Habitat modification effects on anuran food webs in the Colombian tropical dry forest

Abstract

Habitat loss and transformation are major threats to biodiversity and ecosystem functioning, but their effects on species interaction are often poorly understood. We evaluated effects of habitat transformation and seasonality on anuran-prey food webs in Colombian dry-forests. We asked whether anthropic transformation (anthropic vs natural) and/or seasonality (dry, minor and major rain seasons) affect predator load on arthropods, the occurrence of energetic bottlenecks, and the diet overlap of anurans. We selected six dry forest sites in the Caribbean of Colombia, sampled anurans, and identified their stomach contents to construct anuran-prey food webs. We show that the global structure of food webs was affected by disturbance and seasonality, but not by their interaction. Prey vulnerability was higher in anthropic habitats. Habitat transformation enhanced diet overlap among predators, but there was not a differential effect of habitat type according to seasonality for network metrics. Our study shows a strong effect of natural vegetation modification in tropical dry forest on anuran-prey food webs, while seasonality did not seem to further mediate these effects.

Introduction

Ecological communities are connected by direct and indirect associations among species, shaping complex networks of interactions (Lang et al., 2014), whose topology departs from randomness as a consequence of different evolutionary, ecological, and neutral processes (Akin and Winemiller, 2006; Vázquez et al., 2009). Habitat loss and human-driven modification of forests are major threats to biodiversity and ecosystem functioning (Sala et al., 2000; Hooper et al., 2012), but their effects on species interactions can be difficult to describe (Laliberté and Tylianakis, 2010; Gagic et al., 2012; Rivera Vasconcelos et al., 2019). The ways in which species are affected by anthropic disturbances may dictate changes in food web structure; for example, species with few links (i.e., specialists) are more extinction prone than species with several links (i.e., generalists) (Cagnolo et al., 2009; Visser et al., 2011). Consequently, loss of specialists in food webs after anthropic disturbance events may lead to more connected networks (Valladares et al., 2012). Moreover, the loss of species and their interactions may concentrate energy fluxes into fewer links, leading to a reduction in the evenness of interaction frequency (Wootton et al., 1996; Tylianakis et al., 2007; O'Gorman et al., 2012). Studies evaluating effects of human-driven changes in habitat on terrestrial food webs often report reductions in network size and interaction evenness, as well as shortening of food chain lengths (e.g., Tylianakis et al., 2007; Valladares et al., 2012; Muhly et al., 2013).

Land-use change usually reduces the structural complexity of forests (Barlow et al., 2010). In simplified habitats, diversity of micro-habitats and amount of available space is reduced and resilient species tend to co-occur more often (Kay et al., 2017; Zarnetske et al., 2017). Species forced to co-occur consume available prey items, resulting in an increased trophic niche overlap (López et al., 2015; Kuhnen et al., 2017; Smith et al., 2018). High levels of trophic overlap could increase competition, which would affect species' fitness (Sebastián et al., 2015; Buxton and Sperry, 2016; Namukonde et al., 2018).

Disturbance effects on communities could be exacerbated by climatic events. Seasonality has a strong influence on species interaction dynamics and, consequently, in energy flux within an ecosystem (Woodward and Hildrew, 2002; McCann et al., 2005). In ecosystems with strong seasonality (e.g., with rainy and dry seasons), population sizes fluctuate according to temperature and precipitation (Winemiller, 1990; Winemiller and Jepsen, 1998). When prey populations decline, food webs may experience bottlenecks of energy flows, increasing susceptibility to disturbance events (Dunne et al., 2002; Peralta-Maraver et al., 2017). Evidence reflects seasonal changes in consumption patterns (Frauendorf et al., 2013; Santos et al., 2004) and increased trophic width (Santos et al., 2004) for amphibian species during the rainy season.

Anurans are prevalent components of tropical food webs as predators of many types of prey (Vitt and Caldwell, 2014; Toft, 1980a, Toft, 1980b, Toft, 1981). They typically are classified as generalist predators, yet show some degree of selectivity, such as Dendrobatidae and Microhylidae species which prefer to consume ants and termites (Caldweel, 1996; Lotters et al., 2007; Berazategui et al., 2007; Blanco-Torres et al., 2015). As with other taxa, anuran diet is mostly associated with morphological, physiological, and behavioral traits of individuals (Parmelee, 1999; Stuart et al., 2008; Solé and Rödder, 2010; Vitt and Caldwell, 2014); less is known about effects of habitat transformation on interactions. These changes could, in turn, be mediated by climate-driven events affecting phenology, as well as abundance and diversity of prey (Sherwood et al., 2002; Palacios-Vargas et al., 2007; Pizano and García, 2014).

Tropical dry forests in Colombia are one of the most endangered biomes of the world, with >90% of original cover lost due to anthropogenic activities (Pizano and García, 2014; Etter et al., 2017; Romero-Duque et al., 2019). Changes in land use are the major cause of anuran extinctions and have driven several species to be classified as endangered (Ernst and Rödel, 2008; Urbina-Cardona, 2008; Stuart et al., 2008). The transformation of forest habitats is important not only for ethical reasons, but also because the loss of species could affect ecosystem services. For example, anurans play an important role in pest control by consuming a wide range of arthropods (Valencia-Aguilar et al., 2013).

In this study, we evaluated how forest transformation and seasonality affects anuran prey diversity and the overlap of their trophic niches. We examined stomach contents of anurans foraging in human-disturbed habitats in which forest cover has been removed, and in paired pristine forest sites where original plant cover is largely intact. We hypothesized that food webs in disturbed habitats will be simpler than those of undisturbed ones due to the loss of species and fewer overall interactions; moreover, we hypothesized simplification of modified habitats will lead to higher diet overlap of predators. We also expected that these effects would be magnified by seasonality, leading to energetic bottlenecks in disturbed habitats during the dry season.