The importance of natural disturbance in ecological systems

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.   

Disturbance Types

Fire

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).

Figure 1. Natural levels of disturbance vs anthropogenic modification. At natural levels, the impacts of natural disturbance to individual species can have positive effects on landscape heterogeneity, in turn creating opportunities for species colonisation and coexistence with cascading positive outcomes for the community (green boxes). In contrast, human modification of disturbance regimes can have the opposite effect, reducing landscape heterogeneity with cascading negative effects for species coexistence and the ecosystem (brown boxes).  

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

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.

Flooding

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). 

Biotic Disturbances

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).

Figure 2. Rooting behaviour. A Tamworth pig (Sus scrofa domesticus) rooting at Knepp Wildlands, UK. Tamworth pigs exhibit the same rooting behaviour as wild boar – turning over the soil with their snouts in search of food. Image copyright to Knepp Wildlands, knepp.co.uk/new-page-3 (permission for use declared on website).   

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).       

Concluding Remarks

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.   

References

1.Barnosky AD, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, et al. (2011) Has the Earth’s sixth mass extinction already arrived? Nature. 2011; 471: 51–57.
2.Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM. (2015) Accelerated modern human–induced species losses: Entering the sixth mass extinction. Science Advances.  1(5): e1400253, doi: 10.1126/sciadv.1400253.
3.Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B. (2014) Defaunation in the Anthropocene. Science. 345(6195): 401-406, doi: 10.1126/science.1251817.
4.Battisti C, Poeta G, Fanelli G. (2016) Heterogeneity, Dynamism, and Diversity of Natural Systems. In Battisti C, Poeta G, Fanelli G. An Introduction to Disturbance Ecology: A Road Map for Wildlife Management and Conservation. Rome: Springer International Publishing; p. 1-6.
5.Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime J, Hector A, et al. (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science. 294(5543): 804-808, doi: 10.1126/science.1064088.
6.Valiente‐Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, et al. (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology.  29(3): 299-307.
7.Seabloom EW, Borer ET, Martin BA, Orrock JL. (2009) Effects of long‐term consumer manipulations on invasion in oak savanna communities. Ecology. 90: 1356–1365, doi: 10.1890/08-0671.1.
8.Díaz S, Purvis A, Cornelissen JHC, Mace GM, Donoghue MJ, Ewers RM, et al. (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution. 3: 2958–2975, doi: 10.1002/ece3.601.
9.Malhi Y, Doughty CE, Galetti M, Smith FA, Svenning J, Terborgh JW. (2016) Megafauna and ecosystem function from the Pleistocene to the Anthropocene. PNAS. 113(4).
10.Sandom C, Faurby S, Sandel B, Svenning J. (2014) Global late Quaternary megafauna extinctions linked to humans, not climate change. Proceedings of the Royal Society B: Biological Sciences. 2014; 281(1787): 1-9.
11.Hooke RLB, Martín-Duque JF, Pedraza J. (2012) Land transformation by humans: A review. GSA Today. 22: 1-10, doi: 10.1130/GSAT151A.1.
