Seasonal fluctuation of oribatid mite communities in forest microhabitats

Introduction

The stability of belowground systems is driven by biotic (community composition, biodiversity or competition) and abiotic (precipitation, air temperature or soil chemistry/nutrients) factors (Seastedt, 1984; Wardle, 2006; Eisenhauer et al., 2012). Especially nutrient cycling and decomposition are important processes for the persistence of forests and their biota (Peterson & Luxton, 1982; Smith et al., 2014). While functional roles and contributions of soil fauna—for example protozoans, nematodes, collembolans, oribatid mites and earthworms—have been studied to some extent (Bayoumi, 1978; Eisenhauer, 2010; Maaßet al., 2015; Soong & Nielsen, 2016), mechanisms driving soil fauna diversity remain enigmatic (Eisenhauer et al., 2017).

Oribatid mites (Oribatida, Arachnida) are among the most diverse and abundant animal decomposers. The approximately 16,000 described species (Schatz et al., 2011) are collectively ubiquitous, yet individual species are unevenly distributed in all major forests and grasslands, and also in aquatic habitats all over the world (Wallwork, 1983; Schatz, 2005; Schatz & Behan-Pelletier, 2008). In temperate forests, oribatid mite species tend to inhabit different microhabitat patches and therefore their communities are unequally distributed among mineral soil, litter, mosses, lichens, dead wood or tree bark (Aoki, 1967; Arroyo, Kenny & Bolger, 2013; Wehner et al., 2016). This specificity may be caused by differences in microhabitat structure (e.g., small vs wide pores, continuous (litter) vs. insular (tree bark, moss); Nielsen et al., 2008), microclimatic conditions (e.g., moisture, exposure; Nielsen et al., 2010), spatial resource heterogeneity (Nielsen et al., 2010) or biotic interactions (e.g., predation; Hammer, 1972; Gao et al., 2014). While litter and forest soils are continuous and relatively stable habitats (Maraun & Scheu, 2000), the most unique oribatid mite fauna is found on trees (Lindo & Winchester, 2006; Skubala & Gurgul, 2011; Lindo & Winchester, 2012).

Oribatid mite communities in forest soil systems are affected by small- and large-scale environmental factors (Nielsen et al., 2008; Nielsen et al., 2010; Corral-Hernández, Balanzategui & Iturrondobeitia, 2016). Due to their small size and restricted dispersal ability, soil communities and especially oribatid mites therein mainly respond to local rather than regional factors (Erdmann, Scheu & Maraun, 2012; Bolger et al., 2014; Corral-Hernández, Balanzategui & Iturrondobeitia, 2016). Spatio-temporal patterns of oribatid communities inhabiting different forest microhabitats have largely been neglected in the past (Gergócs et al., 2011).

In general, most adult oribatid mite species tend to prefer distinct microhabitats (e.g., litter, moss patches, dead wood, lichens, grassy sods, bark of trees) if conditions are favourable (Wehner et al., 2016). For example, Wehner et al. (2016) reported that the microhabitat ‘litter’ provides the most stable ecological conditions and seems to function as habitat for litter specialists (e.g., Hypochthonius rufulus; Habitat-Hypothesis) and “refuge” for generalists during unfavourable conditions (e.g., Chamobates cuspidatus, Carabodes spp.; “Connector-Hypothesis”). Nevertheless, in more patchy microhabitats such as mosses, dead wood or lichens, overall abundance and diversity of oribatid mite communities can exceed those of litter (Skubala, 2008; Wehner et al., 2016). The interaction of factors driving the distribution patterns of oribatid mite species within and among different microhabitats are complex. Besides high niche dimensionality and resource portioning (Mitchell, 1979; Wardle, 2002) as well as differential rates of activity (Chase & Leibold, 2003), environmental variables and local species interactions are of great importance (Caruso, Toarmina & Migliorini, 2012; Maaßet al., 2015). We further assume local weather and seasonality of community structure to influence distribution pattern of oribatid mite species.

Seasonality of oribatid mites have mainly been investigated in soil and litter habitats in Middle European forests (Harding, 1969; Hammer, 1972; Mitchell, 1977; Schenker, 1984). However, since oribatid mite groups differ in their ecology (i.e., small, fast reproducing Oppiidae vs large, slowly reproducing Nothrina), results of seasonality studies are not always consistent (Schenker, 1984) Generally, seasonality changes seem to be small, but adult oribatid mites tend to show one to two peaks of high abundances (Harding, 1969; Hammer, 1972; Luxton, 1972) caused by their reproductive cycle (i.e., egg deposition in spring, large numbers of nymphs in May and June, adults in late summer; Hammer, 1972).

