Article Winter Geometrid Moths in Oak Forests: Is Monitoring a Single Species Reliable to Predict Defoliation Risk? Lenka Sarvašová 1 ,Ján Kulfan 1,*, Miroslav Saniga 1, Milan Zúbrik 2 and Peter Zach 1 1 Institute of Forest Ecology, Slovak Academy of Sciences, L’.Štúra 2, 960 53 Zvolen, Slovakia; [email protected] (L.S.); [email protected] (M.S.); [email protected] (P.Z.) 2 National Forest Centre, Forest Protection Service Centre, Lesnícka 11, 969 01 Banská Štiavnica, Slovakia; [email protected] * Correspondence: [email protected] Received: 3 February 2020; Accepted: 24 February 2020; Published: 2 March 2020 Abstract: Species within the group of winter moths (Geometridae) are important oak defoliators in European forests. Adults of these species emerge either in late autumn (‘autumn species’) or in early spring (‘spring species’), and caterpillars of both ‘autumn’ and ‘spring’ species appear in spring. The abundance of adults assessed by regular monitoring allows the prediction of the defoliation intensity in trees by caterpillars in the following spring. ‘Autumn species’ (mostly a single one, Operophtera brumata) are monitored by forestry practices as pests, whereas ‘spring species’ are often not paid any attention. We hypothesised that ‘spring species’ could also have an important share in caterpillar assemblages in oak forests. We aimed to study the proportions between ‘autumn’ and ‘spring’ species in adult and larval stages. In a xeric thermophilous oak forest in southern Slovakia, Central Europe, we collected adult moths using sticky bands set up on trunks of Quercus pubescens during the winter of 2014–2015 and caterpillars from other trees belonging to the same oak species over the following spring. We also captured caterpillars from several oak species in various areas and over different years in Slovakia and Bulgaria, and we compiled relevant literature data. ‘Spring species’ recorded from a unique forest as adults during winter and as caterpillars in the following spring were significantly more abundant than ‘autumn species.’ Moreover, ‘spring species’ from Slovakian forests, regardless of the locality, the oak species and the year of sampling, reached high proportions, mostly over 50% of individuals in caterpillar assemblages. The ‘spring species’ Agriopis leucophaearia was the most abundant, followed by the ‘autumn species’ Operophtera brumata. ‘Spring species’ accounted for more than 50% of individuals in caterpillar assemblages in the Balkan Peninsula (Bulgaria) concerning one case, and they were of little importance in northern Greece. We recommend monitoring all winter moth adults (‘autumn’ and ‘spring’ species together) continuously in forestry practices, using sticky bands on oak trees from late autumn to early spring. Keywords: forest protection; geometridae; caterpillars; Quercus; Agriopis leucophaearia 1. Introduction Caterpillars occurring in the spring are important tree defoliators in temperate forests [1–4]. In spring, caterpillar assemblages, some geometrid species of economic importance, belong to a so-called ecological group of winter moths [5]. Adults from this group do not emerge during the growing season, i.e., either in late autumn (‘autumn species’ for this study) or in early spring (‘spring species’). Beside this, females have reduced wings (brachypterous/apterous females) [5]. Operophtera brumata (Linnaeus, 1758) and Erannis defoliaria (Clerck, 1759) are generally considered to be the most important pests within the group of winter moths in Central Europe [1,6–8]. They Forests 2020, 11, 288; doi:10.3390/f11030288 www.mdpi.com/journal/forests Forests 2020, 11, 288 2 of 12 occur very frequently and cause extensive defoliation in oak forests within Europe as well as in North America [9–11]. To monitor the population density of O. brumata and E. defoliaria belonging to ‘autumn species’ and to predict the damage to foliage caused by their larvae in the following spring, sticky bands or glue strips placed on tree trunks are often used [12–19]. Such monitoring of these particular species is usually set up for late autumn and early winter, i.e., when adults occur. Such timing does not allow the monitoring of winter moth adults emerging in late winter and early spring, i.e., ‘spring species’. Caterpillars of these ‘spring species’ co-occur with those of O. brumata and E. defoliaria, causing damage to leaves during spring. In European deciduous forests, the complex of ‘spring species’ consists of species such as Alsophila aescularia (Denis and Schiffermüller, 1775), Agriopis leucophaearia (Denis and Schiffermüller, 1775), Agriopis marginaria (Fabricius, 1776), Apocheima hispidaria (Denis and Schiffermüller, 1775), and Phigalia pilosaria (Denis and Schiffermüller, 1775). In this document, we addressed (1) the ‘spring species’ abundance of winter moths in Europe’s temperate oak forests in comparison to the abundance of ‘autumn species’ and (2) whether monitoring winter moth adults in late autumn and early winter (October–December) is an adequate method to assess the overall significance (performance) of their larvae as pests in oak forests. We hypothesised that ‘spring species’ could reach large proportions in caterpillar assemblages of winter moths on oaks, judged from their high abundance in some regions and years [1,20–26] and, therefore, they could be paid greater attention by being included in programmes of forest pest monitoring. 