Chronic anthropogenic disturbances and aridity negatively affect specialized reproductive traits and strategies of edible fruit plant assemblages in a Caatinga dry forest

Highlights

• Chronic anthropogenic disturbances and aridity pose negative or positive effects on reproductive traits of edible fruit assemblages in a Caatinga dry forest.

• Seventy-five percent of the edible fruit species have specialized reproductive strategies that are negatively affected by chronic disturbances and/or aridity.

• Chronic disturbances and aridity negatively affect specialized reproductive traits and strategies of edible fruit assemblages.

• Aridity mediates the effects of chronic disturbances mainly on the abundance of specialized reproductive strategies of edible fruit assemblages.

• The functional diversity of specialized reproductive strategies of edible fruit assemblages was negatively affected by aridity.

Abstract

Chronic anthropogenic disturbances and climate change are the main threats to biodiversity, acting as potential drivers of assembly reorganization in human-modified tropical landscapes. We aimed to understand how the reproductive traits of edible fruit plant assemblages respond to chronic disturbances and aridity in the Caatinga, a dry forest in northeastern Brazil housing a human population that greatly depends on natural resources for subsistence and is threatened by increasing aridity. The study was carried out across 20 permanent plots of Caatinga, covering gradients of chronic disturbances (livestock grazing, wood extraction and non-timber product exploitation) and aridity (1051 mm to 664 mm). We registered 24 native plant species with fruits that are edible for humans, which were classified according to their flowering/fruiting pattern, floral size and reward, sexual and reproductive systems, pollination systems, and fruit types. They were also grouped into two categories of reproductive strategies (generalists and specialists). We documented that chronic disturbances and aridity pose more negative than positive effects on the reproductive traits of edible fruit plants in terms of trait richness (negative: 29% of the traits; positive: 3.2%) and abundance (negative: 19.3%; positive: 3.2%). In general, we observed that 79.2% of the studied species had at least one reproductive trait that was negatively reduced by increased chronic disturbance and/or aridity in terms of trait richness and abundance. Overall, 75% of the edible fruit species have specialized reproductive strategies that were negatively affected by chronic disturbances and/or aridity. Specifically, individual or combined effects of chronic anthropogenic disturbances or aridity negatively impacted the richness and abundance of specialized reproductive traits such as supra-annual flowering and fruiting patterns and obligatory cross-pollinated edible fruit species. Also, in terms of richness, the reproductive functional diversity of specialized reproductive strategies was negatively affected by increasing aridity. Our findings indicate that in the expected future scenarios of increased land-use and climate change, the Caatinga could face a collapse in the offer of edible fruits to local human communities by impacting the provision of this ecosystem service.

Introduction

Plant community organization in human-modified landscapes is a key ecological issue for ecosystem functioning that has been widely studied in tropical forests (e.g., Carreño-Rocabado et al., 2012, Carreño‐Rocabado et al., 2016; Ribeiro et al., 2015, Ribeiro et al., 2016, Ribeiro et al., 2019, Ribeiro-Neto et al., 2016, Zorger et al., 2019). Anthropogenic disturbances and climate change are the main threats to plant communities as they reorganize the functional profile of species assembly, affecting community functioning and the provision of ecosystem services (e.g., Carreño‐Rocabado et al., 2016, Ribeiro et al., 2019, Silva et al., 2020a,b). Therefore, the responses of plant community functional traits to human-driven environmental changes emerge as an important approach to identify the underlying mechanisms responsible for the biological impoverishment and biotic homogenization of assemblages along environmental gradients (e.g., Ribeiro et al., 2015, Ribeiro et al., 2019, Silva et al., 2020a, Zorger et al., 2019). In this context, community-level changes in the functional traits of organisms in disturbed habitats have implications for forest resilience due to several effects on the provision of ecosystem functioning and ecological services (Carreño‐Rocabado et al., 2016, Ribeiro et al., 2019, Sfair et al., 2018, Silva et al., 2020a,b).

Isolated or combined effects of chronic anthropogenic disturbances (i.e. firewood collection, non-timber products exploitation, livestock farming, hunting) and aridity (i.e. water deficit) impacting both plant and animal populations and human communities have been documented in seasonally dry tropical forests (e.g., Arnan et al., 2018a, Arnan et al., 2018b, Arroyo-Rodríguez et al., 2015, Martorell and Peters, 2005). For instance, chronic disturbances and aridity were accountable for reducing the functional diversity of woody plants (e.g., Rito et al., 2017a, Rito et al., 2017b, Sfair et al., 2018, Silva et al., 2020b) and ants (Arnan et al., 2018a). Also, the reproductive functional diversity of specialized strategies is reduced by increasing chronic disturbances and aridity (Silva et al., 2020b), which is expected, given that specialized traits are more sensitive to disturbance and climate change than generalists (Girão et al., 2007, Lopes et al., 2009, Silva et al., 2019, 2020b). In some cases, considering, for instance, the plant diversity and plant reproductive traits, the effects of increasing aridity may exacerbate the consequences of chronic disturbances (Gibb et al., 2015, Rito et al., 2017a, Silva et al., 2020b), and could aggravate the disruption of plant-animal interactions (Câmara et al., 2019, Silva et al., 2020b). From this perspective, chronic disturbances and aridity are potential drivers that shape community assembly, exerting negative effects on biological diversity at the functional level, favoring the process of biotic homogenization (Ribeiro et al., 2015, 2019) and affecting key mutualistic interactions that are critical to ecosystem functioning and services, such as seed dispersal and pollination (e.g., Kiers et al., 2010, Leal et al., 2014, Memmott et al., 2007, Oliveira et al., 2019, Vilela et al., 2018).

