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ence sites, as only comparing different types of dis- turbed habitats limits the ability to .... ics: Brief history and conceptual domain. Biol J. Linnean Soc 42:3– 16.
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Tropical Conservation

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Perspectives on Local and Global Priorities

EDITED BY A. ALONSO AGUIRRE AND RAMAN SUKUMAR

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EVALUATING THE LINKS BETWEEN BIODIVERSITY, LAND-​USE CHANGE, AND INFECTIOUS DISEASE EMERGENCE IN TROPICAL FRAGMENTED LANDSCAPES

Elizabeth H. Loh, Kris A. Murray, Alessandra Nava, A. Alonso Aguirre, and Peter Daszak

INTRODUC T ION

During the past decade, tropical forests have continued their long-​ term reduction in extent (Hansen et al. 2013), largely due to human activities such as agricultural expansion, deforestation, and conversion of natural habitats to other land uses (Uriarte et al. 2010). These types of land-​u se change have created highly fragmented landscapes and perturbed biotic systems with direct and indirect impacts on human and wildlife populations (Foley et  al. 2005; Hassan et  al. 2005). Land-​u se change is a clear threat to global biodiversity and ecosystem services (Groom et al. 2006). It is also considered a key driver of emerging infectious diseases (EIDs) (Patz et al. 2004; Murray and Daszak 2013), which are defined as those that are increasing in incidence or geographic range; those characterized as newly evolved strains of pathogens, and novel pathogens that have entered human populations for the first time (Jones et  al. 2008). A  systematic quantitative review from the Australian

continent suggests that around one-​fifth of past EID events were linked to some form of land-​u se change (McFarlane et al. 2013). Further, although most human EIDs are zoonotic (Taylor et al. 2001; Woolhouse and Gowtage-​Sequeria 2005)  and increasing in frequency (Jones et al. 2008), current understanding of the relationship between host diversity, disease risk, and land-​u se change is still in its infancy. These relationships are likely complex and other mechanisms, which can influence disease risk, such as human ecology (e.g. human activity, behavior, and occupancy), must also be considered (Wilcox and Gubler 2005; Murray and Daszak 2013). In this chapter, we (1)  illustrate what is currently known about these linkages, focusing on the influence of human-​d riven ecological changes on host diversity and disease risk, (2)  propose a new hypothesis on potential host and pathogen responses to habitat fragmentation, and (3)  provide recommendations on long-​term studies and research efforts to improve current understanding of these relationships,

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Conserving Biodiversity

with potential implications for both biodiversity and human health.

Effects of Fragmentation on Hosts

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Fragmentation of tropical forests has been described as the single greatest threat to global biodiversity (Laurance 1999). Habitat fragmentation L INKS BE T WEEN L AND-​U SE is the landscape-​level process by which habitat loss CHANGE, BIODI VERSI T Y, AND results in the alteration of previously large, continuDISEASE ous habitat into spatially separate, smaller patches During the last half-​century, human activities surrounded by a matrix of altered habitat (Didham have rapidly transformed most of the Earth’s natu- 2010). Although recent studies have confirmed the ral systems (Myers et al. 2013). Significant changes importance of fragment area, shape, and isolation in land use are occurring currently, particularly in in predicting species responses (Ewers et al. 2007; developing, tropical forest countries (Lambin and Prugh et al. 2008; Watling et al. 2011), growing eviMeyfroidt 2011). It is estimated that annual forest dence suggests that the composition and structure loss has averaged 2,101 km 2/​year across the trop- of the matrix is also important in determining how ics between 2000 and 2012, and is increasing glob- species are distributed in fragmented landscapes. Research suggests that the decline and extincally (Hansen et al. 2013). Much of this forest loss tion of vertebrate populations due to fragmentation can be attributed to growing global demand for can be variously attributed to habitat change (e.g., food and natural resources (Cohen 2003; DeFries loss, degradation, edge effects, and isolation), alet  al. 2010). In extent, the most significant form tered species interactions (predation, parasitism), of land-​u se change is the expansion of crop and changed behavior (e.g., edge avoidance, disrupted pastoral lands, which continue to have serious dispersal), introduced species or pathogens, and negative long-​term consequences for the conserstochastic threats (e.g., temperature, weather) vation of global biodiversity (Phalan et  al. 2013), associated with small population size. Further, as agricultural expansion has largely come at the landscape-​ l evel studies have demonstrated that, expense of intact forests (Lambin and Meyfroidt across taxa, species responses to fragmentation and 2011). In fact, in the 30 years following 1950, more disturbance are often species-​ s pecific, sensitive land was converted to cropland than during the 150  years between 1700 and 1850. Today, more to spatial and temporal scales (Ewers and Didham than one-​q uarter of Earth’s terrestrial surface has 2006)  and are strongly molded by the characterbeen converted to agricultural systems (Hassan istics of the prevailing landscape matrix (Ewers and Didham 2006). Gibson et al. (2011) found that et al. 2005). With the exception of the last remaining ex- mammals tended to be less sensitive to disturbances panses of tropical forest in the Amazon and Congo compared to other taxonomic groups such as birds, basins, most tropical landscapes now typically com- and in several cases actually benefited from disturprise a mixture of human-​modified landscapes that bances. This discrepancy, largely attributable to include remnants of old-​growth and secondary-​ higher mammal abundance in certain disturbance growth forests, logged forests, agroforestry systems, types, may be explained by the high level of toleragricultural land and plantations, and urban areas ance to degraded forests displayed by some small (Gardner et al. 2009). In many tropical countries, mammals, particularly rodents and bats. Yet, overthese landscapes are comprised of small, irregularly all, forest conversion and habitat degradation have shaped patches that are highly prone to habitat-​edge been shown to consistently reduce biodiversity in effects (Laurance and Bierregaard 1997; Hill and tropical forest ecosystems and negatively affect Curran 2003). For example, in Brazil, more than tropical biota (Gibson et al. 2011). The general effects of land-​use change on eco80% of remaining Atlantic forest exists in small logical communities include predator loss, decline fragments (