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Article

Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests

by
Essivi Gagnon Koudji
1,*,
Emma Despland
2,
Anne-Sophie Caron
2 and
I. Tanya Handa
1,*
1
Département des Sciences Biologiques, Université du Québec à Montréal (UQAM), 141 av. Président-Kennedy, Montreal, QC H2X 1Y4, Canada
2
Biology Department, Concordia University, 7141 Sherbrooke West, Montreal, QC H4B 1R6, Canada
*
Authors to whom correspondence should be addressed.
Forests 2023, 14(7), 1302; https://doi.org/10.3390/f14071302
Submission received: 6 May 2023 / Revised: 9 June 2023 / Accepted: 14 June 2023 / Published: 25 June 2023
(This article belongs to the Special Issue Herbivory as a Driver of Forest Dynamics and Biodiversity)
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Abstract

:
Outbreaks of defoliator insects are important natural disturbances in boreal forests, but their increasing frequency under warming climate conditions is of concern. Outbreak events can shape ecosystem dynamics with cascading effects through trophic networks. Caterpillar defoliation can alter tree physiology, increase sunlight to the understory, and result in the deposition of large amounts of leaf litter and caterpillar frass to the forest floor. These modifications can thus affect soil organisms through direct (e.g., changes in soil temperature or moisture) or indirect (e.g., changes in detrital and root food webs) mechanisms. We assessed whether a recent (2015 to 2017) outbreak of the forest tent caterpillar (Malacosoma disstria) at the Lake Duparquet Teaching and Research Forest (Abitibi, QC, Canada) affected soil springtail communities, abundant microarthropods in forest soils. In 2018 and 2019, we sampled litter and soil (0–10 cm depth) at eight sites each in aspen-dominated (Populus tremuloides Michx) stands that were undefoliated or had a recent defoliation history. We found no significant difference in springtail abundance (specimens cm−2) or alpha diversity indices between undefoliated sites and those with defoliation history. However, we observed a transient change in springtail community composition 1 year after the outbreak (2018) with the absence of Folsomia nivalis, Anurophorus sp1, and Xenylla christianseni in sites with defoliation history, but no compositional differences were observed in 2019. Certain soil nutrients (P, C, Mg, Mn) were significant predictors of springtail community composition, but soil microbial biomass was not, despite its significant decrease in sites with defoliation history. Our results show that soil springtail communities respond in the short-term to the forest tent caterpillar outbreak with compositional shifts, but seem ultimately resilient to these events.

