By Daniel Maude (Dan is a MRes student at the University of Sussex and produced this outstanding report as part of his research. It gives a really nice overview of what natural disturbance is and why it is important. Restoring natural disturbance regimes is a key goal in rewilding which is why we wanted to share it here. You can follow Dan on Twitter here: @DanMaude_90 )
Ongoing anthropogenic ecosystem changes have caused a substantial reduction in global biodiversity. With it comes the insidious loss of ecological processes, including the often-underappreciated effects of natural disturbance. Disturbance is a fundamental process influencing the coexistence of species and structure of diverse ecological communities. The sources of natural disturbances are themselves diverse, yet of particular note is the importance of disturbance mediated by large mammals. Such species create abiotic and vegetational heterogeneity through their biological, ecological, and behavioural functions, in turn influencing nutrient cycles, floral regeneration, primary productivity, community structure, and ecosystem resilience and resistance. Considerable evidence now highlights that without such processes environments can become increasingly uniform, thus reducing the niche space available to sustain diverse communities.
A Loss of Natural Processes
Biodiversity loss is pervasive, with global species extinction rates now surpassing natural background rates by several orders of magnitude (1,2). Many studies have endeavoured to quantify the impacts of such losses, though often they neglect the influence of lost biological interactions (3). Ecological systems are complex, characterised not solely by their composition and structure, but by their processes, dynamics and histories (4). The diversity of components and processes within a system provide functional and structural variability, enhancing complexity and providing increased tolerance to environmental change (5). Many key functional characteristics of ecosystems are strongly determined by biotic and abiotic processes (6), their loss, therefore, can have widespread consequences, including the acceleration of local extinctions, invasion of exotic species (7), and deterioration of ecosystem functions and services (8).
The simplification of ecosystem components has largely been influenced by human defaunation (see Glossary) (3,9), ongoing since the Late Pleistocene (10). Simultaneously, the conversion of natural landscapes for human use has now transformed over half of the planets ice-free surface (11), hastening declines in biodiversity through the loss, fragmentation and degradation of habitats (12,13). Large-bodied mammals have been especially negatively affected (2), the loss of which not only represents an intrinsic loss of biodiversity but a broader depreciation of ecological interactions (14) thus altering the processes and dynamics of ecosystems. Given that environmental interaction strength is largely determined by body-size such deprivation can result in cascading ecological changes (15).
The loss of complex faunal interactions can facilitate environmental homogenisation (16), reducing the spatial variability of biophysical, chemical, and ecological conditions available for species coexistence (4). Environmental heterogeneity is considered a fundamental factor influencing species richness, generating more niches and more species as a consequence (17,18,19). Such heterogeneity is influenced by both biotic and abiotic variations. Studies suggest environmental heterogeneity is not compatible with traditional ecological concepts of climax and equilibrium (4). Instead, the mechanisms of non-equilibrium are assigned greater influence in explaining the coexistence of species and the structure of diverse ecological communities (20,21). Disturbances are temporally discreet events that perturb environmental systems creating natural variability at different spatiotemporal scales, maintaining an ecosystem in a state of continual non-equilibrium (4). External disturbance events can interfere with the various levels of ecological communities, preventing ecosystems from reaching a hypothetical state of static equilibrium.
Global patterns of rapid change have previously altered, and continue to alter, natural disturbance regimes (22). As we enter the ‘United Nations’ decade on ecological restoration’ (23) it is integral that disturbance is recognised as a fundamental process of ecological systems. As such, this review aims to highlight the importance of disturbance regimes and the consequences of altering or losing such processes. Specific consideration is paid to the influence of large herbivorous mammals, with particular attention to wild boar (Sus scrofa), as these species are often considered for reintroduction in ecological restoration projects (24).
Disturbance in Natural Systems
White and Pickett (25) classically defined disturbance as “any relatively discreet event in time that disrupts ecosystem, community, or population structure and changes resources, substrate availability, or the physical environment”. The potential sources of ecosystem disturbance are immeasurable, with almost any climatic event, such as wind, fire, and flooding, or ecological interaction, including foraging, defecation, and soil excavation, a prospective perturbation at some ecological level. The effects of these disturbances are not necessarily universal among different species, communities, and environments, and are often strongly dependent on their sensitivity to the disturbance event in question (26). This is largely related to the ecological history of distinct species (27), yet the effects of disturbance may also vary among individuals intraspecifically due to differences in fitness, age, sex, and behaviour (26).
