Short-term intensive warming shifts predator communities (Parasitiformes: Mesostigmata) in boreal forest soils

Highlights

• Both Mesostigmata adult and juvenile abundance increased under warming.

• Mesostigmata assemblages shifted and average individual body mass increased.

• Assemblages shifted due to the increased abundances of parthenogenetic species.

• These results align with previous studies on Oribatida assemblages under warming.

Abstract

Increasing global mean surface temperatures from climate change will coincide with longer and more frequent short-term, extreme warming events. Because of this, habitats like boreal forests are predicted to have new temperature regimes. Boreal forest soils contain a diverse array of microarthropods and nematodes, which include the main soil predators, mesostigmatic mites (Acari: Parasitiformes: Mesostigmata). Although extensive research exists on how climate warming affects oribatid mite and collembolan communities, fewer studies have examined how warming effects Mesostigmata communities. We tested the effect of short-term (three months), intensive warming (+8 °C) on Mesostigmata communities from the boreal forest using experimental mesocosms containing forest-floor material. We collected moss mats and underlying forest floor organic material from a boreal forest and incubated them within individual mesocosms at 12 °C and 20 °C for three months, where 12 °C represented the long-term average growing season temperature and 20 °C corresponds to the potential extreme surface temperature from climate warming for the region. We enumerated all extracted microarthropods and nematodes, and identified all Mesostigmata adults to the species-level. In total, we counted 24,080 nematode individuals, and 19,582 total microarthropod individuals, of which 3349 individuals (1899 adults and 1450 juveniles) were mesostigmatic mites, consisting of 14 species. Mesostigmatic juvenile and adult abundances, along with adult community-level body mass were higher under warming, which lead to a shift in community composition. Changes to Mesostigmata communities were driven by the greater abundances of parthenogenetic species, primarily Veigaia mitis (Berlese), under warming—a response that has been shown in oribatid mite communities, but not mesostigmatic communities, before. Overall, we found that warming shifted mesostigmatic mite communities in the boreal forest, which has wide ranging implications for the soil food web.

Introduction

Climate change represents one of the greatest threats to the natural world (Román-Palacios and Wiens, 2020). Already, global mean surface temperatures have risen nearly 1 °C since the mid to late 19^th century (IPCC, 2018), and are expected to increase further over the next century. This temperature increase will coincide with longer and more frequent short-term, extreme warming events (e.g., heat waves) that may last for several days and weeks (Meehl and Tebaldi, 2004; Viceto et al., 2019). Both the magnitude of warming, and the frequency of extreme warming events is high at northern latitudes during the summer months (Bathiany et al., 2018; Price et al., 2013), thus ecosystems such as boreal forests will be greatly affected by climate warming. It is predicted that the annual mean temperature in the boreal forest will increase by 2 °C by 2050, and possibly 4–5 °C by 2100 (Price et al., 2013). In addition, the number of heat wave days where daily temperature rises, on average, 2–3 °C at high latitudes (Perkins-Kirkpatrick and Lewis, 2020), will also increase in the boreal zone (Perkins-Kirkpatrick and Gibson, 2017). Together, suggesting that boreal forests will be under new temperature regimes in the near future.

Soil systems of the boreal forest contain a rich organic layer that is habitat for hyperdiverse soil communities, where diversity is comparable, or can even exceed diversity in tropical forests (Coleman et al., 2018; Maraun et al., 2007). Boreal forest soils are populated mainly by microarthropods, such as mites (Acari: Acariformes, Parasitiformes) and collembolans (Hexapoda: Collembola), along with nematodes (Nematoda). Densities of microarthropods can exceed 800,000 individuals per m² (Behan et al., 1978), and 1,000,000 individuals per m² for nematodes (Petersen and Luxton, 1982), creating a highly connected food web with numerous feeding guilds and trophic levels (Hunt et al., 1987; Moore et al., 2003). Mesostigmatic mites (Acari: Parasitiformes: Mesostigmata) are the dominant predators within boreal forest soils as they regulate the populations of their prey through top-down control and link the basal energy channels (i.e., fungi and bacteria) to one another (Hunt et al., 1987; Moore et al., 2003; Schneider and Maraun, 2009). Mesostigmatic mites are speciose with 650 described species across 46 families recorded in Canada alone, with over half of the families present within the boreal forest, producing diverse soil communities (Beaulieu et al., 2019; Meehan et al., 2018). Mesostigmatic species are also morphologically, physiologically, and functionally diverse, as they vary in body size (200 μm – 4500 μm in adult body length; Lindquist et al., 2009), sexual systems (e.g., diplodiploid, haplodiploid, arrhenotokous, and thelytokous; Norton et al., 1993), and feeding preferences (Beaulieu and Walter, 2007; Walter, 1988; Walter et al., 1988). While the vast majority of mesostigmatic mites are predatory, species can often be broadly categorized as generalist arthropod and nematode feeders, or nematode-feeding specialists, with specialists having greater-top down control on their prey populations than generalists (Laakso and Setälä, 1999).

