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Habitat fragmentation and its lasting impact on Earth’s ecosystems

Habitat fragmentation and its lasting impact on Earth’s ecosystems RESEARCH ARTICLE 2015 © The Authors, some rights reserved; APPLIED ECOLOGY exclusive licensee American Association for the Advancement of Science. Distributed Habitat fragmentation and its lasting impact under a Creative Commons Attribution License 4.0 (CC BY). on Earth’s ecosystems 10.1126/sciadv.1500052 1 2 3 4 5 Nick M. Haddad, *LarsA. Brudvig, Jean Clobert, Kendi F. Davies, Andrew Gonzalez, 6 7 8 9 10 Robert D. Holt, Thomas E. Lovejoy, Joseph O. Sexton, Mike P. Austin, Cathy D. Collins, 11 12 13 14 15 William M. Cook, Ellen I. Damschen, Robert M. Ewers, Bryan L. Foster, Clinton N. Jenkins, 9 16 17 18,19 Andrew J. King, William F. Laurance, Douglas J. Levey, Chris R. Margules, 4 9,20 12 8 8 Brett A. Melbourne, A. O. Nicholls, John L. Orrock, Dan-Xia Song, John R. Townshend We conducted an analysis of global forest cover to reveal that 70% of remaining forest is within 1 km of the forest’s edge, subject to the degrading effects of fragmentation. A synthesis of fragmentation experiments spanning multiple biomes and scales, five continents, and 35 yearsdemonstratesthathabitat fragmentation reduces bio- diversity by 13 to 75% and impairs key ecosystem functions by decreasing biomass and altering nutrient cycles. Effects are greatest in the smallest and most isolated fragments, and they magnify with the passage of time. These findings indicate an urgent need for conservation and restoration measures to improve landscape connectivity, which will reduce extinction rates and help maintain ecosystem services. INTRODUCTION fragment size and increased isolation relative to the widespread and Destruction and degradation of natural ecosystems are the primary pervasive effects of habitat loss in explaining declines in biodiversity causes of declines in global biodiversity (1, 2). Habitat destruction typ- and the degradation of ecosystems (7). Observational studies of the ically leads to fragmentation, the division of habitat into smaller and effects of fragmentation have often magnified the controversy because more isolated fragments separated by a matrix of human-transformed inference from nonmanipulative studies is limited to correlation and land cover. The loss of area, increase in isolation, and greater exposure because they have individually often considered only single aspects of to human land uses along fragment edges initiate long-term changes fragmentation (for example, edge, isolation, and area) (8). However, to the structure and function of the remaining fragments (3). together with these correlative observations, experimental studies re- Ecologists agree that habitat destruction is detrimental to the main- veal that fragmentation has multiple simultaneous effects that are in- tenance of biodiversity, but they disagree—often strongly—on the ex- terwoven in complex ways and that operate over potentially long time tent to which fragmentation itself is to blame (4, 5). Early hypotheses scales (9). based on the biogeography of oceanic islands (6) provided a theoret- Here, we draw on findings of the world’s largest and longest- ical framework to understand fragmentation’s effect on extinction in running fragmentation experiments that span 35 years and disparate terrestrial landscapes composed of “islands” of natural habitat scat- biomes on five continents. Their rigorous designs and long-term im- tered across a “sea” of human-transformed habitat. Central to the con- plementation overcome many limitations of observational studies. In troversy has been a lingering uncertainty about the role of decreased particular, by manipulating and isolating individual aspects of frag- mentation while controlling for others, and by doing so on entire 1 ecosystems, they provide a powerful way to disentangle cause and Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA. effect in fragmented landscapes. Here, we present experimental evi- Department of Plant Biology, Michigan State University, East Lansing, MI 48824–1312, USA. Station d’Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis, 09200 Saint-Girons, dence of unexpected long-term ecological changes caused by habitat France. Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, fragmentation. Boulder, CO 80309, USA. Department of Biology, McGill University, Montreal, Quebec H3A Highlighting one ecosystem type as an example, we first present a 1B1, Canada. Department of Biology, University of Florida, Gainesville, FL 32611, USA. Department of Environmental Science and Policy, George Mason University, Fairfax, VA global analysis of the fragmentation of forest ecosystems, quantifying 22030, USA. Global Land Cover Facility, Department of Geographical Sciences, University of for the first time the global hotspots of intensive historical fragmenta- Maryland, College Park, MD 20702, USA. CSIRO Land and Water Flagship, GPO Box 1700, 10 tion. We then synthesize results from the set of long-term experiments Canberra, Australian Capital Territory 2601, Australia. Department of Biology, Colby conducted in a wide variety of ecosystems to demonstrate consistent College, 5746 Mayflower Hill, Waterville, ME 04901, USA. Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA. Department of Zoology, impacts of fragmentation, how those impacts change over time, and University of Wisconsin, Madison, WI 53706, USA. Department of Life Sciences, Imperial how they align with predictions from theory and observation. Finally, College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK. we identify key knowledge gaps for the next generation of fragmenta- Department of Ecology and Evolutionary Biology and Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047–3759, USA. Instituto de Pesquisas tion experiments. Ecológicas, Rod. Dom Pedro I, km 47, Caixa Postal 47, Nazaré Paulista, São Paulo 12960-000, Brazil. Centre for Tropical Environmental and Sustainability Science and College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland 4878, Australia. 17 18 GLOBAL ANALYSIS OF THE EXTREME MAGNITUDE AND National Science Foundation, Arlington, VA 22230, USA. Centre for Tropical Environmental and Sustainability Science, School of Earth and Environmental Sciences, EXTENT OF FRAGMENTATION James Cook University, Cairns 4878, Australia. Research Center for Climate Change, University of Indonesia, Kota Depok, Java Barat 16424, Indonesia. The Institute for Land, New satellite data sets reveal at high resolution how human activities Water and Society, Charles Sturt University, Thurgoona Campus, Albury, New South Wales are transforming global ecosystems. Foremost among these observations 2640, Australia. *Corresponding author. E-mail: nick_haddad@ncsu.edu are those of forest cover because of the high contrast between forest Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 1of9 RESEARCH ARTICLE and anthropogenic land cover types. Deforestation, which was already Historical data enable the study of the process of forest fragmen- widespread in temperate regions in the mid-18th to 20th centuries tation over time. We reconstructed the historical forest extent and and increased in the tropics over the past half century, has resulted timing of fragmentation in two forested regions of Brazil that provide in the loss of more than a third of all forest cover worldwide (10, 11). a stark contrast in land-use dynamics. The Brazilian Amazon is a Beyond the direct impacts of forest loss and expanding anthropogenic rapidly changing frontier (10), yet most of its forests remain con- land cover(forexample,agricultural fields and urban areas), remnant tiguous and far from an edge despite recent increases in fragmen- forests are likely to suffer from being smaller, more isolated, and with tation (Fig. 1, C and D). In contrast, the Brazilian Atlantic Forest is a greater area located near the edge of the forest (12). a largely deforested landscape, cleared for agriculture and logged We analyzed the world’s first high-resolution map of global tree for timber over the last three centuries (11). This remaining forest cover (13) to measure the magnitude of forest fragmentation. This is dominated by small fragments, with most fragments smaller than analysis revealed that nearly 20% of the world’s remaining forest is 1000 ha and within 1000 m of a forest edge (Fig. 1, E and F) (16). In within 100mof an edge (Fig.1,AandB)—in close proximity to agricul- the Brazilian Amazon, the proportion of forest farther than 1 km from tural, urban, or