Graphical Abstract

1. Introduction

Insect herbivore dynamics are directly affected by global climate change [1,2,3]. Insect outbreaks are increasing in intensity and frequency, due to increases in insect development rate, overwinter survival, and geographic range [4,5]. The forest tent caterpillar (Malacosoma disstria) is a well-known epidemic defoliator in North America [6]. It is a major source of natural disturbance in hardwood forests [6,7]. In Canada’s boreal forest, it has had an outbreak cycle between 9 and 13 years [7,8], and its main host is aspen (Populus tremuloides) [9,10].
The forest tent caterpillar, as other outbreak insects, can significantly decrease tree growth and cause mortality [11,12,13,14], as well as alter tree survival, vegetation regeneration, and canopy openness [15,16,17,18]. Mechanisms include both direct and indirect consequences of defoliation. For example, defoliated trees typically undergo physiological changes leading to direct effects, such as the synthesis of secondary metabolites in leaves that reduce the palatability of leaves for herbivores [19,20]. Another effect is the reduction in tree canopy that can increase temperature, moisture, and light exposure on the forest floor [10,15]. Balducci et al. (2020) [21] showed that insect outbreaks over a long period of time increased soil moisture under balsam fir while reducing its water potential. Outbreak events can thus cause important cascading effects within ecosystems affecting soil food webs and nutrient cycles [22,23,24].
Mechanisms that can prompt changes in soil ecosystems after defoliation include the falling excrement and carcasses of forest tent caterpillar that provide additional nutrient inputs and may affect soil nutrient cycling dynamics [25] and stimulate soil microbial growth [26,27]. Defoliation can also alter resource allocation to roots and root exudation of the plant [9,28]. In general, carbon levels decrease after an insect outbreak, while nitrogen levels do not; this sometimes leads to a decrease in root biomass and root exudates [28,29,30]. All these changes in the aboveground portion of the vegetation may have repercussions on nutrient cycling in the soil [31] and influence the soil food web [23,32]. Indeed, given potential aboveground and belowground interactions, trophic cascades caused by the forest tent caterpillar outbreak could affect soil organisms [29,33,34] as well as soil microclimate and soil nutrients [10,25,35].
Springtails (Collembola) are among the largest, most diverse groups of arthropods in the litter and soil, after mites [36,37,38,39]. Springtail abundance worldwide is impressive with the total biomass of soil springtails currently estimated at 27.5 megatons of carbon, three times more than wild terrestrial vertebrates [39]. Multiple studies have shown that springtails are sensitive to various disturbances in forest ecosystems, and thus are interesting indicators [40,41,42]. In soil food webs, springtails regulate microorganisms, such as bacteria and fungi [43,44,45]. They participate indirectly in the mineralization of soil organic matter by stimulating the microbial community [46,47,48]. They inhabit a variety of environments depending on their diet; within the leaf litter layer (epigeic), between the litter and the soil (hemiedaphic), and at the root level in the soil (euedaphic) [49]. Therefore, understanding the changes that occur in the structure of soil springtail communities, as well as their resilience in response to insect outbreak disturbance can guide us in monitoring soil quality of changing forest ecosystems.
The dynamics of soil arthropod communities in response to natural disturbance, such as insect outbreaks appear to be poorly studied to date. The few studies that have been conducted have shown that defoliator insect outbreaks can alter the density, diversity, and the species composition of the soil decomposer community [10,29]. Reynolds et al. (2003) [11] observed that the abundance of springtails and the biomass of enchytraeid worms increased after insect defoliation, possibly since these invertebrates benefited from increased growth of fungal organisms in the soil due to the addition of nitrogen-rich insect frass. These results are consistent with the results of other studies conducted in microcosms which showed that springtail abundance increased with aphid-induced herbivory [50,51]. In contrast, grasshopper herbivory did not change springtail abundance [50] and a recent study showed a neutral effect after outbreak in a birch forest of the winter moth (Operophtera brumata) in Norway on springtail and mite abundance although diversity of springtails increased [22]. Forest tent caterpillar outbreaks may also affect the community of springtail predators, such as ants [52]. Top-down control by predators could act directly on the springtail communities, for example, decreasing the abundance of the springtails [53,54] and leading to a trophic cascade.
Soil invertebrate communities affected by disturbance, such as defoliation can take several years before returning to pre-disturbance community composition [42,55]. Indeed, the temporal scale of responses to defoliation requires consideration and likely varies between organisms [56]. For example, mites and springtails respond to forest harvesting at different time scales [40]. However, studies assessing the regeneration of a community of soil organisms over time following disturbance remain rare and often limited to abundance and not compositional assessments. For example, Bradford et al. [55] showed that springtail biomass decreased with insect herbivory in a microcosm containing Quercus rubra leaves in the short-term (8 weeks), but recovered over the long-term (16 weeks). An experiment with soil leaf litter addition to simulate herbivory showed that soil microarthropods increased abundance over 2 years [11].
Our objective in this study was to understand whether the recent forest tent caterpillar insect outbreak affected litter and soil-dwelling springtail communities in a boreal hardwood forest dominated by trembling aspen. We also assessed abiotic and biotic soil factors, such as microbial biomass, soil nutrients, canopy openness, and predator populations that might explain springtail community structure following defoliation. We hypothesized that the forest tent caterpillar outbreak would alter communities through increased abundance, dominance, species richness, and diversity [11,22] after defoliation due to direct and indirect changes to the aboveground vegetation. We also expected that the short-term response (1 year post-outbreak) would be more marked than the long-term (2 years post-outbreak) response of springtail communities. Finally, we expected a change in the species composition of springtail communities after defoliation and that community composition would be predicted by biotic and abiotic soil factors.

2. Materials and Methods

2.1. Description of the Study Site and Experimental Design

The study was conducted in the Lake Duparquet Research and Teaching Forest (approximately 48 30′ N, 79 22′ W) in the Abitibi region of western Quebec, Canada which covers an area of 80 km2 [57]. The study site is in the boreal forest of the Canadian Shield in the White Birch-Balsam Fir bioclimatic domain [58]. It is characterized by a mixed forest composed mainly of mature trees of shade-tolerant conifers, such as balsam fir (Abies balsamea L.), white (Picea glauca Moench) and black spruce (Picea mariana Miller), white cedar (Thuja occidentalis L.), and faster growing shade-intolerant trees, such as white birch (Betula papyrifera Marshall), trembling aspen (P. tremuloides Michaux), and jack pine (Pinus banksiana Lamb) [58,59]. The soil consists of clay rich Luvisols generated by clayey lacustrine deposits that are the legacy of proglacial lakes Ojibway and Barlow [57,60]. The climate is continental, and the growing season is from 150 to 160 days. For the period of 1980–2010, the nearest weather station (Mont-Brun) recorded a mean annual temperature of 1.0 °C and mean annual precipitation of 985 mm.
The study forest experienced a severe forest tent caterpillar (Malacosoma disstria) outbreak between 2015 and 2017 [61] with a peak in 2016. In 2018, provincial surveys did not observe any defoliation [62]. We sampled two mature aspen (70–90 years old) stands separated by approximately 10 km with contrasting defoliation histories. Samples of springtail communities dwelling in litter and soil were obtained over 2 years following the outbreak (30 July 2018 and 25 July 2019) in the undefoliated (1 km2) and defoliated (1.5 km2) stand. Within each stand, 8 sites at least 115 m apart from each other were sampled. Raymond-Léonard et al. (2018) [41] demonstrated that over a very small spatial scale of 18 m between common garden sites, springtail communities can change dramatically suggesting that our sites were independent replicates. Under each tree, we sampled three strata (litter, soil 0–5 cm, and soil 5–10 cm) that were subsequently pooled for statistical analyses. Litter was collected in two quadrats (20 cm × 20 cm) and combined. Then, two soil samples of 0–5 cm thickness were obtained with a 5 cm diameter corer from the same location as the litter and combined. The same thing was carried out for soil from the 5–10 cm layer. Litter and soil were transferred to airtight plastic bags and stored at 4 °C for up to 48 h for transport to the laboratory.

