Invertebrate Zoology, 2018, 15(1): 115–130 © INVERTEBRATE ZOOLOGY, 2018

Springtail (Hexapoda: Collembola) fauna in the burnt boreal forests of European Russia

R.A. Saifutdinov1,2, K.B. Gongalsky1, A.S. Zaitsev1,3

1 A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky pr., 33, Moscow 119071 Russia. E-mail: [email protected] 2 Kazan Federal University, Kremlyovskaya str. 18, Kazan 420008 Russia. E-mail: [email protected] 3 Institute of Ecology, Justus-Liebig-University, Heinrich-Buff-Ring 26, 35392 Giessen, Germany. E-mail: [email protected]

ABSTRACT: We investigated fauna and community composition of in the burnt and unburnt boreal forests of European Russia. We also analyzed ecoregional differences in the effect of fire disturbance on collembolan community faunistic similarity on an example of three different ecoregions of the boreal forest biome in the study territory. We collected and identified 6799 individuals representing 14 families, 41 genera and 94 species. In the burnt plots we observed consistent shifts in the springtail community dominance structure across all studied ecoregions. The effect of fire on the faunistic similarity of springtail communities was strongly modulated by ecoregion: within-ecore- gion similarity between plots was always higher than the between-region similarity. Fires resulted in the moderate decrease of the total abundance of springtails with trans-holarctic distribution in all ecoregions and additionally in increase of springtails with west-palaearc- tic distribution in southern ecoregion. We conclude that five years after burning it is very important to standardize fire-induced changes in the faunistic composition of springtail communities to the actual geographic location within spatially extensive biomes. How to cite this article: Saifutdinov R.A., Gongalsky K.B., Zaitsev A.S. 2018. Springtail (Hexapoda: Collembola) fauna in the burnt boreal forests of European Russia // Invert. Zool. Vol.15. No.1. P. 115–130. doi: 10.15298/invertzool.15.1.09

KEY WORDS: soil fauna, taiga, fire disturbance, collembolans, European Russia.

Фауна ногохвосток (Hexapoda: Collembola) в сгоревших бореальных лесах европейской части России

Р.А. Сайфутдинов1,2, К.Б. Гонгальский1, А.С. Зайцев1,3

1 Институт проблем экологии и эволюции им. А.Н. Северцова РАН, Ленинский пр., 33, Москва 119071 Россия. E-mail: [email protected] 2 Казанский федеральный университет, ул. Кремлёвская 18, Казань 420008 Россия. E-mail: [email protected] 3 Институт экологии животных, Университет им. Юстуса-Либиха, Хайнрих-Буфф-Ринг 26, 35392 Гиссен, Германия. E-mail: [email protected]

РЕЗЮМЕ: Исследовали фауну и структуру сообществ ногохвосток в сгоревших и естественных бореальных лесах европейской части России. На примере трёх разных 116 R.A. Saifutdinov et al.

экорегионов анализировали влияние различий в экорегионах при воздействии лес- ных пожаров на фаунистическую структуру таксоценов коллембол. Всего было собрано и определено 6799 экземпляров коллембол, представляющих 14 семейств, 41 род и 94 вида. Сгоревшие участки всех исследуемых экорегионов характеризуют- ся нарушенной структурой доминирования таксоценов коллембол. Таксоцены кол- лембол в большей степени определяются региональными факторами, нежели влия- нием на них лесных пожаров: фаунистическое сходство таксоценов коллембол между участками внутри экорегионов было выше сходства участков между экореги- онами. Пожары привели к сокращению общей численности ногохвосток с транс- голарктическим распределением во всех экорегионах и дополнительно, к увеличе- нию численности ногохвосток с западно-палеарктическим распределением в южном экорегионе. Мы пришли к выводу, что спустя пять лет после лесного пожара важна стандартизация изменений, вызванных пожаром, в фаунистическом составе сооб- ществ ногохвосток к фактическому географическому местоположению в пределах крупных зональных биомов. Как цитировать эту статью: : Saifutdinov R.A., Gongalsky K.B., Zaitsev A.S. 2018. Springtail (Hexapoda: Collembola) fauna in the burnt boreal forests of European Russia // Invert. Zool. Vol.15. No.1. P. 115–130. doi: 10.15298/invertzool.15.1.09

КЛЮЧЕВЫЕ СЛОВА: почвенная фауна, тайга, лесной пожар, коллемболы, Евро- пейская часть России.

