rubra of individuals in each family to determine if there had the lowest number of species and individual were any visual differences in the host preference. specimens followed by Q. petraea with the richest We also calculated diversity (Shannon-Weaver in- communities being found on Q. robur (Table 1). The dex) and evenness (Pielou’s index) of Lepidoptera total number of larvae on Q. rubra was 23 in 1993 larvae on each site. Then we separated species into vs. 44 in 1994, on Q. petraea 87 in 1993 vs. 139 in four seasonal guilds and tested the differences in the 1994 and on Q. robur 216 and 372 in 1993 and 372 number of species and individuals in guilds. This and 347 in 1994. On Q. rubra and Q. robur the maxi- was done separately for each oak to compare if the mum species diversity was found in spring and on pattern was similar. To test differences, matrixes of Q. petraea in early spring or late spring, respectively. presence/absence (species) or abundance (individu- The evenness was quite stable at all sites. als) were constructed. The sum from two samplings A comparison of larval abundance classified into entered the analysis for each guild. All species in families showed the absence (Psychidae, Tineidae, each guild were entered into the matrix separately, Bucculatricidae, Gracillaridae, Ypsolophidae, Oeco- where the rows were species and the columns indi- phoridae) or scarcity () of smaller cated the presence/absence of species or number species on Q. rubra and low numbers on Q. petraea of individuals. Data were transformed as log (x + 1) in both years (Figs. 2a,b). The Geometridae were prior to analysis. ANOVA was performed to evaluate the most abundant family in both years of study, differences among seasonal guilds. This was done followed by Lymantriidae in 1993 and Noctuidae in separately for each tree species. 1994. Only species of the families Coleophoridae,

580 J. FOR. SCI., 55, 2009 (12): 578–590 (a) Q.Q. petrea petraea Q.Q. robur robur 1 1 Q.Q. robur robur 2 2 Q.Q. rubrarubra 100

10

No. of individuals 1 Number of individuals

0.1 Tineidae Pyralidae Tineidae Psychidae Pyralidae Noctuidae Psychidae Noctuidae Lycaenidae Tortricidae Drepanidae Gelechiidae Lycaenidae Tortricidae Gelechiidae Drepanidae Limacodidae Gracillaridae Geometridae Lymantriidae Geometridae Ypsolophidae Limacodidae Ypsolophidae Notodontidae Gracillaridae Lymantriidae Notodontidae Oecophoridae Oecophoridae Coleophoridae Coleophoridae Lasiocampidae Lasiocampidae (b) Bucculatricidae Bucculatricidae Q. petrea Q. robur 1 Q. robur 2 Q. rubra 1,0001000100 Q.Q. petrea petraea Q.Q. robur robur 1 1 Q.Q. robur robur 2 2 Q.Q. rubra rubra

100 10

10

No. of individuals 1 Number of individuals Number of individuals 1

0.1 Tineidae Pyralidae Tineidae Psychidae Noctuidae Pyralidae Tineidae Tortricidae Lycaenidae Psychidae Drepanidae Gelechiidae Pyralidae Noctuidae Psychidae Geometridae Limacodidae Noctuidae Lycaenidae Tortricidae Lymantriidae Ypsolophidae Notodontidae Gracillaridae Drepanidae Gelechiidae Oecophoridae Lycaenidae Tortricidae Gelechiidae Drepanidae Coleophoridae Lasiocampidae Limacodidae Gracillaridae Bucculatricidae Geometridae Lymantriidae Geometridae Ypsolophidae Limacodidae Ypsolophidae Gracillaridae Notodontidae Lymantriidae Notodontidae Oecophoridae Oecophoridae Coleophoridae Coleophoridae Lasiocampidae Lasiocampidae Bucculatricidae Bucculatricidae

Fig. 2. Comparison of larval abundance per family at 4 sites in 1993 (a) and in 1994 (b)