2.2. Extraction and Identification of Springtails

Extraction of soil fauna from litter and soil was carried out using Berlese−Tullgren type extractors during 7 days with temperatures that gradually increased from 20 °C to 50 °C. The extracted fauna was preserved in 70% ethanol and sorted with a stereo microscope to separate springtails (our taxa of interest) from other soil organisms. Before the identification, springtails were cleared in lactic acid at 60 °C to better see structures needed for identification, such as the chaetotaxy and post-antennary organ (PAO). The specimens were mounted between slide and coverslip in Hoyer’s medium (50 mL distilled water, 30 g gum arabic, 200 g chloral hydrate, and 20 mL glycerol). After mounting, the slides were dried on a hot plate at 50 °C for at least 48 h before identification.
The identification of springtails was carried out with a Leica DM1000 LED (Concord, ON, Canada) phase contrast microscope (800×), using keys from Hopkin (2007) [63], Fjellberg (1998, 2007) [64,65], and Christiansen and Bellinger (1998) [66]. Complementary sources of digital identification keys, such as collembola.org and ecotaxonomy.org were also used. We identified springtails to family, genus, and species if possible. In the case where the species identification was difficult to confirm, we grouped specimens of the same genus according to their morphological resemblance under the name of a morphospecies. These groups of similarities were designated by acronyms “sp” followed by a number based on morphology and color (sp1, sp2, sp3, etc.) [67]. These morphospecies were described in detail to include them in the analyses as species. Damaged specimens (0.01% total abundance), for which it was impossible to reach identification to species/morphospecies level (unknown), were excluded from the analyses.

2.3. Soil Microorganisms

Samples for soil microbial biomass (μg microbial-C g−1) were obtained from the same location as the springtail samples by Dansereau-Macias et al. (2023) [68]. To estimate soil microbial biomass, the substrate-induced respiration technique with MicroRespTM plates were used [69] using glucose as a substrate.

2.4. Soil Parameters

Measurements of abiotic soil variables were obtained at each site. Carbon (C) and nitrogen (N) were measured with a Leco TruMac CNS (Saint-Joseph, MI, USA). Elements, such as calcium (Ca), magnesium (Mg), manganese (Mn), and phosphorus (P) were measured with the Perkin-Elmer Optima 7300 DVh (Waltham, MA, USA) following the method of Yash (1998) [70]. Nutrient levels were estimated for all organic and mineral soils combined (0–5 cm and 5–10 cm). The pH was measured with a Thermo Scientific Orion 2-Star (Beverly, MA, USA) apparatus following the referenced method documented by Lewis (2007) [71]. Soil moisture was obtained with a Fieldscout TDR 300 Soil moisture meter (Spectrum Technologies, Inc., Aurora, IL, USA).

2.5. Canopy Openness

At each site, we also measured canopy openness with a densitometer in 2018 and 2019 and used an average of four measurements obtained around the same focal length at each site after bud break, once a month in May, June, and July.

2.6. Statistical Analysis

For all analyses, springtails from the three strata (litter, soil 0–5 cm, and 5–10 cm) were combined for metrics due to the low abundance in the different soil strata (Table 1). The following indices were calculated for each springtail sample: Total abundance, species richness, relative abundance of each species (Pi = Ni/N), Shannon index (H’ = −∑ Pi ln Pi), and Simpson index (D = ∑Ni (Ni − 1)/(N − 1), where Ni was the number of specimens in each sample and N the total number of specimens. Differences in abundance, species richness, Shannon and Simpson indices between control and defoliated stands were assessed by ANOVAs (function aov) and post-hoc Tukey tests (TukeyHSD). In the case where the data did not meet the assumptions of normality (Shapiro.test) and homoscedasticity (bartelett’s.test), we log-transformed the data. Kruskal−Wallis (non-parametric tests) were used if log-transformations did not allow for the assumptions to be met (abundance and Shannon).
To compare the taxonomic structure of springtail communities, a variety of multivariate approaches were used. The variation of springtail community composition between defoliated and undefoliated sites and between years was visualized with non-metric multidimensional scaling (NMDS) on Bray−Curtis distance of springtail species abundances. Robustness of ordination was assessed through stress values according to Clarke’s (1993) [72] guideline: <0.05 = excellent with no potential misinterpretation, <0.1 = good with no real risk of misinterpretation, <0.2 = usable, but with potential misinterpretation. To perform ordination, the metaMDS function in the vegan package was used [73]. To test for the significance between defoliated and undefoliated sites between years, we used similarity analyses (ANOSIM) based on the Bray−Curtis distance of springtail species abundances defoliation history and for year (ANOSIM, permutations = 9999). ANOSIMs were chosen since they are based on the rank order of dissimilarity values, such as NMDS [74]. The effects of defoliation history and of year were also tested by PERMANOVA on the Hellinger distances of the springtail community data (adonis2).
To evaluate the correlation between springtail communities and abiotic and biotic parameters, a redundancy analysis (RDA) was used with the following environmental variables as constraining factors: Carbon, nitrogen, pH, potassium, magnesium, sodium, manganese, canopy cover, soil, humidity, predators, and soil microbial biomass. Before the RDA analysis, we selected the most relevant environmental variables for springtails using Pearson’s correlations with the heatmap function (ggplot2). Between highly covarying variables, the most ecologically relevant ones were retained for analysis based on our current knowledge of springtail communities. All statistical analyses were carried out with R software (version 4.2.1) with a Rstudio environment (v.1.2.13335) (Rstudio Inc., 2022. Boston, MA, USA).

