Intense mycorrhizal root colonization in a human-modified landscape of the Caatinga dry forest
Graphical abstract
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.
Section snippets
Study site
The study was conducted in the Catimbau National Park, a 607-km2 protected area in north-eastern Brazil (Fig. 1). The regional climate is semiarid and is classified as BSh, transitioning to rainy tropical (As') in some areas (Köppen system). Mean annual rainfall varies markedly in the Catimbau, from 1100 mm in the south-east to 480 mm in the north-west, with a mean annual temperature of 23 °C (Rito et al., 2017). Approximately 70% of the park landscape is covered by naturally impoverished
AMF spore density in the soil
Across plots, soil AMF spore density ranged from 0.31 to 2.03 spores/g (~7 fold variation) and averaged 1.0 ± 0.6 spores/g. Spore density at the plot level was not correlated with disturbance, rainfall, or soil available phosphorus, pH or organic matter content (GLM, p > 0.15). It was not revealed any significant relationship between the abundance of focal species and spore density by either CCA or GLM analyses.
AMF root colonization
At species level, AMF mycorrhizal structures, such as spores, hyphae and vesicles,
Discussion
Our results suggest that soils in human-modified landscapes of the Caatinga dry forest support variable, but relatively low AMF spore densities. In contrast to our expectation, spore density was not affected by chronic anthropogenic disturbance, rainfall or soil attributes. Despite these relatively low spore densities, AMF symbiosis appear to be widespread in such landscapes as all our focal species exhibited some level of root colonization. Disturbance, rainfall and soil attributes appear to
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - Brazil) (PELD process 403770/2012-2 and Universal process 470480/2013-0), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Brazil) (Finance Code 001 and PROBRAL CAPES-DAAD process 99999.008131/2015-05) and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE - Brazil) (APQ/PRONEM - 0336-2.03/14). S. Pereira thanks CAPES for doctorate scholarship in
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2022, Journal of Arid EnvironmentsCitation Excerpt :However, only 2% of the former range of tropical dry forest remains intact (Buzzard et al., 2016). Compared with humid forests, few areas of tropical dry forest have protected status, which is of particular concern, given that these forest areas tend to have high levels of human habitation and subjected to recurrent human activities that potentially contribute to losses in biomass and biodiversity, such as the cutting of wood and shrubs for firewood, use in fence construction, and fodder for cattle and goats (Espírito-Santo et al., 2009; Pereira et al., 2020). These activities typical result in the clearing of forest vegetation and development of open areas that, having been exploited for crop cultivation and livestock grazing, are generally abandoned, thereby initiating the process of ecological succession (Coelho et al., 2017).
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2021, Forest Ecology and ManagementCitation Excerpt :Similar to many Caatinga native species, it is capable of germinating over a wide temperature range (from 11.6 °C to 55.4 °C), allowing it to germinate even in the face of an increase in temperature caused by climate change (Gomes et al., 2019). C. microphyllum was selected as our study model because: (1) it is abundant across a variety of habitats in our focal landscape (Rito et al., 2017; Souza et al., 2019), (2) it is frequently adopted by locals to restore Caatinga vegetation, and (3) it belongs to Fabaceae, the most species-rich family in the Caatinga dry forest which is known to be frequently associated with AMF (Bonfil and Trejo, 2010; Frosi et al., 2016b; Pereira et al., 2020). Viable seeds were acquired from the Rede de Sementes do Projeto de Integração do São Francisco – Núcleo de Ecologia e Monitoramento Ambiental (NEMA/UNIVASF) at the Universidade Federal do Vale do São Francisco.