Gelechiidae, Tortricidae, Lycaenidae, Geometridae, Q. rubra (only Teleoides paripunctellus and Pande- Lymantriidae and Noctuidae were found on Q. rubra mis corylana were found in 1993). T. paripunctellus during this study. Lycaenidae, Geometridae, Noto- spins two leaves together and feeds on the internal dontidae, Lymantriidae and Noctuidae represent epidermis + mesophyll, the external epidermis larger Lepidoptera (pupa 10 to 30 mm in length) remains untouched. P. corylana spins together which are generally widely polyphagous (Patočka, several leaves and is more abundant on Q. robur, Turčáni 2005). which has leaves arranged in clusters. In 1994, Coleophoridae, Gelechiidae and Tortricidae single individuals of ibipennella and represent small Lepidoptera which are much more C. lutipennella were found on Q. rubra but they sensitive to food quality and foliage architecture were more abundant on other oak species. several because of their size and feeding strategies. Indi- polyphagous tortricid species were also found on viduals from these families were generally absent on Q. rubra that year.

J. FOR. SCI., 55, 2009 (12): 578–590 581 4–6 6–7 5–6 3–4 5–6 6–7 7–8 7–9 7–9 7–9 6–10 9–12 (mm) 14–17 10–14 Pupa length bivoltine bivoltine Voltinism univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine l998) polyvoltine uni- to polyvoltineuni- to Laštůvka Feeding strategyFeeding sac/case bearing sac/case bearing sac/case bearing sac/case bearing galleries early stagesminer only at conical spun leaf later miner, free living free living spun leafs spun leafs spun leafs early stagesminer from sac at only early stagesminer from sac at only no no no no no no no no no no no no no no Ballooning group Fagus Fagus , Q. pubescens spp. Fagus sylvatica Fagus Castanea sativa Quercus spp., spp. spp., mainly spp. spp. s spp., mosses, and algae lichens Host specificity polyphagous mosses, lichens, algae polyphagous material organic Quercus sylvatica Quercus Quercus Fagaceae, Quercu broadleaf woody plants, polyphagous broadleaf woody plants, polyphagous Quercus Quercus , 1775) , 1775) , 1775) , 1849 , 1775) , 1783) , 1848 , 1759) , 1761) , 1839) & SCHIFFERMUELLER eller & SCHIFFERMUELLER oeze & SCHIFFERMUELLER Z

G , 1767) eller ( oda enis lerck abricius Z P

enis eller F D C ( enis D ( Z ( ( D ( ( ( allas P ( sp. ecophoridae himabacchidae psolophidae Y O C B ucculatricidae C oleophoridae Table 1A. species list A systematic of the recorded duringwith a short study this descriptionTable of life-history to traits system (the according Taxon Psychidae hirsutaCanephora Dahlica Proutia betulina Psyche casta Tineidae sp. Tineidae Bucculatrix ulmella Gracillariidae Gracillariidae sp. alpella Ypsolopha Ypsolopha ustella Ypsolopha Carcina quercana Diurnea fagella Diurnea lipsiella Coleophora ibipennella Coleophora kuehnella

582 J. FOR. SCI., 55, 2009 (12): 578–590 12 7–9 4–6 4–5 4–6 8–9 7–9 7–8 7–9 8–9 8–12 9–10 8–10 (mm) 10–13 11–14 13–17 11–14 11–14 12–15 Pupa length bivoltine Voltinism univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine occasionally mostly bivoltine mostly bivoltine uni- to bivoltine uni- to bivoltine uni- to Feeding strategyFeeding miner from sac spun leaves, skeletonize spun leaves, skeletonize spun leaves, skeletonize free living, young skeletonize spun leaves, leaf fold margin spun leaves spun leaves, as skeletonize young spun leaves spun leaves spun leaves spun leaves transversely rolled leaf spun leaves spun leaves leavesspun apical spun leaves buds, spun shoots spun leaves, sometimes entomophagous no no no no no no no no no no no no no no no no no no no Ballooning

.

