Seasonal dynamics of soil nutrients and microbial activity due to colonization by bracken ferns (Pteridium aquilinum (L.) Kuhn) in a pine forest

Highlights

• Brackens induced sinks of soil nutrient, though with a marked seasonality.

• Brackens increased soil nutrient pools in winter during its senescence.

• Bracken effect on nutrients did not depend on bracken area, density or height.

• Brackens enhanced soil microbial respiration independently of seasons.

Abstract

Bracken (Pteridium aquilinum) is an aggressive colonizer of disturbed and other successional habitats in temperate forests. However, little is known about how bracken colonization modifies soil microbial activity and nutrient cycling. We questioned whether bracken presence alters soil nutrient pools and soil microbial respiration throughout a growing season and whether this effect depends on the size of the bracken patch. To answer these questions, we sampled the soil in bracken patches of different sizes (large, medium and small) and in the surrounding pine forest (paired sampling design) in summer, autumn, winter and spring. We analyzed the samples to determine nutrient contents (C, N and P) and soil microbial respiration. Patch size did not influence soil microbial activity or nutrient pools. Bracken acted as nutrient sink for N pools through the growing season and as source or sink for C and P pools depending on season. Moreover, the effect on nutrient pools did not depend on bracken characteristics (area, density or height). Bracken presence enhanced soil microbial respiration proportionally to patch area. The control that bracken exerts over nutrient pools may determine the successful (or otherwise) establishment of other plant species. This contributes to making bracken a successful colonizer as no particular population threshold (area, density) has to be reached before nutrients becomes limiting to other plant species.

Introduction

Bracken (Pteridium aquilinum (L.) Kuhn) is a common aggressive ruderal in European forests, but little is known on how this species influences soil microbial activity and nutrient pools during its growth cycle. Bracken is one of the most widely dispersed and common plant species worldwide [1,2]. Several of its characteristics contribute to bracken being a successful colonizer. First, the rhizome system stores nutrients and carbohydrates, enabling fast rapid recovery of the plant after disturbance such as fire or harvesting. Second, the high productivity of bracken yields a massive frond canopy, resulting in litter accumulation, water interception and limiting access to light by other plant species. Third, the plant releases several toxic chemicals [[3], [4], [5], [6]], and fourth the bracken reallocates nutrients to the rhizome that will be used to trigger growth in spring [7]. These traits make it difficult for other plant species to become established once bracken colonizes the soil [7]. Bracken has been widely studied as a modifier of plant succession because it can even suppress colonization by trees [7]. Further, research has also focused on bracken because it produces a carcinogenic agent (ptaquiloside) that can affect livestock [8]. In addition, variation in soil nutrient pools has been attributed to uptake and storage as bracken is a very efficient nutrient recycler, sequestering nutrients even after senescence [3,6,9]. However, although there are important contributions studying how the presence of bracken modifies soil microbial respiration and nutrient pools in soils where the plants are established [[10], [11], [12]]; little is known about how the influence of bracken varies between seasons and with the size of bracken patches.

The main aim of the present study was to determine whether bracken affects the nutrient pools and soil microbial respiration in soils where it is present. However, due to the particular growth habits of bracken, it is difficult to compare the effects on soil biochemical parameters in colonized and uncolonized (control) areas, because the bracken forms dense, uniform patches [7]. However, bracken stands may occur in patches due to habitat variability, competition, or even to the effects of bracken on itself [7]. Size of the patches has been related with its age and with the number of clones they comprise [13,14]. In this way, and according to the home-field advantage hypothesis [15] microorganisms should be more adapted to decompose bracken litter more efficiently in larger patches. However, this should largely depend on how fast patches grow. Thus, it could be expected that the influence of bracken being larger in the inner than at the edge of the patches would increase with patch size.

These defined patches of different sizes can be considered habitat-islands (Fig. 1). Habitat-islands play an important role in the study of ecology and evolution, and their particular characteristics (small isolated areas and defined boundaries with surrounding ecosystems) make them suitable sites for scientific research [16]. Habitat-island systems have been studied as oceanic islands per se [17,18] and even as “isolated patches” of communities different from the surrounding communities [19].

We questioned whether the presence of bracken effectively modifies basal soil microbial respiration and nutrient dynamics and whether the particular traits governing growth cycle of brackens, i.e. reallocation of nutrients from the frond to the rhizome in autumn and winter during senescence [20,21], alter the nutrient pools and soil microbial respiration of soil colonized by the bracken. We should expect higher levels of nutrients in autumn, winter and even spring, as a result of decomposition of dead fronds and also because nutrients are provided by the rhizome during the initial stages of growth of fronds [21]. Moreover, if bracken behaves as an invasive species, we would expect increased nutrient contents, especially of nitrogen, underneath the plants, relative to bracken free areas, as it has been shown that bracken, as other invasive plant species, enhance nitrogen pools [[10], [11], [12],22]. However, for brackens this effect is strongly modulated according to pH [12]. Secondly, we also questioned whether the effects of bracken on soil nutrient pools and basal soil microbial respiration depend on the size of the bracken patch. It is known that habitat-island size (hereafter bracken patch) is associated with ecosystem properties and function, as litter mass loss, nutrient content and microbial biomass and activity [17,19]. We, therefore, hypothesized that the effects of bracken on soil nutrient pools and basal soil microbial respiration will increase with patch size and even with bracken density and height.