General Conclusions and Future Research Directions

As a consequence of a rapid increase in the annual number of publications over the past quarter century, ecological understanding has broadened and deepened concerning the influence of land conversion and habitat fragmentation on tropical bats at the level of populations, ensembles, and assemblages. Nonetheless, large geographic and taxonomic biases characterize current understanding.

Although many studies document that human-induced changes in land use alter bat species abundances and taxonomic dimension of biodiversity, surprisingly few studies have explored how these changes manifest with regard to genetic, behavioral, physiological, or disease-related phenomena. Similarly, little is known about the way in which land-use change affects functional or phylogenetic dimensions of biodiversity (but see Cisneros et al. 2015). Studies generally are not conducted in a spatially explicit manner (Fig. 4.4a), so multiscale (e.g., alpha, beta, and gamma diversities) or cross-scale interactions cannot be explored fully, and conclusions must be tempered in the absence of a more integrated understanding of the role of unmodified habitat in rescuing local populations from extinction. Key insights from landscape-scale studies comprise the speciesand ensemble-specific nature of responses, as well as their dependence on spatial scale. The most fundamental developments include the recognition that habitat fragmentation is a complex process involving the nature of patches (i.e., landscape composition and configuration), as well as the nature of the matrix that arises as a consequence of direct, human modifications of the landscape (Fig. 4.4b). Finally, the consequences of changes in the bat fauna from habitat conversion and fragmentation have not been

Fig. 4.4 Two conceptual models that indicate the pathways whereby land-use changes affect bats in ways that a are not spatiotemporally explicit or b are spatiotemporally explicit. In both scenarios, effects of land-use change are mediated by alterations in the vegetation, but the underlying mechanisms differ (contrast the purple boxes with the blue boxes). Nonetheless, populations and assemblages of bats respond via similar mechanisms associated with feeding, roosting, and movement opportunities (green boxes). Generally, studies that explore the effects of habitat conversion (e.g., effects of logging or agriculture) on bats are not spatially explicit. Land-use change is reflected in habitat conversion that directly alters the composition and structure of the vegetation, with effects on the abundance and distribution of food resources or roosts, and the existence of “flyways” whereby bats navigate through the forest. In concert, these three characteristics affect the population dynamics of different bat species and the interaction likelihoods among species (e.g., bat species, other animal species, and disease-causing microorganisms). As a consequence, changes in bat species abundance distributions (e.g., richness, evenness, dominance, diversity, rarity) emerge with cascading effects on the vegetation as a consequence of altered seed dispersal, pollination, or regulation of insect herbivores. Generally, studies of habitat fragmentation are spatially explicit and explore how land-use change affects a focal habitat type (e.g., forest) by creating a network of patches embedded in a matrix of human-modified habitats. Such studies have the potential to explore how patch characteristics (e.g., landscape composition and configuration of forest patches) as well as matrix characteristics (e.g., structural or compositional attributes of the converted land) interact to affect the bat fauna. See text for additional details

quantified with regard to the maintenance of vital ecosystem processes or services. Clearly, we are still far from a comprehensive understanding of how tropical bats respond to habitat modification.

To advance ecological understanding, we have highlighted a number of more specific research needs across all themes in this chapter. We further stress the following key research directions as particularly worthy of pursuit, many of which have been summarized in different context for mammals in general (e.g., Willig 2001).

1. Geographic and taxonomic biases toward the Neotropics and a focus on just one bat family, Phyllostomidae, need to be overcome. Although research efforts in Southeast Asia are gaining momentum (Kingston 2013), Africa deserves greatly intensified research activities. As technological advances now make acoustic sampling of aerial insectivorous bats increasingly timeand costefficient, this ensemble should regularly be targeted in ecological research, including environmental impact assessments.

2. Research should be broadened to encompass the full spectrum of possible responses at the level of populations, ensembles, assemblages, and metacommunities. Novel mechanistic insights could be gained by studies that assess behavioral responses to particular types of habitat conversion or habitat fragmentation. Similarly, studies are needed to investigate physiological and immune responses, as well as disease susceptibility across a broad range of host and vector species. A better understanding of the genetic effects on bats from habitat modification requires integrated research on a suite of different species that explore the link between patterns of genetic variation and species' ecological and life-history traits. In general, the way in which species traits and

environmental factors interact to shape species responses to landscape change is unclear, as trait-based approaches have been rare (but see Farneda et al. 2015). Understanding how functional and phylogenetic biodiversity changes during habitat conversion and secondary succession is investigated rarely and remains poorly understood. Much also remains to be learned about how habitat disruption and modification affect the provisioning of critical ecosystem services, especially flower pollination and arthropod suppression.

3. Multiscale studies provide a more comprehensive understanding of pattern–process relationships in heterogeneous human-modified landscapes than do single-scale assessments. Future research should address bat responses to landscape change with respect to both spatial and temporal dimensions. Considerable progress in the field could be made by directing greater research effort and resources toward long-term studies that are capable of unveiling novel insights, which are hard or impossible to obtain from short-term, crosssectional studies (cf. Lindenmayer et al. 2011). Studies currently underway at the Biological Dynamics of Forest Fragments Project (BDFFP) in Brazil (Meyer et al, unpublished data) or at the Stability of Altered Forest Ecosystems (SAFE) Project in Borneo (e.g., Struebig et al. 2013) provide examples of first efforts in this direction. The need for broader geographic coverage notwithstanding, directing more research to well-studied systems or long-term study sites, allows the responses of bats to land-use change to be compared to those of other taxa (e.g., Barlow et al. 2007; Bicknell et al. 2015; Ewers et al. 2015).

4. We stress the importance of robust study designs for assessing faunal responses to habitat alteration. Studies should have adequate replication (cf. Ramage et al. 2013) and involve controls or reference sites. Lack of controls is an important shortcoming of many of the reviewed studies, which often focused on comparisons of different types of disturbed habitats. This clearly limits their ability to ascribe observed effects to disturbance. We echo Kingston's (2013) call for studies to collect predisturbance, baseline information whenever possible, given that tropical bat assemblages exhibit considerable spatiotemporal variability even in unmodified habitats. In this context, Before–After–Control– Impact designs (e.g., Bicknell et al. 2015), in which sites affected by human disturbance are compared with undisturbed reference sites, both before and after impact, enhance inferential strength (Smith 2013), and add scientific rigor to future assessments of the effects of habitat modification on tropical bats.

Finally, an improved ecological understanding of bat responses to land-use change will be of little use to society unless it can be translated into improved management practices that ensure their long-term conservation and provision of critical ecosystem services. Across all themes in this chapter, we urge bat researchers to apply more of their science to policy and management questions. Examples of such applications include the effectiveness of specific management practices (e.g., farming intensity, cutting cycles) and mitigation measures (e.g., riparian conservation set-asides, artificial roosts).

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