spp and other and other uercus uercus Q. pubescens spp. mainly and spp. Quercus Betula sylvatica Fagus Q. robur Q. pubescensQ. petraea and Carpinus betulus spp. spp., spp. spp. spp., spp., spp., spp., spp. agaceae g. sp., Corylaceae g. sp. etc. f mainly mainly broadleaf woody species Host specificity Quercus Quercus Quercus Quercus Quercus Quercus Quercus Quercus broadleaf trees, polyphagous on broadleaf trees polyphagous on broadleaf woody plants polyphagous on broadleaf woody plants polyphagous on broadleaf trees, occasionally coniferous polyphagous on broadleaf trees sometimes broadleaf on polyphagous Q often plants, woody coniferous polyphagous on broadleaf woody plants broadleaf trees and shrubs Quercus , 1775) , 1775) , 1775) , 1775) , 1775) , 1764) , 1794) , 1758) , 1758) ller , 1838) , 1812) , 1794) , 1794) , 1766) , 1759) & SCHIFFERMUELLER , 1786) , 1813) , 1758) Mü , 1758 ( & SCHIFFERMUELLER & SCHIFFERMUELLER hunberg eller & SCHIFFERMUELLER innaeus & SCHIFFERMUELLER enis T Z ( L bner innaeus bner ( lerck D ( enis ( aworth L abricius C enis enis abricius ( D F H ( Hü Hü ( F ufnagel enis D ( D innaeus ( ( ( ( ( innaeus ( H D L ( L ( (

imacodidae Taxon Taxon Coleophora lutipennella Gelechiidae paripunctellus Teleiodes luculellus Teleiodes decorellus Teleiodes Apoda limacodes Tortricidae viridana Tortrix loeflingiana Aleimma ferruganaAcleris alternellus Tortricodes Exapate congelatella ministrana Eulia Ptycholoma lecheanum xylosteana Archips Choristoneura hebenstreitela corylanaPandemis Table 1A to be 1A to continued Table cerasana Pandemis heparana Pandemis ocellana Spilonota isertanaZeiraphera L

J. FOR. SCI., 55, 2009 (12): 578–590 583 6–8 7–9 7–8 9–10 8–10 9–10 9–10 8–12 (mm) 10–12 20–25 12–16 12–16 12–14 22–26 12–16 13–17 14–17 18–23 18–24 Pupa length bivoltine Voltinism univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine polyvoltine polyvoltine mostly bivoltine uni- or bivoltine uni- or bivoltine mostly univoltine longitudinally folded leaf galleriesinternal nest web nest web nest web nest web nest web free living free living free living free living free living, as skeletonize young free living, as skeletonize young free living free living, as skeletonize young free living free living, free living free living, as skeletonize young Feeding strategyFeeding no no no no no no no no no no no no no no no yes yes yes Ballooning probably no probably . spp Quercus Q. pubescens and Quercus Q. cerris Fagus sylvatica Fagus spp. – galls of Cynipidae spp. spp. spp. , prefers spp. spp. spp. spp., broadleaf spp. and other trees Fagaceae, especiallyFagaceae, Quercus Quercus Quercus Quercus Quercus Quercus often species, woody broadleaf polyphagous on broadleaf trees Quercus Quercus polyphagous on woody species Quercus broadleaf woody species polyphagous polyphagous on broadleaf trees polyphagous on broadleaf trees Quercus polyphagous on broadleaf trees, sometimes herbs Host specificity , 1775) , , 1775) , 1775) , 1775) , 1859) , 1798) , 1810) , 1758) , 1767) , 1758) , 1767) , 1767) , 1799) , 1813) , 1845) & SCHIFFERMUELLER & e , 1761) & SCHIFFERMUELLER , 1767) bner é , 1758) & SCHIFFERMUELLER , 1818) enis bner erneburg bner Hü abricius enis & SCHIFFERMUELLER D ( uen F W ( D enis innaeus innaeus ( ufnagel G Hü Hü ( ufnagel ( innaeus L ( L D ( ( H ( ( L ( H ( innaeus enis ( ( L ufnagel innaeus incken D ( ( L Z H (