3. Results

In total, we collected and identified 1160 specimens of springtails in the litter and soil belonging to 3 orders, 11 families, 30 genera, and a total of 46 species that included 19 morphospecies (n = 8 sites for each year (2018 and 2019) (Table 1, see Tables S1–S3 for absolute abundances per sampled strata). In the undefoliated sites, we had 495 specimens in 2018 belonging to 22 genera and 33 species including 13 morphospecies. In the defoliated sites, we had 225 specimens in 2018 belonging to 13 genera and 33 species including 12 morphospecies. In 2019, we had 305 specimens in the undefoliated sites and 135 specimens in the sites with defoliation history. Springtail abundance (KW chi-squared = 3.49, p = 0.31), species richness (ANOVA F = 3.03; p = 0.06), Shannon index (ANOVA F = 2.78; p = 0.06), and Simpson index (KW chi-squared = 6.07; p = 0.11) of springtail communities did not vary significantly between undefoliated and outbreak sites or between years. Species richness (ANOVA F = 3.03; p = 0.056) and Shannon index (ANOVA F = 2.79; p = 0.059) of communities at the outbreak sites showed a marginally significant decrease in 2019 relative to 2018 (Figure 1; see Figure S1 for the litter community only).
In 2018, the most dominant species at both stands (i.e., relative abundance >3%) was Lepidocyrtus sp1 in the undefoliated sites (13.1%) and sites with defoliation history (38.7%), followed by Desoria sp3 (11.7%) and Parisotoma notabilis in sites with defoliation history (11.3%). The morphospecies Anurophorus sp1 (21.8%), Xenylla christianseni (15.0%), and the species Folsomia nivalis (6.6%) were all present in the undefoliated stand but absent in the stand with a defoliation history (Table 1). In 2019, Lepidocyrtus sp1 largely dominated both undefoliated (67.5%) and defoliated stands (58.9%); Folsomia nivalis (6.8%) followed in the undefoliated stand (3.7%) (Table 1).

Species Composition Response to Defoliation

The springtail communities between the undefoliated and defoliated sites were distinct in 2018, but not distinct from either stand sampled in 2019 (Figure 2; Table 1). Variation in springtail community composition was higher in the defoliated site than in the undefoliated sites (polygon size variation in Figure 2) particularly for 2018, but not for 2019 (Figure 2). The overall composition of the springtail community was significantly influenced by defoliation history (ANOSIM R = 0.12, p = 0.0035, Table 2). This result is confirmed by the pairwise (function betadisper) test after Adonis (p = 0.052; Table 2). The significant influence of site on community composition suggested that some local factors also affected springtail community composition (ANOSIM R = 0.65, p = 0.002, Figure 3). The PERMANOVA showed a significant difference between the springtail communities of the undefoliated and defoliated sites in 2018 (R2 = 0.16 and p = 0.005), but there was no effect on the springtail communities in 2019 between sites with different defoliation history sites (Table 2).
The results of the RDA showed that certain soil variables were correlated to springtail community composition (Figure 3). The first two axes of the RDA explained 43% (26.2% for axes 1 and 16.0% for axes 2) of the observed variation in species composition (Figure 3). The constraint variables carbon (p = 0.016), potassium (p = 0.002), magnesium (p = 0.012), and manganese (p = 0.002) contributed most to the prediction of springtail communities and were negatively correlated to axis 1 (Table 3). Morphospecies and species, such as Anurophorus sp1 and Folsomia nivalis were associated with the undefoliated sites and were strongly correlated to the presence of potassium and manganese (p = 0.001; Table 3), but less to carbon and magnesium concentrations. Other factors, such as canopy openness (p = 0.004; Table 3), pH, soil moisture (p < 0.001; Table 3), microbial biomass based on glucose utilization, nitrogen, sodium, calcium, and predators did not significantly correlate to springtail community structure.