Introduction ed within NW Russia’s boreal forests (see e.g. Zaitsev et al., 2016 for review). Springtails are small invertebrates that in- We tried to address this knowledge gap by habit almost any soil type around the globe studying the effect of forest fires which are (Hopkin, 1997; Rusek, 1998). They form a frequent in the boreal forests of European Rus- considerable part of soil microarthropod biodi- sia. We aimed at understanding, how forest fires versity and contribute to soil decomposition and alter faunistic composition and the diversity of mineralization processes, particularly in the soil microarthropod communities at the local boreal forests (Petersen, Luxton, 1982; Seast- scale and how consistent are the revealed effects edt, 1984; Huhta et al., 1998). At the same time, at the ecoregion scale. springtail community composition may vary considerably across this biome depending on Material and methods climate and dominating species in tree stands (Juceviča, Melecis, 2002; Kuznetsova, 2002). Study sites Despite numerous studies published with this The study was conducted along a 1500 km- respect (see e.g. Kuznetsova, Potapov, 1997; long latitudinal gradient in the boreal forests of Kuznetsova, Krest’yaninova, 1998; Chernova, European Russia (Fig. 1). We selected three Kuznetsova, 2000; Taskaeva, 2009, 2011), not ecoregions in the European Russia: Kola-Kare- much is still known on the impact of different lian, Pribaltiiskiy-Vetluzhskiy and Smolensk- disturbances on fauna and taxonomic composi- Priuralskiy ecoregions (Ogureeva et al., 2015). tion of collembolans (Malmström, 2012). Giv- Studied ecoregions corresponds to the different en that wildfires are one of the most important type of forest within boreal forest biome as disturbances in the boreal forests, they remain follows: Kola-Karelian — northern taiga, Prib- unstudied in terms of soil faunal recovery with altiiskiy-Vetluzhskiy — middle taiga and Smo- respect to macrogeographic gradients present- lensk-Priuralskiy — southern taiga. Springtail fauna in the burnt boreal forests of European Russia 117

Fig. 1. Schematic map of the studied ecoregions (Kola-Karelian, Pribaltiiskiy-Vetluzhskiy and Smolensk- Priuralskiy) within the boreal biome in NW Russia. Gray dots indicate pairs of forest plots (burnt and control) sampled within each ecoregion. Numbers in parentheses refer to respective plots as shown in Table 1. Рис. 1. Схематическая карта исследуемых экорегионов (Кольско-Карельский, Прибалтийско-Вет- лужский, Смоленск-Приуральский) биома бореальных лесов северо-западной части России. Серые точки обозначают пары лесных участков (сгоревших и контрольных), отобранных в каждом экоре- гионе. Номера чисел в скобках обозначают пары исследуемых участков, и соответствуют участкам в таблице 1.

Plots of Kola-Karelian ecoregion are locat- ests (P. sylvestris) with blueberry (V. myrtilis) ed in the Murmansk Region, Kola Peninsula and red bilberry (V. vitis-idaea) in the under- (Fig. 1) and are represented by pine (Pinus growth. Soil types are Lithic Leptosols or Albic sylvestris L., 1753) or pine-spruce (P. sylves- Podzols (WRB, 2015). tris, Picea abies H. Karst., 1881) forest stands Smolensk-Priuralskiy ecoregion forests are (Table 1). The ground vegetation is formed located in the Moscow and Tver Regions and predominantly by red bilberry (Vaccinium vitis- are formed by spruce-birch (P. abies, Betula idaea L., 1753) and blueberry (V. myrtilis L., 1753). Soil type is Albic Podzols according to pendula Roth, 1788), pine-birch (B. pendula, P. World Reference Base for Soil Recourses clas- sylvestris) or spruce-pine-birch stands (B. pen- sification (WRB, 2015). dula, P. abies, P. sylvestris). Ground vegetation Pribaltiiskiy-Vetluzhskiy ecoregion plots are is dominated mainly by red bilberry (V. vitis- located in the Republic of Karelia and the Lenin- idaea) and blueberry (V. myrtilis). Soil type is grad Region. They are represented by pine for- Umbric Albeluvisol (WRB, 2015). 118 R.A. Saifutdinov et al.