( (

repanidae eozephyrus quercus asiocampidae ycaenidae Table 1A to be 1A to continued Table L D L N Pammene albuginana Pammene Pyralidae Elegia similella Phycita roborella repandana Conobathra tumidana Conobathra consociella Acrobasis tremulifolia Phyllodesma Poecilocampa populi binaria Watsonalla Geometridae Semiothisa alternaria Plagodis dolabraria autumnarius Ennomos Selenia tetralunaria Colotois pennaria pilosaria Apocheima Biston strataria Biston betularia Ancylis mitterbacheriana Ancylis Taxon Taxon

584 J. FOR. SCI., 55, 2009 (12): 578–590 8–9 7–9 5–7 9–12 9–10 (mm) 10–14 10–16 12–16 10–12 14–24 13–18 11–16 10–11 12–15 11–13 11–14 12–13 10–12 24–30 14–16 16–18 Pupa length bivoltine bivoltine Voltinism univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine polyvoltine occasionally uni- or bivoltine uni- or bivoltine uni- or bivoltine uni- or bivoltine uni- or bivoltine mostly univoltine mostly univoltine free living free living free living free living, as skeletonize young free living, as skeletonize young free living, as skeletonize young free living, as skeletonize young free living, as skeletonize young free living, as skeletonize young free living free living free living, as skeletonize young free living, as skeletonize young free living free living free living or spun leaves free living free living, gregariously free living free living free living Feeding strategyFeeding no no no no no no no no no no no no no yes yes yes yes yes yes yes yes Ballooning . spp spp. Betula , spp. Larix Larix Vaccinium Padus avium Padus spp. spp. occasionally Quercus spp., spp., Fagus sylvatica Fagus spp. and Quercus Vaccinium Vaccinium spp., Salicaceae g. sp., Prunus spp. mainly, also broadleaf other spp. mainly, also broadleaf other spp. mainly, spp. spp., rarely spp. mainly spp. mainly, also other broadleaf trees broadleaf other also mainly, spp. Quercus trees Quercus trees Betulaceae g. sp., Quercus Quercus and trees broadleaf on polyphagous polyphagous on broadleaf trees broadleaf trees broadleaf woody species, mainly broadleaf woody species polyphagous on herbs and low woody trees mainly on broadleaf trees broadleaf woody species Quercus sylvatica, Fagus Vaccininum broadleaf woody species polyphagous on broadleaf trees, sometimes and coniferous Quercus polyphagous on broadleaf trees Quercus spp. polyphagous on broadleaf trees Host specificity , 1775) , 1775) , 1775) , 1775) , 1775) , 1775) , 1775) , 1775) , 1767) , 1758) , 1767) , 1763) , 1776) , 1758) , 1857 , 1758) , 1799) , 1758) , 1799) & SCHIFFERMUELLER , 1799) e & SCHIFFERMUELLER & SCHIFFERMUELLER SCHIFFERMUELLER & SCHIFFERMUELLER é

& SCHIFFERMUELLER & SCHIFFERMUELLER , 1759) & enis bner enis enis innaeus bner copoli & SCHIFFERMUELLER innaeus bner D uen enis ufnagel L S enis enis D D L ( abricius ( ( ( G D ( H ( D Hü D innaeus Hü F enis innaeus ( Hü ( lerck ( innaeus ( ( L ( ( L enis D ( L C ( ( ( ( D ( ( otodontidae Agriopis aurantiaria defoliaria Erannis similaria Paradarisa Hypomecis roboraria Hypomecis punctinalis Ectropis crepuscularia Lomographa temerata Campaea margaritata Alsophila aceraria Alsophila aescularia aestivariaHemithea linearia Cyclophora Chloroclysta miata Epirrita dilutata Operophtera brumata Eupithecia dodoneata bucephala Phalera Drymonia dodonaea Ptilodon capucina Table 1A to be 1A to continued Table Taxon Agriopis leucophaearia Agriopis marginaria N