Plant-animal interactions play a critical role in pollination and seed dispersal (Jordano, 1987, Ollerton et al., 2011). In particular, mutualistic interactions are important for biodiversity organization and provision of ecosystem services (e.g. Bascompte and Jordano, 2007, Ipbes, 2016). Ecosystem services refer to all nature’s benefits to people, providing quality of life and well-being for humans worldwide (IPBES, 2016). Therefore, the offering of edible fruits is a good example of nature’s gifts [as a holistic valuation of ecosystem services (IPBES, 2016)] to local human communities (e.g., Díaz et al., 2018, Mensah et al., 2017, Paz et al., 2021). As many local communities inhabiting dry forests are poor and highly dependent on natural forest products for livelihood and food, the availability of edible fruits emerges as an ecosystem service that provides a richer, more nutritious diet (e.g., Chaves et al., 2017, Nascimento et al., 2013). However, depending on the intensity, human actions on natural habitats could erode the quality of life of people by reducing nature’s capacity to provide some ecosystem process, such as pollination (Diaz et al., 2019), a crucial plant-animal interaction that many plants species rely on to set fruits (Klein et al., 2007, Ollerton et al., 2011, Paz et al., 2021). Anthropogenic disturbances negatively impact both plant and pollinator diversity (Potts et al., 2010, Tilman and Lehman, 2001), thus affecting pollination and reducing food production (including edible fruits), and risking the food security of indigenous and local communities (e.g. Diaz et al., 2018, 2019; IPBES, 2016).

The Caatinga is the largest continuous expanse of seasonally dry tropical forest on Earth (Silva et al., 2017). It houses a population of approximately 29 million people that greatly depend on natural resources (Silva et al., 2017), forcing local human populations to use animals and plants for their subsistence (Albuquerque et al., 2017, Monteiro et al., 2010). Although family farming is predominant in local communities, the collection of wild food is widely acknowledged (e.g., Albuquerque and Andrade, 2002, Chaves et al., 2017, Cruz et al., 2013, Nascimento et al., 2013, Nunes et al., 2018). The ethnobotanical knowledge of food plants used by local communities reveals more than 50 plant species native to Brazil and occurring in the Caatinga dry forest that are reported as human food sources (Jacob et al., 2020a, Jacob et al., 2020b); this number rises to 129–169 when exotic species are included. Considering only native species, 75% offer fruits and/or seeds that are palatable and consumed by humans (Jacob et al., 2020a, Jacob et al., 2020b, Nascimento et al., 2013). However, the continuous exploitation of natural resources by local communities and the increasing aridity could jeopardize this important service (i.e., edible fruit offering). The major sources of chronic disturbances in the Caatinga are livestock grazing, wood extraction for houses and fences, firewood and charcoal, exploitation of non-timber forest products, and slash-and-burn agriculture (Arnan et al., 2018b, Rito et al., 2017a, Silva et al., 2017). Additionally, the Caatinga dry forest is one of the six ecosystems most vulnerable to climate variability (Seddon et al., 2016), with climate models indicating that it will likely experience a 22% reduction in rainfall and a 3–6 °C increase in temperature by 2100 (IPCC-Intergovernmental Panel on Climate Change, 2014, Magrin et al., 2014). Nevertheless, the isolated and combined effects of chronic disturbances and aridity on the reproductive traits of plant species with edible fruits in the Caatinga dry forest and the impacts of these drivers on ecological services remain unknown.

Here, we aim to understand the isolated and combined effects of chronic disturbances and aridity (i.e., water deficit) on the composition and diversity of reproductive traits and strategies of edible fruit plants. We first report the abundance and richness of reproductive traits of plants with edible fruits in a Caatinga dry forest, then we test the general hypotheses that individual and combined increases in chronic disturbances and aridity levels negatively impact reproductive traits and strategies of those plants due to higher human exploitation and reduction in productivity associated to higher levels of aridity. Specifically, we expect that (1) both increasing chronic anthropogenic disturbances and aridity reduce the abundance, richness and functional diversity of reproductive traits and strategies, (2) there are also combined effects of chronic disturbances and aridity, so that the disturbance effects are contingent on the level of aridity and (3) specialized reproductive traits and strategies are more negatively affected by chronic anthropogenic disturbances and aridity.