other modified environments where impacts on forest the forest edge has decreased from 90% (historical) to 75% (today), ecosystems are most severe (14). More than 70% of the world’sforests and in the Brazilian Atlantic, from 90% to less than 9%. are within 1 km of a forest edge. Thus, most forests are well within the These two forested regions of Brazil define extremes of the frag- range where human activities, altered microclimate, and nonforest mentation process and are representative of the extent of fragmenta- species may influence and degrade forest ecosystems (15). The largest tion in forested landscapes worldwide (Fig. 1), as well as many other contiguous expanses of remaining forests are in the humid tropical re- biomes including temperate grasslands, savannas, and even aquatic gions of the Amazon and Congo River Basins (Fig. 1A). Large areas of systems (17). For example, although a spatial analysis similar to that more disjunct forest also remain in southeastern Asia, New Guinea, of forest is not currently possible in grasslands, 37% of the world’s and the boreal biomes. grassland eco-regions are classified as “highly fragmented” (18, 19). Fig. 1. The global magnitude of forest frag- mentation. (A) Mean distance to forest edge for forested pixels within each 1-km cell. Lines point to locations of ongoing fragmentation exper- iments identified and described in Fig. 2. (B) Proportion of the world’sforestat eachdistance to the forest edge and the cumulative propor- tion across increasing distance categories (green line). (C and E)Inthe BrazilianAmazon(C) and Atlantic Forests (E), the proportion of forest area at each distance to forest edge for both the cur- rent and estimated historic extent of forest. (D and F)Inthe BrazilianAmazon(D) andAtlantic Forests (F), the number of fragments and the total area of fragments of that size. The total number of fragments in the smallest bin (1 to 10 ha) is an underestimate in both the Atlantic Forest and Amazon data sets because not all of the very smallest fragments are mapped. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 2of9 RESEARCH ARTICLE Robust knowledge of how habitat fragmentation affects biodiversity occur in several biomes (Fig. 2 and Supplementary Materials) and and ecosystem processes is needed if we are to comprehend adequately were designed to manipulate specific components of fragmentation— the implications of this global environmental change. habitat size, isolation, and connectivity—while controlling for confounding factors such as the amount of habitat lost across a landscape (Fig. 2). The largest fragments across these experiments match the size of frag- ments commonly created by anthropogenic activities (Figs. 1 and 2). THE VALUE OF LONG-TERM FRAGMENTATION EXPERIMENTS Distances to the edge of experimental fragments range to 500 m, en- Long-term experiments are a powerful tool for understanding the ec- compassing edge distances found in more than half of forests world- ological consequences of fragmentation (20). Whereas observational wide (Fig. 1B). In each experiment, different fragmentation treatments studies of fragmented landscapes have yielded important insights with replication were established, starting from continuous, nonfrag- (9, 21), they typically lack rigorous controls, replication, randomiza- mented landscapes and controlling for background environmental tion, or baseline data. Observational studies have limited ability variation either by experimental design (blocking) or by measurement to isolate the effects of fragmentation from concomitant habitat loss of covariates for use in subsequent analyses. Tests were conducted within and degradation per se (4, 7, 22). Remnant fragments are embedded in fragments that varied experimentally in area or edge, within fragments different types and qualities of surrounding habitat, complicating in- that were experimentally isolated or connected, or within experimental terpretation because the surrounding habitat also influences bio- fragments compared to the same area within continuous habitat. All diversity and ecosystem productivity (23). treatments were replicated. Experiments were created by destroying or The long-term fragmentation experiments we analyze here com- creating precise amounts of habitat across replicate landscapes, allow- prise the entire set of ongoing terrestrial long-term experiments. They ing tests of fragmentation effects independent of habitat loss. The robust Fig. 2. The world’s ongoing fragmentation experiments. All experi- ades). The variables under study in each experiment are checked. The area ments have been running continuously since the time indicated by the is that of the experiment’s largest fragments. Icons under “Fragment” and start of the associated arrow (with the exception of the moss fragmenta- “Matrix” indicate the dominant community and its relative height, with tion experiment, which represents a series of studies over nearly two dec- multiple trees representing succession. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 3of9 RESEARCH ARTICLE and comparable experimental designs allow for powerful tests of the We synthesized results available 31 January 2014 for all studies mechanisms underpinning the ecological impacts of fragmentation, and within these experiments that were conducted in all treatments and the long-term nature of ensuing studies has revealed consistent emer- replicates, and tested fragmentation effects on dispersal, abundance, gent effects. extinction, species richness, community composition, and ecosystem These experiments mimic anthropogenic fragmentation; they are functioning. We first calculated effect sizes of fragmentation as log re- whole-ecosystem manipulations in which all species and processes sponse ratios (Fig. 3). Data from 76 different studies across the five experienced the same treatment (24). Emergent responses thus reflect longest-running experiments were drawn from published and un- the multiple direct and indirect effects of interacting species and published sources (table S1). We synthesized results according to three processes. Further, because experimentally fragmented ecosystems fragmentation treatments: reduced fragment area [the focus of Biolog- are open to fluxes of individuals and resources, fragmentation ical Dynamics of Forest Fragments Project (BDFFP), Wog Wog, and effects can manifest across multiple levels of ecological organization Kansas; see Fig. 2 for identifiers of experiments], increased fragment (Fig. 3). Long-term experiments have the power to detect lagged and/ isolation [Savannah River Site (SRS) and Moss], and increased propor- or chronic impacts. tion of edge (all experiments). Fragmented treatments were compared The first fragmentation experiments, now more than three decades directly to non- or less-fragmented habitats that were either larger or old, were created to test effects of fragment area on both species connected via structural corridors (table S1). persistence and patterns of immigration, reflecting concern in con- servation biology about the role of fragmentation in reducing pop- Strong, consistent, and accumulating effects ulation sizes below viable levels (25) (Fig. 2). Subsequent experiments, of habitat fragmentation created two decades ago, shifted focus to modifying habitat isolation, Our synthesis revealed strong and consistent responses of organisms reflecting recognition of the potential to mitigate negative effects of frag- and ecosystem processes to fragmentation arising from decreased mentation by recreating habitat—specifically with corridors—to increase fragment area, increased isolation, and the creation of habitat edges connectivity among fragments (26) (Fig. 2). The newest experiments test (Fig. 3). emerging questions about potentially deleterious synergies between Community and ecosystem responses emerge from observed re- fragmentation and global changes in climate and land use (Fig. 2). sponses at the level of populations. Reduced area decreased animal Fig. 3. Fragmentation effects propagate through the whole eco- ratio: ln(mean in more fragmented treatment/meaninnon-orless-fragmented system. (A to C) For each fragmentation treatment [reduced area in treatment)] for an ecological process. Effect sizes are statistical, such that BDFFP, Wog Wog, Kansas (A); increased isolation in SRS and Moss (B); negative or positive values could represent degrading function. Horizon- and increased edge in all experiments (C)], we summarize major find- tal bars are the range when a dot is represented by more than one study. ings for ecological processes at all levels of ecological organization. Details, including individual effect sizes for each study, are reported in Each dot represents the mean effect size [computed as log response table S1. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 4of9 RESEARCH ARTICLE residency within fragments, and increased isolation reduced move- ment among fragments, thus reducing fragment recolonization after local extinction (Fig. 3, A and B). Reduced fragment area and increased fragment isolation generally reduced abundance of birds, mammals, insects, and plants (Fig. 3, A and B). This overall pattern emerged de- spite complex patterns of increases or declines in abundance of indi- vidual species (Fig. 3A) with various proximate causes such as release from competition or predation, shifts in disturbance regimes, or alter- ation of abiotic factors (14, 27–29). Reduced area, increased isolation, and increased proportion of edge habitat reduced seed predation and herbivory, whereas increased proportion of edge caused higher fledgling predation that had the effect of reducing bird fecundity (represented together as trophic dynamics in Fig. 3, A to C). Perhaps because of reduced movement and abundance, the ability of species to persist was lower in smaller and more isolated fragments (Fig. 3, A and B). As predictedbytheory(6, 30, 31), fragmentation strongly reduced species richness of plants and animals across experiments (Fig. 3, A and B), often changing the composition of entire communities (Fig. 3, A to C). In tropical forests, reduced fragment size and increased pro- portion of edge habitat caused shifts in the physical environment that led to the loss of large and old trees in favor of pioneer trees (Fig. 3, A and C), with subsequent impacts on the community composition of insects (32). In grasslands, fragment size also affected succession rate, such that increased light penetrationand alteredseedpools in smaller fragments impeded the rate of ecological succession relative to that of larger fragments (33)(Fig. 3A). Consistently, all aspects of fragmentation—reduced fragment area, increased isolation, and increased edge—had degrading effects on a disparate set of core ecosystem functions. Degraded functions included reduced carbon andnitrogenretention (Fig.3,Ato C),productivity (Fig.3C),and pollination(Fig. 3B). In summary, across experiments spanning numerous studies and ecosystems, fragmentation consistently degraded ecosystems, reducing species persistence, species richness, nutrient retention, trophic dynamics, and, in more isolated fragments, movement. Long-term consequences of fragmentation To synthesize all time series of species richness and ecosystem func- tioning gathered across experiments, we measured effects of fragmen- tation over the course of each study. The effect of fragmentation was calculated over time as the proportional change in fragmented relative to non- or less-fragmented treatments (Fig. 4). In most cases, the large and consistent effects of fragmentation re- vealed by the experiments were predicted from theory. However, we Fig. 4. Delayed effects of fragmentation on ecosystem degradation. were struck by the persistence of degradation to biodiversity and eco- (A) The extinction debt represents a delayed loss of species due to frag- system processes and by the increase in many of the effects over time mentation. (B) The immigration lag represents differences in species (Fig. 4). For example, extreme rainfall events at Wog Wog appeared to richness caused by smaller fragment area or increased isolation during delay the decline in plant species richness for 5 years after fragmenta- fragment succession. (C) The ecosystem function debt represents de- layed changes in ecosystem function due to reduced fragment size or tion. In the Kansas Experiment, a lag of 12 years occurred before frag- increased isolation. Percent loss is calculated as proportional change in mentation effects on plant succession were detected. Our results thus fragmented treatments [for example, (no. of species in fragment − no. reveal long-term and progressive effects of fragmentation and provide of species in control)/(no. of species in control) × 100]. Fragments and support for three processes proposed by recent studies in spatial ecol- controls were either the same area before and after fragmentation, frag- ogy: extinction debt, immigration lag, and ecosystem function debt ments compared to unfragmented controls, or small compared to large (Fig. 4). fragments. Filled symbols indicate times when fragmentation effects First, we found strong evidence for temporal lags in extinction [that became significant, as determined by the original studies (see table is, “extinction debt” (30)] in fragments. Species richness of plants, ar- S2). Mean slopes (dashed lines) were estimated using linear mixed (random thropods, and birds sampled in the experiments conducted in mature slopes) models. Mean slope estimates (mean and SE) were as follows: (A) forest fragments and replicated moss landscapes showed decreases of −0.22935 (0.07529); (B) −0.06519 (0.03495); (C) −0.38568 (0.16010). Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 5of9 RESEARCH ARTICLE 20 to 75% after fragmentation (Fig. 4A). Some declines were evident for variation in connectivity and habitat quality within and between almost immediately after fragmentation, whereas others increased in fragments (33, 43–45), spatial dynamics (14, 46), and spatially varying magnitude over the experiment’s duration. Across experiments, average interspecific interactions (47). loss was >20% after 1 year, >50% after 10 years, and is still increasing in Second, experiments have demonstrated that the effects of fragmen- the longest time series measured (more than two decades). The rate of tation are mediated by variation in traits across species. More realistic change appearstobeslowerinlargerfragments [inBDFFP,50% decline predictions of community responses to fragmentation emerged after ex- in bird species after 5 years in 1-ha fragments, but after 12 years in plicit consideration of species traits such as rarity and trophic levels 100-ha fragments; in Moss, 40% decline in arthropod species richness (48, 49), dispersal mode (50–52), reproductive mode and life span (29, 53), of small fragments and 26% reduction in large fragments after 1 year diet (54), and movement behavior (55, 56). Increasingly, the simple theo- (34, 35)]. As predicted by theory (36), the extinction debt appears to retical prediction that fragmentation reduces species richness is being take longer to pay in larger fragments. modified to account for species identity through models that focus on Second, we observed that reduced richness was coincident with an how species vary in their traits (4, 21, 36, 48, 57, 58). Consideration “immigration lag” (37), whereby small or isolated fragments are slower of traits may help to interpret variation around the overarching pat- to accumulate species during community assembly (33, 38)(Fig. 4B). Im- tern that fragmentation consistently reduces species richness across migration lags were observed in experiments conducted in successional many species and biomes (Figs. 3 and 4). systems that were initiated by creating new habitat fragments, rather than by fragmenting existing habitats. After more than a decade, im- migration lags resulted in 5% fewer species after 1 year, and 15% fewer A NEW GENERATION OF FRAGMENTATION EXPERIMENTS species after 10 years in small or isolated fragments compared to large or connected fragments (Fig. 4B). New foci are emerging for studying ecosystem fragmentation, in- Third, we observed an ecosystem function debt caused by fragmen- cluding (i) synergies between fragmentation and global changes, (ii) tation (39) in forest and moss fragments (Fig. 4C). An ecosystem function eco-evolutionary responses of species to fragmentation, and (iii) ecolog- debt is manifest both as delayed changes in nutrient cycling and as ical responses to fragmentation in production landscapes—that is, eco- changestoplant and consumerbiomass.Lossoffunctionamounted to systems whose services are under extreme appropriation by humans (59). 