J. FOR. SCI., 55, 2009 (12): 578–590 585 9–12 (mm) 15–18 13–15 16–18 16–22 13–14 11–13 14–17 14–16 14–16 15–18 10–13 13–15 15–17 13–16 16–19 14–15 12–16 18–25 10–13 Pupa length bivoltine Voltinism univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine univoltine occasionally bi- or trivoltine uni- or bivoltine uni- or bivoltine uni- or bivoltine free living free living, as skeletonize young free living free living free living free living free living free living free living free living free living free living, gregariously free living free living free living free living, as skeletonize young free living free living free living nests Feeding strategyFeeding no no no no no no no no no no no no no no no no no no no no Ballooning spp. Vaccinium Vaccinium Salix Fagus sylvatica Fagus spp., Ulmus Ulmus spp., spp. spp. mainly spp. spp. mainly Quercus Quercus polyphagous on woody plants polyphagous on trees polyphagous on broadleaf trees herbs larva: adult mainly oaks trees, broadleaf polyphagous on broadleaf woody plants, herbs broadleaf trees, oaks mainly Quercus polyphagous on broadleaf woody plants broadleaf trees, oaks mainly Quercus polyphagous polyphagous on broadleaf woody plants polyphagous on broadleaf trees broadleaf trees broadleaf woody species polyphagous on woody plants, spp., Rosaceae mainly broadleaf trees, prefers Quercus Host specificity and Rosaceae , 1775) , 1775) , 1775) , 1775) , 1775) , 1758) 1766) , 1758) , 1766) , 1758) , 1776) , 1758) , 1758) & SCHIFFERMUELLER , 1775) , 1803) , 1775) & SCHIFFERMUELLER , 1809) , 1758) & SCHIFFERMUELLER innaeus & SCHIFFERMUELLER , 1778) , 1819) ufnagel innaeus L & SCHIFFERMUELLER enis L H ( ( ufnagel enis D bner ( bner enis innaeus ( H D enis ufnagel L uessly ( D bner innaeus ( enis ( innaeus D ( H Hü F abricius sbeck L Hü ( L D ( F ( ( ( ( ( innaeus ( O ( Hü L ( ( ( octuidae ymantriidae N L Spatalia argentina alpium Moma psi Acronicta pyramidea Amphipyra Cosmia trapezina Agrochola laevis transversa Eupsilia ornitopus Lithophane Dichonia convergens Orthosia incerta Orthosia cruda Orthosia miniosa Orthosia opima Orthosia cerasi Orthosia munda Pantheidae Colocasia coryli Orgyia recens Orgyia antiqua pudibunda Calliteara similis Euproctis Table 1A to be 1A to continued Table Taxon

586 J. FOR. SCI., 55, 2009 (12): 578–590 Differences among seasonal guilds in species number and abundance were quite uniform for all 9–11 (mm) 18–28 11–13 13–15 oaks. In 1993 the number of FlF was significantly

Pupa length higher than the number of species in other seasonal guilds, except for Q. petraea, where differences be- tween FlF and LSF were not significant (Fig. 3a). In 1994, the FlF guilds had significantly more species on all oaks (Fig. 3b). This pattern was also similar Voltinism univoltine univoltine mostly bivoltine uni- or bivoltine for the number of individuals (Figs. 3c,d). The only exception was an insignificant difference between FlF and LSF on Q. petraea in 1993 (Fig. 3c).

Discussion

Lepidopteran communities account for a high proportion of all in tropical (Lowman, Wittman 1996) and temperate forests (Summer- ville et al. 2003), understanding the variables that determine the species diversity and composition Feeding strategyFeeding free living free living sparsely spun leaves, skeletonize as young free living, as skeletonize young should provide information of high ecological and economic importance. However, the extent to what no no no yes the level of species diversity found on any particular

Ballooning host tree differs from random expectation remains

unclear. Another unanswered question is why large differences among Lepidoptera communities are

