Beyond the Fragmentation Threshold Hypothesis: Regime Shifts in Biodiversity Across Fragmented Landscapes Renata Pardini 1 *, Adriana de Arruda Bueno 1 , Toby A. Gardner 2 , Paulo Ina ´ cio Prado 3 , Jean Paul Metzger 3 1 Departamento de Zoologia, Instituto de Biocie ˆ ncias, Universidade de Sa ˜ o Paulo, Sa ˜ o Paulo, Brazil, 2 Department of Zoology, University of Cambridge, Cambridge, United Kingdom, 3 Departamento de Ecologia, Instituto de Biocie ˆncias, Universidade de Sa ˜o Paulo, Sa ˜o Paulo, Brazil Abstract Ecological systems are vulnerable to irreversible change when key system properties are pushed over thresholds, resulting in the loss of resilience and the precipitation of a regime shift. Perhaps the most important of such properties in human- modified landscapes is the total amount of remnant native vegetation. In a seminal study Andre ´ n proposed the existence of a fragmentation threshold in the total amount of remnant vegetation, below which landscape-scale connectivity is eroded and local species richness and abundance become dependent on patch size. Despite the fact that species patch-area effects have been a mainstay of conservation science there has yet to be a robust empirical evaluation of this hypothesis. Here we present and test a new conceptual model describing the mechanisms and consequences of biodiversity change in fragmented landscapes, identifying the fragmentation threshold as a first step in a positive feedback mechanism that has the capacity to impair ecological resilience, and drive a regime shift in biodiversity. The model considers that local extinction risk is defined by patch size, and immigration rates by landscape vegetation cover, and that the recovery from local species losses depends upon the landscape species pool. Using a unique dataset on the distribution of non-volant small mammals across replicate landscapes in the Atlantic forest of Brazil, we found strong evidence for our model predictions - that patch- area effects are evident only at intermediate levels of total forest cover, where landscape diversity is still high and opportunities for enhancing biodiversity through local management are greatest. Furthermore, high levels of forest loss can push native biota through an extinction filter, and result in the abrupt, landscape-wide loss of forest-specialist taxa, ecological resilience and management effectiveness. The proposed model links hitherto distinct theoretical approaches within a single framework, providing a powerful tool for analysing the potential effectiveness of management interventions. Citation: Pardini R, Bueno AdA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the Fragmentation Threshold Hypothesis: Regime Shifts in Biodiversity Across Fragmented Landscapes. PLoS ONE 5(10): e13666. doi:10.1371/journal.pone.0013666 Editor: Brock Fenton, University of Western Ontario, Canada Received July 1, 2010; Accepted October 6, 2010; Published October 27, 2010 Copyright: ß 2010 Pardini et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was funded by FAPESP - Fundac ¸a ˜o de Amaparo a ` Pesquisa do Estado de Sa ˜o Paulo - http://www.fapesp.br (05/56555-4); CNPq - Conselho Nacional de Desenvolvimento Cientı ´fico e Tecnolo ´ gico - http://www.cnpq.br/BMBF - Bundesministerium fu ¨ r Bildung und Forschung - http://www.bmbf.de (690144/01-6); CAPES - Coordenac ¸a ˜o de Aperfeic ¸oamento de Pessoal de Nı ´vel Superior - http://www.capes.gov.br; and NERC - Natural Environment Research Council - http://www.nerc.ac.uk (NE/F01614X/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: renatapardini@uol.com.br Introduction Regime shifts represent fundamental, sudden changes in ecosystem state, and are usually driven by changes to key-variables that are linked to ecological resilience – the capacity of the system to absorb disturbance and reorganize so as to retain essentially the same function, structure, identity and feedbacks [1]. Multiple stable-states have been experimentally demonstrated in a variety of ecological systems [2], and accumulating evidence suggests that regime shifts can occur in a number of complex ecosystems, with potentially catastrophic consequences to biodiversity, ecosystem services and human well-being [3,4]. The ability to anticipate such dramatic changes is of foremost importance to ecosystem management and has inspired a growing amount of research and modeling work [5–7]. However, our understanding of the mechanisms that may underpin regime shifts is largely limited to aquatic environments and semi-arid rangelands [4,8]. While there is growing support for the notion that human-driven impacts can induce sudden changes in other ecosystems, including tropical forests [9,10], the definition of the key variables and feedbacks governing such shifts remain one of the greatest challenges facing the management of human-modified landscapes especially in the tropics [11]. Candidate drivers of potentially irreversible ecological shifts in human-modified landscapes include changes in (1) the total amount and configuration of native vegetation cover through its effects on landscape connectivity, (2) vegetation structure through its influence on natural disturbance regimes, and (3) species composition and the potential for ecological cascades [12]. Among these options, the total amount of native vegetation cover has been found to be fundamentally important for all major aspects of landscape management [13], with a growing amount of empirical evidence linking changes in total vegetation cover to changes in both biodiversity [14,15] and ecosystem function [16,17]. The relevance of total native vegetation cover as a driver of ecological change in fragmented landscapes was initially suggested by simulation studies. This body of work has shown that total habitat cover is non-linearly related to both patch (e.g. number of PLoS ONE | www.plosone.org 1 October 2010 | Volume 5 | Issue 10 | e13666