Climate warming may impact soil communities through both direct and indirect mechanisms. Directly, warming will increase individual metabolic and population growth rate (Brown et al., 2004). While indirectly, warming may alter soil communities through plant-soil feedbacks through changing litter quality and rhizodeposits (Pugnaire et al., 2019), along with soil moisture content (Holmstrup et al., 2017). As such, the effect of warming on soil faunal communities appears to vary temporally and/or be context dependent. Past studies have shown that soil fauna abundance, richness or diversity can increase or decrease under warming due to habitat differences (Bokhorst et al., 2008; Sjursen et al., 2005) and year-to-year fluctuations in climatic conditions (Harte et al., 1996; Meehan et al., 2020). This is because soil fauna responds strongly to the changing abiotic and biotic environmental conditions induced by warming. For example, warming can decrease soil moisture or water content, resulting in lower soil fauna diversity and biomass (Holmstrup et al., 2017; Vestergård et al., 2015). For predators, like mesostigmatic mites, increased prey abundances under warming may lead to greater predator abundances (Sjursen et al., 2005), as bottom-up mechanisms may affect predator persistence at higher temperatures. Our understanding of soil faunal response to climate warming is also confounded by the duration of warming. Soil faunal response to continuous, long-term warming (5+ years) have shown to weakly affect communities (Alatalo et al., 2017; Holmstrup et al., 2017), whereas studies of short-term (that span weeks or months) or seasonal warming have shown to alter soil fauna composition (Bokhorst et al., 2012; Krab et al., 2013; Lindo, 2015; Markkula et al., 2019). Such short-term changes can be explained by species-level traits, like body size or sexual system. Long-term warming may allow for organisms to acclimate to warmer conditions and communities to reassemble, whereas short-term warming may induce immediate changes to community composition. Soil-dwelling species differ in their ability to acclimate to new temperature conditions (van Dooremalen et al., 2013) and in their response time to environmental change (Lindberg and Bengtsson, 2005). With increasing temperature variability and extreme warming events, the immediate response of fauna, whether it be positive or negative, will shift community structure.

The majority of climate warming studies on soil fauna have focused on collembolan and oribatid mite communities (Alatalo et al., 2017; Holmstrup et al., 2017; Lindo, 2015; Markkula et al., 2019; but see Meehan et al., 2020) without providing species-level information on how mesostigmatic mite communities respond. Mesostigmatic mites are essential contributors to soil functionality due to their high trophic position and providing top-down control on lower trophic levels (Hunt et al., 1987; Moore et al., 2003; Schneider and Maraun, 2009). Meaning, it is important to determine how rising temperatures will affect Mesostigmata assemblages, as changing community structure under warming may alter the strength of their top-down control on their prey (Laakso and Setälä, 1999). Here, we tested the effect of short-term (three months), intensive warming (+8 °C) with a focus on mesostigmatic mite assemblages from the boreal forest using experimental mesocosms. We used both a taxonomic as well as trait-based approach to examined how warming shifted mesostigmatic adult and juvenile abundance, species richness, diversity, evenness, assemblage composition, and average individual body mass within Mesostigmata assemblages. As mesostigmatic mite persistence at higher temperatures may be dependent on prey availability, we enumerated other mite groups, along with collembolans and nematodes to determine how warming affected their assemblages. Because the mesocosm approach controls for any warming-induced indirect effects through plant-soil interactions or changes in soil moisture, we hypothesize that soil mesostigmatic assemblages would respond to warming through metabolic and reproductive increases, and changes (increases) in prey availability.