Effects of forest fragmentation on the plant‐soil‐microbial interactions

Tesis doctoral inédita leída en la Univerisdad Autónoma de Madrid, Facultad de Ciencias, Departamento de Ecología. Fecha de lectura: 23-06-2015Forest fragmentation implies profound ecological transformations worldwide, mainly threatening aboveground biodiversity. However, the complex impacts of forest fragmentation on ecosystem processes are not yet well understood, especially taking into account their interactions with other global change drivers such as the increasing drought, particularly relevant in the Mediterranean area. The interaction of the soil‐microbial system with the standing plants is crucial to fully understand the effects of forest fragmentation over ecosystem processes. The main objective of this thesis is to understand the impacts of forest fragmentation on the edaphic properties and on the structure of soil microbial communities, as well as on their capacity to decompose and metabolize soil organic matter. To fulfill this objective we have used different methodological approaches to study the physicochemical characteristics of soils and the structure and function of soil microbial communities, as influenced by holm oak trees and seedlings. The study has been carried out in fragmented holm oak forests immersed in an active agricultural matrix and located in two climatically different regions of Spain. We have also focused on the functional responses of the plant‐soil‐microbial system to drought, the most important climate change‐related threat in Mediterranean ecosystems. Our results point out to a high complexity of the plant‐soil‐microbial system and reveal important responses of this system to forest fragmentation. Additionally, we have found a differential responsiveness of the soil‐plantmicrobial system to drought, depending on both the physicochemical characteristics of soils and the historical adaptation of soil microbial communities to specific bioclimatic conditions. We found that forest fragmentation has direct effects over the microbial community (structure and diversity), and indirect effects over the soil‐microbial functioning (soil respiration, enzymatic activities and metabolic profile) mediated through the influence of the tree size, which triggers in turn a cascade of causaleffect relations that stimulates soil microbial activity. Moreover, the interaction found between drought and fragment size suggests that depending on the local bioclimatic conditions, forest fragmentation could ameliorate to some extent the negative effect of drought by increasing the fertility and water holding capacity of soils, especially in soils with historic adaptation to droughtLa fragmentación del hábitat implica profundas transformaciones ecológicas en todo el mundo, amenazando principalmente la biodiversidad de las comunidades sobre el suelo. Sin embargo, el complejo impacto de la fragmentación de los bosques en los procesos ecosistémicos todavía no se comprende bien, especialmente tomando en cuenta las interacciones con otros motores de cambio global como el incremento de la sequía, particularmente relevante en los ecosistemas Mediterráneos. La interacción del sistema suelo‐microorganismos con las plantas es crucial para entender los efectos de la fragmentación del bosque sobre los procesos del ecosistema. El principal objetivo de esta tesis es comprender los impactos de la fragmentación del bosque en las propiedades edáficas y en la estructura de las comunidades microbianas del suelo, así como en su capacidad de descomponer y metabolizar la materia orgánica del suelo. Para cumplir con este objetivo se han utilizado diferentes enfoques metodológicos para estudiar las características físico‐químicas del suelo y la estructura y funcionalidad de las comunidades microbianas del mismo, así como la influencia de árboles y plántulas de encinas. El estudio ha sido llevado a cabo en encinares fragmentados inmersos en una matriz agrícola activa, y localizados en dos regiones climáticamente distintas de España. También nos hemos centrado en la respuesta funcional del sistema plantasuelo‐ microorganismos a la sequía, la amenaza relacionada con el cambio climático más importante en los ecosistemas Mediterráneos. Nuestros resultados señalan la elevada complejidad del sistema planta‐suelomicroorganismos y revelan respuestas importantes de este sistema a la fragmentación de los bosques. Adicionalmente, hemos encontrado una respuesta diferencial del sistema planta‐suelo‐microorganismos a la sequía, dependiendo tanto de las características físico‐químicas del suelo y de la adaptación histórica de las comunidades microbianas a condiciones bioclimáticas específicas. Hemos encontrado que la fragmentación del bosque tiene efectos directos sobre la comunidad microbiana (estructura y diversidad), y efectos indirectos sobre el funcionamiento del sistema suelomicroorganismos (respiración del suelo, actividades enzimáticas y perfil metabólico) mediadas a través de la influencia del tamaño del árbol, que desencadena a su vez una cascada de relaciones causa‐efecto que estimula la actividad microbiana del suelo. Además, se ha encontrado una interacción entre sequía y tamaño del fragmento que sugiere que, dependiendo de las condiciones bioclimáticas locales, la fragmentación de los bosques podría aminorar, hasta cierto punto, el efecto negativo del aumento de las sequías mediante el incremento de la fertilidad y la capacidad de retención del agua de los suelos, especialmente en aquellos suelos con adaptación histórica a la sequía.Este trabajo ha sido realizado gracias a la financiación proporcionada por los proyectos VULGLO (CGL2010 22180 C03 03), MyFUNCO (CGL2011‐29585‐C02‐02) y VERONICA (CGL2013‐42271‐P) del Ministerio de Economía y competitividad; REMEDINAL 3‐CM (ref. S2013/MAE‐2719) de la Comunidad de Madrid. Así como al Programa de becarios en el extranjero del Consejo Mexicano de Ciencia y Tecnología (CONACyT) del gobierno de Méxic