In this study, we aimed to (i) investigate seasonal fluctuation in oribatid-mite community structure in, and specificity to three different forest microhabitats (moss, dead wood and litter) and (ii) understand the influence of weather (air temperature and relative air humidity) on community changes. Therefore, we investigated abundance, richness and diversity in these micro-communities monthly over one year and analyzed community structure using microhabitat-specific bipartite networks. Furthermore, we calculated an environmental occurrence niche model (Chisté et al., 2016; Mangels et al., 2017) for each oribatid mite species to understand and explain their distributions among microhabitats and changes in network structure. We hypothesized that (i) the microhabitats (moss, dead wood, litter) differ in their community structure (abundance, species richness and Shannon diversity of oribatid mites) and that (ii) seasonality of species distribution and specialization differs according to community composition and microhabitat structure. We further assumed that (iii) seasonality is driven by weather conditions (air temperature, air humidity) in all three microhabitats.

Materials and Methods

Results

In total, we collected 57,398 adult oribatid mite individuals, representing 57 species; two genera (Carabodes, Tectocepheus) and three families (Brachychthoniidae, Phthiracaridae and Suctobelbidae) were not determined to the species level. In general, Brachypylina were most abundant (50 taxa), followed by Nothrina (five taxa), Enarthronota (four taxa) and Mixonomata (three taxa; Table 1; see Table S2 for detailed overview). We found no species from the infraorders Paleosomata or Parhyposomata.

As expected, air temperatures were highest from April to October (between 11 and 18 °C) and lowest in winter months (between 0.4 °C in December and 7.4 °C in February; Table 2). Relative air humidity (Table 2) was lowest in May (58%), followed by January (79%), April (88%) and September (89%), highest values were measured in March and November (100%), yet there was no clear humidity trend over the year. Air temperature and air humidity were not significantly correlated (Spearman’s rank: ρ_s =  − 0.14, P = 0.66).

All community parameters (total abundance, species richness and effective Shannon diversity) significantly fluctuated over the year (Figs. 1–3). Total abundance of adult oribatid mites (Ind/kg dry weight) showed a microhabitat specific change over the year (Table 3, Fig. 1). Total abundance was highest in moss and lowest in dead wood. Seasonal changes were most pronounced in moss (having highest abundance from March to July) and least in litter (Fig. 1). Both air temperature and air humidity had no significant influence on total abundance (Table 3).

Species richness also showed a significant microhabitat specific trend over the year (Table 3, Fig. 2A), being highest in moss from April to July and in October/November. In January and February, as well as in December, species richness was highest in dead wood and litter. Air temperature significantly influenced species richness in moss, but had no effect on dead wood and litter (Table 3, Fig. 2B). Again, air humidity had no significant effect (Table 3).

Effective Shannon diversity (e^H) showed a significant microhabitat-specific trend over the year (Table 3, Fig. 3A). While e^H was highest from May to November in moss, it remained constant (but lower) in dead wood. In litter, e^H was lowest in April and November, but exceeded e^H of moss in winter (December to March). Again, air temperature had a significant influence on e^H depending on the microhabitat: in moss e^H increased with air temperature, while there were no trends in dead wood and litter (Table 3, Fig. 3B). Air humidity did not influence e^H of oribatid mites in any microhabitat (Table 3).

Network analyses revealed changes in species distribution and specialization to the three microhabitats over the year (Table 1, Figs. 4A–4L). In general, the pooled bipartite network for all months (Fig. 4M) showed that the majority of oribatid mite species occurred in all three microhabitats (but in different frequencies) and thus was highly generalized ($H_2^{\prime }=0.156$). Focusing on individual microhabitats, however, oribatid mites showed higher generalization for moss (d′ = 0.076) as compared to dead wood (d′ = 0.134) and litter (d′ = 0.274). Comparison with null models revealed that this partitioning of mite communities across the microhabitats is a non-random distribution (all null models for every month: observed $H_2^{\prime }\gg$ null model $H_2^{\prime }$; P < 0.001). The monthly network structures were similarly partitioned as the pooled network (Fig. 4), yet $H_2^{\prime }$ changed during the year (Table 2), but the community structures of consecutive months were highly correlated (Fig. 5). Communities of May and June were not correlated (r = 0.10; P > 0.05), resulting in a change of the bipartite network graph (i.e., moss in the central position; Fig. 4) based on d′ of the microhabitats (Table 2). Additionally, the overall microhabitat specificity $H_2^{\prime }$ changed with air temperature (Table 2; Gaussian GLM: F_1,10 = 11.34, P < 0.001), but not with air humidity (Gaussian GLM: F_1,10 = 0.44, P = 0.51), indicating a more generalized distribution of oribatid mites at higher ambient air temperatures.

