Snow microhabitats provide food resources for winter-active Collembola
Introduction
The feeding ecology of soil animals is seldom investigated in winter when the soil is covered with a layer of snow. Collembola tolerate subzero temperatures and often appear in large numbers on snow-covered surfaces (Hågvar, 2010, Zhang et al., 2014). Some species such as Hypogastrura socialis and Isotoma hiemalis are specifically adapted to snow environments (Hågvar, 2000). Winter-active Collembola can migrate from microhabitats under the snow (subnivean) to those in the snow (intranivean) and at the snow surface (supranivean) (Brummer-Korvenkontio and Brummer-Korvenkontio, 1980). They were observed to migrate 0.8–1 m per minute on the snow surface (Hågvar, 1995, Zhang et al., 2017). The winter activities of Collembola, in theory, are sustained by food resources present in snow microhabitats. For example, algae and fungi are important food resources for winter-active Collembola (Hoham and Duval, 2001, Bokhorst and Wardle, 2014). Bacteria inhabiting snow layers may also be ingested by Collembola (Haubert et al., 2006, Ruess et al., 2007). Since bacterial communities in snow differ from those in soil or in the litter layer (Yang et al., 2016, Männistӧ et al., 2018), supranivean Collembola may feed directly on supranivean or intranivean bacteria and therefore probably associate with different bacterial communities than those living in soil and litter. Since Collembola feeding habits were mainly studied during snow-free periods of the year (Anderson and Healey, 1972, Anslan et al., 2018, Ding et al., 2019), the food resources of winter-active species are relatively unknown. We therefore used stable isotope tracing (natural abundance) and bacterial 16S rRNA gene amplicon sequencing techniques to explore the potential food resources of winter-active Collembola.
Nitrogen and carbon stable isotope (δ15N and δ13C) techniques are suitable to study the trophic position and feeding habits of soil animals (Peterson and Fry, 1987, Post, 2002, Potapov et al., 2019). The concentration of heavy nitrogen isotope 15N increases from a food source to its consumers by 3.4 δ units, thus, the higher the trophic position of a species, the higher its 15N concentration (Post, 2002). In contrast, the concentration of 13C changes little from diet to consumer, so it is a tracer of carbon sources used by the consumer (Peterson and Fry, 1987, Post, 2002). In Collembola, the δ13C value is closer to that of roots than that of litter, suggesting that the food supply of Collembola is derived from plants roots (Endlweber et al., 2009). The range of δ15N values is higher in euedaphic Collembola than in other life forms (Potapov et al., 2016), probably because euedaphic species consume a variety of food resources (Ponge, 2000). Microorganisms and non-vascular plants that colonise and grow in snow are potential food resources for Collembola active in winter (Bokhorst and Wardle, 2014, Potapov et al., 2018). Stable isotope signatures can therefore suggest trophic positions of winter-active Collembola in soil food web (Scheu and Falca, 2000, Potapov et al., 2019).
Recent developments in molecular methods have advanced our knowledge of arthropod-microbial associations (Zhu et al., 2018, Ding et al., 2019, Zhang et al., 2019). In contrast to stable isotopes which reflect food resources in a long term, microbiota in animal tissues or organs may suggest those food resources recently ingested by the consumer (Anslan et al., 2016, Gong et al., 2018). The food resources are in the process of being digested and converted into organic substrates, which can be further metabolized to provide energy for consumer or synthesised into storage tissue (Haubert et al., 2006, Bokhorst and Wardle, 2014, Agamennone et al., 2019). Collembola may prefer to feed on certain soil bacteria, such as the widespread Pseudomonas putida (Thimm et al., 1998, Haubert et al., 2006). The food resource bacteria of Collembola may thus differ from those in the environment. In contrast, bacteria detected in Collembola body tissue but rare, or even absent, in the external environment, may function as symbionts helping host to digest certain resources or regulating host physiological functions (Simpson et al., 2015). For example, chitinolytic microorganisms in Folsomia candida may contribute to the degradation of chitin (Borkott and Insam, 1990). Wolbachia, another common colonisers associated with Collembola, are important and widespread symbiotic bacteria that manipulate host reproduction (Werren et al., 2008, Czarnetzki and Tebbe, 2010). In the present study we applied 16S rRNA gene amplicon sequencing technique to identify the bacteria ingested by or associated with winter-active Collembola.
