Restoration for variability: emergence of the habitat diversity paradigm in terrestrial ecosystem restoration

Ecosystem restoration implies focusing on multiple trophic levels and ecosystem functioning, yet higher trophic levels, that is, animals, are less frequently targeted by restoration than plants. Habitat diversity, the spatial heterogeneity between and within habitat patches in a landscape, is a well‐known driver of species diversity, and offers possible ways to increase species diversity at multiple trophic levels. We argue that habitat diversity is central in whole‐ecosystem restoration as we review its importance, provide a practical definition for its components, and propose ways to target it in restoration. Restoration targeting habitat diversity is used commonly in aquatic ecosystems, mostly to increase the physical diversity of habitats, meant to provide more niches available to a higher number of animal species. To facilitate the uptake of habitat diversity in terrestrial ecosystem restoration, we distinguish between compositional and structural habitat diversity, because different animal groups will respond to different aspects of habitat diversity. We also propose four methods to increase habitat diversity: varying the starting conditions to obtain divergent successional pathways, emulating natural disturbances, establishing keystone structures, and applying ecosystem engineer species. We provide two case studies to illustrate how these components and methods can be incorporated in restoration. We conclude that targeting habitat diversity is a promising way to restore habitats for a multitude of species of animals and plants, and that it should become mainstream in restoration ecology and practice. We encourage the restoration community to consider compositional and structural habitat diversity and to specifically target habitat diversity in ecosystem restoration.     

Disentangling vegetation diversity from climate–energy and habitat heterogeneity for explaining animal geographic patterns

Broad‐scale animal diversity patterns have been traditionally explained by hypotheses focused on climate–energy and habitat heterogeneity, without considering the direct influence of vegetation structure and composition. However, integrating these factors when considering plant–animal correlates still poses a major challenge because plant communities are controlled by abiotic factors that may, at the same time, influence animal distributions. By testing whether the number and variation of plant community types in Europe explain country‐level diversity in six animal groups, we propose a conceptual framework in which vegetation diversity represents a bridge between abiotic factors and animal diversity. We show that vegetation diversity explains variation in animal richness not accounted for by altitudinal range or potential evapotranspiration, being the best predictor for butterflies, beetles, and amphibians. Moreover, the dissimilarity of plant community types explains the highest proportion of variation in animal assemblages across the studied regions, an effect that outperforms the effect of climate and their shared contribution with pure spatial variation. Our results at the country level suggest that vegetation diversity, as estimated from broad‐scale classifications of plant communities, may contribute to our understanding of animal richness and may be disentangled, at least to a degree, from climate–energy and abiotic habitat heterogeneity.     

The latitudinal gradient of species diversity among North American grasshoppers (Acrididae) within a single habitat: a test of the spatial heterogeneity hypothesis

Abstract. The spatial heterogeneity hypothesis predicts a positive relationship between habitat complexity and species diversity: the greater the heterogeneity of a habitat, the greater the number of species in that habitat. On a regional scale, this hypothesis has been proposed to explain the increases in species diversity from the poles to the tropics: the tropics are more diverse because they contain more habitats. On the local scale, the spatial heterogeneity hypothesis suggests that the tropics are more diverse because they contain more microhabitats. The positive relationship between habitat heterogeneity and species diversity, on the local scale, is well documented. In this paper, we test whether habitat heterogeneity on the local scale can explain the latitudinal gradient of species diversity on the regional scale. We determined the latitudinal gradient of species diversity of 305 species of North American grasshoppers using published distribution maps. We compared the slope of this multihabitat (regional-scale) gradient with the slope of a within-habitat (local-scale) gradient in the prairie grasslands. Our results show no significant difference between the slopes at the two scales. We tested the generality of our results by comparing multi- and within-habitat latitudinal gradients of species diversity for ants, scorpions and mammals using data from the literature. These results are in accordance with those from grasshoppers. We can therefore reject the local-scale spatial heterogeneity hypothesis as a mechanism explaining the regional-scale latitudinal gradient of species diversity. We discuss alternative mechanisms that produce this gradient.     