Numerous studies highlight disturbance as a key mechanism for species co-existence both directly through the mortality of dominant species (28), and indirectly through increased environmental heterogeneity (29). The classical intermediate disturbance hypothesis (IDH) posits that species richness is greatest where disturbance frequency and intensity are intermediate(20). Empirical support for the IDH has been widely documented (30), including in the meadow-steppe systems of North-East China, where higher plant species diversity was observed at intermediate grazing levels (31). Although, many studies have contradicted the IDH by finding positive, negative, and U-shaped relationships between disturbance and diversity (32). Attempting to reconcile theories, Miller et al. (33) consider the relative importance of the multiple aspects of a disturbance event, notably the intensity, timing, duration, extent, and disturbance interval. Accordingly, by recognising the multifaceted nature of disturbance it is possible to better corroborate its ecological effects, and in doing so improve the understanding of discrepancies between different communities.
Many species have evolved adaptive responses in consequence to historical fire disturbance, making them ecologically competitive in fire-dominated landscapes (34). For example, the recruitment of Scots pine (Pinus sylvestris) seedlings is greatly increased from soil scarification caused by fire in boreal and Central European forests, as fire removes the organic soil and herbaceous layer, essential for pine germination (35). For these systems, the absence of fire can shift the composition of the landscape into an increasingly homogenous mosaic (36)(Figure 1.). For instance, numerous studies have indicated the relative importance of fire in maintaining heterogeneity and biodiversity in Savannah ecosystems (37,38,39).
Because fire disturbance can pose a significant threat to human life and settlements, a considerable amount of funding is spent on fire suppression (40). But, for species and ecosystems dependent on fire, the modification of the disturbance regime can become a significant anthropogenic disturbance in itself. Moreover, fire suppression can reduce the frequency of occurrence but, by producing unnaturally higher fuel loads, can potentiate fire severity when they eventually occur (22). However, in regions of no historical fire disturbance, fire can cause irreversible damage to the ecosystem, altering species composition and interaction (41). Even in systems adapted to fire, a higher frequency, more common with climate change (42), can initiate advancing and irrevocable alterations (43).
Wind constitutes an important natural disturbance, particularly in forest ecosystems, where it can influence structure, function, and successional processes (44). Notably, wind causes tree blowdowns, the extent of which vary dependant on the intensity and duration of the event (45). Such events can alter the distributions of tree age, size, and species at stand and landscape scales (46). For instance, past disturbances were found to have strongly influenced the size and age structure of current Norway spruce (Picea abies) forests in the Western Carpathians (47).Wind disturbance to dense canopies provides light and soil resources to understory plants (45). These effects are important in secondary forest landscapes, including those of the North-Eastern USA, where 19th-century agricultural abandonment has created extensive and contiguous forest homogeneity (48). Wind also influences the distribution of woody debris and dead plant matter (49), the deposition of which can increase the biodiversity of saproxylic taxa, including fungi and arthropods (50), as well as non-saproxylic species such as litter-dwelling vertebrates, invertebrates, and cavity-nesting birds (51,52). At the microsite-level, tree fall creates unique substrates and microtopographical structures, such as raised rootwads and soil hollows which can provide ephemeral wet conditions, den opportunities, and nest sites (45). Nevertheless, the frequency and intensity of severe wind disturbance events (e.g., hurricanes) is predicted to increase (53) which could result in irreversible change.
Flood disturbances can increase environmental heterogeneity by creating wet environments, depositing organic matter, removing established vegetation, and generating a dynamic structure and turnover of plant communities (41). Flood disturbance is especially central to riparian zones, where flood regimes organise communities into distinct vegetation belts across a gradient of wet to dry (54), resulting in a markedly heterogenous environment. For example, the flood regime was identified as the predominant predictor of the floodplain forest structure of the lower Wisconsin River, USA, influencing the occurrence, composition and abundance of trees (55). Recurrent flooding events also increase the habitat available to migratory wetland birds (56,41).