Quercus found on taxonomically closely related host species growing in the same vicinity. The lepidopteran community structure may be influenced by many factors originating from diffe- rent environmental parameters such as pressure from natural enemies to differences among individu- als of the same host tree. Hunter et al. (1997) found

spp. spp. that the budburst phenology of individual oaks was a dominant factor determining the spatial distribu- tion of O. brumata and T. viridana. The extent to Host specificity polyphagous on broadleaf trees, spp. mainly Quercus Quercus polyphagous on broadleaf trees what this pattern (differences in lepidopteran com- munities among crowns of the same host species) is a result of the random distribution of lepidopteran individuals has been tested recently (Crist et al. 2003). Some information is known about the spa- tial effect on the species distribution in small areas (< 1 km). Lastly, lepidopteran communities vary significantly between seasons (Summerville, Crist

, 1758) 2003; Summerville et al. 2003). Summerville et al.

, 1758) (2003) also studied how lepidopteran communities , 1772) in temperate forests are structured. They determined

innaeus several important mechanisms that play a role in L ( copoli

innaeus forming arboreal communities, e.g. seasonal vari- S (ESPER, 1785) L (

( ation influenced caterpillar communities most sig- nificantly; the similarity of larval assemblages is not closely related to phylogenetic relationships among host trees (they studied three tree genera). Another message from this study is that the host specificity olidae ycteola revayana Lymantria dispar Lymantria Table 1A to be 1A to continued Table Taxon Parocneria detrita Pseudoips prasinanus N N of Lepidoptera may be less prevalent than previously

J. FOR. SCI., 55, 2009 (12): 578–590 587 30 40 (a) (b) 30 30 a 40 2540 a a a 30 25 2025 30 30 a 20 1520 b 20 a b 15 102015 20 a a b 10 b 10 a b Number of species of Number 10 5 c species of Number No. of species No. of species b,c 10 c 10 b c c c b

Number of species of Number c 5 c b b species of Number Number of species of Number 5 species of Number 0 c 0 b b c b b 0 0 0 Q. petrea Q. robur 1 Q. robur 2 Q. rubra Q. petrea Q. robur 1 Q. robur 2 Q. rubra Q. petrea Q. robur 1 Q. robur 2 Q. rubra Q.Q.Q. petraea petreapetrea Q. Q. robur robur 1 1 Q. Q. robur robur 2 2 Q. Q. rubra rubra Q.Q. petraea petrea Q. robur 1 Q. robur 2 Q. rubra (c) (d) 150 250 250 a 150 150250 a 200 100 a 200 200 150 a b 100 100 b b 150 150 100 b 50 100 a 10050 a 50 50 a b,c b 50 a 50 individuals of Number b,c c

Number of individuals of Number 0 0 a No. of individuals b c b b c b,c c b b c c c b b b

No. of individuals b Number of individuals of Number Number of individuals of Number Number of individuals of Number 0 b Number of individuals of Number 0 00 b b Q. petrea Q. robur 1 Q. robur 2 Q. rubra Q. petrea Q. robur 1 Q. robur 2 Q. brubra b Q. petrea Q. robur 1 Q. robur 2 Q. rubra Q.Q. petreapetraea petrea Q. Q. robur robur 1b 1 Q. Q.robur robur 2 2 Q. rubra Q. rubra Q.Q. petraea petrea Q. robur 1 Q. robur 2 Q. brubra b Flush Feeders Late Spring feeders Flush Feedersfeeders Late springSpring feeders SummerFlush Feeders feeders AutumnLate Spring feeders feeders Summer feeders Autumn feeders Fig. 3. DifferencesSummer feeders in the number of speciesAutumn and individuals feeders in seasonal guilds: (a) comparison of species in 1993; (b) comparison of species in 1994; (c) comparison of individuals in 1993; and (d) comparison of individuals in 1994. The columns designated by different letters are significantly differentP ( < 0.05) among the seasonal guilds on individual oak species (ANOVA, LSD test)