12.Foley JA, DeFries R, Asner GP, Barford C, Bonnan G, Carpenter SR, et al. (2005) Global Consequences of Land Use. Science. 309: 570–574, doi: 10.1126/science.1111772.
13.Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW. (2010) Global Biodiversity: Indicators of Recent Declines. Science. 328(5982): 1164-1168, doi: 10.1126/science.1187512
14.Forbes ES, Cushman JH, Burkepile DE, Young TP, Klope M, Young HS. (2019) Synthesizing the effects of large, wild herbivore exclusion on ecosystem function. Functional Ecology. 33: 1597–1610, doi: 10.1111/1365-2435.13376.
15.Borer ET, Seabloom EW, Shurin JB, Anderson KE, Blanchette CA, Broitman B, et al. (2006) What determines the strength of a trophic cascase? Ecology. 86(2): 528–537.
16.Newman M, Mitchell FJG, Kelly DL. (2014) Exclusion of large herbivores: Long-term changes within the plant community. Forest Ecology and Management. 321: 136-144.
17.MacArthur RH, MacArthur RW. (1961) On Bird Species Diversity. Ecology. 42(3): 594-598, doi: 10.2307/1932254.
18.Stein A, Gerstner K, Kreft H. (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters. 17(7): 866–880.
19.Tews J, Brose U, Grimm V, Tielbörger L, Wichmann MC, Schwager M, et al. (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography. 2004; 31(1): 79-92.
20.Connell JH. (1978) Diversity in Tropical Rain Forests and Coral Reefs. Science. 199(4335): 1302-1310, doi: 10.1126/science.199.4335.130.
21.Collins SL, Glenn SM. (1998) Intermediate disturbance and its relationship to within and between-patch dynamics. New Zealand Journal of Ecology. 21(1): 103-110.
22.Turner MG. (2010) Disturbance and landscape dynamics in a changing world. Ecology. 91(10): 2833–2849, doi: 10.1890/10-0097.1.
23.United Nations. (2021) Decade on restoration. [Online]. [cited 2021/1/11. Available from: https://www.decadeonrestoration.org.
24.Svenning JC, Munk M, Schweiger A. (2019) Trophic rewilding: ecological restoration of top-down trophic interactions to promote self-regulating biodiverse ecosystems. In Pettorelli N, Durant SM, du Toit JT,  Rewilding. Cambridge: Cambridge University Press. p. 73-98.
25.White PS, Pickett STA. (1985) Natural disturbance and patch dynamics: an introduction. In White PS, Pickett STA. The ecology of natural disturbance and patch dynamics. New York, New York, USA: Academic Press. p. 3-13.
26.Battisti C, Poeta G, Fanelli G. (2016) The Concept of Disturbance. In An Introduction to Disturbance Ecology: A Road Map for Wildlife Management and Conservation. Rome: Springer International Publishing.
27.Sousa WP. (1980) The Responses of a Community to Disturbance: The Importance of Successional Age and Species’ Life Histories. Oecologia. 45: 72-81.
28.Pulungan MA, Suzuki S, Krizna M, Gavina A, Tubay J, Ito H, et al. (2019) Grazing enhances species diversity in grassland communities. Nature: Scientific Reports. 9(11201): 1-8, doi: 10.1038/s41598-019-47635-1.
29.Horčičková E, Brůna J, Vojta J. (2019) Wild boar (Sus scrofa) increases species diversity of semidry grassland: Field experiment with simulated soil disturbances. Ecology and Evolution. 9: 2765–2774, doi: 10.1002/ece3.4950.
30.Roxburgh SH, Shea K, Wilson JB. (2004) The intermediate disturbance hypothesis: patch-dynamics and mechanisms of species coexistence. Ecology. 85: 359–371, doi: 10.1890/03-0266.
31.Yan R, Xin X, Yan Y, Wang X, Zhang B, Yang G, et al.  (2015) Impacts of Differing Grazing Rates on Canopy Structure and Species Composition in Hulunber Meadow Steppe. Rangeland Ecology & Management.  68(1): 54-64, doi: 10.1016/j.rama.2014.12.001.