Table 1. Brief description of investigated forest plots. Even plot numbers refer to the burnt and odd numbers to the control forests within the respective plot pair. Таблица 1. Краткая характеристика исследуемых лесных участков. Чётные номера обозначают сгоревшие и нечётные — контрольные участки в пределах соответствующей пары.

In each ecoregion, we selected four forest gions. At each plot we randomly collected four plots burnt in 2010 and four respective controls. intact soil samples for springtails with a soil In total we examined 12 pairs of plots (burnt- corer. To avoid possible edge effect during control). Some further details on the investigat- sampling we took soil monoliths not closer than ed plots are provided in Table 1. For a more 3 m from the plot edge. Each soil sample had the detailed description of particular plots please diameter of 5 cm and a depth of 6–8 cm (de- refer to the project webpage: https://forestfire. pending on the thickness of the organic hori- biogeo.ru/index.php/en/. zon). In total we collected 96 samples. Collect- ed samples were put into plastic bags and trans- Sampling ferred to the laboratory in isothermic containers The sampling was performed between May at a temperature below +10°C. 25 and June 20, 2015. Exact sampling dates were chosen for each ecoregion with the aim of Extraction and Identification their phenological synchronization. We referred In the laboratory soil samples were extract- to the beginning of bird cherry (Prunus padus ed using Tullgren funnels into the mixture of L., 1753) flowering (World atlas…, 1964) to alcohol, water and ethylene glycol with a ratio calculate the lag in sampling between the re- of 80:15:5 respectively. Extraction lasted for Springtail fauna in the burnt boreal forests of European Russia 119 four days. This time was sufficient for the sub- normalization. Clustering was performed using strate to reach air-dry condition. All springtails Biodiversity Pro 2.0 software. were slide-mounted in the cavity slides using a mixture of lactic acid and glycerol with a ratio of Results 3:1 respectively. were then identified to the species level using applicable determina- Ecoregional differences in the spe- tion keys (Babenko et al., 1994; Fjellberg, 1998, cies composition 2007; Bretfeld, 1999; Potapov, 2001; Hopkin, 2007). After identification we assigned each In total we collected and identified 6799 species to one of the biogeographic distribution springtail individuals representing 14 families, types (trans-holarctic, trans-palaearctic, west- 41 genera and 94 species. Data on the average ern-palaearctic, eastern-palaearctic, cosmopol- species abundance and their biogeographic dis- itan or unknown) following Babenko and Fjell- tribution type are provided in Appendix 1. berg (2006) and Babenko (2012). Total springtail abundance significantly in- creased from north (18608 ind. m–2) to south –2 Statistical analysis (57152 ind. m ) (ANOVA, F=15.8, P<0.0001), but was not affected by “Fire” treatment. Aver- Samples collected within the same forest age species richness in the same manner in- plot were considered pseudoreplicates (Kozlov, creased from north (12 species) to south (21 2014). Thus all values derived from them were species) (ANOVA, F=9.1, P<0.002), with no averaged to represent a single data unit per plot. effect of “Fire”. The highest total number of Differences between the means in burnt and species was observed in Smolensk-Priuralskiy control forests were tested with a two-way ecoregion (68 species); it was a bit lower in ANOVA with the categorical factors “Fire” and Pribaltiiskiy-Vetluzhskiy ecoregion (55 species) “Ecoregion” and their interaction. Data normal- and the lowest in Kola-Karelian ecoregion (35) ity and heterogeneity were tested prior to the species. No significant difference in springtail analysis. Because abundance of most species diversity measured by Shannon diversity index had non-normal distribution, we performed was found between treatments. Highest Shan- ln(x+1) transformation of data. In a case of non diversity was observed in burnt plots of testing the collembolans abundance belonging Smolensk-Priuralskiy and in control plots of to different biogeographic distribution types, Pribaltiiskiy-Vetluzhskiy ecoregions and low- we left the data untransformed. If ANOVA est in burnt plots of Kola-Karelian ecoregion. returned significant results, we further tested the Pielou evenness index was higher in burnt plots significance of differences between the means of Kola-Karelian ecoregion and lowest in con- with the Tukey HSD test (p<0.05). ANOVAs trol plots of Smolensk-Priuralskiy ecoregion were done using Statistica 10.0 software pack- (Appendix 1). age. For the analysis of the dominance structure The most frequent species found in all stud- of collembolan communities we recognized ied ecoregions were Isotoma viridis, Lepidocyr- species with the relative abundance not less than tus lignorum, L. lanuginosus, Entomobrya ni- 12.4% as dominant ones (Engelmann, 