Light heterogeneity affects understory plant species richness in temperate forests supporting the heterogeneity–diversity hypothesis

One of the most important drivers for the coexistence of plant species is the resource heterogeneity of a certain environment, and several studies in different ecosystems have supported this resource heterogeneity–diversity hypothesis. However, to date, only a few studies have measured heterogeneity of light and soil resources below forest canopies to investigate their influence on understory plant species richness. Here, we aim to determine (1) the influence of forest stand structural complexity on the heterogeneity of light and soil resources below the forest canopy and (2) whether heterogeneity of resources increases understory plant species richness. Measures of stand structural complexity were obtained through inventories and remote sensing techniques in 135 1‐ha study plots of temperate forests, established along a gradient of forest structural complexity. We measured light intensity and soil chemical properties on six 25 m² subplots on each of these 135 plots and surveyed understory vegetation. We calculated the coefficient of variation of light and soil parameters to obtain measures of resource heterogeneity and determined understory plant species richness at plot level. Spatial heterogeneity of light and of soil pH increased with higher stand structural complexity, although heterogeneity of soil pH did not increase in conditions of generally high levels of light availability. Increasing light heterogeneity was also associated with increasing understory plant species richness. However, light heterogeneity had no such effects in conditions where soil resource heterogeneity (variation in soil C:N ratios) was low. Our results support the resource heterogeneity–diversity hypothesis for temperate forest understory at the stand scale. Our results also highlight the importance of interaction effects between the heterogeneity of both light and soil resources in determining plant species richness.     

When humans work like beavers: riparian restoration enhances invertebrate gamma diversity and habitat heterogeneity

Restoration has the potential to increase habitat heterogeneity through the creation of unique habitat patches that, in turn, increase regional species richness or gamma diversity. While biological diversity and habitat heterogeneity are important factors to consider under a shifting climate, restoration actions and outcomes rarely examine these components. In this study, we examined the effects of riparian beaver dam analog (BDA) restoration on aquatic invertebrate diversity and habitat heterogeneity. Although the effects of BDAs on hydrology, geomorphology, and salmonid habitat have been explored, we are unaware of any studies assessing their effects on aquatic invertebrate diversity and the food web that supports them. We sampled aquatic invertebrates, basal carbon resources, dissolved nutrients, turbidity, and water temperature in pre- and post-BDA pond, side channel, and mainstem habitat over a three-year period. The BDAs functioned similarly to natural beaver dams and created slow-water environments that accumulated fine particulate organic material and increased pelagic phytoplankton production. Nonmetric multidimensional scaling, permutation multivariate analysis of variance, and Mantel's tests demonstrated that these changes led to the formation of a unique invertebrate community populated by lentic macroinvertebrates and zooplankton, which increased beta-diversity and gamma diversity. Further, BDAs in our study maintained high densities of invertebrates and buffered water temperatures in comparison to adjacent lotic habitats. These results support our hypothesis that BDAs can enhance invertebrate beta and gamma diversity through the creation and colonization of unique pond habitat and improve habitat and resource heterogeneity for native fishes under variable climate conditions.     

Influence of clay licks on the diversity and structure of an Amazonian forest

The spatial heterogeneity of resource availability is a major driver of biodiversity patterns. Some environmental conditions and resources are characterized by large‐scale patterns of variation within the landscape. Clumped local discontinuities or discrete elements also increase spatial heterogeneity, promoting local ‘biodiversity hot spots’ by modifying habitat characteristics and promoting plant–animal interactions. Clay licks are faunal attractors owing to their role in the nutritional ecology of the user species; nevertheless, the effect of their presence on the surrounding vegetation has been poorly quantified. Here, we use data from 100 × 10 m transects and evaluate the effects of the presence of clay licks on forest diversity and structure at local and landscape scales. In clay lick areas, there was a higher abundance of certain species, which helps to homogenize species composition between localities counteracting the natural distance‐decay of compositional similarity between transects without clay lick influence (controls). Compared to control sites, clay lick′s forests had higher palm densities, shorter but more variable individuals in the canopy and understory, a thinner canopy layer, and denser herbaceous and ground level covers. These differences were found along the whole length of transects in both sampled areas types. These results reveal that the presence of discrete elements (i.e., clay licks) may help to explain the compositional and structural heterogeneity of Amazonian forests influencing ecological processes such as seed dispersal and trampling. These considerations may be relevant for other biomes where clay licks are present and give weight to their inclusion in conservation initiatives in tropical forests.     