thought. They also suggested that resource speciali- This different pattern on Q. petraea in some sea- zation may occur at the taxonomic level of the host sons may be attributable to budburst which occurred genus or family (also suggested by Stork et al. 1997). later than on Q. robur and Q. rubra and resulted in a In our study, we focused on the genus Quercus and low number of early hatching species which by com- found quite large differences in richness and also in parison were abundant on Q. robur. At the Q. robur the species composition on oaks. sites there was also a better food supply due to the Results also showed a steady decrease in the presence of other early flushing tree species (Betula number of species and individuals from early spring spp., Ulmus spp., Salix spp.). Polyphagous species to autumn. This pattern is well known from the may survive on these early flushing species and “Quercus type” of host tree (Niemelä, Haukioja later move to Q. robur. Significant differences were 1982). These authors suggested that this effect was found between LSF and both SF and AF at majority, due to a decline in available resources. Another but there were no significant differences between theory was presented e.g. by Feeny (1970), Kamata SF and AF. Both SF and AF guilds were of low abun- and Igarashi (1996), who stated that tougher leaves dance and species number. While oaks produce the with a higher concentration of tannin contributed majority of their leaves in spring, there is also some to the lower richness of Lepidoptera later in the production of “May sprouts” (Lammas shoots?) or oak and beech growing season. In addition, a recent leaf regeneration after defoliation events in late May study by Forkner et al. (2004) confirmed a nega- or early June. This is a source of fresh food in early tive correlation between some specialist oak feeders summer and is used as a niche by specialized species and condensed tannins in the canopy of Q. alba and (e.g. Minutia lunaris). understorey of Q. velutina. Their results generally indicated a negative response from both specialists conclusions and generalists to condensed tannins. We have no in- formation about condensed tannins from our study This study documents the types of communities sites, but the number of species and individuals was found on three different oak species. We found significantly higher early in spring on almost all the that the number of species in four seasonal guilds oak species studied; only Q. petraea was excluded (flush, late spring, summer and autumn feeders) from this general pattern. had a similar pattern on each of the studied oaks:

