Artificial bat roosts did not accelerate forest regeneration in abandoned pastures in southern Costa Rica

Highlights

• We tested whether artificial bat roosts can accelerate forest succession in tropical pastures.

• Over 2 years, bats rarely used roosts in pastures, but they extensively used roosts in forest.

• Seed rain abundance increased logarithmically with frugivorous bat detections in roosts.

• But seedling recruitment did not increase with bat detections or seed rain abundance in 2 years.

• We conclude that artificial bat roosts did not accelerate succession in Costa Rican pastures.

Abstract

Artificial roosts have been proposed as a tool for augmenting bat populations and catalyzing tropical forest regeneration. In the best case scenario, roosts would attract seed-carrying bats (Family Phyllostomidae) into degraded pastures and form nucleating patches of native vegetation. We tested this scenario by monitoring 48 artificial roosts in pastures and adjacent forest fragments in southern Costa Rica over 2 years. Half of the pasture roosts were exposed to direct sunlight and half were affixed to 4-m living stakes of Erythrina poeppigiana (Walp.) O.F. Cook that provided shade. After 2 years, 94% of roosts in forest and 40% of roosts in pasture had been used by bats at least once – primarily for nocturnal feeding. Maximum daily temperature inside of roosts was the best microclimatic predictor of bat visitation. We identified at least five species of bats that visited roosts, including two frugivores (Carollia and Glossophaga spp.). Bat-mediated seed dispersal increased with the number of frugivorous bat detections at roosts, but seedling recruitment did not increase with either bat detections or seed abundance over a 2-year period. Given that bats rarely used roosts in pastures, and bat visitation did not increase seedling recruitment, our data suggest that artificial bat roosts did not accelerate forest regeneration in abandoned, premontane pastures in southern Costa Rica. This method could be refined by investigating alternative roost designs, barriers to seedling recruitment below roosts, improvement of roost microclimatic conditions in pastures, and ability of bats to detect roosts in different habitats.

Introduction

Tropical deforestation exacerbates climate change, undermines rural livelihoods, and disarticulates the most diverse terrestrial communities on the planet (Chhatre and Agrawal, 2009, Myers et al., 2000, Pan et al., 2011). Some 27 million hectares of tropical forest were cleared between 2000 and 2005, two-thirds of which were in Latin America (Hansen et al., 2008). The impacts of this forest loss can be partially mitigated through ecological restoration – the process of assisting the recovery of degraded ecosystems to their historic trajectories (SER, 2004, Lamb et al., 2005, Rey Benayas et al., 2009). Many degraded lands will regenerate naturally (Chazdon, 2003, Letcher and Chazdon, 2009), but when succession is arrested or time is of the essence, active intervention may be necessary to overcome barriers to recovery (Holl and Aide, 2011, Martínez-Garza and Howe, 2003).

Cattle pastures are ubiquitous throughout the tropics and frequently represent an endpoint in the process of land conversion following deforestation. As grazed hillsides become eroded and rural farmers seek opportunities in cities, these lands are often sold or abandoned (Rey Benayas et al., 2007). As such, pastures have become a focus in the literature on tropical forest restoration (Holl and Kappelle, 1999). Natural regeneration in pastures is limited by a suite of factors including sparse seed banks and seed rain, high seed predation, and poor germination, survival, and growth (Aide and Cavelier, 1994, Cubiña and Aide, 2001, Holl, 1999, Nepstad et al., 1996). Of these, seed rain is often considered a primary limitation because other barriers to establishment come into play only when seeds are present. Because the majority of Neotropical trees have seeds dispersed by animals (Howe and Smallwood, 1982), a challenge for practitioners is to increase animal visitation to areas with reduced habitat resources, stressful microclimate, and increased predation risk.

Standard restoration practice in tropical pastures is to plant trees. Tree planting is an effective strategy because it ameliorates multiple barriers to natural regeneration including seed limitation (Cole et al., 2010, Lindell et al., 2013) and seedling survival and growth (Cole et al., 2011). Establishing tree plantations, however, is expensive and can result in significant legacy effects, such as altered nutrient cycling and tree species composition compared to natural secondary forests (Celentano et al., 2011). As a result, many researchers are now exploring more low-cost, light-handed interventions to catalyze forest regeneration. These have included: bird perches (Aide and Cavelier, 1994, Holl, 1998a, Miriti, 1998, Zanini and Ganade, 2005), essential oils of bat-dispersed fruits (Bianconi et al., 2012), giant stakes (Zahawi, 2008), artificial bat roosts (Kelm et al., 2008), and applied nucleation (Holl et al., 2011).

Among these novel applications, artificial bat roosts are particularly promising. Neotropical fruit bats (family Phyllostomidae) are among the most important seed dispersers in fragmented and early successional ecosystems (Fleming, 1988, Galindo-González et al., 2000, Arteaga et al., 2006, Muscarella and Fleming, 2007, Mello et al., 2008), but deforestation and forest degradation threaten many populations (Fenton et al., 1992, Schultze et al., 2000, Hutson et al., 2001). Bats in deforested landscapes may be limited by shortages of food or suitable roosts, excessive pesticides, or persecution by humans (Mickleburgh et al., 2002, Evelyn and Stiles, 2003, RELCOM, 2009). Frugivorous Phyllostomids in Costa Rica use a variety of roost types including caves, hollow trees, vine tangles, human infrastructures, and foliage (Foster and Timm, 1976, Fleming, 1988, Fenton et al., 2000). The premise of the artificial roost strategy is that by provisioning suitable roosts for frugivorous bats, restoration practitioners may attract bats and overcome seed rain barriers in degraded pastures. In the only existing study on this method, researchers installed simulated tree cavities in forest fragments in northern Costa Rica (Kelm et al., 2008). Within a few weeks, up to 10 species of bats colonized the roosts in large numbers (up to ∼200 individuals per roost). These bats included several frugivores (Carollia and Glossophaga spp.), and seed rain around the roosts increased significantly compared to seed rain far from the roosts. It is still unknown whether artificial roosts outside of forest fragments will attract bats, or whether increases in seed rain actually translate to increased seedling establishment; a variety of studies demonstrate that seedling recruitment should not be taken for granted (reviewed in Reid and Holl, 2012).

The purpose of this experiment was to test whether artificial bat roosts can be used to accelerate forest regeneration in tropical pastures. To do so, we monitored bat activity, seed rain, soil nutrients, and seedling establishment at 48 artificial roosts in abandoned pastures and forests in southern Costa Rica over 2 years. Our experiment was designed to evaluate (1) whether bats will use artificial roosts in pastures; (2) whether bat activity in roosts increases seed rain and plant-available soil nutrients (N, P); and (3) whether increases in seed rain translate to greater seedling recruitment. We predicted that bats would prefer roosts with greater vegetation cover due to improved microclimate and that bat activity in roosts would increase seed rain and soil nutrients via guano deposition (Duchamp et al., 2010) but not seedling recruitment due to low seed germination and survival in pastures (Holl, 1999).