30% after 1 year, rising to 80% after a decade in small and isolated frag- First, conclusions from experiments thus far are likely to have been ments when compared to larger and more connected fragments (Fig. 4C). conservative because impacts from other environmental changes have Functional debts can result from biodiversity loss, as when loss of nutri- been mostly excluded. Most forms of global change known to reduce ents and reduction in decomposition are caused by simplification of food population sizes and biodiversity will be exacerbated by fragmentation webs. Alternatively, the impact is exhibited through pathways whereby (58, 60), including climate change (61), invasive species (62, 63), hunting fragmentation changes biotic (for example, tree density in successional (64), pollution [including light, noise, and chemicals (65)], and altered systems) or abiotic conditions (for example, light regimes or humidity) disturbance regimes (66). in ways that alter and potentially impair ecosystem function [for ex- More complex experiments with unparalleled control and capacity ample, biomass collapse in fragments; Figs. 3 and 4; altered nitrogen to simultaneously manipulate fragmentation and other global changes and carbon soil dynamics (40)]. are now under way (53). The Metatron, created in 2011 in southern France (67), enables ecologists to assess effects of variation in tempera- A new understanding of the effects of fragmentation ture and other abiotic factors in addition to habitat isolation. The By testing existing theory, experiments play a pivotal role in advancing SAFE Project is being created in the rainforest of Borneo (68)and will ideas and developing new theory. We draw on experimental evidence to embed a fragmentation experiment within a production agricultural plantation in which poaching will occur. Other synergies should be highlight two ways that the understanding of fragmentation has been investigated experimentally, including the interaction between frag- enriched by the interplay between long-term experiments and develop- mentation and hunting, fire, infectious disease outbreaks, or nitrogen ment of theory. deposition. Within these experiments, fragmentation and loss of hab- First, island biogeography (6) was among the earliest theories to pre- itat can then be varied independently. dict extinction and immigration rates and patterns of species richness in isolated biotas, which were later used to predict the effects of fragmen- Second, current experiments have stopped short of examining how tation on these variables. Experiments in continental settings tested the fragmentation drives evolution through genetic bottlenecks, ecological theory and gave rise to fresh perspectives. For example, islands are sur- traps, changing patterns of selection, inbreeding, drift, and gene flow rounded by sea, a thoroughly inimical matrix for island-dwelling species. (69–72). Extensive fragmentation has occurred over many years, and Habitat islands, or fragments, are surrounded by a matrix that may not in some regions over millennia (11). Changes caused by fragmentation be so unsuitable for some species. In terms of all of the ecological varia- undoubtedly lead to altered patterns of selection and trait evolution. bles studied in our long-term experiments, our results support the con- Evolutionary responses to fragmentation have already been suggested clusion that ecological dynamics in human-modified fragments are a (73, 74), and it is likely that such changes will, in turn, feed back to stark contrast to the dynamics in intact habitats that remain. Obser- influence population persistence and ecosystem resilience in fragmen- vational studies that have devoted more detailed consideration to the ted landscapes. Linking long-term experiments with the tools of land- countryside within which fragments are embedded explain the diversity scape genetics (75) may provide powerful insights into the evolutionary of ecological responses in remaining fragments (41). At the sametimeas dynamics of species inhabiting fragmented landscapes. experiments supported the core predictions of classical theories about Third, new experiments should address the management of natural effects of fragment size and isolation (Figs. 3 and 4), they spurred and habitats in production landscapes by monitoring vegetation, networks tested new theories such as metacommunity theory (42) to account of interacting species, and ecosystem services at ecologically relevant Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 6of9 RESEARCH ARTICLE spatial and temporal scales (76–78). Some ecosystem services have Theeffectsofcurrent fragmentationwillcontinuetoemergefor dec- global consequences, for example, local carbon sequestration affects ades. Extinction debts are likely to come due, although the counteract- global atmospheric CO . However, in many cases the benefits obtained ing immigration debts may never fully be paid. Indeed, the experiments by people depend on their proximity to habitat fragments (79). For ex- here reveal ongoing losses of biodiversity and ecosystem functioning ample, crop pollination and biological pest control from natural areas two decades or longer after fragmentation occurred. Understanding adjacent to farms are made available by the very process of habitat the relationship between transient and long-term dynamics is a substan- fragmentation, bringing people and agriculture closer to those services. tial challenge that ecologists must tackle, and fragmentation experiments Yet, further fragmentation reduces access to many services and ulti- will be central for relating observation to theory. mately may push landscapes past tipping points, beyond which essen- Experimental results to date show that the effects of fragmentation tial ecosystem services are not merely diminished but lost completely are strong and markedly consistent across a diverse array of terrestrial (80). This complex relationship creates a double-edged sword, for systems on five continents. Increasingly, these effects will march in con- which locally optimal levels and arrangements of habitat must be cert with other global changes. New experiments should be coupled sought. New fragmentation experiments should consider how multiple with emerging technologies, landscape genetics, and detailed imagery fragments in a landscape interact, creating an ecological network in of our planet, and should be coordinated with current ecological the- which the collective benefit of ecosystem services may be greater than ory to understand more deeply the coupled dynamics of ecological the sum of services provided by individual fragments (81, 82). Ex- and social systems. These insights will be increasingly critical for those perimental inferences may then be tested beyond their spatiotemporal responsible for managing and prioritizing areas for preservation and domains and, if successful, extrapolated across scales. Such research will ecological restoration in fragmented landscapes. be aided by satellite monitoring of ecosystems and human land use across the globe. The most powerful research programs will integrate SUPPLEMENTARY MATERIALS experiments, observational studies, air- and space-borne imaging, and Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/ modeling. full/1/2/e1500052/DC1 Materials and Methods Fig. S1. Map of the BDFFP experiment and location within Brazil. Fig. S2. Map of the Kansas fragmentation experiment. CONCLUSIONS Fig. S3. Map of the Wog Wog experiment and location within Australia. Fig. S4. Map of the SRS experiment showing locations of the eight blocks in the second SRS Fragmentation experiments—some of the largest and longest-running Corridor Experiment within the SRS, South Carolina, USA. experiments in ecology—provide clear evidence of strong and typically Fig. S5. Design of the Moss experiment. degrading impacts of habitat fragmentation on biodiversity and ecolog- Fig. S6. Design of the Metatron experiment with 48 enclosed fragments and adjoining enclosed corridors. ical processes. The findings of these experiments extend to a large frac- Fig. S7. Map of the SAFE experiment and location within Borneo [after Ewers et al.(68)]. tion of the terrestrial surface of the Earth. Much of the Earth’s remaining Table S1. Metadata for Fig. 3 in the main text. forest fragments are less than 10 ha in area, and half of the world’sforest Table S2. Metadata for Fig. 4 in the main text. is within 500 m of the forest edge—areas and distances matched to existing long-term experiments (Figs. 1 and 2) from which consistent REFERENCES AND NOTES effects of fragmentation have emerged (Figs. 3 and 4). Reduced fragment area, increased isolation, and increased edge ini- 1. H. M. Pereira, P. W. Leadley, V. Proenca, R. Alkemade, J. P. W. Scharlemann, J. F. Fernandez-Manjarres, tiate changes that percolate through ecosystems (Fig. 3). Fragmenta- M. B. Araujo,P.Balvanera, R. Biggs, W. W. L. Cheung,L.Chini,H.D.Cooper, E. L. Gilman, tion has the capacity to generate persistent, deleterious, and often S. Guenette, G. C. Hurtt, H. P. Huntington, G. M. Mace, T. Oberdorff, C. Revenga, P. Rodrigues, unpredicted outcomes, including surprising surges in abundance of R. J. Scholes, U. R. Sumaila, M. 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Levey, C. R. Margules, S. Polasky, J. Rockstrom, J. Sheehan, S. Siebert, D. Tilman, D. P. M. Zaks, Solutions for a B. A. Melbourne, A. O. Nicholls, J. L. Orrock, D.-X. Song, J. R. Townshend, Habitat fragmentation cultivated planet. Nature 478,337–342 (2011). and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015). Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 9of9 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Science Advances Pubmed Central