588 J. FOR. SCI., 55, 2009 (12): 578–590 the highest number of species was found among Kulfan M., Šepták L., Degma P., 1997. Lepidoptera FlF, a significantly lower number of species among larvae communities on oaks in SW Slovakia. Biologia, 52: LSF and both these groups supported a significantly 247–252. higher number of species than summer and autumn Laštůvka Z. et al., l998. Checklist of Lepidoptera of the feeders with several exceptions. The differences be- Czech and Slovak Republics. Brno, Konvoj: 117. tween SF and AF were found not to be significant. The same pattern was also found for the number of Lowman M.D., Wittman P.K., 1996. Forest canopies: individuals. The only exception was an insignificant methods, hypotheses, and future directions. Annual Review difference between FlF and LSF on Q. petraea in of Ecology and Systematics, 27: 55–81. some seasons, insignificant difference between LSF Niemelä P., Haukioja E., 1982. Seasonal patterns in and AF on Q. robur in some seasons and permanent species richness of herbivores: Macrolepidoptera larvae insignificant difference between LSF, SF and AF on on Finnish deciduous trees. Ecological Entomology, 7: Q. rubra. 169–175. Acknowledgements Patočka J., 1954. Húsenice na duboch v ČSR. Bratislava, Štátne pôdohospodárske nakladateľstvo: 262. We would like to thank the reviewers who gave Patočka J., 1980. Die Raupen und Puppen der Eichen- us useful comments and improved the quality of schmetterlinge Mitteleuropas. Monografie Angewandte the manuscript. Thanks also to Dr. Shinsaku Koji, who gave us valuable comments and recommenda- Entomologie 23. Hamburg und Berlin, Paul Parey: 188. tions on early versions of the manuscript and to Patočka J., Turčáni M., 2005. Lepidoptera Pupae of Alan Flynn and Dr. Peter Fedor, who checked Central Europe. Stenstrup, Apollo Books. the English. Patočka J., Čapek M., Charvát K., 1962. Contribution to research of canopy fauna of on oaks in Slovakia References with special regard to Lepidoptera. Biologické práce VIII/5. Bratislava, SAV: 154. Crist T.O., Veech J.A., Summerville K.S., Gering Patočka J., Kulfan J., Turčáni M., 1999. Schmetter- J.C., 2003. Partitioning species diversity across landscapes linge (Lepidoptera) als Eichenschädlinge. In: Patočka J., and regions: a hierarchical analysis of alpha, beta, and Krištín A., Kulfan J., Zach P. (eds), Die Eichenschäd- gamma diversity. American Naturalist, 162: 734–743. linge und ihre Feinde. Zvolen, institute for Forest Ecology Feeny P., 1970. Seasonal changes in oak leaf tannins and of SAV: 152–250. nutrient as a cause of spring feeding by winter cater- Stolina M. et al., 1985. Ochrana lesa. Bratislava, Príroda: pillars. Ecology, 51: 565–581. Forkner R.E., Marquis R.J., Lill J.T., 2004. Feeny re- 480. visited: condensed tannins as anti-herbivore defences in Stork N.E., Didham R.K., Adis J., 1997. Canopy arthro- leaf-chewing herbivore communities of Quercus. Ecological pod studies for future. In: Stork N.E., Adis J., Didham Entomology, 29: 174–187. R.K. (eds), Canopy Arthropods. London, Chapman and Gerasimov A.M., 1952. Nasekomye cheschuekrylye I., 2, Hall: 551–561. Gusenitsy. Moskva, Leningrad, Izdateľstvo AN SSSR: 339. Summerville K.S., Crist T.O., 2003. Determinants of Hunter M.D., Varley G.C., Grandwell G.R., 1997. lepidopteran community composition and species diversity Estimating the relative roles of top-down and bottom-up in eastern deciduous forests: roles of season, eco-region forces on herbivore populations: A classic study re- and patch size. Oikos, 100: 134–148. visited. Proceedings of the National Academy of Sciences, Summerville K.S., Crist T.O., Kahn J.K., Gering J.C., 94: 9176–9181. 2003. Community structure of arboreal caterpillars within Kamata N., Igarashi I., 1996. Seasonal and annual and among four tree species of the eastern deciduous forest. change of a folivorous insect guild in the Siebolds beech for- Ecological Entomology, 28: 747–757. ests associated with the outbreaks of the beech caterpillar, Quadricalcarifera punctatela (Motschulsky) (Lep., Noto- Received for publication May 13, 2009 dontidae). Journal of Applied Entomology, 120: 213–220. Accepted after corrections August 4, 2009 Kulfan M., Degma P., 1999. Seasonal dynamics of lepido- pteran larvae communities diversity and equitability on oaks in the Borská nížina Lowland. Ekológia, 18: 100–105.

J. FOR. SCI., 55, 2009 (12): 578–590 589 Sezonní gildy housenek na některých dubech (Quercus spp.) – Případová studie

AbstraKt: V letech 1993 a 1994 byly na Slovensku studovány rozdíly společenstev motýlů na dubu. Vzorky byly odebírány ze tří druhů dubů (Quercus robur, Q. petraea, Q. rubra) od dubna do října. Byly zkoumány bionomické vlastnosti housenek, na jejichž základě byl vysvětlován rozdíl v sezonních společenstvech jednotlivých dubů. Spo- lečenstva vykazovala variabilitu ve struktuře i abundanci. Druhová pestrost čtyř společenstev (defoliátoři časného jara, pozdního jara, léta a podzimu) vykazovala podobný vzor na všech studovaných druzích dubů. Společenstvo časného jara bylo druhově nejbohatší, následovalo společenstvo pozdních jarních defoliátorů, přičemž obě skupiny byly statisticky významně bohatší než společenstva letních a podzimních defoliátorů.

Klíčová slova: společenstva motýlích housenek; Slovensko; duby; sezonní gildy

Corresponding author:

Prof. Ing. Marek Turčáni, Ph.D., Česká zemědělská univerzita v Praze, Fakulta lesnická a dřevařská, 165 21 Praha 6-Suchdol, Česká republika tel.: + 420 224 383 738, fax: + 420 234 381 860, e-mail: [email protected]

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