4. Discussion

Our study explored aboveground and belowground interactions in aspen-dominated stands of the boreal forest ecosystem with the aim to understand whether changes at the tree level following a forest tent caterpillar outbreak may influence the taxonomic structure and composition of soil springtail communities. Our results did not support our first hypothesis that abundance or diversity of springtail communities would be altered following the forest tent caterpillar outbreak (Figure 1). This result contrasts to the observed reduction in microbial abundance following defoliation [68], as well as a reduction in species richness and an increase in evenness of ant communities following defoliation [68,75] in the same stands and years. However, Shannon diversity showed a tendency toward lower diversity with defoliation history in 2019, which is a reminder that interannual seasonal variation can modulate community structure (Figure 1). The general lack of response of springtail abundance and diversity that we observed are in partial agreement with those who observed that springtail abundance was not affected by the autumnal moth (Epirrita autumnata) and winter moth (O. brumata) epidemic, although they observed an increase in springtail diversity [22]. Similarly, Slawski and Slawska (2023) [42] showed that springtail abundance was not affected by an outbreak of Acantholyda posticalis in a pine forest. During an experiment with harvested litter in forest dominated by Q. rubra and A. rubrum following an epidemic (forest livery, oak thorn caterpillars, and walking sticks), an increase in the abundance and diversity of springtails was observed in contrast to our study [11]. Although responses remain varied depending on defoliator and ecosystem type, our results show that springtail abundance and diversity did not differ, and compositional shifts were short-term. Previous work has shown that the rapid reproductive cycle of springtails can facilitate population recovery from disturbance in the long-term [76,77,78], as shown by Bradford et al. (2008) [55] who showed a recovery of the springtail community 16 weeks after defoliation. However, the response of soil organisms, such as springtails could be related to the nature of the defoliator insect type, the intensity of the epidemic, as well as to the dynamics of nutrients in the soil through the decrease in the quantity and quality of litter and increasing nitrogen levels via insect excreta.
In support of our second hypothesis, we observed that species composition of springtail communities in the first year (2018) was influenced by the forest tent caterpillar outbreak (Figure 2, Table 2). This short-term change in the composition of springtail communities could be explained by the different mechanisms that the tree uses to distribute nutrients [78] and the availability of feeding resources for the springtails. However, in the second year (2019), there was no effect of defoliation history on community composition. These results suggest that springtail communities are altered 1 year after the collapse of a forest tent caterpillar outbreak, but in the second year, the effect of defoliation history gradually faded. Several studies have shown relationships between the vertical distribution of springtails, the root system, and the distribution of microorganisms [79,80,81]. It is believed that springtail species feed based on their soil habitat by either consuming or grazing on litter on the forest floor surface or feeding on bacteria or fungi associated with roots [49,82,83,84]. In addition, other studies as those of Potapov et al. (2016) [49] and Raymond-Léonard et al. (2019) [85] have shown that species-specific feeding patterns vary depending on habitat and mandibular morphology. Among the springtail species or morphospecies strongly responding in 2018 that were absent from the previously defoliated stand (Table 1, Figure 3), Mesaphorura sp1, Anurophorus sp1, and Xenylla christianseni live between the litter and the soil (hemiedaphic life form) and Folsomia nivalis lives in the soil (euedaphic). These springtails typically feed on decomposed detritus, microorganisms, and root exudates [50]. In contrast, Lepidocyrtus sp1 was less affected by defoliation (Table 1, Figure 3) and generally demonstrates a good tolerance to disturbed environments [86,87]. Species from this genus live on the litter-layer surface (epigeic), feeding on litter-bound fungi [83,88,89]. They can change their diet based on resource availability [90], and thus are less likely to be affected by changing soil conditions. Therefore, it is possible that the more sensitive species in 2018 were responding to changes in the carbon budget of the defoliated aspen trees leading to reduced allocation of belowground carbon to roots and root exudates and a possible decreased abundance of ectomycorrhizal fungi [29,91,92]. Further support for this interpretation comes from the concurrent study by Dansereau-Macias et al. (2023) [68] who took samples immediately adjacent to our soil cores and showed a consistent decrease in soil microbial biomass in response to the recent outbreak over both years suggesting a decrease in resource availability in the 0–5 cm soil layer. The diet of springtail species remains poorly understood and a better understanding of the relationship between springtail populations and microbial communities could be achieved by measuring consumption traits (mandibles) and food resources of springtails (fungal, bacterial, and litter trait composition) to understand the underlying mechanism of this direct interaction [85].
Our exploration of whether springtail species composition correlated with other local environmental variables yielded mixed results. Neither top-down food web control estimated by the inclusion of predator abundances [75] nor soil resources estimated by glucose-induced soil microbial biomass [69] showed a significant correlation to species composition. However, sites with a defoliation history showed a trend of lower C, P, Mg, and Mn concentrations (Table S4) and Anurophorus sp1 and Folsomia nivalis were negatively correlated with these soil nutrients (Figure 3). Song et al. (2016) [93] pointed out that euedaphic and hemiedaphic springtails are more sensitive to nitrogen addition than epigeic springtails. This suggests that the soil nutrients associated with our study may better explain soil-associated springtails than those living in the litter layer which were dominant in our community (Table S2). Carbon is an important source of nutrients for springtails, as it has been shown that springtails ingest carbon from both litter and soil [49]. The response of springtail communities to soil carbon concentrations may indicate that both surface-dwelling and soil springtail communities were sensitive to the availability of soil organic matter (SOM) as organic matter quality is an important predictor of variation in springtail communities [94,95]. Phosphorus concentration in the soil may have affected variation in the springtail community [96] as higher phosphorus levels in the soil can lead to increased springtail abundance [96,97,98,99] and richness of arbuscular mycorrhizal fungi communities [100], which are also a resource for springtails. In the case of our study, Anurophorus sp1 and Folsomia nivalis, which are respectively hemiedaphic and euedaphic, responded more favorably to the presence of phosphorus than the epigeic Lepidocyrtus sp1, as highlighted in the study by song et al. [93] in the case of nitrogen. However, other studies have reported that excess phosphorus may have an opposite effect on springtails [101]. The soils of both stands (undefoliated and sites with defoliation history) were dominated by fungi (fungal to bacteria ratio was 0.86) [68], which could support our interpretation that hemiedaphic and euedaphic species close to the roots are linked to ectomycorrhizal fungi. The trace elements concentration in the soil can also influence the community of springtails [101]. In the case of our study, the species Anurophorus sp1 and Folsomia nivalis are linked to the presence of the trace elements Mg and Mn in the undefoliated site. These trace elements are known to be very important in the physiological regulation of invertebrates [102], for example, Mn is known to participate in cuticle construction [102], despite its toxicity at a given threshold [103,104].
Microsite variation in soil moisture did not show a significant correlation with species composition which was surprising as this parameter is generally an important predictor of springtail community structure [105]. Previous work has shown that canopy opening can result in the movement of soil organisms, including some springtail species [106]. Canopy openness is known to have a greater impact on the structure and composition of the ground-dwelling edaphic arthropods, such as millipedes and beetles [106], but springtails also respond, such as the Tomoceridae and Hypogastruridae families [107]. The high presence of species of epigeic springtails (Lepidocyrtus sp1) that were numerically more abundant in the sites with a recent defoliation history suggests consistency with canopy opening favoring these surface-dwelling communities.