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RESEARCH ARTICLE 2015 © The Authors, some rights reserved; APPLIED ECOLOGY exclusive licensee American Association for the Advancement of Science. Distributed Habitat fragmentation and its lasting impact under a Creative Commons Attribution License 4.0 (CC BY). on Earth’s ecosystems 10.1126/sciadv.1500052 1 2 3 4 5 Nick M. Haddad, *LarsA. Brudvig, Jean Clobert, Kendi F. Davies, Andrew Gonzalez, 6 7 8 9 10 Robert D. Holt, Thomas E. Lovejoy, Joseph O. Sexton, Mike P. Austin, Cathy D. Collins, 11 12 13 14 15 William M. Cook, Ellen I. Damschen, Robert M. Ewers, Bryan L. Foster, Clinton N. Jenkins, 9 16 17 18,19 Andrew J. King, William F. Laurance, Douglas J. Levey, Chris R. Margules, 4 9,20 12 8 8 Brett A. Melbourne, A. O. Nicholls, John L. Orrock, Dan-Xia Song, John R. Townshend We conducted an analysis of global forest cover to reveal that 70% of remaining forest is within 1 km of the forest’s edge, subject to the degrading effects of fragmentation. A synthesis of fragmentation experiments spanning multiple biomes and scales, five continents, and 35 yearsdemonstratesthathabitat fragmentation reduces bio- diversity by 13 to 75% and impairs key ecosystem functions by decreasing biomass and altering nutrient cycles. Effects are greatest in the smallest and most isolated fragments, and they magnify with the passage of time. These findings indicate an urgent need for conservation and restoration measures to improve landscape connectivity, which will reduce extinction rates and help maintain ecosystem services. INTRODUCTION fragment size and increased isolation relative to the widespread and Destruction and degradation of natural ecosystems are the primary pervasive effects of habitat loss in explaining declines in biodiversity causes of declines in global biodiversity (1, 2). Habitat destruction typ- and the degradation of ecosystems (7). Observational studies of the ically leads to fragmentation, the division of habitat into smaller and effects of fragmentation have often magnified the controversy because more isolated fragments separated by a matrix of human-transformed inference from nonmanipulative studies is limited to correlation and land cover. The loss of area, increase in isolation, and greater exposure because they have individually often considered only single aspects of to human land uses along fragment edges initiate long-term changes fragmentation (for example, edge, isolation, and area) (8). However, to the structure and function of the remaining fragments (3). together with these correlative observations, experimental studies re- Ecologists agree that habitat destruction is detrimental to the main- veal that fragmentation has multiple simultaneous effects that are in- tenance of biodiversity, but they disagree—often strongly—on the ex- terwoven in complex ways and that operate over potentially long time tent to which fragmentation itself is to blame (4, 5). Early hypotheses scales (9). based on the biogeography of oceanic islands (6) provided a theoret- Here, we draw on findings of the world’s largest and longest- ical framework to understand fragmentation’s effect on extinction in running fragmentation experiments that span 35 years and disparate terrestrial landscapes composed of “islands” of natural habitat scat- biomes on five continents. Their rigorous designs and long-term im- tered across a “sea” of human-transformed habitat. Central to the con- plementation overcome many limitations of observational studies. In troversy has been a lingering uncertainty about the role of decreased particular, by manipulating and isolating individual aspects of frag- mentation while controlling for others, and by doing so on entire 1 ecosystems, they provide a powerful way to disentangle cause and Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA. effect in fragmented landscapes. Here, we present experimental evi- Department of Plant Biology, Michigan State University, East Lansing, MI 48824–1312, USA. Station d’Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis, 09200 Saint-Girons, dence of unexpected long-term ecological changes caused by habitat France. Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, fragmentation. Boulder, CO 80309, USA. Department of Biology, McGill University, Montreal, Quebec H3A Highlighting one ecosystem type as an example, we first present a 1B1, Canada. Department of Biology, University of Florida, Gainesville, FL 32611, USA. Department of Environmental Science and Policy, George Mason University, Fairfax, VA global analysis of the fragmentation of forest ecosystems, quantifying 22030, USA. Global Land Cover Facility, Department of Geographical Sciences, University of for the first time the global hotspots of intensive historical fragmenta- Maryland, College Park, MD 20702, USA. CSIRO Land and Water Flagship, GPO Box 1700, 10 tion. We then synthesize results from the set of long-term experiments Canberra, Australian Capital Territory 2601, Australia. Department of Biology, Colby conducted in a wide variety of ecosystems to demonstrate consistent College, 5746 Mayflower Hill, Waterville, ME 04901, USA. Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA. Department of Zoology, impacts of fragmentation, how those impacts change over time, and University of Wisconsin, Madison, WI 53706, USA. Department of Life Sciences, Imperial how they align with predictions from theory and observation. Finally, College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK. we identify key knowledge gaps for the next generation of fragmenta- Department of Ecology and Evolutionary Biology and Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047–3759, USA. Instituto de Pesquisas tion experiments. Ecológicas, Rod. Dom Pedro I, km 47, Caixa Postal 47, Nazaré Paulista, São Paulo 12960-000, Brazil. Centre for Tropical Environmental and Sustainability Science and College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland 4878, Australia. 17 18 GLOBAL ANALYSIS OF THE EXTREME MAGNITUDE AND National Science Foundation, Arlington, VA 22230, USA. Centre for Tropical Environmental and Sustainability Science, School of Earth and Environmental Sciences, EXTENT OF FRAGMENTATION James Cook University, Cairns 4878, Australia. Research Center for Climate Change, University of Indonesia, Kota Depok, Java Barat 16424, Indonesia. The Institute for Land, New satellite data sets reveal at high resolution how human activities Water and Society, Charles Sturt University, Thurgoona Campus, Albury, New South Wales are transforming global ecosystems. Foremost among these observations 2640, Australia. *Corresponding author. E-mail: nick_haddad@ncsu.edu are those of forest cover because of the high contrast between forest Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 1of9 RESEARCH ARTICLE and anthropogenic land cover types. Deforestation, which was already Historical data enable the study of the process of forest fragmen- widespread in temperate regions in the mid-18th to 20th centuries tation over time. We reconstructed the historical forest extent and and increased in the tropics over the past half century, has resulted timing of fragmentation in two forested regions of Brazil that provide in the loss of more than a third of all forest cover worldwide (10, 11). a stark contrast in land-use dynamics. The Brazilian Amazon is a Beyond the direct impacts of forest loss and expanding anthropogenic rapidly changing frontier (10), yet most of its forests remain con- land cover(forexample,agricultural fields and urban areas), remnant tiguous and far from an edge despite recent increases in fragmen- forests are likely to suffer from being smaller, more isolated, and with tation (Fig. 1, C and D). In contrast, the Brazilian Atlantic Forest is a greater area located near the edge of the forest (12). a largely deforested landscape, cleared