Habitat fragmentation is linked to cascading effects on soil functioning and CO2 emissions in Mediterranean holm-oak-forests

We studied key mechanisms and drivers of soil functioning by analyzing soil respiration and enzymatic activity in Mediterranean holm oak forest fragments with different influence of the agricultural matrix. For this, structural equation models (SEM) were built including data on soil abiotic (moisture, temperature, organic matter, pH, nutrients), biotic (microbial biomass, bacterial and fungal richness), and tree-structure-related (basal area) as explanatory variables of soil enzymatic activity and respiration. Our results show that increased tree growth induced by forest fragmentation in scenarios of high agricultural matrix influence triggered a cascade of causal-effect relations, affecting soil functioning. On the one hand, soil enzymatic activity was strongly stimulated by the abiotic (changes in pH and microclimate) and biotic (microbial biomass) modifications of the soil environment arising from the increased tree size and subsequent soil organic matter accumulation. Soil CO2 emissions (soil respiration), which integrate releases from all the biological activity occurring in soils (autotrophic and heterotrophic components), were mainly affected by the abiotic (moisture, temperature) modifications of the soil environment caused by trees. These results, therefore, suggest that the increasing fragmentation of forests may profoundly impact the functioning of the plant-soil-microbial system, with important effects over soil CO2 emissions and nutrient cycling at the ecosystem level. Forest fragmentation is thus revealed as a key albeit neglected factor for accurate estimations of soil carbon dynamics under global change scenarios

Complex effects of habitat fragmentation on plant‐soil microbial interactions in Mediterranean Holmoak forests

Póster presentado en el 1st Global Soil Biodiversity Conference (2-5 December 2014 - Dijon, France)The adverse effects of habitat fragmentation on biodiversity have been widely explored; however, little research has been conducted to understand its effects on ecosystem functioning. Effects of forest fragmentation are tightly linked to the surrounding matrix in terms of nutrient inputs and spatial constraints, leading to complex edge effects. Soil ecosystem processes related to carbon cycling are particularly important since soils are the largest carbon pool in terrestrial ecosystems, and habitat fragmentation affects their sink capacity and their vulnerability to global change. Soil organic matter (SOM) decomposition is affected directly by the canopy cover. Thus, the effects of an agricultural matrix could be overridden by the direct effects of canopy rather than by habitat fragmentation itself. In order to evaluate which key factors could be driving SOM decomposition in fragmented landscapes, we analyzed potential enzymatic activities (β-glucosidase, chitinase and phosphatase acid) and field soil respiration in fragmented Mediterranean Holm oak forests. We evaluated if the impact of fragmentation on soil microbial functioning could be explained through its effect on microhabitat characteristics by using structural equation models. Variables measured included biotic (microbial biomass), abiotic (soil moisture, temperature, organic matter, pH, nutrients) and tree structural (stem diameter, canopy projection, leaf area index) characteristics. Tree effects on soil functioning (enzymatic activities) were potentiated by the influence of the agricultural matrix. As expected, trees created a microenvironment where the increment of SOM modified the pH, increasing soil moisture and decreasing temperature, rising the amount of microbial biomass and, therefore, improving the functioning of soil microbial community. Agricultural matrix influence on SOM decomposition was mainly indirect, through its positive effect on tree size. Mediterranean fragmented forests with high influence of agricultural matrix could increase SOM decomposition rates, decreasing soil carbon sink capacity.Peer reviewe

