Microhabitat complexity

Soil represents a challenging habitat to study. It is an intricately structured three-dimensional habitat which, due to the small size of the soil organisms, is subject to considerably more layering than even the most extensively vertically layered aboveground habitats such as tropical forests21. Considering the fabric of belowground habitats in extinction ecology is an exceptionally important point. The nature and structure of soil also gives rise to unparalleled microhabitat complexity with numerous physiochemical gradients, for example, aerobic and anaerobic microhabitats can occur directly adjacent to each other (that is, within a few dozen micrometres) due to diffusion limitation in pore networks22. The resulting high complexity of the soil landscape could render soil biota considerably more resistant to change than aboveground organisms, as suggested in the landscape-moderated insurance hypothesis23. In addition, soils may be insulated against many drivers of climate change, including drought, warming and extreme events. For example, natural CO 2 levels in the soil atmosphere are much higher than in the air above, because of soil biological activity (including root and microbial respiration) coupled with gas diffusion limitation. Also, soil offers temperature insulation, and at the microscale it may be partially insulated against drought events through capillary water reserves. By contrast, in the short-term soil communities may be particularly susceptible to anthropogenic stressors such as ploughing. Thus, the features of the soil (micro-)habitat alone impose a range of distinct considerations for the ecologist delving into belowground extinction susceptibility.

Extinction models

Extinction models for belowground organisms are currently unavailable; thus, soil ecologists at the moment have no choice but to generalize the predictions for aboveground biota to their system24,25. Yet, the ecology of belowground biota differs considerably from that of the aboveground organisms that have so far been considered in extinction models (Fig. 1)—at least with regard to their niche structure which we consider in the following. The most conspicuous difference relates to body size variability which, even without considering belowground microbes, is several orders of magnitude larger in soils (Fig. 1b). Unlike their aboveground relatives, microbial organisms in soil also represent the base trophic level of their food webs26 and are responsible for overall ecosystem functioning. While aboveground ecologists can afford to overlook microbes in community models, this is not possible in soil ecology. The small size of the organisms in soil also translates to greater population sizes than for most currently considered aboveground taxa (Fig. 1b). Even though the Baas–Becking postulate, an intensely debated tenet according to which ‘everything is everywhere but the environment selects’, has been convincingly rejected for many groups of microbial organisms27 (but see ref. 28), microbes are still believed to generally occupy extensive geographic ranges relative to their size29. Extensive biogeographical distribution may lead to large populations of soil organisms, which from an extinction ecology perspective, are important because these are subject to very long extinction trajectories following habitat loss (Fig. 2a). An additional difference is the fact that most groups of belowground taxa can propagate asexually (for example, bacteria, fungal mitospores) often in addition to having sexual reproduction. Asexual organisms can be subject to population dynamic forces quite different from those of sexually reproducing species. Especially relevant for extinction ecology is the fact that for asexual organisms, a single individual can be a viable population and also many properties important for sexual reproduction such as the sex ratio do not apply. Furthermore, specifically for microbial taxa, the fact that they can be extremely physiologically and functionally versatile represents an additional facet of differentiation from existing aboveground extinction ecology. For example, microbes possess an arsenal of cryptic genes (that is, phenotypically silent genes) that allow them to cope with environmentally adverse conditions for extensive periods30. Soil microbial taxa can also concurrently or consecutively pursue functionally very divergent lifestyles such as those of a root-endophytic parasite and a decomposer of soil organic matter (many soil fungi31) or of a nitrogen fixer and a free-living symbiont (bacteria of the genus Azospirillum32). Still other belowground taxa may possess ecophysiolocal traits comparable to macroscopic species that live aboveground. These pronounced ecological dissimilarities can affect the relative susceptibility of different taxa to habitat changes and need to be accounted for in extinction models (Fig. 2b,c). Finally, many microbes possess the ability to form resting structures for extensive periods of time, even exceeding those known from seed banks of plants33. This coupled with the high prevalence of conditionally rare microbial taxa observed in soil34 result in highly complex population dynamics that are exceptionally tricky to either monitor or model.

Figure 2: Particularities of extinction susceptibility for soil biota. Differential extinction susceptibility as influenced by three particularities of belowground food webs, (a) extreme population sizes—population sizes for belowground organisms may exceed considerably the minimal viable population thresholds, or alternatively for asexual organisms the minimal viable population could coincide with a single individual; (b) physiological versatility—definitions of habitat loss for belowground organisms differ considerably from those for aboveground organisms and physiologically versatile organisms may suffer less from changes in their habitat; (c) high adaptation potential1,84 that is particularly relevant to the microbial taxa (in the panel population size factors that could affect adaptation speed were not considered but could have exacerbated differences). Representative examples of each group of belowground organisms are presented in the images on the right of each panel. For modelling extinction debt a hyperbolic extinction trajectory over time was assumed. Figure design based on the study by Kuussaari et al.35 Image credits: top left panel—Anika Lehmann; middle and bottom left panels—Diana Andrade; top and bottom right panels—Stefanie Maaß; Middle right panel—Karoline Weißhuhn. Reproduced with permission from the authors. Full size image

Temporal scales of extinction

The fact that extinctions do not happen instantaneously adds an additional layer of challenges to belowground extinction ecologists. Extinction debt35 reflects the delay in diversity loss after habitat contraction before the species richness reaches the level predicted by the species–area relationship. The relaxation time of this process has been linked to habitat size36. As argued in the previous paragraph, in soil we expect this relaxation time to be disproportionally high for a subset of organisms due to large population sizes and asexual propagation (Fig. 2a). This could very well mean that humanity has not yet witnessed the full consequences of soil habitat destruction, even given the already well-appreciated adverse effects of agriculture, erosion and desertification. On the other hand, if soil habitat could be restored, impending extinctions could be forestalled. Preserving a handful of suitably interconnected soil habitats at an adequate spatial scale might be adequate. Placing susceptibility to extinction of belowground organisms in an extinction-debt framework makes apparent that pronounced differences across organismal groups are likely, much larger than those that have so far been considered in aboveground extinction models (Fig. 2). We need to also be very careful about extrapolating or applying concepts of extinction dynamics to microbes: here we enter exciting, but unchartered territory.

