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

Influencia de la fragmentación y el clima en procesos clave para la regeneración del encinar

Recibido el 7 de mayo de 2014, aceptado el 10 de julio de 2014[EN] This paper reviews the main results of several lines of research on the effects of global change on Holm oak forests surrounded by an agricultural matrix and their regeneration capacity. We discuss our research on continuous and fragmented oak forests at two climatically contrasted locations. Our results suggest that fragmentation processes could mitigate some negative effects of climate change, namely the decreased productivity of Holm oak associated with an increased water stress. This attenuation would be verified by both the release of competition for water between trees near the edge and changes in microbial communities and functional properties of the soil. Because climate change operates directly on other processes such as phenology of trees and dispersants, it could lead to decoupling between the two groups of organisms and adversely affect their mutualism. The phenological decoupling between oaks and rodents observed in the more xeric populations might increase the vulnerability of oaks to global warming. Fragmentation had a negative effect on the quality of acorns dispersal due to the lack of safe places for dispersal agents and by decreasing intraspecific competition. It is conceivable that the combined effects of climate change and fragmentation threaten oak regeneration despite the counterintuitive positive effects of fragmentation on the physiology of oaks and on acorn production.[ES] El presente trabajo revisa los resultados principales de tres líneas de investigación sobre los efectos del cambio global sobre los encinares rodeados de una matriz agrícola y su capacidad de regeneración. Se resumen y discuten resultados sobre encinares continuos y fragmentados en dos localidades de clima contrastado. Nuestros resultados sugieren que los procesos de fragmentación podrían atenuar algunos efectos negativos del cambio climático, en concreto la disminución de productividad de la encina asociada al creciente estrés hídrico. Esta atenuación se verificaría tanto por la liberación de competencia por el agua entre los árboles próximos al borde como por los cambios en las comunidades microbianas y en las propiedades funcionales de los suelos. Dado que el cambio climático opera directamente sobre otros procesos como la fenología de los árboles y de los dispersantes, podría llevar a desacoples entre los ritmos vitales de ambos grupos de organismos y afectar negativamente al mutualismo entre ambos. El desacoplamiento fenológico entre encinas y roedores observado en las poblaciones más xéricas tendería a aumentar la vulnerabilidad de los encinares frente al calentamiento global. La fragmentación tuvo en conjunto un efecto negativo sobre la calidad de dispersión de las bellotas debido a la falta de zonas de refugio para los dispersantes y a la disminución de la competencia intraspecífica. Cabe pensar que los efectos combinados del cambio climático y la fragmentación amenazan la regeneración del encinar a pesar de los contraintuitivos efectos positivos de la fragmentación sobre la fisiología de las encinas y la producción de bellota.La financiación para los estudios que se resumen aquí procedió del proyecto VULGLO (CGL2010-22180-C03-03) del Plan Nacional del Ministerio de Ciencia y Tecnología.Peer reviewe

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

Some positive effects of the fragmentation of holm oak forests: Attenuation of water stress and enhancement of acorn production

The effects of fragmentation on acorn production should be mediated by their impacts on the physiological status of oaks during seed development particularly in water-limited systems, such as Mediterranean forests. The creation of forests edges reduces tree-to-tree competition, which may in turn temper water shortage during summer and, as a result, enhance acorn production. To test these two hypotheses we monitored acorn production and predawn water potential during the 2012-2014 period in two holm oak (Quercus ilex) forest archipelagos of the Iberian Peninsula.Acorn production and fragmentation effects did not differ between localities despite of their contrasting climatic conditions (accumulated water deficit from April to August was a 60% higher in the South). In general, forest interiors showed a high proportion of non-producing trees (~50%) while trees at small forest fragments showed high acorn crops (acorn score ≥3, ~40% of studied trees). Our results confirmed the expectation that intraspecific competition in small forest fragments was reduced, which alleviated summer water shortage of the trees studied. This reduced water stress entailed an increased acorn production. Overall, our results show that local processes such as fragmentation may counteract climatic differences among localities and could even override the impacts of increased aridity on acorn crops.Fil: Morán López, Teresa. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Consejo Superior de Investigaciones Científicas; EspañaFil: Forner, Alicia. Consejo Superior de Investigaciones Científicas; EspañaFil: Flores Rentería, Dulce. Consejo Superior de Investigaciones Científicas; EspañaFil: Díaz, Mario. Consejo Superior de Investigaciones Científicas; EspañaFil: Valladares, Fernando. Consejo Superior de Investigaciones Científicas; Españ