Habitat Fragmentation can Modulate Drought Effects on the Plant-soil-microbial System in Mediterranean Holm Oak (Quercus ilex) Forests

© 2015, Springer Science+Business Media New York. Ecological transformations derived from habitat fragmentation have led to increased threats to above-ground biodiversity. However, the impacts of forest fragmentation on soils and their microbial communities are not well understood. We examined the effects of contrasting fragment sizes on the structure and functioning of soil microbial communities from holm oak forest patches in two bioclimatically different regions of Spain. We used a microcosm approach to simulate the annual summer drought cycle and first autumn rainfall (rewetting), evaluating the functional response of a plant-soil-microbial system. Forest fragment size had a significant effect on physicochemical characteristics and microbial functioning of soils, although the diversity and structure of microbial communities were not affected. The response of our plant-soil-microbial systems to drought was strongly modulated by the bioclimatic conditions and the fragment size from where the soils were obtained. Decreasing fragment size modulated the effects of drought by improving local environmental conditions with higher water and nutrient availability. However, this modulation was stronger for plant-soil-microbial systems built with soils from the northern region (colder and wetter) than for those built with soils from the southern region (warmer and drier) suggesting that the responsiveness of the soil-plant-microbial system to habitat fragmentation was strongly dependent on both the physicochemical characteristics of soils and the historical adaptation of soil microbial communities to specific bioclimatic conditions. This interaction challenges our understanding of future global change scenarios in Mediterranean ecosystems involving drier conditions and increased frequency of forest fragmentation

Agricultural matrix affects differently the alpha and beta structural and functional diversity of soil microbial communities in a fragmented Mediterranean holm oak forest

The chapter III of: FLORES-RENTERÍA, Dulce. Effects of forest fragmentation on the plant‐soil‐microbial interactions = Efectos de la fragmentación del encinar en las interacciones planta‐suelo‐microorganismos (2016), is relationed with the paper: Agricultural matrix affects differently the alpha and beta structural and functional diversity of soil microbial communities in a fragmented Mediterranean holm oak forest. Soil Biology and Biochemistry 92: 79-90 (2016). http://hdl.handle.net/10261/151312El capítulo III de la tesis doctoral: FLORES-RENTERÍA, Dulce. Efectos de la fragmentación del encinar en las interacciones planta‐suelo‐microorganismos = Effects of forest fragmentation on the plant‐soil‐microbial interactions (2016, está relacionado con el artículo: Agricultural matrix affects differently the alpha and beta structural and functional diversity of soil microbial communities in a fragmented Mediterranean holm oak forest. Soil Biology and Biochemistry 92: 79-90 (2016). http://hdl.handle.net/10261/151312Given the increase in habitat fragmentation in the Mediterranean forests, understanding its impacts over the ecology of soil microbial communities, responsible for many ecosystem functions, and their capacity to metabolize different substrates from soil organic matter, is of upmost importance. We evaluated how the influence of the agricultural matrix, as one of the main consequences of forest fragmentation, may affect both the composition and the functioning of soil microbial communities in Mediterranean holm oak forests. We determined structural and functional alpha and beta-diversity of microbial communities, as well as microbial assemblages and metabolic profiles, by using a commonly used fingerprinting technique (Denaturing Gel Gradient Electrophoresis) and a community level physiological profiles (CLPP) technique (EcoPlate). Key drivers of soil microbial structure and metabolism were evaluated by using structural equation models (SEM) and multivariate ordination (envfit) approaches. Our results pointed out that forest fragmentation affects microbial community structure and functioning through a complex cascade of causal-effect interactions with the plant–soil system, which ultimately affects the nutrient cycling and functioning of forest soils. We also found a strong scale-dependency effect of forest fragmentation over the ecology of microbial communities: fragmentation increases the local (alpha) diversity, but affected negatively microbial diversity at the landscape scale (beta diversity). This homogenization of the microbial communities and their metabolism at landscape scale resulting from habitat fragmentation may have unknown potential consequences on the capacity of these communities, and hence these ecosystems, to respond to the climate change. Finally, we found a consistent relation between the structure and functional diversity of bacterial community, which further showed the important role that the assemblage of microbial communities might have over their functioning.This work was supported by the Spanish Ministry for Economy and Competitiveness (formerly known as Innovation and Science) with the projects VULGLO (CGL2010 22180 C03 03), VERONICA (CGL2013-42271-P) and MyFUNCO (CGL2011-29585-C02-02), and the project REMEDINAL 3-CM (S2013/MAE-2719) funded by the Comunidad de Madrid.Peer Reviewe