5. Conclusions

Our study is one of the first to explore the effect of forest tent caterpillar defoliation on springtail communities sampled in the field in boreal trembling aspen stands following a natural outbreak event. Neither abundance nor diversity indices differed in response to defoliation history. However, the species composition of springtail communities was altered in the short-term, in the first year following the outbreak with certain morphospecies completely absent in sites with a recent defoliation history. These morphospecies typically live in habitats between the litter and soil, and thus close to roots. In addition, they degrade organic matter which suggests that aspen trees may be mediating compositional shifts due to changes in their own carbon balance. Moreover, compositional changes may be linked to lower soil nutrients that were measured in sites with a recent defoliation history, but species composition changes were transient, and communities appeared to recover in the second year although overall diversity was lower in both forest stands. Our results suggest that feeding guilds may drive responses in springtail responses to defoliation, but this remains to be tested directly over time in the same way as any subsequent disruption of soil ecological functions, such as nutrient cycling in forests following severe defoliation by the forest tent caterpillar.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f14071302/s1, Table S1: Abundance of springtail (species and morphospecies) sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history during the 2015–2017 outbreak (litter and soil combined). The unidentified genus is noted as ‘’Unknown”. Table S2: Abundance of springtail in litter only (species and morphospecies) sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history during the 2015–2017 outbreak. The unidentified genus is noted as ‘’Unknown”. Table S3: Abundance of springtail in soil only (species and morphospecies) sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history during the 2015–2017 outbreak. The unidentified genus is noted as ‘’Unknown”. Table S4: Summary description of biotic and abiotic factors in soils with contrasting defoliation histories sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history during the 2015–2017 outbreak. Each factor is presented as mean (± SE). Significant values are also present. *** = p < 0.001; ** p < 0.01 =; * p < 0.05. Figure S1: Mean abundance (A), species richness (B alpha diversity) Shannon-Wiener index (C) and dominance (Simpson index) (D) of springtail communities in undefoliated and defoliated forests in 2018 and 2019 (n = 8) in the litter. Each whisker box has the lower boundary indicating the 25th percentile, the bold line inside the box marks the median, and the upper boundary of the box the 75th percentile. The whiskers indicate the 10th and 90th percentiles. Dots are outliers (>Q3 + 1.5 × interquartile range).

Author Contributions

E.G.K., E.D. and I.T.H. contributed to the conception and design; I.T.H. and E.G.K. elaborated the methodology; E.G.K. and A.-S.C. acquired field samples; E.G.K. acquired and analyzed the data with support from A.-S.C.; E.G.K. prepared the original manuscript with support from E.D. and I.T.H.; A.-S.C., E.D. and I.T.H. reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The QCBS provided a seed grant to I.T.H. and E.D. in 2018. E.G.K. was funded through an NSERC Collaborative Research and Development Grant 522722-17 to E.D. and I.T.H. and an NSERC Discovery Grant RGPIN-2019-07215 to I.T.H. SERG international provided a grant to E.D.