1978). valis, Folsomia quadrioculata, Parisotoma no- Shannon diversity index (H’) and Pielou even- tabilis, cf secundarius, Isot- ness index (J’) were calculated according to omiella minor, Micraphorura absoloni, Wille- Shannon-Pielou index (Magurran, 1988). Sim- mia anophthalma, W. denisi, Mesaphorura yosii, ilarity of springtail communities of the studied M. tenuisensillata, and Micranurida pygmaea. ecoregions was assessed with the cluster analy- Among them I. minor, M. yosii, P. notabilis, F. sis (Bray-Curtis similarity index, complete link- quadrioculata and W. anophthalma dominated age design). Before the analysis, the abundance (Bold in Appendix 1). of all species was square root transformed for The average abundance of I. minor and W. 120 R.A. Saifutdinov et al. anophthalma was significantly lower in the burnt plots (ANOVA, F=6.57, P<0.04). Also, some plots than in the controls (ANOVA, F=4.46, species such as Mesaphorura critica, M. hylo- P<0.049 and F=6.73, P<0.018, respectively). In phila, M. macrochaeta, P. pseudovanderdrifti, addition, total abundance of I. minor was signif- C. inermis, Xenylla cf. maritima, Desoria nivea, icantly higher in middle and southern ecore- Folsomia fimetarioides, Pachyotoma crassi- gions, than in northern taiga ecoregion (ANO- cauda, E. nicoleti, Lepidocyrtus pallidus, Smin- VA, F=5.96, P<0.01), while the abundance of thurides malmgreni, S. cf. signatus, S. schoetti, W. anophthalma fluctuated between the ecore- Pygmarrhopalites cf. secundarius and Smin- gions. It was the highest in Pribaltiiskiy- thurus viridis were found only in burnt plots. Vetluzhskiy ecoregion (ANOVA, F=12.02, (Appendix 1). P<0.0005). The average abundance of F. quad- At the species level we found only few rioculata, P. notabilis and M. absoloni signifi- significant differences in the abundance be- cantly increased from northern to southern ecore- tween burnt and control forests. In addition, gion (ANOVA, F=6.21, P<0.009; F=49.9, some springtail individuals (e.g. most of juve- P<0.000001 and F=25.06, P<0.00001 respec- niles) were identified only to a family level. To tively). Other species did not show significant include them into the analysis we also studied differences between the treatments. the effect of burning on the abundance of col- The dominance structure of springtail com- lembolan families. The abundance of collembo- munities was also affected by fire. Control plots lans from Arrhopalitidae family was signifi- were always dominated by I. minor. Dominant cantly lower in burnt plots (ANOVA, F=6.25, species in the burnt plots varied across ecore- P<0.02) with no effect of “Ecoregion” on it. The gions. M. yosii was the most abundant species in abundance of Onychiuridae springtails was sig- Kola-Karelian, I. minor in Pribaltiiskiy-Vetluzh- nificantly affected by “Ecoregion” and by its skiy and Mesaphorura hylophila in Smolensk- interaction with “Fire”. It was much higher in Priuralskiy ecoregion respectively. the burnt plots of Smolensk-Priuralskiy ecore- In Kola-Karelian ecoregion I. minor was gion, but lower in the burnt plots of Pribalti- clearly more numerous in the control plots iskiy-Vetluzhskiy ecoregion compared to the (ANOVA, F=9.128, P<0.02), than in the burnt respective controls (ANOVA, F=4.53, P<0.02). ones. The decrease of the abundance of W. The abundance of springtails belonging to Iso- anophthalma in the burnt plots was only mar- tomidae and Neelidae families significantly in- ginally significant (ANOVA, F=4.74, P<0.072). creased from north to south (ANOVA, F=4.66, Several species like Mesaphorura krausbaueri, P<0.02 and F=4.44, P<0.03 respectively), how- Protaphorura subarctica and P. pseudovan- ever, their abundance was not significantly af- derdrifti were recorded only in the burnt plots fected by burning. Other families were signifi- (Appendix 1). cantly affected by none of the factors nor their In Pribaltiiskiy-Vetluzhskiy ecoregion, none interaction. of the springtail species were significantly af- fected by “Fire” treatment. Although many spe- Faunistic similarity cies with low abundance were found only in The cluster analysis revealed considerable burnt plots: Chouretinula inermis, Xenylla tull- modulation effect of “Ecoregion” on the fire- bergi, Friesea truncata, Cryptopygus cf. bi- induced changes in the faunistic composition of punctatus, Desoria hiemalis, Folsomia dovren- collembolan assemblages. Burnt and unburnt sis, Proisotoma minima, Vertagopus haagvari, plots from Kola-Karelian ecoregion were clear- Entomobrya nicoleti, Orchesella cincta and ly dissimilar to the others and formed a separate Sminthurinus concolor. cluster (Fig.2). The communities from burnt In Smolensk-Priuralskiy ecoregion the abun- and unburnt forests of Pribaltiiskiy-Vetluzhskiy dance of Pygmarrhopalites principalis was sig- ecoregion served as the core of the second nificantly higher in control than in the burnt cluster and were the most similar between each Springtail fauna in the burnt boreal forests of European Russia 121