32.Mackey RL, Currie DJ. (2001) The Diversity-Disturbance Relationship: Is It Generally Strong and Peaked? Ecology. 82(12): 3479-3492, doi: 10.2307/2680166.
33.Miller AD, Roxburgh SH, Shea K. (2011) How frequency and intensity shape diversity–disturbance relationships. PNAS. 108(14): 5643–5648, doi: 10.1073/pnas.1018594108.
34.Spanos IA, Daskalakoub EN, Thanos CA. (2000) Postfire, natural regeneration of Pinus brutia forests in Thasos island, Greece. Acta Oecologica. 21(1): 13-20, doi: 10.1016/S1146-609X(00)00107-7.
35.Hille M, den Ouden J. (2004) Improved recruitment and early growth of Scots pine (Pinus sylvestris L.) seedlings after fire and soil scarification. European Journal of Forest Research. 123: 213–218, doi: 10.1007/s10342-004-0036-4.
36.Levick SR, Asner GP, Kennedy-Bowdoin T, Knapp DE. (2009) The relative influence of fire and herbivory on savanna three-dimensional vegetation structure. Biological Conservation. 2009; 142: 1693–1700, doi: 10.1016/j.biocon.2009.03.004.
37.Bond WJ, Keeley JE. (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends in Ecology and Evolution. 20(7): 387-394, doi: 10.1016/j.tree.2005.04.025.
38.Bond WJ. (2008) What limits trees in C4 grasslands and savannas? Annual Review of Ecology, Evolution, and Systematics. 39: 641-659, doi: 10.1146/annurev.ecolsys.39.110707.173411.
39.Abreu RCR, Hoffmann WA, Vasconcelos H, Pilon NA, Rossatto DR, Durigan G. (2017) The biodiversity cost of carbon sequestration in tropical savanna. Science Advances.  3(8): e1701284, doi: 10.1126/sciadv.1701284.
40.Zhuang J, Payyappalli VM, Behrendt B, Lukasiewicz K. (2017) Total Cost of Fire in the United States. Buffalo, New York, USA.
41.Battisti C, Poeta G, Fanelli G. (2016) Categories of Natural Disturbances. In An Introduction to Disturbance Ecology: A Road Map for Wildlife Management and Conservation. Rome: Springer International Publishing. p. 59-71.
42.Shuman JK, Foster AC, Shugart HH, Hoffman-Hall A, Krylov A, Loboda T, et al. (2017) Fire disturbance and climate change: implications for Russian forests. Environmental Research Letters. 12: 035003, doi: 10.1088/1748-9326/aa5eed.
43.Hinojosa MB, Albert-Belda E, Gómez-Muñoz B, Moreno JM. (2021) High fire frequency reduces soil fertility underneath woody plant canopies of Mediterranean ecosystems. Science of the Total Environment. 752: 141877, doi: 10.1016/j.scitotenv.2020.141877.
44.Meigs GW, Keeton WS. (2018) Intermediate-severity wind disturbance in mature temperate forests: legacy structure, carbon storage, and stand dynamics. Ecological Applications. 28(3): 798–815, doi: 10.1002/eap.1691.
45.Mitchell SJ. (2012) Wind as a natural disturbance agent in forests: a synthesis. Forestry. 86: 147-157, doi: 10.1093/forestry/cps058.
46.Cowden MM, Hart JL, Schweitzer CJ, Dey DC. (2014) Effects of intermediate-scale wind disturbance on composition, structure, and succession in Quercus stands: Implications for natural disturbance-based silviculture. Forest Ecology and Management. 330: 240-251, doi: 10.1016/j.foreco.2014.07.003.
47.Janda P, Trotsiuka V, Mikolášab M, Bačea R, Nagel TA, Seidl R, et al. (2017) The historical disturbance regime of mountain Norway spruce forests in the Western Carpathians and its influence on current forest structure and composition. Forest Ecology and Management. 388: 67-78, doi: 10.1016/j.foreco.2016.08.014.
48.Urbano AR, Keeton WS. (2017) Carbon dynamics and structural development in recovering secondary forests of the northeastern U.S. Forest Ecology and Management. 392: 21-35, doi: 10.1016/j.foreco.2017.02.037.