Data Availability Statement

Not applicable for the moment.

Acknowledgments

We are grateful to J. Jarry, S. Jarry, E. Dansereau-Macias, and L. Rousseau for field assistance, to L.J. Raymond-Léonard for advice in the lab and comments on an earlier draft, E. Dansereau-Macias for sharing microbial biomass data and comments on an earlier draft, R. Sepulveda-Mina and J. Rodriguez for help with statistical analyses. We thank B. Lafleur for providing soil data, M. Montoro Girona and David Paré for soil data interpretation. B. Lafleur, M. Bouchard, F. Guay, S. Légaré, J.P. Lessard, and L. Nowell collaborated in the NSERC CRD grant.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 01302 g001 550
Figure 1. Mean abundance (A), alpha diversity (B), Shannon−Wiener index), dominance (C), Simpson index), and species richness (D) of springtail communities sampled in 2018 and 2019 in undefoliated forest and forests with a defoliation history (“Outbreak”) during the forest tent caterpillar outbreak from 2015 to 2017 (n = 8). Springtail communities from the litter and the soil layers were combined. Each whisker box has the lower and upper boundary indicating the 25th and 75th percentile, respectively and the bold line inside the box marking the median. Whiskers indicate the 10th and 90th percentiles and dots are outliers (>Q3 + 1.5 × interquartile range). Lower case letters indicate significant post-hoc contrasts following the overall statistical result indicated in the upper right corner.
Figure 1. Mean abundance (A), alpha diversity (B), Shannon−Wiener index), dominance (C), Simpson index), and species richness (D) of springtail communities sampled in 2018 and 2019 in undefoliated forest and forests with a defoliation history (“Outbreak”) during the forest tent caterpillar outbreak from 2015 to 2017 (n = 8). Springtail communities from the litter and the soil layers were combined. Each whisker box has the lower and upper boundary indicating the 25th and 75th percentile, respectively and the bold line inside the box marking the median. Whiskers indicate the 10th and 90th percentiles and dots are outliers (>Q3 + 1.5 × interquartile range). Lower case letters indicate significant post-hoc contrasts following the overall statistical result indicated in the upper right corner.
Forests 14 01302 g001
Forests 14 01302 g002 550
Figure 2. Non-metrical distance scaling (NMDS) of the springtail community composition in 2018 and 2019 in the aspen-dominated boreal forest arranged by sites in the undefoliated stand and sites occurring in a stand with defoliation history (“Outbreak”) during the 2015 to 1017 forest tent caterpillar outbreak. Associated ANOSIM R values are based on Bray−Curtis distance (perm = 9999). C1 = Undefoliated site 2018; D1 = Outbreak site 2018; C2 = Undefoliated site 2019; and D2 = Outbreak site 2019.
Figure 2. Non-metrical distance scaling (NMDS) of the springtail community composition in 2018 and 2019 in the aspen-dominated boreal forest arranged by sites in the undefoliated stand and sites occurring in a stand with defoliation history (“Outbreak”) during the 2015 to 1017 forest tent caterpillar outbreak. Associated ANOSIM R values are based on Bray−Curtis distance (perm = 9999). C1 = Undefoliated site 2018; D1 = Outbreak site 2018; C2 = Undefoliated site 2019; and D2 = Outbreak site 2019.
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Forests 14 01302 g003 550
Figure 3. Redundancy analysis (RDA) of Hellinger-transformed springtail communities and significant explanatory soil variables. Black stars designate species, blue circles are the undefoliated sites, and the gray circles are sites with a recent defoliation history.
Figure 3. Redundancy analysis (RDA) of Hellinger-transformed springtail communities and significant explanatory soil variables. Black stars designate species, blue circles are the undefoliated sites, and the gray circles are sites with a recent defoliation history.
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Table
Table 1. Relative abundance of springtails (species and morphospecies) sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history (“Outbreak”) during the 2015–2017 outbreak. The unidentified genus is noted as ‘’Unknown”. Relative abundance was calculated as the abundance of the sampled species/total abundance × 100. The dominant species in both stands (>3%) are indicated in bold.
Table 1. Relative abundance of springtails (species and morphospecies) sampled in 2018 and 2019 on undefoliated sites and sites with a defoliation history (“Outbreak”) during the 2015–2017 outbreak. The unidentified genus is noted as ‘’Unknown”. Relative abundance was calculated as the abundance of the sampled species/total abundance × 100. The dominant species in both stands (>3%) are indicated in bold.
Genera and Species or MorphospeciesRelative Abundance (%)