2. Materials and Methods 2.1. Collection of Moths We collected adult moths according to a method [27] using sticky bands in the Krupinská planina plateau (southern Slovakia, Central Europe; 48◦1000.19” N, 18◦59046.08” E) from November 2014 to April 2015. We set up sticky bands for moths on the trunks of 45 randomly selected mature trees belonging to pubescent oak (Quercus pubescens Willd.) in a xeric thermophilous oak forest dominated by pubescent oak and Turkey oak (Quercus cerris L.). The study area was approximately 50 ha. We regularly controlled these bands and replaced them with fresh ones to avoid their saturation by moth males. Captured moths were identified to the species level [28] and counted in the laboratory. Over the following spring, in early May 2015, we captured caterpillars from pubescent oaks in the same forest area by the method known as beating. We knocked them off from the lower branches of mature trees. These trees were different from the trees used for obtaining adults during the previous winter. We used a stick and a circular beating tray (diameter of 1.0 m) to obtain caterpillars. The heights for sampling varied from 1.0 to 3.0 m, measured from the ground. A total of 23 trees were sampled. One sample constituted caterpillars that were collected from three branches (each branch 1 m long) from each tree. The larvae were preserved in 70% ethanol and identified in the laboratory [3,29]. From both winter and spring samples, only individuals belonging to winter moth geometrids were selected and separated into ‘autumn’ and ‘spring’ species. To obtain wider knowledge about proportion between numerous caterpillars of ‘autumn’ and ‘spring’ geometrids, we also collected winter moth larvae from several oak species in various areas, as well as over years in Slovakia and Bulgaria (for more details, see Samples S08–S12 and S15, Table1). We further analysed relevant data from the literature [25,30–32]. The available data refer to caterpillars on Q. cerris, Q. pubescens, Quercus frainetto Ten., Quercus dalechampii Ten., Quercus polycarpa Schur and a few other oak species in Slovakia, Bulgaria and Greece. Caterpillars were captured from trees, mostly by the beating method [30]; samples were obtained by hand collecting. For more details, see Table1. Forests 2020, 11, 288 3 of 12 Table 1. Survey of sampling caterpillar assemblages on oaks in Slovakia (SVK), Bulgaria (BGR) and Greece (GRC). Sample Country Area Coordinates Oak Species Year Sample Data Source Malé Karpaty 48 19 N S01 W SVK ◦ 0 Q. dalechampii 2000–2002 150 branches Kulfan (2012) Mountains 17◦170 E Malé Karpaty 48 22 N S02 W SVK ◦ 0 Q. dalechampii 2000–2002 150 branches Kulfan (2012) Mountains 17◦190 E Malé Karpaty 48 29 N S03 W SVK ◦ 0 Q. dalechampii 2000–2002 225 branches Kulfan (2012) Mountains 17◦230 E Malé Karpaty 48 32 N S04 W SVK ◦ 0 Q. dalechampii 2000–2002 150 branches Kulfan (2012) Mountains 17◦310 E Malé Karpaty 48 32 N S05 W SVK ◦ 0 Q. cerris 2000–2002 225 branches Kulfan (2012) Mountains 17◦310 E Malé Karpaty 48 44 N S06 W SVK ◦ 0 Q. polycarpa 2011 340 branches Parák et al. (2012) Mountains 17◦460 E Malé Karpaty 48 44 N S07 W SVK ◦ 0 Q. pubescens 2011 140 branches Parák et al. (2012) Mountains 17◦460 E Podunajská 48 12 N Q. cerris, S08 SW SVK pahorkatina ◦ 0 2014 100 branches original data 18 24 E Q. petraea upland ◦ 0 Podunajská 48 12 N Q. cerris, S09 SW SVK pahorkatina ◦ 0 2015 100 branches original data 18 24 E Q. petraea upland ◦ 0 Krupinská 48 10 N Q. cerris S10 S SVK ◦ 0 2015 102 branches original data planina plateau 18◦590 E (adult trees) Krupinská 48 10 N Q. cerris S11 S SVK ◦ 0 2016 60 branches original data planina plateau 18◦590 E (young trees) Krupinská 48 10 N Q. pubescens S12 S SVK ◦ 0 2016 60 branches original data planina plateau 18◦590 E (young trees) Q. dalechampii, Q. frainetto, Mount 40 25 N 710 Kalapanida and S13 N GRC ◦ 0 Q. trojana, 1997–1998 ≈ Holomontas 23 30 E branches Petrakis (2012) ◦ 0 Q. pubescens, Q. pedunculiflora Q. cerris, BGR Q. frainetto, 42 03 N Georgieva et al. S14 (N, S, E, W, ◦ 0 Q. petraea, 2009–2011 300 oaks 24 54 E (2014) Central) ◦ 0 Q. robur, Q. pubescens Rhodope 41 20 N S15 S BGR ◦ 0 Q. frainetto 2017 540 branches original data Mountains 25◦220 E 2.2. Statistical Data Analysis Generalized estimating equations (GEE) [33] were applied to make inferences about populations of winter moths developing on oak trees.