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Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter
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Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter A. Gerlach a,b , D.J. Russell b,∗ , B. Jaeschke a,b , J. Römbke c a b c
Biodiversity and Climate Research Centre Frankfurt, Senckenberganlage 25, 60325 Frankfurt am Main, Germany Senckenberg Museum of Natural History, am Museum 1, 02826 Görlitz, Germany ECT Oekotoxikologie GmbH, 65439 Flörsheim/Main, Germany
a r t i c l e
i n f o
Article history: Received 5 February 2013 Received in revised form 7 February 2014 Accepted 11 February 2014 Keywords: Feeding activity Primary leaf litter decomposition Introduced leaf litter Isopoda Laboratory choice tests
a b s t r a c t Due to current predictions for Central Europe that forecast higher frequencies of hot and dry summers, Mediterranean drought-tolerant oak species are being evaluated as future forest trees for German forest sites that are becoming increasingly damaged by water deficit. As a result of planting foreign tree species, the leaf litter composition and thus the food resources of native saprophagous macroarthropods will change, possibly altering primary decomposition processes. Therefore, experiments concerning the acceptance and palatability of introduced versus native litter for native isopods were undertaken. Consumption rates of four native isopod species (Porcellio scaber, Oniscus asellus, Trachelipus rathkii, Trachelipus ratzeburgii) were investigated in laboratory choice tests with introduced (Quercus pubescens, Quercus frainetto, Quercus ilex) and comparable native (Fagus sylvatica, Quercus robur) leaf litter. Litter was characterized by measurement of C/N-ratios and lignin content. Although species-specific preferences of isopods could be observed in the experiments, Mediterranean oak litter was consumed by all investigated species. Furthermore, two isopod species even preferred the leaf litter of the introduced Q. ilex. Compared to native beech or oak litter, litter from these introduced tree species thus apparently do not negatively influence the consumption rates of terrestrial isopods. Possible reasons for the determined preferences are discussed. © 2014 Published by Elsevier B.V.
1. Introduction Current climate models predict a scenario for Central Europe that implies an increasing frequency of hot and dry summers as well as a raise of the average summer temperature of approximately 4 ◦ C within the next 50–100 years (Schär et al., 2004). As a long-term consequence of the altered climate, a change in the composition of native forest ecosystems can be expected (Kölling and Zimmermann, 2007; Pompe et al., 2009). The impact of increasing drought stress can already be observed in some forest sites in southern Hesse, Germany, where native tree species such as Fagus sylvatica and Quercus robur show strong water-deficit damage, intensified by human-induced groundwater drawdown (pers. comm.: Forestry Office Hesse). To prevent further forest degradation and to maintain sustainable forest ecosystems, a long-term study is ongoing to evaluate the potential of more drought tolerant Mediterranean oak species such as Quercus pubescens, Quercus
∗ Corresponding author. Tel.: +49 358147605502. E-mail address: [email protected] (D.J. Russell).
frainetto and Quercus ilex, among others, as future forest trees in these Central European sites (cf. Brüggemann et al., 2009; Holland and Brüggemann, 2011). Leaf litter decomposition is an important process in the nutrient cycle of forests (Chew, 1974; Swift and Anderson, 1989). The feeding activity of saprophagous macroarthropods, such as earthworms, diplopods and isopods, and the associated fragmentation of plant litter material plays an essential role in the incorporation of organic matter into soils. As a result of planting foreign tree species, the leaf litter composition and thus the food resources of the native soil macrofauna will change. To ensure that the introduction of foreign tree species into local forests does not affect primary decomposition processes, it is therefore necessary to assess how foreign leaf litter affects the feeding activity of the local macrofaunal decomposers. Results of a previous experiment, in which the consumption rate of local populations of the abundant diplopod species Glomeris marginata (Villers, 1789) from the experimental forest sites in southern Hesse was measured, indicate that consumption of introduced Mediterranean-oak leaf litter takes place at equivalent or even higher rates than that of domestic leaf species (Gerlach
http://dx.doi.org/10.1016/j.apsoil.2014.02.006 0929-1393/© 2014 Published by Elsevier B.V.
Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006
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et al., 2012). It could thus been shown that this diplopod species does feed on the introduced leaf litter, at least in the absence of other food resources. These first results gave rise to the question how other native decomposer species respond to the changed nutrient resources caused by the altered litter sources. Terrestrial isopods also feed predominantly on fallen leaf litter and soft, decaying plant material (Gruner, 1966) and are also abundant in the forest study sites in question. Additionally their selective feeding behaviour (Hassall and Rushton, 1984; Ihnen and Zimmer, 2008; Loureiro et al., 2006; Zimmer et al., 2002) and sensitivity towards changes in diet (Caseiro et al., 2000; Farkas et al., 1996; Hornung et al., 1998) render isopods suitable test organisms for such experiments. The aim of the study was therefore to determine whether local isopod populations will feed on Mediterranean leaf litter, which litter species is preferred when given the choice between leaf litter of introduced (Q. pubescens, Q. frainetto, Q. ilex) and comparable native (F. sylvatica, Q. robur) tree species, and whether isopod consumption of the various litter species differ. Fig. 1. Setup of the chambered containers used in the feeding preference experiments.
2. Material and methods Feeding-preference experiments were carried out with four isopod species obtained from forest sites in southern Hesse, Germany, where Mediterranean oak species are being introduced. Trachelipus rathkii (Brandt, 1833), Porcellio scaber Latreille, 1804 and Oniscus asellus Linnaeus, 1758 were collected from mixed forests near Rüsselsheim (N49◦ 57 16.5 , E8◦ 24 58.4 ) and Trachelipus ratzeburgii (Brandt, 1833) from deciduous forests near Lampertheim (N49◦ 35 7.2 , E8◦ 34 42.3 ). In the laboratory, the animals were kept species-specifically in round transparent containers (diameter: 14 cm; height: 7 cm) with a bottom coating of a plaster of paris and activated charcoal mixture (20:1; 1 cm layer) and above that a 1 cm high soil mixture (obtained from the same forest sites from which the animals were collected), which was moistened bi-weekly. deadwood, bark, mosses and especially moistened fieldcollected litter (Q. robur, F. sylvatica, Tilia cordata, Carpinus betulus, Acer platanoides and more rarely Q. rubra) were added to the containers as food resources as well as concealment possibilities. The litter was provided ad libitum. Maximally 30 individuals of single species were kept in one container. The containers with the animals were maintained in a climate chamber with a 13:11-h light:dark rhythm and a diurnal temperature regime of 12 ◦ C (nighttime) to maximally 20 ◦ C (daytime). For the experiments, freshly fallen litter of the tree species F. sylvatica, Q. frainetto, Q. robur and Q. pubescens was collected in October and November 2008 from the Palmengarten and Botanical Garden in Frankfurt am Main (Hesse) as well as the Botanical Garden in Tharandt (Saxony) and air dried. Due to the low leaf abscission of the evergreen Q. ilex and resulting lack of litter in Germany, litter of this species was collected from its natural distributional area in southern France. Freshly fallen litter is decidedly less consumed than microbially pre-decomposed litter (Bertrand and Lumaret, 1992; Dunger, 1958; Gerlach et al., 2012; Hassall and Rushton, 1984). The litter was therefore exposed in litterbags (mesh size: 5 mm) for six months in the same woodlands from which the animals were obtained. After this, the litter was returned to the laboratory, air dried and stored dried until use in the experiments. For the experiments, litter was then used that showed no macroscopic signs of advanced decomposition. Parallel studies on field decomposition showed a litter decomposition rate of, on average, ca. 15% after six months, with the Mediterranean species being somewhat more decomposed than the Central European species (unpubl. data).