However, like fire, flooding can cause substantial damage to human landscapes. Anthropogenic infrastructure that mitigates flooding, including flood defences and drainage systems, are common, yet they can confer a negative impact on biodiversity by altering the natural disturbance regime (57,58). For instance, the presence of flood defences in Yorkshire, UK was found to significantly reduce plant richness and abundance in comparison to undefended sites (58). However, as climate change is projected to increase the frequency and magnitude of precipitation events (53), riparian zones could be at risk from over inundation, potentially reducing environmental heterogeneity and biodiversity (59,60).
The ecological traits of an organism can be a disturbance to other organisms within the system. Animal disturbances, in particular, are a common feature of natural environments and relate to the diverse biological, ecological, and behavioural functions and interactions carried out by a species across their life cycle (41). As body-size is a strong determinant of interaction strength (15), large mammals can contribute a significant amount of ecological disturbance (61).
Large Mammals: Agents of Landscape Disturbance
There is considerable growing evidence of the importance of large animals for ecosystem function and biodiversity (62). Top-down interactions are shown to influence the spatial structure and functionality of many ecosystems, both independently and synergistically with bottom-up controls (63,64). Notable attention is paid to the role that large herbivores play in shaping heterogeneity across a range of ecosystems, including grassland (65), savannah (36), steppe (66), and forest (67). Large herbivores respond to environmental heterogeneity by selecting feeding and resting locations (68,69). Doing so, they augment abiotic and vegetational variability by creating irregular patterns of consumption, nutrient deposition, and physical disturbance (70). These patterns can influence nutrient cycles, plant regeneration, primary productivity, plant community structure, and ecosystem resilience and resistance (14). Indeed, the modification or loss of such processes from past and present defaunation can shift the composition of the entire system (Box 1.) (3,71).
Foraging can have varying direct effects on vegetation, and is largely dependent on the herbivore species involved, plant species consumed, and climatic conditions (41). In general, at intermediate frequencies and densities, grazing disturbance can maintain high floral diversity, as animals preferentially select palatable plants for consumption thus facilitating the growth of unpalatable species (65). Grazing also supresses the domination of competitive species, allowing the coexistence of competitively inferior plants (28). For instance, plant species richness was found to be positively affected by low-intensity cattle grazing at coastal grasslands in the North-Eastern USA (72). Yet, other studies have shown grazing can negatively affect plant diversity in nutrient poor, or arid environments where regrowth may be limited by the availability of resources (73,74), as well as in systems with no historical influence of grazing, such as areas recently cleared for domestic livestock (41). Similarly, browsing of woody species can alter the morphology of plant height and structure. A notable example is the distinct browse-line often observed in large herbivore occupied forests (75). Furthermore, bark stripping by large browsers can induce tree mortality and create gaps in densely forested systems, promoting spatial variability (76). Typically, bark stripping affects a relatively small proportion of trees within a community, with extensive surveys indicating that red deer (Cervus elaphus) disturb between 1–3.4% of conifers per-year (77). Although, this can increase dramatically if the frequency and intensity of the disturbance is increased, such as when deer are confined at high densities in small areas (78).
Large herbivore mediated disturbance is not solely restricted to the direct impacts of grazing and browsing, but also involves the individual or combined effect of trampling. In African savannah ecosystems elephants can promote and maintain a mosaic habitat structure through the downing and trampling of trees, to the benefit of light demanding plants (64,79). Trampling by ungulates is further considered important for the creation of bare ground patches amongst dense ground-flora, facilitating the colonisation of early successional and ephemeral plant species (80). Trampling has also been shown to affect ecosystem hydrology. In arid and semi-arid systems trampling can compact soil pores reducing the infiltration of water and increasing run-off (81). Yet, if hooves break through biotic soil-crusts, common to such systems, then water infiltration can temporarily increase before surface seals reform (82). In mesic systems, low moisture soils are similarly compressed through trampling, reducing pore space available for water storage, but in wet soils, hooves leave deep prints that easily disturb ground-flora, creating space for colonisation (70). Studies also show trampling can enhance the breakdown of leaf litter thus accelerating nitrogen incorporation to the soils of regularly trampled areas (83), though this effect is more strongly observed in mesic systems than arid (84).
