Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant–plant mutualistic networks in the Caatinga, a Brazilian dry forest

Abstract

Anthropogenic disturbance and climate change might negatively affect the ecosystem services provided by mutualistic networks. However, the effects of such forces remain poorly characterized. They may be especially important in dry forests, which (1) experience chronic anthropogenic disturbances (CADs) as human populations exploit forest resources, and (2) are predicted to face a 22% decline in rainfall under climate change. In this study, we investigated the separate and combined effects of CADs and rainfall levels on the specialization of mutualistic networks in the Caatinga, a seasonally dry tropical forest typical of north-eastern Brazil. More specifically, we examined interactions between plants bearing extrafloral nectaries (EFNs) and ants. We analysed whether differences in network specialization could arise from environmentally mediated variation in the species composition, namely via the replacement of specialist by generalist species. We characterized these ant-plant networks in 15 plots (20 × 20 m) that varied in CAD intensity and mean annual rainfall. We quantified CAD intensity by calculating three indices related to the main sources of disturbance in the Caatinga: livestock grazing (LG), wood extraction (WE) and miscellaneous resource use (MU). We determined the degree of ant-plant network specialization using four metrics: generality, vulnerability, interaction evenness and H '. Our results indicate that CADs differentially influenced network specialization: we observed positive, negative, and neutral responses along LG, MU and WE gradients, respectively. The pattern was most pronounced with LG. Rainfall also shaped network specialization, markedly increasing it. While LG and rainfall were associated with changes in network species composition, this trend was not related to the degree of species specialization. This result suggests that shifts in network specialization might be related to changes in species behaviour, not species composition. Our study highlights the vulnerability of such dry forest ant-plant networks to climate change. Moreover, dry forests experience highly heterogeneous anthropogenic disturbances, creating a geographic mosaic of selective forces that may shape the co-evolution of interactions between ants and EFN-bearing plants.

Anthropogenic disturbance and rainfall variation threaten the stability of plant–ant interactions in the Brazilian Caatinga

“…Mean annual rainfall ranged from 510 to 940 mm, representing almost a 50% variation in rainfall over a small geographic area. Past studies conducted in the same study area using the same plots and Worldclim data, showed strong effects of climate gradients on plant (Rito et al 2017) and ant (Arnan et al 2018b) communities, and in their interactions (Câmara et al 2018, Oliveira et al 2019. Thus, the Catimbau National Park provides an excellent opportunity to investigate the effects of rainfall variation on the stability of interaction networks.…”

“…1 (< www. Past studies conducted in the same study area using the same plots and Worldclim data, showed strong effects of climate gradients on plant (Rito et al 2017) and ant (Arnan et al 2018b) communities, and in their interactions (Câmara et al 2018, Oliveira et al 2019. We downloaded the dataset at 30 arc seconds resolution, and the mean annual rainfall at each plot was extracted using the 'maptools' package (Bivand and Lewin-Koh 2015) in the R software ver.…”

“…Despite the wide range of ecosystems where EFN-bearing plants interact with ants (Rico-Gray and Oliveira 2007), there is some evidence that this protective service is more effective in arid environments (Leal and Peixoto 2016). These human activities can threaten important ecosystem services provided by mutualists, such as ant-mediated seed-dispersal (Leal et al 2014) and plant protection against herbivores (Leal et al 2015, Câmara et al 2018. These human activities can threaten important ecosystem services provided by mutualists, such as ant-mediated seed-dispersal (Leal et al 2014) and plant protection against herbivores (Leal et al 2015, Câmara et al 2018.…”

“…However, the Caatinga is continuously degraded by human activities such as wood extraction, overgrazing by livestock (cattle and goats) and collection of non-timber forest products (Albuquerque et al 2007, Ramos and Albuquerque 2012, Ribeiro et al 2015, Arnan et al 2018a). These human activities can threaten important ecosystem services provided by mutualists, such as ant-mediated seed-dispersal (Leal et al 2014) and plant protection against herbivores (Leal et al 2015, Câmara et al 2018. In addition, the Caatinga is also threatened by climate change, with an increase of mean annual temperature between 1.7°C and 6.7°C and a reduction in rainfall of 22-40% predicted for the end of the twenty-first century (IPCC 2014).…”

Structural changes over time in individual‐based networks involving a harvester ant, seeds, and invertebrates

“…rainfall, temperature), seem to exert a great influence on plant species phenology, influencing the availability of plant-derived resources (López-Carretero et al, 2018) and, subsequently, the harvester ant diet (Belchior et al, 2012). For instance, in ant-plant networks mediated by the presence of extrafloral nectaries, rainfall increases the specialisation (the level at which species interact with more species) (Câmara et al, 2018), as well as network nestedness, which is also positively associated with temperature (Rico-Gray et al, 2012). Nestedness is an interaction pattern in which specialist species tend to interact with a core subset of interacting generalist species, which implies a reduction of effective interspecific competition and enhancement of species coexistence (Bastolla et al, 2009).…”