for agriculture and logged We analyzed the world’s first high-resolution map of global tree for timber over the last three centuries (11). This remaining forest cover (13) to measure the magnitude of forest fragmentation. This is dominated by small fragments, with most fragments smaller than analysis revealed that nearly 20% of the world’s remaining forest is 1000 ha and within 1000 m of a forest edge (Fig. 1, E and F) (16). In within 100mof an edge (Fig.1,AandB)—in close proximity to agricul- the Brazilian Amazon, the proportion of forest farther than 1 km from tural, urban, or other modified environments where impacts on forest the forest edge has decreased from 90% (historical) to 75% (today), ecosystems are most severe (14). More than 70% of the world’sforests and in the Brazilian Atlantic, from 90% to less than 9%. are within 1 km of a forest edge. Thus, most forests are well within the These two forested regions of Brazil define extremes of the frag- range where human activities, altered microclimate, and nonforest mentation process and are representative of the extent of fragmenta- species may influence and degrade forest ecosystems (15). The largest tion in forested landscapes worldwide (Fig. 1), as well as many other contiguous expanses of remaining forests are in the humid tropical re- biomes including temperate grasslands, savannas, and even aquatic gions of the Amazon and Congo River Basins (Fig. 1A). Large areas of systems (17). For example, although a spatial analysis similar to that more disjunct forest also remain in southeastern Asia, New Guinea, of forest is not currently possible in grasslands, 37% of the world’s and the boreal biomes. grassland eco-regions are classified as “highly fragmented” (18, 19). Fig. 1. The global magnitude of forest frag- mentation. (A) Mean distance to forest edge for forested pixels within each 1-km cell. Lines point to locations of ongoing fragmentation exper- iments identified and described in Fig. 2. (B) Proportion of the world’sforestat eachdistance to the forest edge and the cumulative propor- tion across increasing distance categories (green line). (C and E)Inthe BrazilianAmazon(C) and Atlantic Forests (E), the proportion of forest area at each distance to forest edge for both the cur- rent and estimated historic extent of forest. (D and F)Inthe BrazilianAmazon(D) andAtlantic Forests (F), the number of fragments and the total area of fragments of that size. The total number of fragments in the smallest bin (1 to 10 ha) is an underestimate in both the Atlantic Forest and Amazon data sets because not all of the very smallest fragments are mapped. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 2of9 RESEARCH ARTICLE Robust knowledge of how habitat fragmentation affects biodiversity occur in several biomes (Fig. 2 and Supplementary Materials) and and ecosystem processes is needed if we are to comprehend adequately were designed to manipulate specific components of fragmentation— the implications of this global environmental change. habitat size, isolation, and connectivity—while controlling for confounding factors such as the amount of habitat lost across a landscape (Fig. 2). The largest fragments across these experiments match the size of frag- ments commonly created by anthropogenic activities (Figs. 1 and 2). THE VALUE OF LONG-TERM FRAGMENTATION EXPERIMENTS Distances to the edge of experimental fragments range to 500 m, en- Long-term experiments are a powerful tool for understanding the ec- compassing edge distances found in more than half of forests world- ological consequences of fragmentation (20). Whereas observational wide (Fig. 1B). In each experiment, different fragmentation treatments studies of fragmented landscapes have yielded important insights with replication were established, starting from continuous, nonfrag- (9, 21), they typically lack rigorous controls, replication, randomiza- mented landscapes and controlling for background environmental tion, or baseline data. Observational studies have limited ability variation either by experimental design (blocking) or by measurement to isolate the effects of fragmentation from concomitant habitat loss of covariates for use in subsequent analyses. Tests were conducted within and degradation per se (4, 7, 22). Remnant fragments are embedded in fragments that varied experimentally in area or edge, within fragments different types and qualities of surrounding habitat, complicating in- that were experimentally isolated or connected, or within experimental terpretation because the surrounding habitat also influences bio- fragments compared to the same area within continuous habitat. All diversity and ecosystem productivity (23). treatments were replicated. Experiments were created by destroying or The long-term fragmentation experiments we analyze here com- creating precise amounts of habitat across replicate landscapes, allow- prise the entire set of ongoing terrestrial long-term experiments. They ing tests of fragmentation effects independent of habitat loss. The robust Fig. 2. The world’s ongoing fragmentation experiments. All experi- ades). The variables under study in each experiment are checked. The area ments have been running continuously since the time indicated by the is that of the experiment’s largest fragments. Icons under “Fragment” and start of the associated arrow (with the exception of the moss fragmenta- “Matrix” indicate the dominant community and its relative height, with tion experiment, which represents a series of studies over nearly two dec- multiple trees representing succession. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 3of9 RESEARCH ARTICLE and comparable experimental designs allow for powerful tests of the We synthesized results available 31 January 2014 for all studies mechanisms underpinning the ecological impacts of fragmentation, and within these experiments that were conducted in all treatments and the long-term nature of ensuing studies has revealed consistent emer- replicates, and tested fragmentation effects on dispersal, abundance, gent effects. extinction, species richness, community composition, and ecosystem These experiments mimic anthropogenic fragmentation; they are functioning. We first calculated effect sizes of fragmentation as log re- whole-ecosystem manipulations in which all species and processes sponse ratios (Fig. 3). Data from 76 different studies across the five experienced the same treatment (24). Emergent responses thus reflect longest-running experiments were drawn from published and un- the multiple direct and indirect effects of interacting species and published sources (table S1). We synthesized results according to three processes. Further, because experimentally fragmented ecosystems fragmentation treatments: reduced fragment area [the focus of Biolog- are open to fluxes of individuals and resources, fragmentation ical Dynamics of Forest Fragments Project (BDFFP), Wog Wog, and effects can manifest across multiple levels of ecological organization Kansas; see Fig. 2 for identifiers of experiments], increased fragment (Fig. 3). Long-term experiments have the power to detect lagged and/ isolation [Savannah River Site (SRS) and Moss], and increased propor- or chronic impacts. tion of edge (all experiments). Fragmented treatments were compared The first fragmentation experiments, now more than three decades directly to non- or less-fragmented habitats that were either larger or old, were created to test effects of fragment area on both species connected via structural corridors (table S1). persistence and patterns of immigration, reflecting concern in con- servation biology about the role of fragmentation in reducing pop- Strong, consistent, and accumulating effects ulation sizes below viable levels (25) (Fig. 2). Subsequent experiments, of habitat fragmentation created two decades ago, shifted focus to modifying habitat isolation, Our synthesis revealed strong and consistent responses of organisms reflecting recognition of the potential to mitigate negative effects of frag- and ecosystem processes to fragmentation arising from decreased mentation by recreating habitat—specifically with corridors—to increase fragment area, increased isolation, and the creation of habitat edges connectivity among fragments (26) (Fig. 2). The newest experiments test (Fig. 3). emerging questions about potentially deleterious synergies between Community and ecosystem responses emerge from observed re- fragmentation and global changes in climate and land use (Fig. 2). sponses at the level of populations. Reduced area decreased animal Fig. 3. Fragmentation effects propagate through the whole eco- ratio: ln(mean in more fragmented treatment/meaninnon-orless-fragmented system. (A to C) For each fragmentation treatment [reduced area in treatment)] for an ecological process. Effect sizes are statistical, such that BDFFP, Wog Wog, Kansas (A); increased isolation in SRS and Moss (B); negative or positive values could represent degrading function. Horizon- and increased edge in all experiments (C)], we summarize major find- tal bars are the range when a dot is represented by more than one study. ings for ecological processes at all levels of ecological organization. Details, including individual effect sizes for each study, are reported in Each dot represents the mean effect size [computed as log response table S1. Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 4of9 RESEARCH ARTICLE residency within fragments, and increased isolation reduced move- ment among fragments, thus reducing fragment recolonization after local extinction (Fig. 3, A and B). Reduced fragment area and increased fragment isolation generally reduced abundance of birds, mammals, insects, and plants (Fig. 3, A and B). This overall pattern emerged de- spite complex patterns of increases or declines in abundance of indi- vidual species (Fig. 3A) with various proximate causes such as release from competition or predation, shifts in disturbance regimes, or alter- ation of abiotic factors (14, 27–29). Reduced area, increased isolation, and increased proportion of edge habitat reduced seed predation and herbivory, whereas increased proportion of edge caused higher fledgling predation that had the effect of reducing bird fecundity (represented together as trophic dynamics in Fig. 3, A to C). Perhaps because of reduced movement and abundance, the ability of species to persist was lower in smaller and more isolated fragments (Fig. 3, A and B). As predictedbytheory(6, 30, 31), fragmentation strongly reduced species richness of plants and animals across experiments (Fig. 3, A and B), often changing the composition of entire communities (Fig. 3, A to C). In tropical forests, reduced fragment size and increased pro- portion of edge habitat caused shifts in the physical environment that led to the loss of large and old trees in favor of pioneer trees (Fig. 3, A and C), with subsequent impacts on the community composition of insects (32). In grasslands, fragment size also affected succession rate, such that increased light penetrationand alteredseedpools in smaller fragments impeded the rate of ecological succession relative to that of larger fragments (33)(Fig. 3A). Consistently, all aspects of fragmentation—reduced fragment area, increased isolation, and increased edge—had degrading effects on a disparate set of core ecosystem functions. Degraded functions included reduced carbon andnitrogenretention (Fig.3,Ato C),productivity (Fig.3C),and pollination(Fig. 3B). In summary, across experiments spanning numerous studies and ecosystems, fragmentation consistently degraded ecosystems, reducing species persistence, species richness, nutrient retention, trophic dynamics, and, in more isolated fragments, movement. Long-term consequences of fragmentation To synthesize all time series of species richness and ecosystem func- tioning gathered across experiments, we measured effects of fragmen- tation over the course of each study. The effect of fragmentation was calculated over time as the proportional change in fragmented relative to non- or less-fragmented treatments (Fig. 4). In most cases, the large and consistent effects of fragmentation re- vealed by the experiments were predicted from theory. However, we Fig. 4. Delayed effects of fragmentation on ecosystem degradation. were struck by the persistence of degradation to biodiversity and eco- (A) The extinction debt represents a delayed loss of species due to frag- system processes and by the increase in many of the effects over time mentation. (B) The immigration lag represents differences in species (Fig. 4). For example, extreme rainfall events at Wog Wog appeared to richness caused by smaller fragment area or increased isolation during delay the decline in plant species richness for 5 years after fragmenta- fragment succession. (C) The ecosystem function debt represents de- layed changes in ecosystem function due to reduced fragment size or tion. In the Kansas Experiment, a lag of 12 years occurred before frag- increased isolation. Percent loss is calculated as proportional change in mentation effects on plant succession were detected. Our results thus fragmented treatments [for example, (no. of species in fragment − no. reveal long-term and progressive effects of fragmentation and provide of species in control)/(no. of species in control) × 100]. Fragments and support for three processes proposed by recent studies in spatial ecol- controls were either the same area before and after fragmentation, frag- ogy: extinction debt, immigration lag, and ecosystem function debt ments compared to unfragmented controls, or small compared to large (Fig. 4). fragments. Filled symbols indicate times when fragmentation effects First, we found strong evidence for temporal lags in extinction [that became significant, as determined by the original studies (see table is, “extinction debt” (30)] in fragments. Species richness of plants, ar- S2). Mean slopes (dashed lines) were estimated using linear mixed (random thropods, and birds sampled in the experiments conducted in mature slopes) models. Mean slope estimates (mean and SE) were as follows: (A) forest fragments and replicated moss landscapes showed decreases of −0.22935 (0.07529); (B) −0.06519 (0.03495); (C) −0.38568 (0.16010). Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 5of9 RESEARCH ARTICLE 20 to 75% after fragmentation (Fig. 4A). Some declines were evident for variation in connectivity and habitat quality within and between almost immediately after fragmentation, whereas others increased in fragments (33, 43–45), spatial dynamics (14, 46), and spatially varying magnitude over the experiment’s duration. Across experiments, average interspecific interactions (47). loss was >20% after 1 year, >50% after 10 years, and is still increasing in Second, experiments have demonstrated that the effects of fragmen- the longest time series measured (more than two decades). The rate of tation are mediated by variation in traits across species. More realistic change appearstobeslowerinlargerfragments [inBDFFP,50% decline predictions of community responses to fragmentation emerged after ex- in bird species after 5 years in 1-ha fragments, but after 12 years in plicit consideration of species traits such as rarity and trophic levels 100-ha fragments; in Moss, 40% decline in arthropod species richness (48, 49), dispersal mode (50–52), reproductive mode and life span (29, 53), of small fragments and 26% reduction in large fragments after 1 year diet (54), and movement behavior (55, 56). Increasingly, the simple theo- (34, 35)]. As predicted by theory (36), the extinction debt appears to retical prediction that fragmentation reduces species richness is being take longer to pay in larger fragments. modified to account for species identity through models that focus on Second, we observed that reduced richness was coincident with an how species vary in their traits (4, 21, 36, 48, 57, 58). Consideration “immigration lag” (37), whereby small or isolated fragments are slower of traits may help to interpret variation around the overarching pat- to accumulate species during community assembly (33, 38)(Fig. 4B). Im- tern that fragmentation consistently reduces species richness across migration lags were observed in experiments conducted in successional many species and biomes (Figs. 3 and 4). systems that were initiated by creating new habitat fragments, rather than by fragmenting existing habitats. After more than a decade, im- migration lags resulted in 5% fewer species after 1 year, and 15% fewer A NEW GENERATION OF FRAGMENTATION EXPERIMENTS species after 10 years in small or isolated fragments compared to large or connected fragments (Fig. 4B). New foci are emerging for studying ecosystem fragmentation, in- Third, we observed an ecosystem function debt caused by fragmen- cluding (i) synergies between fragmentation and global changes, (ii) tation (39) in forest and moss fragments (Fig. 4C). An ecosystem function eco-evolutionary responses of species to fragmentation, and (iii) ecolog- debt is manifest both as delayed changes in nutrient cycling and as ical responses to fragmentation in production landscapes—that is, eco- changestoplant and consumerbiomass.Lossoffunctionamounted to systems whose services are under extreme appropriation by humans (59). 