Fig. 2. Cluster analysis of springtail communities in the burnt and unburnt forests of the three studied ecoregions (Bray-Curtis index of similarity, Complete linkage). Data is square root transformed. Ecoregions are abbreviated as follows: KK — Kola-Karelian, PV — Pribaltiiskiy-Vetluzhskiy, SP — Smolensk- Priuralskiy. Рис. 2. Дендрограмма кластерного анализа сообществ коллембол в сгоревших и контрольных лесах, трёх исследуемых экорегионов (индекс сходства Брея-Кёртиса, метод полной связи). Данные трансформированы извлечением квадратного корня. Сокращения: KK — Кольско-Карельский экорегион, PV — Прибалтийско-Ветлужский экорегион, SP — Смоленск-Приуральский экорегион. other among all plots included into the analysis controls (ANOVA, F=4.7, p<0.02) (Fig.3). (Bray-Curtis similarity level of 70%) (Fig. 2). “Ecoregion” had a strong effect on the total Similarity between the communities in the Smo- abundance of cosmopolitan, trans-palaearctic lensk-Priuralskiy burnt and unburnt plots was and trans-holarctic species. Their abundance the lowest and these communities were more significantly increased from northern to south- similar to those from the Pribaltiiskiy-Vetluzhs- ern ecoregion (ANOVA, F=24.4, p<0.00001; kiy ecoregion (Bray-Curtis similarity level 47% F=4.49, p<0.03 and F=12.33, p<0.0004, re- between each other) (Fig. 2). spectively) (Fig. 3). Also, abundance of trans- holarctic species was higher in the control plots Biogeographic distribution types than in the burnt forests (ANOVA F=6.52, The abundance and species richness of p<0.02). springtail species sharing certain biogeographic Average species richness of cosmopolitan distribution types was significantly different species significantly increased from north to between the studied ecoregions (Fig.3 and Fig.4). south (ANOVA, F=18.3, p<0.00005) (Fig. 4). Total abundance of west-palaearctic species Species richness of west-palaeartic species was was significantly affected by interaction of affected by interaction of factors “Ecoregion” “Ecoregion” and “Fire” treatments. It was con- and “Fire”. It was higher in controls than in siderably higher in the burnt plots than in the burnt plots of Kola-Karelian ecoregion, while in controls in Smolensk-Priuralskiy ecoregion and Smolensk-Priuralskiy ecoregion was reverse in the Kola-Karelian ecoregion abundance of situation (ANOVA, F=4.28, p<0.03). Average west-palaearctic springtail was higher in the species richness of trans-palaearctic and trans- 122 R.A. Saifutdinov et al.