The feeding-preference experiments were carried out under the same climatic conditions in plastic containers of the same size and treated as mentioned above (however, without added organic material). For each of the four isopod species, six replicates (=containers) with isopods and six replicates without isopods (=controls) were studied (24 replicates + 24 controls total). The mass of the isopod individuals was, on average, 44.4 ± 13.0 mg (O. asellus), 23.9 ± 5.9 mg (P. scaber), 31.9 ± 10.8 mg (T. rathkii), and 20.0 ± 11.4 mg (T. ratzeburgii). In each replicated container, 400 mg ± 2 mg air-dried litter of each tree species, which was steeped in water for 24 h before beginning the experiments, and five previously weighed individuals of the respective isopod species (absent in the controls) was added. The interior space of the containers was divided into five chambers (Fig. 1), which ensured that the different litter species did not become mixed. To determine the initial dry weight of the litter, a portion (ca. 100 mg) of the airdried litter of each species was dried at 60 ◦ C to constant mass and weighed. All experiments continued for 10 days. After this period, the remaining litter was collected species-specifically, dried at 60 ◦ C to constant mass and weighed. The calculation of consumption by isopods (=mass loss) was performed according to the formula of David (1998):
C=
Wi − Wi D − Wf
D=
(SQRT(1 − D)) Wi − Wf
Wi
whereby C is the consumed litter in mg, Wi the initial dry weight of the litter sample before soaking in water, Wf the dry weight of the litter sample after the experiment and D the respective mass loss of the litter in the controls without animals. Consumption was calculated as per day values and was based on the total mass of the isopod individuals in the respective container. Since the palatability of the different litter species was expected to be limited by more indigestible components, the C/N-ratio and lignin content was quantified for each litter species used in the experiments. For this characterization, a portion of the litter exposed in the field for six months was first dried at 60 ◦ C and ground to a particle size of <1 mm. For each litter species, 6–7 mg of ground litter was sealed airtight in zinc capsules (8 replicates per species) and the total carbon and nitrogen contents measured in a vario PYRO cube element analyzer (Elementar Analysensysteme
Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006
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GmbH). The C/N-ratio of each litter species was calculated from these values (averages of the replicates). The least decomposable carbohydrates (acid-insoluble lignin = “Klason-lignin”) of each litter species was quantified via a two-step acid hydrolysis (cf. Hatfield et al., 1994; Hatfield and Fukushima, 2005). For this, 2 ml of 72% sulfuric acid (H2 SO4 ) was added to 200 mg of the dried and ground litter material (8 replicates of each litter species), homogenized and the mixture placed in a shaker for 60 min. at 30 ◦ C. Subsequently, 56 ml distilled water was added, resulting in a 2.5% H2 SO4 concentration. This mixture was then placed in an autoclave at 120 ◦ C for 60 min. to ensure a total hydrolysis. After allowing the mixture to cool, it was passed through a fibreglass filter (GF 92), rinsed six times with boiling distilled water until acid-free and subsequently dried at 105 ◦ C for 24 h. The mass of the remaining material was weighed and this “lignin” content calculated with the formula KLi =
(mLi × 100%) mEi
whereby KLi is the acid-insoluble lignin content of the litter sample in percent, mLi the mass of the remaining material (lignin) after the acid hydrolysis and mEi the mass of the original sample before hydrolysis (ca. 200 mg). To test for significant differences in the consumption of the different litter species, for each isopod species the data (consumed litter mass) was submitted to a variance analysis with leaf litter species as the main factor. Significance was tested using a nonparametric one-way ANOVA for multiple observations (=samples) per cell (=leaf litter species) (modified Friedman test; Zar, 1999). This ANOVA is based on ranked per sample data for each leaf litter species, on the r 2 rather than the F distribution and can easily handle unbalanced sampling designs (e.g., resulting from missing replicates caused by two exceptional cases of mortality during the experiments). A post hoc Tukey-like multiple comparison procedure for this non-parametric ANOVA (Zar, 1999) tested for significant differences of consumption between leaf litter species. The modified Friedman test was also used to test for significant differences in total consumption among the different isopod species as well as in the C/N-ratios and lignin content of the various litter species. To test for significant influences of C/N-ratio or lignin content of the litter, a covariance analysis (GLM Function of Statistica V. 10, StatSoft) was performed for each isopod species with the litter consumption (data of all litter species together) as the dependant variable and C/N-ratio and lignin content as covariables. For this analysis, all data were (ln + 1)-transformed. 3. Results 3.1. Chemical characterization of the litter species The largest C/N-ratios were measured in the litter of F. sylvatica (Table 1). Significantly lower values (r 2 = 27.040) were found in the litter of Q. robur (p < 0.05) and Q. ilex (p < 0.001). Little difference was found in the C/N-ratios of the deciduous oak species. Among the southern European oak litter, significant differences were found between Q. ilex and Q. pubescens (p < 0.01) as well as Q. frainetto (p < 0.05). Detected differences in the “lignin” contents of the oak species were not large (Table 1). The lowest lignin contents were found in the beech litter, which were significantly lower (r 2 = 14.010) than that of Q. robur as well as Q. ilex (p < 0.05). 3.2. Preferential consumption experiments The different isopod species used in the experiments exhibited significantly different total rates of litter consumption
Fig. 2. Consumption rates of the tested isopod species on total litter. Different letters denote significant differences in consumption. LW live weight.
