Tree Species Identity Shapes Earthworm Communities

Article Tree Species Identity Shapes Earthworm Communities Stephanie Schelfhout 1,2,*, Jan Mertens 1, Kris Verheyen 2, Lars Vesterdal 3, Lander Baeten 2, Bart Muys 4 and An De Schrijver 2,5 1 Department of Applied Biosciences, Faculty of Bioscience Engineering, Ghent University, Valentin Vaerwyckweg 1, 9000 Gent, Belgium; [email protected] 2 Forest & Nature Lab, Department of Forest and Water Management, Faculty of Bioscience Engineering, Geraardsbergsesteenweg 267, 9090 Gontrode, Belgium; [email protected] (K.V.); [email protected] (L.B.); [email protected] (A.D.S.) 3 Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C, Denmark; [email protected] 4 Division of Forest, Nature and Landscape, Department of Earth & Environmental Sciences, KU Leuven, Celestijnenlaan 200 E, Box 2411, 3001 Leuven, Belgium; [email protected] 5 Faculty of Science and Technology, University College Ghent, Brusselsesteenweg 161, 9090 Melle, Belgium * Correspondence: [email protected]; Tel.: +32-9264-90-46 Academic Editor: Laurent Augusto Received: 25 January 2017; Accepted: 13 March 2017; Published: 17 March 2017 Abstract: Earthworms are key organisms in forest ecosystems because they incorporate organic material into the soil and affect the activity of other soil organisms. Here, we investigated how tree species affect earthworm communities via litter and soil characteristics. In a 36-year old common garden experiment, replicated six times over Denmark, six tree species were planted in blocks: sycamore maple (Acer pseudoplatanus), beech (Fagus sylvatica), ash (Fraxinus excelsior), Norway spruce (Picea abies), pedunculate oak (Quercus robur) and lime (Tilia cordata). We studied the chemical characteristics of soil and foliar litter, and determined the forest floor turnover rate and the density and biomass of the earthworm species occurring in the stands. Tree species significantly affected earthworm communities via leaf litter and/or soil characteristics. Anecic earthworms were abundant under Fraxinus, Acer and Tilia, which is related to calcium-rich litter and low soil acidification. Epigeic earthworms were indifferent to calcium content in leaf litter and were shown to be mainly related to soil moisture content and litter C:P ratios. Almost no earthworms were found in Picea stands, likely because of the combined effects of recalcitrant litter, low pH and low soil moisture content. Keywords: biogeochemistry; litter quality; soil fauna; soil acidification; plant–soil interactions; biological indicator of soil quality; Oligochaeta 1. Introduction Earthworms have been studied for a long time (e.g., Darwin [1]), and it is known that soil and forest floor characteristics profoundly affect the composition and abundance of earthworm populations [2–4]. On the other hand, earthworms are ecosystem engineers [5,6] that can physically, chemically and biologically modify their environment, impacting the habitat and the resources for other organisms [7–9] and consequently providing a wide diversity of ecosystem services including facilitation of nutrient cycling and formation of stable humic compounds [6] and mineral soil C sequestration [10,11]. Earthworm species all have distinct feeding niches varying from fresh leaf litter to humus and even animal dung, fungal hyphae or soil [12]. The simultaneous occurrence of species from different Forests 2017, 8, 85; doi:10.3390/f8030085 www.mdpi.com/journal/forests Forests 2017, 8, 85 2 of 20 Forests 2017, 8, 85 2 of 20 Earthworm species all have distinct feeding niches varying from fresh leaf litter to humus and even animal dung, fungal hyphae or soil [12]. The simultaneous occurrence of species from different ecologicalecological groups groups can can have have synergistic synergistic outcomes, outcomes, and lossand ofloss species of species can lead can tolead significant to significant changes changes in thein ecosystem the ecosystem services services they provide they provide [13]. [13]. EarthwormEarthworm species species can becan classified be classified according according to their to morphologicaltheir morphological features, features, habitat habitat choice andchoice feedingand feeding habits into habits three into ecological three ecological groups: groups: epigeic, epigeic, endogeic endogeic and anecic and earthworms anecic earthworms (Figure1 ,[(Figure14]). 1, First,[14]). epigeic First, earthworms, epigeic earthworms, or ‘litter-dwellers’, or ‘litter‐dwellers’, are detrivorous are detrivorous species species feeding feeding mainly mainly on fresh on orfresh partiallyor partially decomposed decomposed litter onlitter or on near or thenear soil the surface. soil surface. They They contribute contribute to litter to litter fragmentation, fragmentation, but but havehave too too little little muscular muscular power power to enter to enter the the mineral mineral soil. soil. Given Given the the important important organic organic acid acid production production in accumulatingin accumulating forest forest floors, floors, most most epigeic epigeic species species are are tolerant tolerant to acidto acid conditions conditions [15 ].