30% after 1 year, rising to 80% after a decade in small and isolated frag- First, conclusions from experiments thus far are likely to have been ments when compared to larger and more connected fragments (Fig. 4C). conservative because impacts from other environmental changes have Functional debts can result from biodiversity loss, as when loss of nutri- been mostly excluded. Most forms of global change known to reduce ents and reduction in decomposition are caused by simplification of food population sizes and biodiversity will be exacerbated by fragmentation webs. Alternatively, the impact is exhibited through pathways whereby (58, 60), including climate change (61), invasive species (62, 63), hunting fragmentation changes biotic (for example, tree density in successional (64), pollution [including light, noise, and chemicals (65)], and altered systems) or abiotic conditions (for example, light regimes or humidity) disturbance regimes (66). in ways that alter and potentially impair ecosystem function [for ex- More complex experiments with unparalleled control and capacity ample, biomass collapse in fragments; Figs. 3 and 4; altered nitrogen to simultaneously manipulate fragmentation and other global changes and carbon soil dynamics (40)]. are now under way (53). The Metatron, created in 2011 in southern France (67), enables ecologists to assess effects of variation in tempera- A new understanding of the effects of fragmentation ture and other abiotic factors in addition to habitat isolation. The By testing existing theory, experiments play a pivotal role in advancing SAFE Project is being created in the rainforest of Borneo (68)and will ideas and developing new theory. We draw on experimental evidence to embed a fragmentation experiment within a production agricultural plantation in which poaching will occur. Other synergies should be highlight two ways that the understanding of fragmentation has been investigated experimentally, including the interaction between frag- enriched by the interplay between long-term experiments and develop- mentation and hunting, fire, infectious disease outbreaks, or nitrogen ment of theory. deposition. Within these experiments, fragmentation and loss of hab- First, island biogeography (6) was among the earliest theories to pre- itat can then be varied independently. dict extinction and immigration rates and patterns of species richness in isolated biotas, which were later used to predict the effects of fragmen- Second, current experiments have stopped short of examining how tation on these variables. Experiments in continental settings tested the fragmentation drives evolution through genetic bottlenecks, ecological theory and gave rise to fresh perspectives. For example, islands are sur- traps, changing patterns of selection, inbreeding, drift, and gene flow rounded by sea, a thoroughly inimical matrix for island-dwelling species. (69–72). Extensive fragmentation has occurred over many years, and Habitat islands, or fragments, are surrounded by a matrix that may not in some regions over millennia (11). Changes caused by fragmentation be so unsuitable for some species. In terms of all of the ecological varia- undoubtedly lead to altered patterns of selection and trait evolution. bles studied in our long-term experiments, our results support the con- Evolutionary responses to fragmentation have already been suggested clusion that ecological dynamics in human-modified fragments are a (73, 74), and it is likely that such changes will, in turn, feed back to stark contrast to the dynamics in intact habitats that remain. Obser- influence population persistence and ecosystem resilience in fragmen- vational studies that have devoted more detailed consideration to the ted landscapes. Linking long-term experiments with the tools of land- countryside within which fragments are embedded explain the diversity scape genetics (75) may provide powerful insights into the evolutionary of ecological responses in remaining fragments (41). At the sametimeas dynamics of species inhabiting fragmented landscapes. experiments supported the core predictions of classical theories about Third, new experiments should address the management of natural effects of fragment size and isolation (Figs. 3 and 4), they spurred and habitats in production landscapes by monitoring vegetation, networks tested new theories such as metacommunity theory (42) to account of interacting species, and ecosystem services at ecologically relevant Haddad et al. Sci. Adv. 2015;1:e1500052 20 March 2015 6of9 RESEARCH ARTICLE spatial and temporal scales (76–78). Some ecosystem services have Theeffectsofcurrent fragmentationwillcontinuetoemergefor dec- global consequences, for example, local carbon sequestration affects ades. Extinction debts are likely to come due, although the counteract- global atmospheric CO . However, in many cases the benefits obtained ing immigration debts may never fully be paid. Indeed, the experiments by people depend on their proximity to habitat fragments (79). For ex- here reveal ongoing losses of biodiversity and ecosystem functioning ample, crop pollination and biological pest control from natural areas two decades or longer after fragmentation occurred. Understanding adjacent to farms are made available by the very process of habitat the relationship between transient and long-term dynamics is a substan- fragmentation, bringing people and agriculture closer to those services. tial challenge that ecologists must tackle, and fragmentation experiments Yet, further fragmentation reduces access to many services and ulti- will be central for relating observation to theory. mately may push landscapes past tipping points, beyond which essen- Experimental results to date show that the effects of fragmentation tial ecosystem services are not merely diminished but lost completely are strong and markedly consistent across a diverse array of terrestrial (80). This complex relationship creates a double-edged sword, for systems on five continents. Increasingly, these effects will march in con- which locally optimal levels and arrangements of habitat must be cert with other global changes. New experiments should be coupled sought. New fragmentation experiments should consider how multiple with emerging technologies, landscape genetics, and detailed imagery fragments in a landscape interact, creating an ecological network in of our planet, and should be coordinated with current ecological the- which the collective benefit of ecosystem services may be greater than ory to understand more deeply the coupled dynamics of ecological the sum of services provided by individual fragments (81, 82). Ex- and social systems. These insights will be increasingly critical for those perimental inferences may then be tested beyond their spatiotemporal responsible for managing and prioritizing areas for preservation and domains and, if successful, extrapolated across scales. Such research will ecological restoration in fragmented landscapes. be aided by satellite monitoring of ecosystems and human land use across the globe. The most powerful research programs will integrate SUPPLEMENTARY MATERIALS experiments, observational studies, air- and space-borne imaging, and Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/ modeling. full/1/2/e1500052/DC1 Materials and Methods Fig. S1. Map of the BDFFP experiment and location within Brazil. Fig. S2. Map of the Kansas fragmentation experiment. CONCLUSIONS Fig. S3. Map of the Wog Wog experiment and location within Australia. Fig. S4. Map of the SRS experiment showing locations of the eight blocks in the second SRS Fragmentation experiments—some of the largest and longest-running Corridor Experiment within the SRS, South Carolina, USA. experiments in ecology—provide clear evidence of strong and typically Fig. S5. Design of the Moss experiment. degrading impacts of habitat fragmentation on biodiversity and ecolog- Fig. S6. Design of the Metatron experiment with 48 enclosed fragments and adjoining enclosed corridors. ical processes. The findings of these experiments extend to a large frac- Fig. S7. Map of the SAFE experiment and location within Borneo [after Ewers et al.(68)]. tion of the terrestrial surface of the Earth. Much of the Earth’s remaining Table S1. Metadata for Fig. 3 in the main text. forest fragments are less than 10 ha in area, and half of the world’sforest Table S2. 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