Fig. 3. Abundance of springtails (103 ind. m–2, n=4) sharing different biogeographic distribution types in the burnt and control forests of the three studied ecoregions. Рис. 3. Численность ногохвосток (103 экз. м–2, n=4) с разными типами биогеографического распро- странения в сгоревших и контрольных лесах, трёх исследуемых экорегионов.

Fig. 4. Average species richness of springtails (n=4) sharing different biogeographic distribution types in the burnt and control forests of the three studied ecoregions. Рис. 4. Среднее число видов ногохвосток (n=4) с разными типами биогеографического распростра- нения в сгоревших и контрольных лесах, трёх исследуемых экорегионов. Springtail fauna in the burnt boreal forests of European Russia 123 holarctic species was lower in northern taiga like I. minor. Probably, this is ensured by thick- ecoregion that in southern and middle ecore- er layer of ground litter made of needles, the gions (ANOVA, F=3.8, p<0.04 and F=9.33, level of which is higher in middle taiga in p<0.002, respectively). In addition, the number comparison with other subregions of boreal of trans-holarctic species in control plots was forest (Bazilevich, 1993; Borisov, Ganzhara, higher than in burnt forests, but this effect was 2008). only marginally significant (ANOVA, F=4.28, It is remarkable that several species with p<0.053). Average species richness of species relatively low abundance were found mainly in with unknown distribution was lower in burnt burnt plots (e.g. P. subarctica, P. armata, C. plots that in controls (ANOVA, F=5.9, p<0.025) inermis, M. macrochaeta, F. quadrioculata, E. (Fig. 4). corticalis and others). Perhaps, that could be explained as after moderate disturbances pro- Discussion portion of non-dominant species is increased and this leads to diversification of springtail In our study we revealed approximately one community structure (see Kuznetsova, Potapov, half of the total springtail species richness known 1997). Moreover, proportion of species found- by now for the European Russia’s boreal forests ed only in burnt plots is increasing from north to (Kuznetsova, 1985; Chernova, Kuznetsova, south, suggesting that in middle and southern 2000; Kuznetsova, 2002). According to Kuz- taiga regions with more favorable climatic con- netsova and Krest’yaninova (1998), indigenous ditions, colonization rate of disturbed habitats springtail communities in this biome are mainly by collembolans is relatively higher compared dominated by I. minor, which shows the clear to northern taiga. This further points at the preference to forested habitats. The absence of importance of considering ecoregional differ- this species among dominants of soil microar- ences during the analysis of the effect of fire on thropod communities is assumed to indicate soil springtails. The revealed ecoregional specifici- disturbance (Kuznetsova, Krest’yaninova, ty is even more important if we analyze collem- 1998). Our findings on the effects of fire on the bolan communities at the family level. The springtail dominance structure further support reduction of Arrhopalitidae abundance in the this assumption for two ecoregions, as the abun- burnt plots and the respective increase of the dance of I. minor considerably decreased in the number of Onychiuridae only in Smolensk-Pri- burnt forests in Kola-Karelian and Smolensk- uralskiy ecoregion further highlights a very com- Priuralskii ecoregions. Similar pattern was dis- plex interaction between the effect of macroen- covered for the abundance of W. anophthalma. vironmental factors and fire effects across ex- Relatively high abundance and good represen- tensive biomes like boreal forests (Hennig-Sev- tation of the mentioned species allows suppos- er et al., 2001; Urbanovičova et al., 2013). ing them as good indicators of disturbances Unlike the abundance, forest fires have a associated with recent forest fires. Indeed Malm- quite moderate effect on the springtail commu- ström (2012) during her long-term study of the nity faunistic composition five years after burn- post fire recovery of springtail communities ing. Fire-induced shifts in the faunistic compo- also found this species among ones who demon- sition are overruled by ecoregional differences. strated reduced abundance for many years after This points at the necessity of considering local a fire event. Nevertheless, in Pribaltiiskiy- environmental conditions when making spatial- Vetluzhskiy ecoregion, total abundance of ly extensive projections of the fire effects on soil I.minor was slightly higher in burnt plots than in communities and soil biodiversity in particular controls. We explain this by higher thermal (Zaitsev et al., 2016). Despite that, fires had the insulation of the lower soil layer, which could ecoregion-specific impact on the springtail abun- provide better survival for soil living species dance and richness of species sharing certain biogeographic distribution types. The increase 124 R.A. Saifutdinov et al. of west-palaearctic species richness and abun- Babenko A.B., Chernova N.M., Potapov M.B., Stebaeva dance in the burnt forest plots of Smolensk- S.K. 1994. [Collembola of Russia and adjacent coun- tries: Family Hypogastruridae]. Moscow: Nauka. 