Soil legacies determine the resistance of an experimental plant-soil system to drought

This study examines the effects of climate and the degree of forest fragmentation legacies on response of oak to drought. A microcosm approach was set up with holm oak seedlings from three provenances grown in soils coming from two regions of contrasting climate (drier vs. wetter), and three scenarios of forest fragmentation (low, mid, and high agricultural matrix influence). We measured different indicators of the plant-soil system functioning such as ecosystem respiration, net ecosystem exchange, gross primary productivity, stomatal conductance, quantum yield, biomass allocation, and mycorrhization. Legacies of the bioclimatic region and the degree of forest fragmentation on soil properties drove the response to drought of an experimental plant-soil system, masking the effects of seedling provenance. The system was functionally more resistant to drought in soils from forest fragments with more agricultural influence and from the drier region. Our results indicate that the degree of forest fragmentation and bioclimatic legacies on soil properties exerted a much more decisive effect on the response of the plant-soil system to drought than holm-oak seedling provenance.This work was supported by the Spanish Ministry for Economy and Competitiveness (MINECO) with the projects VULGLO (grant number CGL2010 22180 C03 03), VERONICA (grant number CGL2013-42271-P) and MyFUNCO (grant number CGL2011-29585-C02-02), and by the Comunidad de Madrid with the project REMEDINAL 3-CM (grant number S2013/MAE-2719). DFR held a pre-doctoral fellowship awarded by the Mexican Council of Science and Technology (CONACyT, grant number 310849).Peer Reviewe

Effect of temperature on ectomycorrhizal fungi associated with Pinus sylvestris L. in organic vs. mineral soils

This work was supported by the projects S2009/AMB-1511 and CGL2011-29585Peer Reviewe

Fragmentation reduces severe drought impacts on tree functioning in holm oak forests

Fragmentation and increased summer drought are two main threats to Mediterranean forests. Forest fragmentation has many negative impacts on forests but could attenuate water stress on Mediterranean species by reducing intraspecific competition or improving soil properties at forest edges. However, little is known about the combined effects of drought and fragmentation on tree functioning. We evaluated the effect of forest fragmentation on tree functioning under severe drought periods in continental holm oak forests (Quercus ilex). We monitored the functional response of focal trees before and during summer drought in two regions of the Iberian Peninsula with contrasting climates. Forest interiors, edges and small forest fragments were compared. Predawn leaf water potential (Ψ), leaf stomatal conductance to water vapor (g), maximum leaf photochemical efficiency (F/F), ground (F) and maximum (F) fluorescence in dark adapted, fully-developed leaves were assessed in the field. Trees located at forest interiors and edges showed strong stomatal closure and clear symptoms of photochemical inhibition, revealing that the trees were operating at predawn water potential beyond tolerance thresholds. In contrast, trees located in small forest fragments were able to maintain high levels of functionality for all ecophysiological parameters during the drought. These differences in tree functioning among fragments were more noticiable in the driest region. Our results prove that forest fragmentation attenuates drought impacts on tree functioning, and that these positive effects become more important during extremely dry periods. These novel findings are essential for realistic predictions of the functionality of fragmented forests under increasing and more severe droughts.A.F. was supported by JAE-predoc (CSIC), cofunded by the European Union (Fondo Social Europeo). This work was supported by the Spanish Ministry of Economy and Competitiveness with the grants VULGLO (CGL2010-22180-C03-03), SEDIFOR (AGL2014-57762-R), ECOMETAS (CGL2014-53840-REDT), the project of the Autonomous Community of Madrid REMEDINALTE-CM S2018/EMT-4338, and the grant COMEDIAS, funded by FEDER/Spanish Ministry of Science, Innovation and Universities (CGL2017-83170)

Hypothesis 1 ascomycota and spp richness dryad b

Data on the percentage of fungi from the division ascomycota and ectomycorrhizal fungal species richness used to test hypothesis 1. This file includes GenBank accession numbers and species identity information for the species richness data