Undefoliated 2018Outbreak 2018Undefoliated 2019Outbreak
2019
Anurophorus sp131.93-3.571.47
Arrthopalites sp10.400.43--
Desoria sp10.40-0.325.15
Desoria sp20.601.30--
Desoria sp32.0111.74--
Desoria sp4-0.87--
Entomobrya sp10.600.87--
Entomobrya sp2-1.30--
Entomobrya sp3-3.04--
Folsomia candida Willen, 19020.20---
Folsomia nivalis Packard, 18736.63-6.823.68
Folsomia similis Bagnall, 1939--0.32-
Friesea mirabilis Tullberg, 18711.003.482.275.88
Friesea pentacantha Mills, 1934-0.43--
Heteromurus nitidus Templeton et Westwood, 1836-0.431.30-
Hypogastrura sp1-1.30-0.74
Isotoma viridis Bourlet, 18390.400.43--
Isotomiella minor Schäffer, 18962.21-1.30-
Isotomorus palustri Müller, 1776--1.30-
Lepidocyrtus sp113.0538.7067.5358.82
Mesaphorura sp13.015.221.621.47
Mesaphorura sp20.40---
Metisotoma grandiceps Reuter, 18911.00-0.65-
Neanura muscorum Templeton, 1836-6.091.30-
Morulodes serratus Folsom, 1916--1.3011.03
Orchesella sp10.60--0.74
Paranura sp1---0.74
Parisotoma ekmani Fjellberg, 19772.010.433.258.09
Parisotoma notabilis Schäffer, 18960.2011.303.571.47
Pseudachorutes simplex Maynard, 19512.21---
Pseudachorutes sp11.00---
Sinela sp10.20-1.95-
Sminthurides lepus Mills, 19340.400.43--
Sminthurides occultus Mills, 19341.203.48--
Sminthurides pumilis Krausbauer, 1878-4.78--
Sminthurides quadrimaculatus Ryder, 18780.80---
Sminthurides sp10.201.74--
Plutomurus californicus Folsom, 19130.40---
Pogonognathellus celsus Christensen, 1965--0.32-
Tomocerus curtus Christensen, 19640.40---
Pogonognathellus elongatus Maynard, 1951--0.32-
Pogonognathellus flavescens Tullberg, 18712.81---
Tomocerina lamellifera Mills, 19340.20---
Xenylla christianseni Yosii, 196021.89---
Xenyllodes armatus Axelson, 19030.60---
Xenyllodes sp10.40---
Unknown species0.602.170.970.74
Table
Table 2. Summary statistics for PERMANOVA testing the effect of defoliation history (undefoliated and defoliated) and years on the taxonomic composition of springtail communities on the combined strata (total litter and soil) after the Hellinger transformation according to defoliation history. Df = degree of freedom; SS = sum of squares; F = F value by permutation; R2 = coefficient of determination; *** = p < 0.001; * p < 0.05.
Table 2. Summary statistics for PERMANOVA testing the effect of defoliation history (undefoliated and defoliated) and years on the taxonomic composition of springtail communities on the combined strata (total litter and soil) after the Hellinger transformation according to defoliation history. Df = degree of freedom; SS = sum of squares; F = F value by permutation; R2 = coefficient of determination; *** = p < 0.001; * p < 0.05.
DfSSR2Fp
History31.61150.167961.88410.005 ***
Year10.63420.06612.12330.021 *
Residual287.98310.83204
Total319.59461
Table
Table 3. Summary of ANOVA results showing effects of environmental variables on the abundance of springtail communities on the different strata combined (total litter and soil). Df = degree of freedom; F = Fisher; *** p < 0.001; ** p < 0.01; For clarity, only environmental variables that showed significant conditional effects (bold writing) during the direct selection procedure are presented.
Table 3. Summary of ANOVA results showing effects of environmental variables on the abundance of springtail communities on the different strata combined (total litter and soil). Df = degree of freedom; F = Fisher; *** p < 0.001; ** p < 0.01; For clarity, only environmental variables that showed significant conditional effects (bold writing) during the direct selection procedure are presented.
Factors DfFp
Carbon (C)12.41160.0160 **
Nitrogen (N)11.12210.3510
pH11.80490.0870
Phosphorus (P)12.95310.0020 ***
Calcium (Ca)10.78620.6660
Magnesium (Mg)12.53950.0120 **
Sodium (Na)11.42690.2280
Manganese (Mn)13.89320.0020 ***
Canopy cover11.58240.1480
Soil humidity10.74310.7010
Predator11.34140.1910
Microbial biomass11.31360.2390
Residual3
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Gagnon Koudji, E.; Despland, E.; Caron, A.-S.; Handa, I.T. Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests. Forests 2023, 14, 1302. https://doi.org/10.3390/f14071302

AMA Style

Gagnon Koudji E, Despland E, Caron A-S, Handa IT. Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests. Forests. 2023; 14(7):1302. https://doi.org/10.3390/f14071302

Chicago/Turabian Style

Gagnon Koudji, Essivi, Emma Despland, Anne-Sophie Caron, and I. Tanya Handa. 2023. "Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests" Forests 14, no. 7: 1302. https://doi.org/10.3390/f14071302

APA Style

Gagnon Koudji, E., Despland, E., Caron, A. -S., & Handa, I. T. (2023). Soil Springtail Communities Are Resilient to Forest Tent Caterpillar Defoliation in Quebec Mixed Hardwood Forests. Forests, 14(7), 1302. https://doi.org/10.3390/f14071302

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