49.Ford SA, Kleinman JS, Hart JL. (2018) Effects of wind disturbance and salvage harvesting on macrofungal communities in a Pinus woodland. Forest Ecology and Management. 401: 31-46, doi: 10.1016/j.foreco.2017.10.010.
50.Stokland J, Siitonen J, Jonsson BG. (2012) Biodiversity in Dead Wood Cambridge: Cambridge University Press.
51.Fauteux D, Imbeau L, Drapeau P, Mazerolle MJ. (2012) Small mammal responses to coarse woody debris distribution at different spatial scales in managed and unmanaged forests. Forest Ecology and Management. 266: 194-205, doi: 10.1016/j.foreco.2011.11.020.
52.Seibold S, Bässler C, Brandl R, Gossner MM, Thorn S, Ulyshen MD, et al. (2015) Experimental studies of dead-wood biodiversity – A review identifying global gaps in knowledge. Biological Conservation. 191: 139-149, doi: 0.1016/j.biocon.2015.06.006.
53.IPCC. (2007) IPCC Fourth Assessment Report.
54.Ström L, Jansson R, Nilsson C, Johansson ME, Xiong S. (2011) Hydrologic effects on riparian vegetation in a boreal river: an experiment testing climate change predictions. Global Change Biology. 17(1): 254-267, doi: 10.1111/j.1365-2486.2010.02230.x.
55.Turner MG, Gergel SE, Dixon MD, Miller JR. (2004) Distribution and abundance of trees in floodplain forests of the Wisconsin River: Environmental influences at different scales. Journal of Vegetation Science. 15: 729-73.
56.Hagy HM, Hine CS, Horath MM, Yetter AP, Smith RV, Stafford JD. (2017) Waterbird response indicates floodplain wetland restoration. Hydrobiologia. 804: 119-137, doi: 10.1007/s10750-016-3004-3.
57.Beauchamp VB, Stromberg JC. (2008) Changes to herbaceous plant communities on a regulated desert river. River Research and Applications. 24(6): 754-770, doi: 10.1002/rra.1078.
58.Pettifer E, Kay P. (2012) The effects of flood defences on riparian vegetation species richness and abundance. Water and Environmental Journal. 26: 343–351, doi: 10.1111/j.1747-6593.2011.00294.x.
59.Garssen AG, Baattrup‐Pedersen A, Voesenek LACJ, Verhoeven JTA, Soons MB. (2015) Riparian plant community responses to increased flooding: a meta‐analysis. Global Change Biology. 21(8): 2881-2890, doi: 10.1111/gcb.12921.
60.Faragó S, Hangya K. (2012) Effects of water level on waterbird abundance and diversity along the middle section of the Danube River. Hydrobiologia. 687: 15–21, doi: 10.1007/s10750-012-1166-1.
61.Laws RM. (1970) Elephants as agents of habitat and landscape change in East Africa. Oikos.  21(1): 1-15, doi: 10.2307/3543832.
62.Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, et al. (2011) Trophic Downgrading of Planet Earth. Science. 333(6040): 301-306.
63.Adler PB, Raff DA, Lauenroth WK. (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia. 128: 465–479.
64.Bakker ES, Gill JL, Johnson CN, Vera FWM, Sandom CJ, Asner GP, et al. (2016) Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation. PNAS. 113(4): 847–855.
65.Olff H, Ritchie ME. (1998) Effects of herbivores on grassland plant diversity. Trends in Ecology and Evolution. 13(7): 261-265.
66.Zhu H, Wang D, Wang L, Bai Y, Fang J, Liu J. (2012) The effects of large herbivore grazing on meadow steppe plant and insect diversity. Journal of Applied Ecology. 49: 1075–1083, doi: 10.1111/j.1365-2664.2012.02195.x.
67.Kirby KJ. (2004) A model of a natural wooded landscape in Britain as influenced by large herbivore activity. Forestry. 77(5): 405-420, 10.1093/forestry/77.5.405.
68.Palmer SCF, Hester AJ. (2000) Predicting spatial variation in heather utilization by sheep and red deer within heather/grass mosaics. Journal of Applied Ecology. 2000; 37: 616-631.