Landscape heterogeneity in relation to variations in epigaeic beetle diversity of a Mediterranean ecosystem. Implications for conservation

Habitat heterogeneity is a determinant cause of biological diversity in natural ecosystems, and therefore its preservation should be a priority when planning conservation strategies. Sierra de Baza, in southern Spain, is a protected natural area in which biotopes of particular interest still remain, but extensive afforestation with pine species has been widespread in recent decades and, in some cases, continues. The aim of this paper is to test the role of habitat heterogeneity at the landscape scale in generating epigaeic beetle diversity in Sierra de Baza. After two-year-long cycles of sampling epigaeic beetles, differences in local diversity at nine sites, and differences in the pattern of species turnover between sites, have been measured. Local communities differed among sites, 74% of the species being scarce (less than 0.41% of total beetle abundance), and thus species replacement differed markedly between sites. Comparisons between habitat types showed that the planted pine forests support less diverse fauna. Our results identify habitat heterogeneity at the landscape scale as the main source of epigaeic beetle diversity at the landscape scale, practices such as extensive afforestation diminishing landscape heterogeneity and consequently local beetle diversity. Preservation of landscape heterogeneity should be encouraged for an adequate beetle biodiversity conservation.     

Food plant diversity as broad-scale determinant of avian frugivore richness

The causes of variation in animal species richness at large spatial scales are intensively debated. Here, we examine whether the diversity of food plants, contemporary climate and energy, or habitat heterogeneity determine species richness patterns of avian frugivores across sub-Saharan Africa. Path models indicate that species richness of Ficus (their fruits being one of the major food resources for frugivores in the tropics) has the strongest direct effect on richness of avian frugivores, whereas the influences of variables related to water-energy and habitat heterogeneity are mainly indirect. The importance of Ficus richness for richness of avian frugivores diminishes with decreasing specialization of birds on fruit eating, but is retained when accounting for spatial autocorrelation. We suggest that a positive relationship between food plant and frugivore species richness could result from niche assembly mechanisms (e.g. coevolutionary adaptations to fruit size, fruit colour or vertical stratification of fruit presentation) or, alternatively, from stochastic speciation-extinction processes. In any case, the close relationship between species richness of Ficus and avian frugivores suggests that figs are keystone resources for animal consumers, even at continental scales.     

Environmental heterogeneity as a universal driver of species richness across taxa,biomes and spatial scales

Environmental heterogeneity is regarded as one of the most important factors governing species richness gradients. An increase in available niche space, provision of refuges and opportunities for isolation and divergent adaptation are thought to enhance species coexistence, persistence and diversification. However, the extent and generality of positive heterogeneity–richness relationships are still debated. Apart from widespread evidence supporting positive relationships, negative and hump‐shaped relationships have also been reported. In a meta‐analysis of 1148 data points from 192 studies worldwide, we examine the strength and direction of the relationship between spatial environmental heterogeneity and species richness of terrestrial plants and animals. We find that separate effects of heterogeneity in land cover, vegetation, climate, soil and topography are significantly positive, with vegetation and topographic heterogeneity showing particularly strong associations with species richness. The use of equal‐area study units, spatial grain and spatial extent emerge as key factors influencing the strength of heterogeneity–richness relationships, highlighting the pervasive influence of spatial scale in heterogeneity–richness studies. We provide the first quantitative support for the generality of positive heterogeneity–richness relationships across heterogeneity components, habitat types, taxa and spatial scales from landscape to global extents, and identify specific needs for future comparative heterogeneity–richness research.     

Habitat and climate heterogeneity maintain beta-diversity of birds among landscapes within ecoregions