335 Priuralskiy ecoregion suggests that this group is p. [In Russian] biogeographically more closely bound to the Babenko A.B., Fjellberg A. 2006. Collembola Septentrio- study biome. More consistent decrease of trans- nale. A catalogue of springtails of the Arctic regions. holarctic species richness and abundance in Moscow: KMK Scientific Press. 190 p. burnt plots could be explained by wider distri- Bazilevich N.I. 1993. [Biological Productivity of Ecosys- tems in Northern Eurasia]. Moscow: Nauka. 293 p. [In bution of this group, which probably leads to Russian] reduced resistance to regional-specific distur- Borisov B.A., Ganzhara N.F. 2008. Geographical features bances. of the distribution and renewal of easily decompos- We conclude that five years after burning, able organic matter in virgin and arable zonal soils of European Russia // Eurasian Soil Sci. Vol.41. No.9. springtail community faunistic composition in P.946–952. the Russian North-West taiga forest is only Bretfeld G. 1999. Synopses on Palearctic Collembola. slightly affected by fire-induced disturbances // Abh. Ber. Naturkundemus. Görlitz. and is rather determined by ecoregional differ- Vol. 71. No.1. P.1–318. ences. There is a certain group of springtail Chernova N.M., Kuznetsova N.A. 2000. Collembolan community organization and its temporal predictabil- species, which benefit from the post-fire effects. ity // Pedobiologia. Vol.44. No.3. P.451–466. Obviously, this positive response of some spe- Engelmann H.D. 1978. Zur Dominanzklassifizierung von cies to burning occurred due to lack of predation Bodenarthropoden // Pedobiologia. Vol.18. P.378– and higher ecological plasticity of these spring- 380. Fjellberg A. 1998. Collembola of Fennoscandia and Den- tail species. However, even slight shifts in the mark: Poduromorpha. Part I. Leiden: Brill. 184 p. species composition after fire result in the chang- Fjellberg A. 2007. Collembola of Fennoscandia and Den- es of the spectra of the species biogeographic mark: Entomobryomorpha and Symphypleona. Part distribution types in pyrogenic forests. It is very II. Leiden: Brill. 266 p. important to encounter for the type of distur- Henig-Sever N., Poliakov D., Broza M. 2001. A novel method for estimation of wild fire intensity based on bance when estimating the sensitivity of species ash pH and soil microarthropod community // Pedobi- to the environmental degradation processes. ologia. Vol.45. No.2. P.98–106. Hopkin S.P. 1997. Biology of the springtails (Insecta: Collembola). Oxford: Oxford University Press. 340 p. Acknowledgments Hopkin S.P. 2007. A key to the Collembola (springtails) of The authors are grateful to the regional for- Britain and Ireland. Shrewsbury: Field Studies Coun- est authorities of the Murmansk, Moscow, and cil. 245 p. Tver Regions, as well as the Republic of Karelia Huhta V., Persson T., Setälä H. 1998. Functional implica- tions of soil fauna diversity in boreal forests // Appl. for providing us with the data on the location Soil Ecol. Vol.10. No.3. P.277–288. and history of burnt forests. We express our IUSS Working Group WRB. 2015. World Reference Base gratitude to Dr. Arne Fjellberg and Dr. Mikhail for Soil Resources 2014, update 2015 International Potapov for valuable taxonomic advice during soil classification system for naming soils and creat- this work. We thank D. Korobushkin, S. Sha- ing legends for soil maps // World Soil Resources Reports No. 106. FAO. Rome. 193 p. khab, T. Yazrikova, A. Gorbunova, and A. Juceviča E., Melecis V. 2002. Long-term dynamics of Zaytseva for the assistance during sampling and Collembola in a pine forest ecosystem: Proceedings of extraction of animals. the Xth international Colloquium on Apterygota, Èeské The study was supported by the Russian Budìjovice 2000: Apterygota at the Beginning of the Third Millennium // Pedobiologia. Vol.46. No.3. Science Foundation grant # 14-14-00894. P.365–372. Kozlov M.V. 2014. [Planning of ecological research: the- ory and practical recommendations]. Moscow: KMK References Scientific Press. 171 p. [In Russian] Kuznetsova N.A. 1985. [Fauna and population of spring- Babenko A.B. 2012. Springtails (Hexapoda, Collembola) tails in coniferous forests of the European part of the of tundra landscapes of the Kola Peninsula // Entomol. USSR] [Candidate’s Dissertation in Biology]. Mos- Rev. Vol.92. No.5. P.497–515. cow. 286 p. [In Russian] Springtail fauna in the burnt boreal forests of European Russia 125