69.Dupke C, Bonenfant C, Reineking B, Hable R, Zeppenfeld T, Ewald M, et al. (2017) Habitat selection by a large herbivore at multiple spatial and temporal scales is primarily governed by food resources. Ecography. 40: 1014–1027, doi: 10.1111/ecog.02152.
70.Hobbs NT. (2006) Large herbivores as sources of disturbance in ecosystems. In Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge: Cambridge University Press. p. 261-288.
71.Sandom CJ, Ejrnæs R, Hansen MD, Svenning JC. (2014) High herbivore density associated with vegetation diversity in interglacial ecosystems. PNAS. 111(11): 4162-4167.
72.Kinnebrew E, Champlin LK, Neill C. (2019) Interactions between cattle grazing, plant diversity, and soil nitrogen in a northeastern U.S. coastal grassland. Applied Vegetation Science. 22: 317–325, doi: 10.1111/avsc.12422.
73.Stewart GG, Pullin AS. (2008) The relative importance of grazing stock type and grazing intensity for conservation of mesotrophic ‘old meadow’ pasture. Journal for Nature Conservation. 16: 175–185, doi: 10.1016/j.jnc.2008.09.005.
74.Proulx M, Mazumder A. (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology. 79: 2581–2592. doi: 10.1890/0012-9658.
75.Smit C, Putman R. (2011) Large herbivores as ‘environmental engineers’. In Putman R, Apollonio M, Andersen R, editors. Ungulate Management in Europe. Cambridge: Cambridge University Press. p. 260-283.
76.Vera FWM. (2000) Grazing ecology and forest history. 1st ed. Wallingford: CABI Publishing.
77.Gill RMA, Webber J, Peace A. (2000) The Economic Implications of Deer Damage: a Review of Current Evidence. Inverness.
78.Scott D, Welch D, Thurlow M, Elston DA. (2000) Regeneration of Pinus sylvestris in a natural pinewood in NE Scotland following reduction in grazing by Cervus elaphusForest Ecology Management. 130: 199–211.
79.Asner GP. (2012) Landscape-scale effects of herbivores on treefall in African savannas. Ecology Letters. 15(11): 1211–1217.
80.Hester A, Bergman M, Iason G, Moen J. (2006) Impacts of large herbivores on plant community structure and dynamics. In Danell K, Bergström R, Duncan P, Pastor J, editors. Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge University Press: Cambridge. p. 97-141.
81.Cantón Y, Chamizo S, Rodriguez-Caballero E, Lázaro R, Roncero-Ramos B, Román JR, et al. (2020) Water Regulation in Cyanobacterial Biocrusts from Drylands. Water. 12(720): 1-24, doi: 10.3390/w12030720.
82.Chamizo S, Cantón Y, Lázaro R, Solé-Benet A, Domingo F. (2012) Crust composition and disturbance drive Infiltration through biological soil crusts in semiarid ecosystems. Ecosystems.  15: 148–161, doi: 10.1007/s10021-011-9499-6.
83.Facelli JM, Pickett STA. (1991) Plant Litter: Its Dynamics and Effects on Plant Community Structure. The Botanical Review. 57(1): 1-31.
84.Chuan X, Carlyle CN, Bork EW, Chang SX, Hewins DB. (2018) Long-Term Grazing Accelerated Litter Decomposition in Northern Temperate Grasslands. Ecosystems. 21: 1321–1334, doi: 10.1007/s10021-018-0221-9.
85.McMillan BR, Cottam MR, Kaufman DW. (2000) Wallowing behavior of American bison (Bos bison) in tallgrass prairie: an examination of alternate explanations. American Midland Naturalist. 144: 159-167.
86.McMillan B, Pfeiffer KA, Kaufman DW. (2011) Vegetation responses to an animal-generated disturbance (Bison Wallows) in tallgrass prairie. American Midland Naturalist. 165(1): 60-73, doi: 10.1674/0003-0031-165.1.60.
87.Nickell Z, Varriano S, Plemmons E, Moran MD. (2018) Ecosystem engineering by bison (Bison bison) wallowing increases arthropod community heterogeneity in space and time. Ecosphere. 9(9): e02436, doi: 10.1002/ecs2.2436.