It is unequivocal that at temporal scales exceeding single geological periods, soil organisms do go extinct; a number of organisms that are known to have existed several millions of years ago are only distantly related to existing species37. For a subset of soil biota persistence is tightly linked to hosts such as plants, through symbiosis, so extinction risk can likely be tied strongly to the demographics of these hosts (Fig. 3b). Another subset of soil biota such as soil decomposers that may not be host specific (but see ref. 38) but have evolved a high affinity to specific compounds (for example, white-rot fungi and lignin) could be susceptible to high-impact events that can modify the availability of their substrate. For example, microbes apparently responded strongly to the Permian and the Triassic mass extinction events39 and they could respond similarly to the high ongoing extinction rates currently observed5. On the other hand, the hotspots of extinction for belowground organisms could be very different from those for aboveground organisms. This is because there is only a loose relationship between aboveground and belowground diversity. For example Tedersoo et al.40 showed that the plant/soil fungus richness ratio declines as a negative exponential from equator to pole, suggesting a decoupling between aboveground and soil diversities. In another study, Ramirez et al.41 compared local versus global diversity patterns of soil bacteria and fungi, finding comparable gamma diversity estimates for the two kinds of data sets.

Figure 3: Macro- and micro-scale perspectives of habitat loss belowground. (a) A more anthropocentric perspective of what represents habitat loss for belowground ecosystems: tillage, urbanization, pollution; (b) from a soil biota perspective the drivers of extinctions can be localized, however, at a more intricate, microscopic level. At this microscale level, the effects of (1) water availability and aeration; (2) host extinction; (3) loss of soil structure; (4) declines in carbon substrate availability are depicted within a soil habitat. The three macroscopic examples of habitat loss are linked to various effects at the microscopic level. For instance tillage can compromise aeration, lead to extinction of arthropod hosts and impair soil aggregation; urbanization other than impacting arthropod hosts can have pronounced effects on substrate availability; and soil pollution can affect carbon substrate availability. Note scale in images. Image credits (Author, ‘description’, year, modifications (license)): left panel—We El, ‘Beploegd veld’, cropped, 2005 (CC BY-SA 3.0), central panel—Baba Ovian, ‘Dwarka Expressway’, cropped, 2013 (CC BY-SA 3.0), right panel—Nils Ally, ‘Litter’, cropped, 2010 (CC BY 3.0). Source: Wikipedia. Used according to the terms of a GNU Free Documentation License. Full size image

Niche versus neutral processes

Up to this point we have highlighted the specific features of soil and its inhabitants. Another approach for modelling extinction is to ignore the niche structure of belowground communities and implement a neutral approach. Using a neutral approach could be advantageous because many of the challenges related to characterizing ecological niches of soil biota could be bypassed. However, in the case of a neutral model, there are some important considerations. On the one hand, the trophic structure of belowground food webs is poorly resolved and for some organisms it is hard to identify the trophic level to which they belong, in part due to widespread omnivory26. This is important because neutral theories are most suitable for organisms within a single trophic level. On the other hand defining the concept of species for microbes is not as straightforward as it tends to be for macroorganisms, because these definitions rely on assignments of dissimilarity in sequence data. Up to now neutral models have relied on robust definitions of species and this could represent a major issue. Moreover, even with reliable quantification of soil taxa abundances, fitting neutral models could be problematic because of the sheer size of belowground communities. Large population sizes imply low sensitivity of the organisms involved in stochastic events, which represent the driving forces of extinctions in neutral models9 but also spell difficulties in assessing neutral theory parameters based on observations within scientifically feasible monitoring timespans (Fig. 2a).

As stated above, our ignorance of how widespread functional redundancy may be in soil represents one of the important issues that soil extinction ecologists face, because this determines how imperative soil conservation measures are for securing ecosystem services. A hypothetical scenario in which organisms go extinct at low frequencies and where there is a high functional redundancy across organisms would imply a low priority of conservation efforts compared with a scenario where extinctions occur at a high rate and there is little to no functional redundancy. Moreover, the extent of potential functional redundancy differs across ecosystem functions with some functions being performed by specialized organisms, such as ammonia oxidation, and others by a broader suite of soil biota, such as denitrification. In an influential study addressing functional redundancy in plant communities, Isbell et al.42 showed that broadening the study of the functional role of plant species to multiple growth seasons and environmental conditions resulted in no plant species being identified as functionally redundant. It is very likely that functional redundancy in soils could behave similarly. Unravelling the degree of functional redundancy in soil could represent a huge step in explaining microbial community dynamics over time28. It could also hint at the relative importance of niche versus neutral dynamics in soils. If redundancy in soil is common then it is likely that a lot of functionally ‘equivalent’ taxa exist and that stochastic drivers are of particular importance in driving soil communities; these can be better studied through neutral models. If, however, there is little to no redundancy across soil organisms then the challenge is in attaining sufficiently sophisticated extinction models that consider components of the niche structure of the soil biota, which can be used for predictive purposes.