Since bacterial communities may vary with phylogenetic affinity of the host (Delsuc et al., 2014, Gong et al., 2018), we compared the bacterial communities in two congeneric species from Isotomidae, Desoria sp.1 and Desoria sp.3 (following Zhang et al., 2014), with that of a species from another family, Tomocerus cf. jilinensis (Tomoceridae). We considered the three species as the model winter-active arthropods in our study system. The two Desoria species are extremely abundant at the snow surface but not found in the growing season (Chang et al., 2013, Zhang et al., 2014). Tomocerus cf. jilinensis, however, is rare supranivealy but frequent in subnivean habitats (D. Wu, pers. comm.). Adaptation to extreme winter and to different snow microhabitats among the three species thus provides an opportunity for studying the feeding ecology of typical soil arthropods in winter. Since Desoria and Tomocerus cf. jilinensis live in different microhabitats, they are likely to harbour different microbial communities and may differ in stable isotope signatures.
In the study we aimed at providing evidences on microbiomes and stable isotope signatures of the winter-active Collembola species, with a specific focus on the potential food resources. We hypothesised that: (i) more food resources of winter-active Collembola are derived from snow than litter; (ii) the food resources of the two winter-active supranivean Desoria species will be similar, and their diets will differ from that of Tomocerus cf. jilinensis, which live in subnivean habitats partly in contact with litter; and (iii) winter-active Collembola have a large proportion of bacteria absent in the environment, which are potential symbionts. Finally, we discussed the possibility that metabolic functions were related to the presence of ingested and symbiotic bacteria in the winter-active Collembola.
Section snippets
Study site
This study was conducted in a wetland region dominated by Calamagrostis angustifolia at the Sanjiang Mire Wetland Experimental Station (47°35′N, 133°31′E) in Heilongjiang Province, northeastern China. This region is a low alluvial plain formed by the Heilong, Songhua, and Wusuli rivers and has a temperate-humid to sub-humid continental monsoon climate. Mean annual temperature ranges from 1.4 to 4.3 °C, with an average maximum of 21–22 °C in July and an average minimum of -21 to -18 °C in
Stable isotope signatures
Both δ13C and δ15N indicated that winter-active Collembola probably fed on resources from snow and partly on resources from litter depending on the species or their microhabitats (δ13C, F4,10 = 30.59, P < 0.001; δ15N, F4,10 = 82.79, P < 0.001, one-way ANOVA; Fig. 1). The two supranivean Desoria species had higher δ13C values than that of litter, while the subnivean Tomocerus cf. jilinensis had an intermediate δ13C value, higher than litter but more similar to snow. The δ15N of Tomocerus cf.
Food resources of winter-active Collembola
By combining stable isotope techniques and microbiome analysis, our results indicate that winter-active Collembola mainly fed on resources from snow microhabitats and partly on resources from litter, supporting the first hypothesis. Snow microhabitats, compared with litter, have higher values of δ13C and δ15N. Collembola feeding on the food resources in snow microhabitats are thus enriched in stable isotopes. Phototrophic microorganisms, including algae and cyanobacteria, may be these food
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This present study was supported by the National Natural Science Foundation of China (No. 41671259 and No. 41430857), the Program of Introducing Talents of Discipline to Universities (No. B16011), the National Science & Technology Fundamental Resources Investigation Program of China (No. 2018FY100300), the Open Project Program of Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University (No. 1300289104) and the Key Research Program of Frontier
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2022, Journal of Thermal BiologyCitation Excerpt :However, some arthropods remain active even at temperatures close to or below 0 °C. Invertebrates active during winter include species from oligochaetes, gastropods, centipedes (e.g., Aitchison, 1979), springtails (e.g., Hågvar, 2010; Hao et al., 2020), stoneflies (e.g., Hågvar, 2010), earwigs (e.g., Soszyńska-Maj and Jaskuła, 2013), ground beetles (e.g., Jaskuła and Soszyńska-Maj, 2011), dipterans, snow fleas (e.g., Hågvar, 2010), and spiders (e.g., Hågvar, 2010; Korenko et al., 2010). Spiders of temperate zones usually surpass the harsh winter period in a state of dormancy, hibernating in different ontogenetic stages (the adult, juvenile, or egg stages), depending on how their developmental cycles are controlled by environmental temperature and photoperiod (Schaefer, 1977).
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These authors contributed equally to this paper.