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и

космополит биогеографического восточно

: C — Типы , EP — , n=4). встречающихся

часто

ошибка . гренландский распространения

станд Тип , G — . ± Численность среднее , шрифтом

–2 (2012). м . экз палеарктический ( - жирным

Бабенко

, mean ± SE, n=4). Biogeographic distribution types are provided according и –2 западно выделена

(2006) экорегионах

, WP — . Фъельбергу экорегионах

и исследуемых

в

палеарктический - Бабенко

по

исследуемых распространением

найденных

транс всех

во

, TP — представлены неизвестным ногохвосток

с найденных видов

, , Unk — голарктический - видов

Список Appendix 1 Species list of springtails found in the studied ecoregions (indiv. m ческий транс ных распространения Babenko and Fjellberg (2006) (2012). The abundance of the most frequent abundant collembolan species found in a ecoregions shown in bold. Species range: C — cosmopolitan, TH trans-holarctic, TP trans-palaearctic, WP west-palaearctic, groenlandic, EP — east-palaearctic, Unk unknown distribution. Springtail fauna in the burnt boreal forests of European Russia 127 128 R.A. Saifutdinov et al. Springtail fauna in the burnt boreal forests of European Russia 129 130 R.A. Saifutdinov et al. . идентификации

для

значимых , хет

групп

или

тела

частей

отсутствия

ввиду

определены

не

виды * species was not identified due to missing body parts or groups of setae relevant for identification. *