Effects on Selected Species Interactions

In recent years, bats have moved to the forefront of public attention, mostly as a result of accumulating evidence that they comprise important reservoir hosts for numerous zoonotic viruses (e.g., lyssaviruses, SARS, Ebola) that may pose a serious health risk to humans (Calisher et al. 2006; Hayman et al. 2013, Chap. 10). Recent studies have highlighted the urgency of gaining a better understanding of how habitat loss, land-use change and disturbance and an associated increase in bat–human interactions may, for instance, accelerate viral spillover (Peel et al. 2013). However, few studies to date have explored to what extent these stressors influence patterns of parasite and disease prevalence and transmission, as well as physiological stress responses in bats (Fig. 4.3b).

Cottontail et al. (2009) found that trypanosome prevalence in A. jamaicensis was significantly higher in fragmented sites than in continuous forest, linked to a loss of bat species richness and fragmentation-related changes in vegetation cover that may favor disease transmission. The negative relationship between trypanosome prevalence and bat species richness reflects the “dilution effect,” i.e., a situation in which high host species richness reduces parasite transmission if vectors feed on multiple host species that vary in their ability to contract, amplify, or transmit the pathogen (Ostfeld and Keesing 2012). In contrast, prevalence of hemoparasitic nematodes (Litomosoides spp.) showed no significant difference among habitats, probably as a result of greater host specificity (Cottontail et al. 2009). In another study, fragmentation affected the physiological condition of

A. obscurus, as evidenced by elevated hematocrit levels in forest fragments versus continuous forest, even though similar abundances in both habitats indicated a high degree of fragmentation tolerance. The opposite pattern was documented for A. jamaicensis, suggesting that abundance may in many instances be misleading as a metric of fragmentation sensitivity (Henry et al. 2007a). Pilosof et al. (2012) found a significant effect of anthropogenic disturbance on the abundance of ectoparasitic bat flies in three of four widespread Neotropical host bat species, whereby the direction of response differed among species. Species-specific roosting habits likely play a key role in mediating the effects of disturbance on parasite transmission. A study in Mexico found significantly lower prevalence of antirabic antibodies in non-hematophagous bats in disturbed agricultural areas (22.7 %) compared to relatively undisturbed dry forest sites (51.9 %), a pattern which may arise because of more frequent interspecies encounters in the undisturbed habitat (Salas-Rojas et al. 2004).

The important role of animalivorous, frugivorous, and nectarivorous bats in arthropod suppression, seed dispersal, and pollination in tropical ecosystems is widely acknowledged (Kunz et al. 2011). The degree to which such interactions are susceptible to habitat modification and disturbance is generally better understood for seed dispersal than for pollination or arthropod suppression. Mostly using fecal analysis or seed traps, numerous studies in various human-modified landscapes across the Neotropics have documented the quantity and diversity ofseeds carried by bats (mostly Carollia spp., Sturnira spp., Artibeus spp.) into a diverse range of disturbed habitats including pastures, agricultural areas, coffee plantations, and secondary forests (Medellín and Gaona 1999; Galindo-González et al. 2000; García et al. 2000; Aguiar and Marinho-Filho 2007; Hanson et al. 2007; Wieland et al. 2011; Castro-Luna and Galindo-González 2012b; GarcíaEstrada et al. 2012; García-Morales et al. 2012; Gorchov et al. 2013). Voigt et al. (2012) showed that bats of the genus Carollia were likely to carry seeds from midsuccessional forest into adjacent primary forest, suggesting that directionality of seed transfer between disturbed areas and undisturbed forest may change with forest recovery. Isolated fig trees in abandoned pastures are attractive for many frugivores and may function as regeneration nuclei that effectively facilitate forest recovery (Guevara et al. 2004). Overall, these studies provide little evidence for major disruptions of seed dispersal mutualisms in response to habitat fragmentation and disturbance, although minor effects were detectable. For instance, small frugivorous bats disperse fewer large seeds in small, disturbed compared to large, undisturbed forest patches (Melo et al. 2009), suggesting a negative impact of disturbance on the dispersal of larger-seeded trees. Although Old World fruit bats in some areas may disperse seeds of early successional species (Hamann and Curio 1999), seed input into deforested or degraded areas tends to be low in humanmodified landscapes in the Paleotropics (Duncan and Chapman 1999; Ingle 2003). Pteropodids generally play a much less significant role as dispersers of early successional plants compared to phyllostomids, but are important dispersers of late successional canopy trees (Muscarella and Fleming 2007). How habitat modification affects seed dispersal of large-seeded canopy trees by pteropodid fruit bats in Paleotropical forests requires further detailed study.

Research in fragmented Central American dry forest ecosystems found a decline in flower visitation rates, number of pollen grains deposited, and fruit set of certain bombacaceous tree species, suggesting that habitat disruption can impair the pollination services of nectarivorous phyllostomids, with negative consequences for plant reproductive success (Stoner et al. 2002; Quesada et al. 2003). However, effects were dependent on plant species (Quesada et al. 2004), making general predictions regarding the effects of habitat modification on the disruption of bat pollination difficult. Through its influence on bat foraging behavior, habitat disturbance may also limit pollen exchange between trees, leading to higher progeny relatedness in isolated trees relative to those in undisturbed forest (Quesada et al. 2013). In a fragmented landscape in tropical Australia, common blossom bats (Syconycteris australis) were high-quality pollinators of the rain forest tree Syzygium cormiflorum, as inferred based on pollen loads, visitation rates, and movement patterns (Law and Lean 1999). Nectarivorous bats often attain higher abundance in response to anthropogenic disturbance (see Sect. 4.5), suggesting that provisioning of pollination services may potentially be resistant and resilient to environmental perturbation.

Key research needs:

• Detailed studies that address the causal links between human-induced landscape change and bat physiological and immune responses, as well as disease susceptibility.

• Studies, particularly in the Paleotropics, that document the full dispersal

cycle—from seed deposition through germination, seedling establishment, and recruitment—and how it is affected by habitat alteration.

• Further studies across a range of pollinator and plant species, as well as frag-

mented landscapes with different degrees of connectivity, to directly relate behavior and movement of pollinators with reproductive success and gene flow of trees.

• Studies that address the extent to which arthropod suppression services are

affected by more intensive forms of habitat alteration and disturbance such as those associated with secondary forests, tree plantations, or cropland (see Wanger et al. 2014).

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