In addition, the standardized Kullback–Leibler divergence d′, representing the exclusiveness of the species found in a particular microhabitat per month, changed during the year (Table 2) and the three microhabitats differed significantly within each month (pairwise comparisons of $H_2^{\prime }$-distances; all P < 0.01). Similar to the complementary specialization of the whole bipartite network ($H_2^{\prime }$), d′ values were lower in spring/summer (indicating a more generalized community in a given microhabitat) and higher in winter (indicating a more specialized community). Again, d′ values (Table 2) in microhabitats over the year were significantly influenced by air temperature (MANOVA: Wilk’s λ = 0.32, F_1,10 = 5.58, P = 0.023), but not by relative air humidity (MANOVA: Wilk’s λ = 0.67, F_1,10 = 1.29, P = 0.34). The effect of air temperature on d′ was driven by the changes of species exclusiveness in dead wood (univariate ANOVA: F = 18.72, P = 0.001) and moss (univariate ANOVA: F = 9.53, P = 0.012), while litter remained stable (univariate ANOVA: F = 1.61, P = 0.23).

The environmental occurrence niche analysis for air temperature μ_i (ϑ) revealed a generally broad temperature niche (=standard deviation of μ_i, Fig. 6) for each oribatid mite species (5.3 ± 1.3 °C; mean ± SD). Comparisons with null models showed 39 out of 55 taxa had a non-random distribution across all months (and affiliated air temperatures), thus showing significant temperature niches μ_i (ϑ) (see asterisks in Fig. 7). While 35% of the species significantly occurred at higher air temperatures, 10% occurred in colder months, 25% reacted neutral with a μ_i (ϑ) near the mean annual air temperature (ϑ ≈ 10°C) and 30% showed no significant response (Fig. 7; Table S3). The environmental niche for relative humidity μ_i (RH) was also relatively broad for most oribatid mite species (12.0 ± 4.5%RH; mean ± SD), and according to null model comparisons 44 out of 55 taxa showed a non-random distribution related to relative air humidity across the year (see Fig. S1). Compared to air temperature, however, 60% of all species showed a significant neutral reaction to air humidity, while only 9% and 10% occurred at drier or wetter conditions, respectively, and 20% showed no significant response (see Table S4). Both environmental niches must be understood as “occurrence or distribution niche”, meaning that a certain oribatid mite species could most likely be found in the microhabitats investigated at a species-specific temperature or humidity range.

Discussion

Most oribatid mite species were generally found in all three investigated microhabitats, but their distribution among them was unequal and fluctuated over the year. Moss had the highest individual abundance, but showed the strongest seasonal changes. When air temperatures were high, moss also had the highest species richness and diversity. Dead wood was characterized by a stable Shannon diversity indicating that this microhabitat is mainly inhabited by dead wood specialists that also occur in other microhabitats in low numbers. Litter was the most stable microhabitat over the year showing no influences of ambient air temperature and diversity only tended to increase with increasing air humidity.

All community parameters (abundance, species richness, diversity) confirmed former studies. The presence of a highly abundant oribatid mite community in mosses is well known (Aoki, 1967; Glime, 2013; Skubala, 2016; Wehner et al., 2016). Many oribatid mite species use mosses as microhabitat during their life cycle, for food or shelter, and associations can even be mutualistic (Cronberg, Natcheva & Hedlund, 2006; Glime, 2013). Dead wood is a special microhabitat that changes during its decomposition and provides special climatic conditions (Lachat et al., 2012). Mites associated with dead wood seem to increase the suitability of organic particles for decomposers (Norton, 1990) and contribute to both nutrient cycling and soil formation (Wallwork, 1979). Depending on the type of woody debris (e.g., coniferous or deciduous forests), reported densities and diversity values of dead wood-dwelling oribatid mite communities vary (Seastedt, Reddy & Cline, 1989; Skubala & Duras, 2008; Skubala, 2008). Additionally, the proportion of dead-wood specialists in such micro-communities has been controversial (see Skubala, 2008). While the proportion of specialists seems low in many studies and most dead-wood inhabitants can also be found on the forest floor (Seastedt, Reddy & Cline, 1989; Johnston & Crossley, 1996; Wehner et al., 2016), Skubala & Duras (2008) considered 63% of the species in downed logs to be specialists.

Although many studies on oribatid mites focus on the litter layer, this microhabitat is characterized by lower abundances compared to moss and dead wood. Nevertheless, litter provides a continuous refuge supplying food and protection for both litter specialists and those species retreating from microhabitats that are more disturbed (e.g., from moss patches if they are flooded or desiccated), indicated by constant abundances but fluctuating diversity parameters. Overall, our results confirmed the expectation that oribatid mite assemblage in moss, dead wood and litter differ in their community structure. Therefore, the variety of microhabitats contributes to the general animal species diversity in forest soil communities (Hammer, 1972; Wardle, 2002; Caruso, Toarmina & Migliorini, 2012; Bolger et al., 2014).