88.Uno GE. (2019) Dynamics of plants in buffalo wallows: Ephemeral pools in the Great Plains. In The Evolutionary Ecology Of Plants. New York, New York: Routledge. p. 431-444.
89.Busby WH, Brecheisen WR. (1997) Chorusing Phenology and Habitat Associations of the Crawfish Frog, Rana areolata (Anura: Ranidae), in Kansas. The Southwestern Naturalist. 42(2): 210-217.
90.Bakker ES, Olff H, Boekhoff M, Gleichman JM, Berendse F. (2004) Impact of herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia. 138: 91–101, doi: 10.1007/s00442-003-1402-5.
91.Augustine DJ, Frank DA. (2001) Effects of migratory grazers on spatial heterogeneity of soil nitrogen properties in a grassland ecosystem. Ecology. 82: 3149–3162, doi: 10.1890/0012-9658.
92.Owen-Smith N. (1971) Territoriality in White Rhinoceros (Ceratotherium simum) Burchell. Nature. 231: 294–296, doi: 10.1038/231294a0.
93.Veldhuis MP, Gommers MI, Olff H, Berg MP. (2018) Spatial redistribution of nutrients by large herbivores and dung beetles in a savanna ecosystem. Journal of Ecology. 106: 422–433, doi: 10.1111/1365-2745.12874.
94.McNaughton SJ. (1993) Grasses and Grazers, Science and Management. Ecological Applications.  3(1): 17-20, doi: 10.2307/1941782.
95.Steinauer EM, Collins SL. (1995) Effects of Urine Deposition on Small‐Scale Patch Structure in Prairie Vegetation. Ecology. 74(4): 1195-1205, doi: 10.2307/1940926.
96.Steinauer EM, Collins SL. (2001) Feedback loops in ecological hierarchies following urine deposition in tallgrass prairie. Ecology. 82: 1319–1329, doi: 10.1890/0012-9658.
97.Knapp AK, Blair JM, Briggs JM. (1999) The keystone role of bison in North American tallgrass prairie. Bison increase habitat heterogeneity and alter a broad array of plant, community, and ecosystem processes. Biosicence. 49: 39–50, doi: 10.1525/bisi.1999.49.1.39.
98.Barton PS, McIntyre S, Evans MJ, Bump JK, Cunningham SA, Manning AD. (2016) Substantial long-term effects of carcass addition on soil and plants in a grassy eucalypt woodland. Ecosphere. 7(10): e01537, doi: 10.1002/ecs2.1537.
99.Risch AC, Frossard A, Schütz M, Frey B, Morris AW, Bump JK. (2020) Effects of elk and bison carcasses on soil microbial communities and ecosystem functions in Yellowstone, USA. Functional Ecology. 34: 1933–1944, doi: 10.1111/1365-2435.13611.
100.Towne EG. (2000) Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia. 122: 132-139.
101.van Klink R, van Laar-Wiersma J, Vorst O, Smit C. (2020) Rewilding with large herbivores: Positive direct and delayed effects of carrion on plant and arthropod communities. PLoS ONE. 15(1): e0226946, doi: 10.1371/journal.pone.0226946.
102.European Commission. (2009) Regulation (EC) No 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing regulation.
103.Smith FA, Smith REE, Lyons SK, Payne JL. (2018) Body size downgrading of mammals over the late Quaternary. Science. 360(6386): 310–313, doi: 10.1126/science.aao5987.
104.Sims NK, John EA, Stewart AJA. (2014) Short-term response and recovery of bluebells (Hyacinthoides non-scripta) after rooting by wild boar (Sus scrofa). Plant Ecology. 215: 1409-1416, doi: 10.1007/sl 1258-014-0397-9.
105.Sandom CJ, Hughes J, MacDonald DW. (2013) Rewilding the Scottish Highlands: Do Wild Boar, Sus scrofa, Use a Suitable Foraging Strategy to be Effective Ecosystem Engineers? Restoration Ecology. 21(3): 336–343, doi: 10.1111/j.1526-100X.2012.00903.x.
106.Barrios-Garcia MN, Ballari SA. (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biological Invasions. 14: 2283–2300 doi: 10.1007/s10530-012-0229-6.