Wallowing is a behaviour observed in many large herbivores, with bison (Bison bison) wallowing in the North American Prairies particularly well studied (85,86,87). Large, bare soil patches are created and rolled in for insect protection, grooming, social interaction, and thermoregulation (85). The subsequent wallow is revisited numerous times, forming a distinct depression from soil compaction. Results from Konza Prairie Biological Station, Kansas, indicate buffalo wallowing can create distinctive plant community patches (86), which can promote local arthropod biodiversity (87). In addition, frequent visitation increases soil compaction, causing greater surface-water retention, which can lead to the formation of ephemeral ponds (88) benefiting breeding amphibians (89).
Nutrients obtained through foraging are returned to the ecosystem as faeces, urine, and carcasses by all large herbivores (90). These processes can be considered a natural disturbance because large herbivores deposit sizable amounts in relatively few patches, creating spatial heterogeneity in nutrient availability (91). For instance, white rhinoceros (Ceratotherium simum) export large quantities of nutrients from grazing areas to middens, areas of communal defecation for territorial marking (92), in savannah ecosystems (93). Similarly, ungulates are known to graze and rest in distinct areas, resulting in increased faeces and urine deposition in resting zones (94). Such nutrient additions can dramatically alter nitrogen availability to plants at local scales, causing a shift in community composition (70). Urine deposition, for example, can increase the composition of late successional species that are strong nitrogen competitors (95). In areas of high urine deposition above-ground biomass can increase 4-fold within one-year, in turn increasing the likelihood of future grazing in these areas, thus augmenting the original disturbance in a positive-feedback loop (96).
Animal carcasses add substantial nutrient pulses to discreet landscape patches in excess of all other sources (97). Carcass inputs can elevate nutrient availability across multiple growing seasons, creating ‘hotspots’ of resources that alter plant community composition and landscape heterogeneity (98,99). For instance, bison carcasses in tallgrass prairies are reported to create patches of high soil fertility approximately 5m in diameter, within which the vegetation can be distinctly different from the surrounding area (100). Even in relatively nutrient-rich systems, carcasses can have significant positive impacts on plant biomass and species richness, which can subsequently increase local arthropod abundances (101). Notably, in Western Europe, carcass decomposition has become an increasingly infrequent process, as deceased animals are regularly removed from the landscape (102).
Extensive losses to the diversity and abundance of large herbivores globally can be considered a downgrading of ecological processes and a simplification of ecosystems (6,62,103). However, despite past losses, there is a growing effort to restore the natural functionality of degraded systems, often through the reintroduction of absent species (Box 2.).
Wild Boar Disturbance
Wild boar (Sus scrofa) rooting provides a disturbance regime distinct from those previously covered. Rooting refers to the excavation of surface vegetation and/or soil layers whilst foraging, resulting in localised patches of disturbance similar in appearance to mechanical ploughing (104)(Figure 1.). Resultantly, wild boar have been considered ecosystem engineers, as their rooting can create considerable heterogeneity within vegetated field layers (105). Despite being native to Eurasia, wild boar are now present on every continent excluding Antarctica (106), and given their capacity to modify environments, the impacts of their associated disturbance are well studied across their native and introduced range (105,107,108).
The immediate ecological impact of rooting is the loss of above and below-ground vegetation cover, causing depreciations in plant species abundance and richness (109). Yet, by creating patches of bare ground, wild boar increase the opportunity for the subsequent colonisation of annual and early successional plants. For example, the introduction of wild boar to the forest reserve Dalby Söderskogthe, Southern Sweden, resulted in increased species richness of herbaceous summer plants over three-years (108). Similar results are observed in Mediterranean garrigue landscapes, characterised by woody shrubs, as rooting reduced dominant herb coverage (110), and also in Central European grasslands, albeit through simulated disturbance (29). However, in the majority of introduced studies, wild boar are typically reported to administer a negative effect on native biodiversity (111).