Aim  Habitat and climate heterogeneity may affect patterns of species diversity from the relatively local scale of communities to the broad biogeographical scale of continents. However, the effects of heterogeneity on species diversity have not been studied as widely at intermediate scales although differences among landscapes in local climate and habitat should maintain beta-diversity.
Location  Bailey ecoregions in the USA.
Methods  Using a geographically extensive dataset on bird distribution and abundance in 35 ecoregions, we tested for the effects of habitat and climate heterogeneity on beta-diversity at two discrete spatial scales: among sample points within landscapes, and among landscapes within ecoregions.
Results  Landscape-level beta-diversity typically accounted for 50% or more of gamma-diversity and was significantly and positively related to habitat heterogeneity (elevational range within an ecoregion) and climate heterogeneity (variation in potential evapotranspiration). Contrary to predictions, point-level beta-diversity was negatively related to habitat and climate heterogeneity, perhaps because heterogeneity constrains alpha-diversity at the landscape level. The geographical spatial separation of landscapes within an ecoregion did not significantly affect beta-diversity at either scale.
Main conclusions  Our results suggest that habitat selection and adaptation to local climate may be the primary processes structuring bird diversity among landscapes within ecoregions, and that dispersal limitation has a lesser role in influencing beta-diversity among landscapes.     

Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient

Habitat heterogeneity contributes to the maintenance of diversity, but the extent that landscape-scale rather than local-scale heterogeneity influences the diversity of soil invertebrates—species with small range sizes—is less clear. Using a Scottish habitat heterogeneity gradient we correlated Collembola and lumbricid worm species richness and abundance with different elements (forest cover, habitat richness and patchiness) and qualities (plant species richness, soil variables) of habitat heterogeneity, at landscape (1 km²) and local (up to 200 m²) scales. Soil fauna assemblages showed considerable turnover in species composition along this habitat heterogeneity gradient. Soil fauna species richness and turnover was greatest in landscapes that were a mosaic of habitats. Soil fauna diversity was hump-shaped along a gradient of forest cover, peaking where there was a mixture of forest and open habitats in the landscape. Landscape-scale habitat richness was positively correlated with lumbricid diversity, while Collembola and lumbricid abundances were negatively and positively related to landscape spatial patchiness. Furthermore, soil fauna diversity was positively correlated with plant diversity, which in turn peaked in the sites that were a mosaic of forest and open habitat patches. There was less evidence that local-scale habitat variables (habitat richness, tree cover, plant species richness, litter cover, soil pH, depth of organic horizon) affected soil fauna diversity: Collembola diversity was independent of all these measures, while lumbricid diversity positively and negatively correlated with vascular plant species richness and tree canopy density. Landscape-scale habitat heterogeneity affects soil diversity regardless of taxon, while the influence of habitat heterogeneity at local scales is dependent on taxon identity, and hence ecological traits, e.g. body size. Landscape-scale habitat heterogeneity by providing different niches and refuges, together with passive dispersal and population patch dynamics, positively contributes to soil faunal diversity. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Soil pH and species diversity in coastal dunes

Soil pH was measured at two different spatial scales in coastal dunes on Norderney, North Sea, and in Mecklenburg-Vorpommern, Baltic Sea, Germany. Relationships between the variability in soil pH, species richness and species diversity are presented. Species richness and diversity were highest in grey dunes, where soil pH was at intermediate levels; both variables were lower in yellow and brown dunes. The variability in pH increased with increasing species diversity and also with scale. Overall, soil pH variability decreased with increasing vegetation cover. The lowest pH heterogeneity was found in heath dominated by Empetrum nigrum L. and grey dunes dominated by Campylopus introflexus (Hedw.) Brid. Increasing abundance of dominant species and decreasing species diversity of vegetation apparently reduces soil heterogeneity. Decreasing species diversity of vegetation is likely to explain decreasing variability in soil pH.     

Biome transitions as centres of diversity: habitat heterogeneity and diversity patterns of West African bat assemblages across spatial scales

It is widely accepted that species diversity is contingent upon the spatial scale used to analyze patterns and processes. Recent studies using coarse sampling grains over large extents have contributed much to our understanding of factors driving global diversity patterns. This advance is largely unmatched on the level of local to landscape scales despite being critical for our understanding of functional relationships across spatial scales. In our study on West African bat assemblages we employed a spatially explicit and nested design covering local to regional scales. Specifically, we analyzed diversity patterns in two contrasting, largely undisturbed landscapes, comprising a rainforest area and a forest‐savanna mosaic in Ivory Coast, West Africa. We employed additive partitioning, rarefaction, and species richness estimation to show that bat diversity increased significantly with habitat heterogeneity on the landscape scale through the effects of beta diversity. Within the extent of our study areas, habitat type rather than geographic distance explained assemblage composition across spatial scales. Null models showed structure of functional groups to be partly filtered on local scales through the effects of vegetation density while on the landscape scale both assemblages represented random draws from regional species pools. We present a mixture model that combines the effects of habitat heterogeneity and complexity on species richness along a biome transect, predicting a unimodal rather than a monotonic relationship with environmental variables related to water. The bat assemblages of our study by far exceed previous figures of species richness in Africa, and refute the notion of low species richness of Afrotropical bat assemblages, which appears to be based largely on sampling biases. Biome transitions should receive increased attention in conservation strategies aiming at the maintenance of ecological and evolutionary processes.     

Avian taxonomic and functional diversity in early stage of longleaf pine (Pinus palustris) stands restored at agricultural lands: variations in scale dependency

In agricultural landscapes, the longleaf pine initiative (LLPI) and the Bobwhite Quail Initiative (BQI) aim to restore longleaf pine forests and early successional habitats, respectively. The early stage of longleaf pine stands and grass and forb vegetation produced by a combination of both restoration programs (LLPI‐BQI) may form habitat conditions favorable to early successional bird species and other birds, increasing avian diversity. We investigated how the LLPI and BQI programs affected taxonomic and functional diversity of birds and abundance of early successional birds (grassland and scrub/shrub species), and what environmental characteristics were associated with the diversity and abundance of birds. Our study was performed at 41 fields in Georgia, United States, during 2001–2002 by considering environmental characteristics at two spatial scales: local‐scale vegetation features and restoration program type (LLPI or LLPI‐BQI) and landscape‐scale vegetation features and landscape heterogeneity. Functional evenness, species richness, and abundance of grassland and scrub/shrub species did not show a clear association with local‐ or landscape‐scale variables. Shannon‐Wiener diversity was slightly influenced by restoration program type (local‐scale variable) with higher value at LLPI‐BQI stands than at LLPI stands despite no significant differences in local vegetation features between those stands. Functional divergence was strongly positively associated with landscape‐scale variables. That is, niche differentiation increased with increasing shrub coverage within a landscape, reducing competition between abundant bird species and others. Our results suggest that although a combination of BQI and LLPI program may have a positive effect on avian taxonomic diversity, it is important to consider shrub vegetation cover within a landscape to improve functional diversity.     

Habitat heterogeneity drives the geographical distribution of beta diversity: the case of New Zealand stream invertebrates

To define whether the beta diversity of stream invertebrate communities in New Zealand exhibits geographical variation unexplained by variation in gamma diversity and, if so, what mechanisms (productivity, habitat heterogeneity, dispersal limitation, disturbance) best explain the observed broad‐scale beta diversity patterns. We sampled 120 streams across eight regions (stream catchments), spanning a north–south gradient of 12° of latitude, and calculated beta diversity (with both species richness and abundance data) for each region. We explored through a null model if beta diversity deviates from the expectation of stochastic assembly processes and whether the magnitude of the deviation varies geographically. We then performed multimodel inference analysis on the key environmental drivers of beta diversity, using Akaike's information criterion and model and predictor weights to select the best model(s) explaining beta diversity. Beta diversity was, unexpectedly, highest in the South Island. The null model analysis revealed that beta diversity was greater than expected by chance in all eight regions, but the magnitude of beta deviation was higher in the South Island, suggesting differences in environmental filtering and/or dispersal limitation between North and South Island. Habitat heterogeneity was the predominant driver of beta diversity of stream macroinvertebrates, with productivity having a secondary, and negative, contribution. This is one of the first studies accounting for stochastic effects while examining the ecological drivers of beta diversity. Our results suggest that local environmental heterogeneity may be the strongest determinant of beta diversity of stream invertebrates, more so than regional‐ or landscape‐scale variables.     

Small-scale heterogeneity shapes grassland diversity in low-to-intermediate resource environments

Questions

Soil resource heterogeneity influences the outcome of plant–plant interactions and, consequently, species co-existence and diversity patterns. The magnitude and direction of heterogeneity effects vary widely, and the processes underlying such variations are not fully understood. In this study, we explored how and under what resource conditions small-scale heterogeneity modulates grassland plant diversity.

Location

Oderhänge Mallnow, Potsdam, Brandenburg, Germany.

Methods

We expanded the individual-based plant community model (IBC-grass) to incorporate dynamic below-ground resource maps, simulating spatial heterogeneity of resource availability. Empirical centimeter-scale data of soil C/N ratio were integrated into the model, accounting for both configurational and compositional heterogeneity. We then analyzed the interplay between small-scale heterogeneity and resource availability on the interaction and co-existence of plant species and overall diversity.

Results

Our results showed significant differences between the low- and high-resource scenarios, with both configurational and compositional heterogeneity having a positive effect on species richness and Simpson's diversity, but only under low-resource conditions. As compositional heterogeneity in the fine-scale C/N ratio increased, we observed a positive shift in Simpson's diversity and species richness, with the highest effects at the highest level of variability tested. We observed little to no effect in nutrient-rich scenarios, and a shift to negative effects at the intermediate resource level. The study demonstrates that site-specific resource levels underpin how fine-scale heterogeneity influences plant diversity and species co-existence, and partly explains the divergent effects recorded in different empirical studies.

Conclusions

This study provides mechanistic insights into the complex relationship between resource heterogeneity and diversity patterns. It highlights the context-dependent effects of small-scale heterogeneity, which can be positive under low-resource, neutral under high-resource, and negative under intermediate-resource conditions. These findings provide a foundation for future investigations into small-scale heterogeneity–diversity relationships, contributing to a deeper understanding of the processes that promote species co-existence in plant communities.     

A wavelet‐based approach to evaluate the roles of structural and functional landscape heterogeneity in animal space use at multiple scales

The functional relationship between habitat utilization and landscape spatial heterogeneity is fundamental to understanding the spatial nature of animal distribution across scales. Although structural and functional properties of landscape spatial heterogeneity can have different consequences for animal species, few studies have explicitly considered both forms of heterogeneity, partly due to the lack of general methods for direct assessment of scale‐specific associations between variables. We present a wavelet‐based approach to evaluate the roles of structural and functional landscape spatial heterogeneity in animal space use at multiple spatial scales. As a case study, we examined scale‐specific space use patterns of American black bears Ursus americanus in response to structural and functional spatial heterogeneity as well as spatial patterns of vegetation age‐classes in a Canadian boreal forest. We found strong differences in the effects of structural and functional spatial heterogeneity and the scales at which they are associated with the patterns of habitat use by black bears. Functional heterogeneity alone affected space use at 800 and 1600‐m scales, but had significant effects when interacting with structural heterogeneity at 400, 800, and 1600‐m scales. Compared with male bears, female black bears were most sensitive to patterns of forage abundance at intermediate scales, or more specifically, in young and regenerating forests that provide abundant soft mast in boreal forests. Our study highlights the importance of accounting for scale‐dependent properties of (structural and functional) spatial heterogeneity in assessing the ecological effects of landscape components and the effectiveness of the wavelet transform technique in identifying such scale‐specific relationships.     

Terminology and quantification of environmental heterogeneity in species‐richness research

Spatial environmental heterogeneity (EH) is an important driver of species diversity, and its influence on species richness has been analysed for numerous taxa, in diverse ecological settings, and over a large range of spatial scales. The variety and ambiguity of concepts and terminology, however, have hampered comparisons among studies. Based on a systematic literature survey of 192 studies including 1148 data points, we provide an overview of terms and measures related to EH, and the mechanisms that relate EH to species richness of plants and animals in terrestrial systems. We identify 165 different measures used to quantify EH, referred to by more than 350 measure names. We classify these measures according to their calculation method and subject area, finding that most studies have analysed heterogeneity in land cover, topography, and vegetation, whereas comparatively few studies have focused on climatic or soil EH. Overall, elevation range emerged as the most frequent measure in our dataset. We find that there is no consensus in the literature about terms (such as ‘habitat diversity’ or ‘habitat complexity’), their meanings and associated quantification methods. More than 100 different terms have been used to denote EH, with largely imprecise delimitations. We reveal trends in use of terms and quantification with respect to spatial scales, study taxa, and locations. Finally, we discuss mechanisms involved in EH–richness relationships, differentiating between effects on species coexistence, persistence, and diversification. This review aims at guiding researchers in their selection of heterogeneity measures. At the same time, it shows the need for precise terminology and avoidance of ambiguous synonyms to enhance understanding and foster among‐study comparisons and synthesis.