Intense mycorrhizal root colonization in a human-modified landscape of the Caatinga dry forest

Highlights

• Caatinga's abundant woody plants are widely colonized by AMF.

• Soil pH and rainfall are important modulating drives of colonization by AMF.

• AMF colonization frequency doesn’t respond to human disturbance in Caatinga dry forest.

Abstract

Arbuscular mycorrhizal fungi (AMF) symbioses are thought to help plants to cope with harsh environments and to affect not only plant fitness, but also ecological organization from population to ecosystem level. Here, we investigated to what extent this association was present, and what the major environmental drivers were in a human-modified landscape of the Caatinga dry forest in north-eastern Brazil. AMF spore density in the soil and the frequency of AMF root colonization were examined at the species and forest-stand level for the nine most abundant and widespread woody plant species in 18 forest plots across gradients of chronic anthropogenic disturbance, rainfall and soil attributes. Soil spore density was low (1.0 ± 0.6 spore/g soil) across all conditions. However, AMF were present across all species, and colonization frequencies were high (50%, on average) throughout the entire environmental gradients. At species level, AMF colonization frequency only responded to environmental variables (disturbance, rainfall, soil available phosphorus, soil organic matter and soil pH) in one species (Cnidoscolus pubescens). At forest-stand level, colonization frequency responded positively to both soil pH and rainfall, but not to chronic anthropogenic disturbance. Our results suggest AMF symbiosis is widespread among the plant species and ecological conditions in the Caatinga. Moreover, this symbiosis, which in this case was mediated by rainfall, is likely affecting the resilience of the Caatinga dry forest as it is associated with the most abundant and biomass-relevant forest species and in the harshest conditions for plant survival and reproduction (i.e. nutrient-poor soils and dry habitats).

Introduction

Human disturbances are reorganizing the biodiversity of tropical forests, causing impacts from population to ecosystem level, including forest dynamics and ecosystem resilience (Tabarelli et al., 2010, Malhi et al., 2014, García-Valdés et al., 2015). Human-driven disturbances include the continuous removal of small portions of aboveground forest biomass via, for example, firewood collection, exploitation of non-timber forest products and livestock grazing (i.e. chronic anthropogenic disturbance, sensu Singh, 1998) by forest-dependent people. This removal of forest biomass can result in more open forest habitats with hotter and drier microclimates (e.g. Hardwick et al., 2015; Marengo and Bernasconi, 2015; Silva et al., 2019), depleted levels of soil nutrients and water content as well as increased compaction (Guadarrama et al., 2014; Schultz et al., 2016; Van der Heyde et al., 2017). Such harsh conditions or high-stress environments have been proposed to reorganise woody plant assemblages (Ribeiro et al., 2019), with cascading effects on biotic interactions (e.g. disruption of mutualisms) and the ecosystem functions and services they provide (Leal et al., 2014, Oliveira et al., 2019). In addition to chronic anthropogenic disturbances, several tropical biotas are currently experiencing significant impacts due to climate change. At organism level, changes in morphology, phenology and physiology have been observed as a result of climate change (Martínez-García et al., 2012, García-Valdés et al., 2015, Allen et al., 2017). Furthermore, changes in species distribution and abundance (Parmesan and Yohe, 2003, Mair et al., 2014), biotic interactions (Rubenstein, 1992, Martínez-García et al., 2012, Silva et al., 2019) and patterns of ecosystem functioning (Walther et al., 2002, Allen et al., 2017) have been also associated with climate change (Walther et al., 2002). Consequently, there has been increasing concern over the potential connections between local human disturbances and climate change, such as the emergence of physically harsher habitats and their cascading effects on biological organization (Hirota et al., 2011, Rito et al., 2017). For example, reduced rainfall has been a constant threat to seedling recruitment and plant performance across human-disturbed semiarid regions, where soil water availability is typically a limiting factor (Brodie et al., 2012, Santos et al., 2014, Allen et al., 2017, Ribeiro et al., 2019).

On the other hand, there is some evidence that symbioses between plants and arbuscular mycorrhizal fungi (AMF) could reduce some of the negative effects of human disturbance and climate change on plant establishment and performance (Violi et al., 2008, Uibopuu et al., 2009). AMF colonize the roots of approximately 80% of terrestrial plants (Smith and Read, 2008). By affecting performance of host plants, e.g. improving seedling survival (Miranda and Miranda, 2001), AMF symbiosis can influence not only plant community structure, but also patterns of ecosystem productivity, nutrient cycling and resilience (Van der Heijden et al., 2015). Indeed, AMF symbiosis may be crucial for plant establishment, especially in the face of soil water deficit, as AMF can increase the gain and transfer of water to the plant through the hyphae (Hardie, 1985, Ruiz-Lozano and Azcón, 1995). AMF symbiosis can also increase soil water retention properties (Augé, 2001, Rillig and Mummey, 2006), and improve osmotic adjustment (Augé et al., 1992; Kubikova et al., 2001; Ruiz-Lozano et al., 1995), increase gas exchange and water use efficiency (Augé et al., 1992, Ruiz-Lozano et al., 1995, Frosi et al., 2016b) and protect from oxidative damage generated by drought (Porcel et al., 2004, Porcel et al., 2003, Ruiz-Lozano et al., 2001). Finally, AMF may facilitate the establishment of plants in unfertile soils by increasing their capacity to absorb nutrients, especially phosphorus (Karanika, et al., 2008, Dostálek et al., 2013). In synthesis, AMF symbiosis may be crucial for plant establishment because it improves soil aggregation and promotes increased biomass and plant survival in habitats with limiting conditions (Rillig and Mummey, 2006, Violi et al., 2008, Frosi et al., 2016b, Pánková et al., 2018).

The Caatinga dry forest covers around 1 million km² in north-eastern Brazil and is the largest and most biodiverse seasonally dry tropical forest (SDTF) globally (Pennington et al., 2009, Silva et al., 2017). Similar to other SDTFs, the Caatinga supports dense rural populations, whose livelihoods are heavily dependent on the use of local natural resources; i.e. forest-dependent people (Silva et al., 2017). Additionally, the Caatinga biota is expected to experience a decline in rainfall of 22% by 2100 (IPCC, 2014). Increased human disturbance, low soil fertility (particularly in sandy soils) and reduced water availability, as well as frequent prolonged droughts as a result of declining rainfall, might favour AMF symbioses due to the harsher conditions imposed by these abiotic factors. Thus, verifying the extent to which AMF colonization is affected by disturbance, climate regime and soil conditions is essential to understand the importance of this association to the establishment of woody plants in the Caatinga dry forest. This is particularly relevant as AMF symbioses are essential for plant establishment and performance.

Here, we examined the relevance of AMF symbioses in a human-modified landscape in the Caatinga dry forest in north-eastern Brazil and their driving forces. More precisely, we assessed soil spore density at forest stand level and AMF root colonization across the nine most abundant woody plant species (i.e. species level) and at forest stand level across our focal landscape. In addition, we investigated the potential impacts of chronic anthropogenic disturbance, rainfall and soil attributes on these symbiosis-related attributes. We expected higher spore densities and frequencies of effective colonization as chronic human disturbance increased and soil fertility and rainfall decreased, because sporulation often increases under such stressful conditions (Zangaro et al., 2013), while AMF colonization would favour plant establishment and growth via better uptake of soil water and nutrients (Augé, 2001, Caravaca et al., 2003, Alguacil et al., 2011, van der Heyde et al., 2017). Finally, we discuss the uncovered patterns in light of the drivers of these symbioses and their ecological relevance, including for the resilience of the Caatinga dry forest.