Rooting is an effective natural disturbance to break dense monocultures of ground-flora. In the Scottish Highlands, bracken (Pteridium aquilinum) has become an increasingly problematic species for conservationists and foresters, as its rhizome network allows it to outcompete other native plants (112). A twelve-month study of wild boar within a large experimental enclosure indicated that rooting had successfully reduced bracken frond density by 64% in comparison to unrooted areas (113). Graminoidspecies coverage of rooted plots two-years post-cessation of the wild boar experiment was 14% greater, yet the authors observed the steady recolonisation of bracken in subsequent years, suggesting the restoration of a recurrent rooting regime may be necessary (113). However, the efficacy of wild boar to reduce monoculture patches has caused concern in certain iconic native ecosystems. Dense monospecific bluebell (Hyacinthoides non-scripta) stands are locally abundant in the UK but globally rare. Wild boar are documented to reduce the percentage cover and density of bluebells in Southern British woodlands, with the effects, likewise to the Scottish Highlands, lasting up to two-years before successful re-establishment (104). Nevertheless, regardless of their visual spectacle it could be suggested that such monospecific stands may actually be the product of diminished large mammal disturbances (104). Rooting has been reported to vary spatially and temporally (105,114) resulting in heterogeneity in the intensity, frequency and extent of disturbance, which may mitigate large-scale, long-term reductions of important species such as bluebells. Indeed, many studies have recognised the short-term impacts of wild boar (e.g., compositional changes directly proceeding rooting), but few have documented their longer-term effects (106,111).
High rooting intensities, like many previously discussed disturbances, can significantly reduce plant species diversity and abundance, though most of these reports come from historically non-native areas (107,115). Importantly, many studies that utilise exclosures in comparison to accessible areas fail to quantify local wild boar abundances (111), which impedes the evaluation of their ecological impacts. At natural population densities wild boar are estimated to annually root up to 15,600m2/km2 (116,117), approximately 1.56% of their inhabited area. Confirmation of such estimations are observed in mesic Swedish grasslands (114), yet when aridity increases, levels of rooting decrease, as reported in Central Europe (29) and the Mediterranean (118). In many negative examples of wild boar disturbance the species may have exceeded natural population densities, or be exploiting highly nutritious agricultural crops to sustain larger populations (119). It could be suggested that at natural densities wild boar can increase the spatial heterogeneity of the landscape, as rooting disturbs a relatively small proportion of the inhabited area, presenting opportunities for colonisation and increased species diversity. Although, negative effects could still occur if wild boar preferentially target certain plant species, particularly those of conservation significance, yet no specific preference is observed for the aforementioned British bluebell (120).
Extensive human modification of the planet has caused pervasive losses of natural habitats and biodiversity. Yet, often overlooked and perhaps far more insidious is loss of natural ecological processes. Disturbance is fundamental to the maintenance and diversity of many ecosystems as it can create heterogeneity in resources, substrate availability, and the physical environment. Climatic disturbances are shown to increase the spatiotemporal heterogeneity of landscapes, permitting the coexistence of species. However, anthropogenic ecosystem changes have modified many natural disturbance regimes. Direct disturbance suppression from mitigation infrastructure and management, as well as indirect potentiation of the frequency and intensity of disturbance events through modification of the climate system, can both reduce environmental heterogeneity and biodiversity.
Defaunation represents a notable loss of natural disturbance, with the defaunation of large-bodied herbivores particularly ecologically detrimental. Large herbivores augment abiotic and vegetational heterogeneity by generating irregular patterns of forage consumption, nutrient deposition, and physical disturbance. Considerable evidence is presented in this review to highlight that the loss of such species and their interactions can promote the homogenisation of systems. Wild boar represent a model example of the importance of disturbance, as their rooting behaviour creates opportunities for colonising plants by reducing monospecific patches and creating bare ground.
As we enter the ‘decade of ecological restoration’ it is vital that natural disturbance regimes are recognised as an integral part of naturally functioning ecosystems. This can be further facilitated through future research (see Outstanding Questions), including a better understanding of the long-term effects of disturbances, with specific reference to wild boar. Finally, improved comprehension of the different characteristics of disturbance, including the timing, intensity, interval, duration, and frequency, will be beneficial in determining the impact of such events, which is crucial if disturbance regimes are to be restored amongst an increasingly human dominated world.
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