Although the distribution pattern and composition of oribatid mite communities are known from many studies, the mechanisms that affect these different community structures are more difficult to understand (Gergócs et al., 2011). Factors driving the distribution pattern of oribatid mite assemblages comprise niche dimensionality, resource portioning and resource quality, dispersal ability, local interactions and environmental filtering processes (Scheu & Drossel, 2007; Caruso, Toarmina & Migliorini, 2012; Maaßet al., 2015) and may affected by seasonality of communities. Our results indicate that seasonality of oribatid mite assemblages differ among microhabitats. Changes in abundances over the year were most pronounced in moss, probably due to strong alterations of the microhabitat structure during harsh environmental conditions such as drought or snow (Glime, 2013). Furthermore, changes in species richness and Shannon diversity may point to the usage of mosses as food resource by many different species. Seasonal changes of species abundances in litter were very low while fluctuations of diversity parameters were more pronounced, yet the exclusive specialization (d′) of oribatid mites towards this habitat also remained stable These results further emphasize the stability of the litter microhabitat and its function as an oribatid mite pool and transitional substrate for species dispersing to other microhabitats (“Connector-Hypothesis”; see Wehner et al., 2016).

In general, the composition of oribatid mite communities seems not to be seasonal but somehow related to temperature (Mitchell, 1977; Schenker, 1984; Stamou & Sgardelis, 1989; Webb et al., 1998; Irmler, 2006; Gergócs et al., 2011). Already, Schenker (1984) found species diversity to be higher at warmer temperatures. Irmler (2006) conducted a study in a beech forest in Germany over a period of seven years and observed no seasonality, but instead detected strong connection to annual mean air temperature. Similarly, Gergócs et al. (2011) found no seasonal change or recurring pattern of oribatid mite communities in a study over one and a half years in leaf litter and foerna substrates, but communities in moss were influenced by temperature (Gergócs et al., 2011).

Generally, the results of our study support the importance of ambient air temperature for structuring oribatid mite communities and again illustrate the need to investigate different microhabitats in order to obtain a complete picture of diversity at a forest site. However, differences in diversity are temperature-dependent rather than static. The complementary specialization of oribatid mite species towards different microhabitats changed from being slightly specialized at lower temperatures to more generalized (i.e., species are more equally distributed among litter, moss and dead wood) if air temperatures were high. While $H_2^{\prime }$ followed this clear trend, the communities on which the networks based were highly correlated with each other. Only the months May and June were not correlated, because the exclusive specializations (d′) for moss and litter were much lower in June compared to May, yielding a lower overall $H_2^{\prime }$. This again indicates a relatively high stability of microhabitat specialization of oribatid mite assemblages in consecutive months.

The increase of generalization at higher air temperatures is probably due to a broad environmental temperature occurrence niche of most oribatid mite species. However, while 30% did not react to air temperature, more species (35%) occurred at warmer air temperatures. For example, Cymberemaeus cymba and Camisia segnis occurred in moss, dead wood and litter only at air temperatures above the mean value of about 10 °C. Both species are known as typical inhabitants of tree bark (Behan-Pelletier & Walter, 2000; Erdmann et al., 2007) which is an insular microhabitat as compared to the continuous litter. Oribatid mite species living in these specialized, insular microhabitats must disperse more significant distances than litter species and the dispersal behavior that takes them into the litter ‘highway’, for example, may have some temperature threshold. If conditions are unfavorable for them to actively disperse, they ‘stay home’, i.e., the specialists enter a dispersal mode only at warmer air temperatures.

Furthermore, juveniles of highly specialized species are tightly bound to the microhabitat (e.g., burrowers in wood and lichen; Lebrun et al., 1991), while adults actively disperse only when development is complete. Additionally, the effect of temperature may be indirect via changing resource availability, the reproductive success or potentially predation pressure that forces oribatid mites to leave their favorite microhabitats. However, these assumptions need further investigation in future studies.

Conclusions

Microhabitat specificity seems to increase at months with lower air temperatures. Most adult oribatid mite species have broad environmental temperature occurrence niches preferring higher temperatures. Therefore, if climatic conditions are unfavorable, species, especially those in specific, insular microhabitats, do not enter the dispersal mode but retreat to their specific terrain. Generally, seasonal changes in abundances are lowest in litter, intermediate in dead wood and highest in mosses, pointing to differences in microhabitat stability during seasons. On the other hand, seasonal changes of diversity parameters may be explained by dispersal dynamics of oribatid mite species among different microhabitats probably due to changing food conditions at warmer temperatures.

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