107.Barrios-Garcia MN, Classen AT, Simberloff D. (2014) Disparate responses of above and belowground properties to soil disturbance by an invasive mammal. Ecosphere. 5(4): 1-13, doi: 10.1890/ES13-00290.1.
108.Brunet J, Hedwall P, Holmström E, Wahlgren E. (2016) Disturbance of the herbaceous layer after invasion of an eutrophic temperate forest by wild boar. Nordic Journal of Botany.  34: 120–128, doi: 10.1111/njb.01010.
109.Siemann E, Carrillo JA, Gabler CA, Zipp R, Rogers WE. (2009) Experimental test of the impacts of feral hogs on forest dynamics and processes in the southeastern US. Forest Ecology and Management. 258: 546–553, doi: 10.1016/j.foreco.2009.03.056.
110.Dovrat G, Perevolotsky A, Ne’eman G. (2014) The response of Mediterranean herbaceous community to soil disturbance by native wild boars. Plant Ecology. (215): 531-541, doi: 10.1007/sl 1258-014-0321-3.
111.Genov PV, Focardi S, Morimando F, Scillitani L, Ahmed A. (2017) Ecological Impact of Wild Boar in Natural Ecosystems. In Ecology, Conservation and Management of Wild Pigs and Peccaries. Cambridge : Cambridge University Press. p. 404-419, doi: 10.1017/9781316941232.
112.Pakeman R, Le Duc M, Marrs R. Pakeman, R., M. Le Duc, and R. Marrs. (2000) Bracken distribution in Great Britain: strategies for its control and the sustainable management of marginal land. Annals of Botany. 85: 37–46, doi: 10.1006/anbo.1999.1053.
113.Sandom CJ, Macdonald DW. (2015) What next? Rewilding as a radical future for the British countryside. In Wildlife Conservation on Farmland: Managing for Nature on Lowland Farms. Oxford: Oxford University Press. p. 291-316.
114.Welander J. (2002) Spatial and temporal dynamics of wild boar (Sus scrofa) rooting in a mosaic landscape. Journal of Zoology. 252: 263-271, doi: 10.1111/j.l469-7998.2000.tb0062.x.
115.Tierney TA, Cushman JH. (2006) Temporal changes in native and exotic vegetation and soil characteristics following disturbances by feral pigs in a California grassland. Biological Invasions. 8: 1073–1089, doi: 10.1007/s10530-005-6829-7.
116.Sandom CJ, Donland CJ, Svenning JC, Hansen DM. (2013) Rewilding. In Key Topics in Conservation Biology 2. Oxford: Blackwell Publishing. p. 430-451.
117.Sandom CJ, Hughes J, Macdonald DW. (2013) Rooting for Rewilding: Quantifying Wild Boar’s Sus scrofa Rooting Rate in the Scottish Highlands. Restoration Ecology. 21(3): 329–335, doi: 10.1111/j.1526-100X.2012.00904.x.
118.Cahill S, Llimona F, Gràcia J. (2003) Spacing and nocturnal activity of wild boar Sus scrofa in a Mediterranean metropolitan park. Wildlife Biology. 9: 3-13, doi: 10.2981/wlb.2003.058.
119.Caley P. (1993) Population dynamics of feral pigs (Sus Scrofa) in a tropical riverine habitat complex. Wildlife Research. 20: 625–636, doi: 10.1071/WR9930625.
120.Harmer R, Straw N, Williams D. (2011) Boar, bluebells and beetles. Quarterly Journal of Forestry. 2011; 105(3): 195-202.
121.Corlett RT. (2016) Restoration, Reintroduction and Rewilding in a Changing World. Trends in Ecology and Evolution. 31(6): 453-462.
122.Svenning J, Pedersen PBM, Donlan CJ, Ejrnæs R, Faurby S, Galetti HDM, et al. (2016) Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research. PNAS.  113(4): 898–906.
123.Vera FWM. (2009) Large-scale nature development – The Oostvaardersplassen. British Wildlife. 20(5): 20-36.
124.Zimov SA. (2005) Pleistocene Park: Return of the Mammoth’s Ecosystem. Science. 308: 796-798, doi: 10.1126/science.1113442.

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s

%d bloggers like this: