Metacommunity Size Research Articles

Identification of metacommunities in bioregions with historical habitat networks.

Although metacommunity theory provides many useful insights for conservation planning, the transfer of this knowledge to practice is hampered due to the difficulty of identifying metacommunities in bioregions. This study aims to identify the spatial extent of metacommunities at bioregional scales using current and historical habitat data, especially because contemporary biodiversity patterns may be a result of time-lagged responses to historical habitat configurations. Further, this estimation of the metacommunity spatial extent is based on both the habitat structure and the dispersal ability of the species. Focusing on dragonfly and damselfly (odonate) species in the eastern Swiss Plateau, the research uses wetland habitat information spanning over 110 years to create a time series of nine habitat networks between 1899 and 2010. From these networks, we identified the spatial extents of metacommunities based on the year of habitat information as well as on watershed boundaries. To identify the best metacommunity spatial extents, the study investigates whether patch pairs within a metacommunity exhibit greater similarity in species composition (i.e. lower beta-diversity) than patch pairs between metacommunities. For the different metacommunities, we further investigated correlations between gamma diversity and metacommunity size and compare them to theoretical expectations. In both analyses we found that augmenting spatial metacommunity identification with historical geographical proximity results in stronger associations with biodiversity patterns (beta and gamma diversity) than when using only current-day habitat or watershed information.

Emergent dual scaling of riverine biodiversity

A prevailing paradigm suggests that species richness increases with area in a decelerating way. This ubiquitous power law scaling, the species-area relationship, has formed the foundation of many conservation strategies. In spatially complex ecosystems, however, the area may not be the sole dimension to scale biodiversity patterns because the scale-invariant complexity of fractal ecosystem structure may drive ecological dynamics in space. Here, we use theory and analysis of extensive fish community data from two distinct geographic regions to show that riverine biodiversity follows a robust scaling law along the two orthogonal dimensions of ecosystem size and complexity (i.e., the dual scaling law). In river networks, the recurrent merging of various tributaries forms fractal branching systems, where the prevalence of branching (ecosystem complexity) represents a macroscale control of the ecosystem's habitat heterogeneity. In the meantime, ecosystem size dictates metacommunity size and total habitat diversity, two factors regulating biodiversity in nature. Our theory predicted that, regardless of simulated species' traits, larger and more branched "complex" networks support greater species richness due to increased space and environmental heterogeneity. The relationships were linear on logarithmic axes, indicating power law scaling by ecosystem size and complexity. In support of this theoretical prediction, the power laws have consistently emerged in riverine fish communities across the study regions (Hokkaido Island in Japan and the midwestern United States) despite hosting different fauna with distinct evolutionary histories. The emergence of dual scaling law may be a pervasive property of branching networks with important implications for biodiversity conservation.

The environment drives microbial trait variability in aquatic habitats.

A prerequisite to improve the predictability of microbial community dynamics is to understand the mechanisms of microbial assembly. To study factors that contribute to microbial community assembly, we examined the temporal dynamics of genes in five aquatic metagenome time-series, originating from marine offshore or coastal sites and one lake. With this trait-based approach we expected to find gene-specific patterns of temporal allele variability that depended on the seasonal metacommunity size of carrier-taxa and the variability of the milieu and the substrates to which the resulting proteins were exposed. In more detail, we hypothesized that a larger seasonal metacommunity size would result in increased temporal variability of functional units (i.e., gene alleles), as shown previously for taxonomic units. We further hypothesized that multicopy genes would feature higher temporal variability than single-copy genes, as gene multiplication can result from high variability in substrate quality and quantity. Finally, we hypothesized that direct exposure of proteins to the extracellular environment would result in increased temporal variability of the respective gene compared to intracellular proteins that are less exposed to environmental fluctuations. The first two hypotheses were confirmed in all data sets, while significant effects of the subcellular location of gene products was only seen in three of the five time-series. The gene with the highest allele variability throughout all data sets was an iron transporter, also representing a target for phage infection. Previous work has emphasized the role of phage-prokaryote interactions as a major driver of microbial diversity. Our finding therefore points to a potentially important role of iron transporter-mediated phage infections for the assembly and maintenance of diversity in aquatic prokaryotes.

A simulation‐based approach to understand how metacommunity characteristics influence emergent biodiversity patterns

To understand controls over biodiversity, it is necessary to take a multi‐scale approach to understand how local and regional factors affect the community assembly processes that drive emergent patterns. This need is reflected in the growing use of the metacommunity concept to interpret multi‐scale measures of biodiversity, including metrics derived from diversity partitioning (e.g. α, β and γ diversity) and variation partitioning (e.g. spatial and environmental components of compositional turnover) techniques. However, studies have shown limited success using these metrics to characterize underlying community assembly dynamics. Here we demonstrate how a metacommunity simulation package (MCSim) can be used to evaluate when and how biodiversity metrics can be used to make inferences about metacommunity characteristics. We examined a wide range of parameter settings representing ecologically relevant scenarios. We used artificial neural networks (ANNs) to assess the sensitivity of diversity and variation partitioning metrics (calculated from simulation outcomes) to metacommunity parameter settings. In the scenarios examined in this study, the niche‐neutral gradient strongly influenced most biodiversity metrics, metacommunity size exhibited a marginal influence over some metrics, and dispersal dynamics only affected a subset of variation partitioning outcomes. Variation partitioning response curves along the niche‐neutral gradient were not monotonic; however, simulation outcomes suggest other biodiversity metrics (e.g. dissimilarity saturation) can be used in combination with variation partitioning metrics to make inferences about metacommunity properties. With the growing availability of archived ecological data, we expect future work will apply simulation‐based techniques to better understand links between biodiversity and the metacommunity characteristics that are presumed to control the underlying community assembly processes.

Community assembly is a race between immigration and adaptation: eco‐evolutionary interactions across spatial scales

Both ecological and evolutionary mechanisms have been proposed to describe how natural communities become assembled at both regional and biogeographical scales. Yet, these theories have largely been developed in isolation. Here, we unite these separate views and develop an integrated eco‐evolutionary framework of community assembly. We use a simulation approach to explore the factors determining the interplay between ecological and evolutionary mechanisms systematically across spatial scales. Our results suggest that the same set of ecological and evolutionary processes can determine community assembly at both regional and biogeographical scales. We find that the importance of evolution and community monopolization effects, defined as the eco‐evolutionary dynamics that occur when local adaptation of early established immigrants is fast enough to prevent the later immigration of better pre‐adapted species, are not restricted to adaptive radiations on remote islands. They occur at dispersal rates of up to ten individuals per generation, typical for many species at the scale of regional metacommunities. Dispersal capacity largely determines whether ecological species sorting or evolutionary monopolization structure metacommunity diversity and distribution patterns. However, other factors related to the spatial scale at which community assembly processes are acting, such as metacommunity size and the proportion of empty patches, also affect the relative importance of ecology versus evolution. We show that evolution often determines community assembly, and this conclusion is robust to a wide range of assumptions about spatial scale, mode of reproduction, and environmental structure. Moreover, we found that community monopolization effects occur even though species fully pre‐adapted to each habitat are abundant in the metacommunity, a scenario expected a priori to prevent any meaningful effect of evolution. Our results strongly support the idea that the same eco‐evolutionary processes underlie community assembly at regional and biogeographical scales.

Phylogenies support out-of-equilibrium models of biodiversity.

There is a long tradition in ecology of studying models of biodiversity at equilibrium. These models, including the influential Neutral Theory of Biodiversity, have been successful at predicting major macroecological patterns, such as species abundance distributions. But they have failed to predict macroevolutionary patterns, such as those captured in phylogenetic trees. Here, we develop a model of biodiversity in which all individuals have identical demographic rates, metacommunity size is allowed to vary stochastically according to population dynamics, and speciation arises naturally from the accumulation of point mutations. We show that this model generates phylogenies matching those observed in nature if the metacommunity is out of equilibrium. We develop a likelihood inference framework that allows fitting our model to empirical phylogenies, and apply this framework to various mammalian families. Our results corroborate the hypothesis that biodiversity dynamics are out of equilibrium.

Metacommunity size influences aquatic community composition in a natural mesocosm landscape

Ecosystems are often arranged in naturally patchy landscapes with habitat patches linked by dispersal of species in a metacommunity. The size of a metacommunity, or number of patches, is predicted to influence community dynamics and therefore the structure and function of local communities. However, such predictions have yet to be experimentally tested using full food webs in natural metacommunities. We used the natural mesocosm system of aquatic macroinvertebrates in bromeliad phytotelmata to test the effect of the number of patches in a metacommunity on species richness, abundance, and community composition. We created metacommunities of varying size using fine mesh cages to enclose a gradient from a single bromeliad up to the full forest. We found that species richness, abundance, and biomass increased from enclosed metacommunities to the full forest size and that diversity and evenness also increased in larger enclosures. Community composition was affected by metacommunity size across the full gradient, with a more even detritivore community in larger metacommunities, and taxonomic groups such as mosquitoes going locally extinct in smaller metacommunities. We were able to divide the effects of metacommunity size into aquatic and terrestrial habitat components and found that the importance of each varied by species; those with simple life cycles were only affected by local aquatic habitat whereas insects with complex life cycles were also affected by the amount of terrestrial matrix. This differential survival of obligate and non‐obligate dispersers allowed us to partition the beta‐diversity between metacommunities among functional groups. Our study is one of the first tests of metacommunity size in a natural metacommunity landscape and shows that both diversity and community composition are significantly affected by metacommunity size.SynthesisNatural food webs are sensitive to meta‐community size, i.e. the number of patches connected through dispersal. We provide an empirical test using the aquatic foodweb associated within bromeliads as a model system. When we reduced the number of bromeliad patches connect through dispersal, we found a clear change of the foodweb in terms of population sizes, beta diversity, community composition and predator‐prey ratios. The response of individual taxa was predictable based on species traits including dispersal modes, life cycle, and adult resource requirements. Our study demonstrates that community structure is strongly influenced by the interplay of species traits and landscape properties.

Use of Multispecies Occupancy Models to Evaluate the Response of Bird Communities to Forest Degradation Associated with Logging

Forest degradation is arguably the greatest threat to biodiversity, ecosystem services, and rural livelihoods. Therefore, increasing understanding of how organisms respond to degradation is essential for management and conservation planning. We were motivated by the need for rapid and practical analytical tools to assess the influence of management and degradation on biodiversity and system state in areas subject to rapid environmental change. We compared bird community composition and size in managed (ejido, i.e., communally owned lands) and unmanaged (national park) forests in the Sierra Tarahumara region, Mexico, using multispecies occupancy models and data from a 2-year breeding bird survey. Unmanaged sites had on average higher species occupancy and richness than managed sites. Most species were present in low numbers as indicated by lower values of detection and occupancy associated with logging-induced degradation. Less than 10% of species had occupancy probabilities >0.5, and degradation had no positive effects on occupancy. The estimated metacommunity size of 125 exceeded previous estimates for the region, and sites with mature trees and uneven-aged forest stand characteristics contained the highest species richness. Higher estimation uncertainty and decreases in richness and occupancy for all species, including habitat generalists, were associated with degraded young, even-aged stands. Our findings show that multispecies occupancy methods provide tractable measures of biodiversity and system state and valuable decision support for landholders and managers. These techniques can be used to rapidly address gaps in biodiversity information, threats to biodiversity, and vulnerabilities of species of interest on a landscape level, even in degraded or fast-changing environments. Moreover, such tools may be particularly relevant in the assessment of species richness and distribution in a wide array of habitats.

Life history affects how species experience succession in pen shell metacommunities

In nature, very few species are common and broadly distributed. Most species are rare and occupy few sites; this pattern is ubiquitous across habitats and taxa. In spatially structured communities (metacommunities), regional distribution and local abundance may change as the relative effects of within-habitat processes (e.g., species interactions) and among-habitat processes (e.g., dispersal) may vary through succession. A field experiment with the marine benthic inhabitants of pen shells (Atrina rigida) tested how common and rare species respond to succession and metacommunity size. I followed community development through time and partitioned species into sessile and motile based on their natural history. Rare species drive diversity patterns and are influenced by metacommunity size: there are strong abundance-distribution differences between common and rare species in large metacommunities, but motile species show lower rates of change than sessile species. In small metacommunities both common and rare species have similar changes through time; the dichotomous distinction of common and rare species is not present. Edge effects in metacommunities affect species' changes in distribution and abundance. In large metacommunities diversity is higher in edge habitats relative to small metacommunities during early succession. However, edge effects benefit motile species over time in small metacommunities showing a rapid increase in diversity. Individual mobility is sensitive to regional community size and allows individuals to sort among different communities. In contrast, sessile species do not show this edge effect. Metacommunity theory is a useful framework for understanding spatially structured communities, but the natural history of coexisting species cannot be ignored.

Relaxation Time and the Problem of the Pleistocene

Although changes in habitat area, driven by changes in sea level, have long been considered as a possible cause of marine diversity change in the Phanerozoic, the lack of Pleistocene extinction in the Californian Province has raised doubts, given the large and rapid sea-level changes during the Pleistocene. Neutral models of metacommunities presented here suggest that diversity responds rapidly to changes in habitat area, with relaxation times of a few hundred to a few thousand years. Relaxation time is controlled partly by metacommunity size, implying that different provinces or trophic levels might have measurably different responses to changes in habitable area. Geologically short relaxation times imply that metacommunities should be able to stay nearly in equilibrium with all but the most rapid changes in area. A simulation of the Californian Province during the Pleistocene confirms this, with the longest lags in diversity approaching 20 kyr. The apparent lack of Pleistocene extinction in the Californian Province likely results from the difficulty of sampling rare species, coupled with repopulation from adjacent deep-water or warm-water regions.

Community differentiation on landscapes: drift, migration and speciation

Theories of the differentiation of ecological communities on landscapes have typically not considered evolutionary dynamics. Here we analytically study the expected differentiation among local communities in a large metacommunity, undergoing speciation, ecological drift and intercommunity dispersal, in the context of neutral theory. We demonstrate that heterogeneity in species diversity and abundance arises among communities when local communities are small and intercommunity migration is infrequent. We propose a new measure to describe community differentiation, defined as the average correlation or the average probability (Cst) that two randomly sampled individuals of the same species within local communities are from the same ancestor. The effects of driving forces (migration, mutation, and ecological drift) are incorporated into the two‐level hierarchical community structure in a finite island model of neutral communities. Community differentiation can increase the effective metacommunity size or the Hubbell's fundamental species diversity in the metacommunity by a factor (1−Cst)−1. Significant community differentiation arises when Cst≠0. Intercommunity migration promotes species diversity in local communities but reduce species diversity in the metacommunity. In either the finite or infinite island case, one can estimate the number of intercommunity migrants by using multiple local community datasets when the speciation is negligible in the neutral local communities, or by using the metacommunity dataset when the speciation is included in the local neutral communities. These results highlight the significance of the evolutionary mechanisms in generating heterogeneous communities in the absence of complicated ecological processes on large landscapes.

Dispersal, edaphic fidelity and speciation in species‐rich Western Australian shrublands: evaluating a neutral model of biodiversity

Over evolutionary time, the number of species in a community reflects the balance between the rate of speciation and the rate of extinction. Over shorter time‐scales local species richness is also affected by how often species move into and out of the local community. These processes are at the heart of Hubbell's ‘unified neutral theory of biodiversity’ (Hubbell 2001). Hubbell's spatially implicit, dispersal‐limited neutral model is the most widely used of the many implementations of neutral theory and it provides an estimate of the rate of speciation in a metacommunity (if metacommunity size is known) and the rate at which species migrate into the local community from the wider metacommunity. Recently, this neutral model has been used to compare rates of speciation and migration in the species‐rich fynbos of South Africa and in neotropical forests. Here we use new analytical methods for estimating the neutral model's parameters to infer speciation and dispersal rates for three sites in species‐rich sclerophyll shrublands (equivalent to fynbos) in Western Australia (WA). Our estimates suggest that WA shrublands are intermediate between fynbos and tropical rainforest in terms of speciation and dispersal. Although a weak test, the model predicts species abundance distributions and species accumulation curves similar to those observed at the three sites. The neutral model's predictions also remain plausible when confronted with independent data describing: (1) known edaphic relationships between sites, (2) estimates of metacommunity species richness and (3) rates of speciation among resprouters and nonsprouters. Two of the site pairs, however, show species turnovers significantly different from those predicted by the spatially implicit form of the neutral model that we use. This suggests that non‐neutral processes, in this case probably edaphic specialisation, are important in the WA shrubland metacommunity. The neutral model predicts similar rates of speciation in resprouter and sprouter taxa, a finding supported by recent molecular phylogenies. Finally, when converted into temporally scaled speciation rates and species longevities, the estimates produced by the neutral model seem implausible. The apparent departure from neutrality in the turnover of species between some sites and the implausible temporal dynamics may be due to the particular model chosen and does not reduce the significance of our other results, which confirm that local dispersal limitation, coupled with broader scale edaphic fidelity, combine to structure this biodiverse metacommunity.

Habitat destruction and metacommunity size in pen shell communities

1. In spatially structured communities, habitat destruction can have two effects: first, a main effect that occurs because of the loss of habitat area within a larger region, and a secondary effect due to changes in the spatial arrangement of local communities. Changes to the spatial arrangement can, in turn, affect the migration and extinction rates within local communities. 2. Our study involved the experimental destruction of entire local communities within larger regions in natural marine microcosms. Large and small arrays of dead pen shells were created in a shallow bay in north Florida, and the colonization by both encrusting and motile species on this empty substrate were followed through time. After most species had become established, half of the large arrays were perturbed to create small arrays by removal of half the shells, simulating habitat destruction. 3. After 48 days of further community development, comparisons of the large arrays, reduced arrays and original small arrays suggested that the mechanisms by which habitat destruction affects diversity could depend upon the size of the region affected and the natural history of the species being studied. 4. Habitat destruction reduced the diversity of motile species to a level lower than that found in the undisturbed small arrays, suggesting that the species that assembled in the original large metacommunities negatively influenced the species that occurred ultimately in the converted small arrays. 5. With sessile species, habitat destruction created richness levels that were intermediate to those of small and large arrays. The initial predestruction richness appears to have had a positive effect; because sessile species cannot disperse as adults, they may not respond to significant shifts in metacommunity size later in succession. Initial metacommunity size may be important for allowing individuals to select appropriate habitats before they settle.

Species diversity in neutral metacommunities: a network approach

Biologists seek an understanding of the processes underlying spatial biodiversity patterns. Neutral theory links those patterns to dispersal, speciation and community drift. Here, we advance the spatially explicit neutral model by representing the metacommunity as a network of smaller communities. Analytic theory is presented for a set of equilibrium diversity patterns in networks of communities, facilitating the exploration of parameter space not accessible by simulation. We use this theory to evaluate how the basic properties of a metacommunity - connectivity, size, and speciation rate - determine overall metacommunity gamma-diversity, and how that is partitioned into alpha- and beta-components. We find spatial structure can increase gamma-diversity relative to a well-mixed model, even when theta is held constant. The magnitude of deviations from the well-mixed model and the partitioning into alpha- and beta-diversity is related to the ratio of migration and speciation rates. gamma-diversity scales linearly with metacommunity size even as alpha- and beta-diversity scale nonlinearly with size.

A dispersal‐limited sampling theory for species and alleles

The importance of dispersal for biodiversity has long been recognized. However, it was never advertised as vigorously as Stephen Hubbell did in the context of his neutral community theory. After his book appeared in 2001, several scientists have sought and found analytical expressions for the effect of dispersal limitation on community composition, still in the neutral context. This has been done along two relatively independent lines of research that have a different mathematical approach and focus on different, yet related, types of results. Here, we study both types in a new framework that makes use of the sampling nature of the theory. We present sampling distributions that contain binomial or hypergeometric sampling on the one hand, and dispersal limitation on the other, and thus views dispersal limitation as ubiquitous as sampling effects. Further, we express the results of one line of research in terms of the other and vice versa, using the concept of subsamples. A consequence of our findings is that metacommunity size does not independently affect the outcome of neutral models in contrast to a previous assertion (Ecol. Lett., 7, 2004, p. 904) based on an incorrect formula (Phys. Rev. E, 68, 2003, p. 061902, eqns 11-14). Our framework provides the basis for development of a dispersal-limited non-neutral community theory and applies in population genetics as well, where alleles and mutation play the roles of species and speciation respectively.

Persistence and Area Effects in a Stochastic Tritrophic Model

Previous articleNext article No AccessPersistence and Area Effects in a Stochastic Tritrophic ModelH. B. Wilson, M. P. Hassell, and R. D. HoltH. B. WilsonDepartment of Biology and NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom Search for more articles by this author , M. P. HassellDepartment of Biology and NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom Search for more articles by this author , and R. D. HoltMuseum of Natural History, Department of Systematics and Ecology, University of Kansas, Lawrence, Kansas 66045 Search for more articles by this author Department of Biology and NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, United KingdomMuseum of Natural History, Department of Systematics and Ecology, University of Kansas, Lawrence, Kansas 66045PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 151, Number 6June 1998 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/286144 Views: 20Total views on this site Citations: 15Citations are reported from Crossref HistoryReceived June 13, 1997Accepted December 16, 1997 Keywordsdemographic stochasticitytritrophic communitiesarea effectsmetapopulations© 1998 by The University of Chicago.PDF download Crossref reports the following articles citing this article: Theoretical Advances in Species–Area Relationship Research, (Mar 2021): 155–318.https://doi.org/10.1017/9781108569422.011Robert D. Holt, Dominique Gravel, Adrian Stier, James Rosindell On the Interface of Food Webs and Spatial Ecology: The Trophic Dimension of Species–Area Relationships, (Mar 2021): 289–318.https://doi.org/10.1017/9781108569422.017Danyhelton D. F. Dantas, Adriano Caliman, Rafael D. Guariento, Ronaldo Angelini, Luciana S. Carneiro, Sergio M. Q. Lima, Pablo A. Martinez, José L. Attayde Climate effects on fish body size–trophic position relationship depend on ecosystem type, Ecography 42, no.99 (Jun 2019): 1579–1586.https://doi.org/10.1111/ecog.04307Coline C. Jaworski, Christophe Thébaud, Jérôme Chave, Caroline Brophy Dynamics and persistence in a metacommunity centred on the plant Antirrhinum majus : theoretical predictions and an empirical test, Journal of Ecology 104, no.22 (Jan 2016): 456–468.https://doi.org/10.1111/1365-2745.12515Kevin L. S. Drury, Jesse D. Suter, Jacob B. Rendall, Andrew M. Kramer, John M. Drake Immigration can destabilize tri-trophic interactions: implications for conservation of top predators, Theoretical Ecology 8, no.33 (Jan 2015): 285–296.https://doi.org/10.1007/s12080-014-0249-1Robin M. LeCraw, Pavel Kratina, Diane S. Srivastava Food web complexity and stability across habitat connectivity gradients, Oecologia 176, no.44 (Sep 2014): 903–915.https://doi.org/10.1007/s00442-014-3083-7Robin M. LeCraw, Diane S. Srivastava, Gustavo Q. Romero Metacommunity size influences aquatic community composition in a natural mesocosm landscape, Oikos 123, no.88 (Apr 2014): 903–911.https://doi.org/10.1111/oik.01253Gaku Takimoto, David M. Post Environmental determinants of food-chain length: a meta-analysis, Ecological Research 28, no.55 (Apr 2012): 675–681.https://doi.org/10.1007/s11284-012-0943-7Gaku Takimoto, David M. Post, David A. Spiller, Robert D. Holt Effects of productivity, disturbance, and ecosystem size on food-chain length: insights from a metacommunity model of intraguild predation, Ecological Research 27, no.33 (Feb 2012): 481–493.https://doi.org/10.1007/s11284-012-0929-5Daniela O. Maionchi, S.F. dos Reis, M.A.M. de Aguiar Chaos and pattern formation in a spatial tritrophic food chain, Ecological Modelling 191, no.22 (Jan 2006): 291–303.https://doi.org/10.1016/j.ecolmodel.2005.04.028 Manojit Roy , Robert D. Holt , and Michael Barfield Temporal Autocorrelation Can Enhance the Persistence and Abundance of Metapopulations Comprised of Coupled Sinks. M. Roy et al., The American Naturalist 166, no.22 (Jul 2015): 246–261.https://doi.org/10.1086/431286R. D. Holt, D. M. Debinski Reflections on Landscape Experiments and Ecological Theory: Tools for the Study of Habitat Fragmentation, (Jan 2003): 201–223.https://doi.org/10.1007/978-3-662-05238-9_12Robert D. Holt Food webs in space: On the interplay of dynamic instability and spatial processes, Ecological Research 17, no.22 (May 2002): 261–273.https://doi.org/10.1046/j.1440-1703.2002.00485.xM. P. Hassell Host-parasitoid population dynamics*, Journal of Animal Ecology 69, no.44 (Jul 2000): 543–566.https://doi.org/10.1046/j.1365-2656.2000.00445.xRobert D. Holt, John H. Lawton, Gary A. Polis, Neo D. Martinez TROPHIC RANK AND THE SPECIES–AREA RELATIONSHIP, Ecology 80, no.55 (Jul 1999): 1495–1504.https://doi.org/10.1890/0012-9658(1999)080[1495:TRATSA]2.0.CO;2