[15]. For For example, example, DendrobaenaDendrobaena octaedra octaedracan can occur occur in Pinus in Pinus, Picea, Piceaor Fagus or Fagusstands stands with with soil soil pH H2OpHH2Oof lessof less than than 4.0 4.0 [16 [16,17].,17]. Secondly,Secondly, endogeic endogeic earthworms, earthworms, or ‘soil-dwellers’,or ‘soil‐dwellers’, are are geophagous geophagous earthworms earthworms feeding feeding on on largelylargely humified humified soil soil organic organic matter matter and and dead dead roots. roots. They They are are literallyliterally eatingeating their way through through the theshallow shallow soil soil and, and, thereby, thereby, ingesting ingesting large large quantities quantities of of soil soil and and mixing mixing this this with with organic organic material, material, i.e., i.e.,bioturbation bioturbation [12]. [12]. Most Most of of these these species species are are very very sensitive sensitive to to soil soil acidification acidification [15,17], [15,17], for for example, example, the thefitness fitness of of AporrectodeaAporrectodea caliginosa caliginosa declineddeclined in in acid acid soils soils (pH (pHH2OH2O < 4.8,< 4.8, [18]). [18 ]). Thirdly,Thirdly, anecic anecic earthworms, earthworms, or ‘deep-burrowers’,or ‘deep‐burrowers’, are are also also detrivorous detrivorous but but differ differ from from epigeic epigeic earthwormsearthworms by theirby their ability ability to create to create deep deep vertical vertical burrows burrows in the in the mineral mineral soil. soil. They They can can pull pull leaf leaf litter litter fromfrom the the soil soil surface surface into into their their burrows. burrows. The The anecic anecic species speciesLumbricus Lumbricus terrestris terrestrisis known is known for for removing removing significantsignificant quantities quantities of litterof litter from from the the forest forest floor floor [12 ][12] while while casts casts are are mainly mainly deposited deposited at theat the soil soil surfacesurface [19 ].[19]. This This species species can can occur occur in a in broad a broad pH-range pH‐range (pH (pHH2O H2O4.0–7.2 4.0–7.2 [17 ,[17,20])20]) of soilof soil acidity acidity but but main main occurrenceoccurrence of theof the anecic anecic species speciesAporrectodea Aporrectodea longa longaand andLumbricus Lumbricus terrestris terrestrisis is at at pH pHH2OH2Oabove above 4.6 4.6 [ [21].21]. FigureFigure 1. Illustration 1. Illustration of the of the three three ecological ecological earthworm earthworm groups groups according according to their to their food food preference preference and and behavior.behavior. The The brown brown zone zone represents represents the soil.the soil. Reproduced Reproduced from from [22]. [22]. In forests, the environmental factors that regulate earthworm communities include litter traits In forests, the environmental factors that regulate earthworm communities include litter traits and soil characteristics, mainly clay content, pH, base saturation, soil moisture content, organic and soil characteristics, mainly clay content, pH, base saturation, soil moisture content, organic matter matter content and aluminium (Al) toxicity [2,23]. Soil pH correlates strongly positively with soil content and aluminium (Al) toxicity [2,23]. Soil pH correlates strongly positively with soil calcium (Ca) calcium (Ca) and negatively with soil Al concentration, and is among the most important drivers for and negatively with soil Al concentration, and is among the most important drivers for anecic and anecic and endogeic earthworms, i.e., the burrowing earthworm community. A study in multiple endogeic earthworms, i.e., the burrowing earthworm community. A study in multiple Fagus sylvatica Fagus sylvatica stands on a gradient from acid to limestone soils showed that burrowing earthworm stands on a gradient from acid to limestone soils showed that burrowing earthworm densities were densities were most strongly positively linked with the presence of a limestone layer and almost most strongly positively linked with the presence of a limestone layer and almost absent from Ca-poor absent from Ca‐poor soils [24]. soils [24]. Tree species can significantly modify most of these soil characteristics [25–28]. For instance, N2‐ Tree species can significantly modify most of these soil characteristics [25–28]. For instance, fixing

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