(r 2 = 17.340, p < 0.001; Fig. 2). P. scaber (p < 0.05) and T. ratzeburgii (p < 0.01) both consumed more than double as much litter in total than O. asellus or T. rathkii. Clear differences in the preference for specific litter species could be determined for some of the studied isopod species (Fig. 3). O. asellus clearly preferred the native oak litter. The litter of the Mediterranean species was somewhat less consumed and no significant difference in the preference of the species could be determined. The beech litter was most strongly avoided and was significantly less consumed than the other central European species, Q. robur (r 2 = 11.370, p < 0.01). P. scaber preferred litter from Q. ilex and Q. robur, whereby the other three litter species were considerably less consumed. The average consumption of Q. ilex was significantly more (r 2 = 21.230) than that of F. sylvatica (p < 0.05), Q. pubescens (p < 0.01) or Q. frainetto (p < 0.01). Differences to Q. robur were generally not significant, with only Q. pubescens being less consumed than Q. robur (p < 0.05). The litter of the central European Q. robur and the Mediterranean Q. pubescens were utilized the most by T. rathkii, although no significant difference in consumption and thus no preference for any litter species could be detected (r 2 = 9.030, p = 0.06). T. ratzeburgii clearly preferred litter from Q. ilex, the consumption of which was significantly more (r 2 = 19.730) than that of F. sylvatica (p < 0.05), Q. robur (p < 0.001) or Q. pubescens (p < 0.01). No significant differences in the consumption of the litter of the deciduous tree species were detected. The central European Q. robur was the least preferred litter species. An effect of litter chemical parameters on consumption could be detected with some of the isopod species. A significant relationship between C/N-ratio and litter consumption was only found with O. asellus and T. ratzeburgii (Table 2), whereby as expected consumption was higher in litter with lower C/N-ratios. A significant effect of litter lignin content on consumption was detected with all isopod species except T. rathkii, which had showed no preference for
Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006
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Table 1 C/N-ratios and acid-insoluble “lignin” content (in %) of the litter species used in the experiments. Different letters represent significant differences between the litter species.
C/N-ratio “Lignin“
F. sylvatica
Q. robur
Q. pubescens
Q. frainetto
Q. ilex
43.01 ± 2.98 (a) 29.16 ± 2.44 (a)
33.51 ± 3.01 (b,c) 33.49 ± 2.80 (b)
36.77 ± 6.37 (a,b) 30.03 ± 3.63 (a,b)
36.09 ± 4.00 (a,b) 30.24 ± 2.40 (a,b)
24.62 ± 1.91 (c) 33.21 ± 2.07 (b)
Fig. 3. Consumption rates of the various isopod species on the five tested litter species. Different letters denote significant differences in consumption by the respective isopod species. LW live weight.
Table 2 Results of the covariance analyses of litter consumption by the tested isopod species (influence of litter parameters on consumption). C/N
O. asellus P. scaber T. rathkii T. ratzeburgii
Lignin
Error SS
SS
F
p
SS
F
p
2.234 0.120 1.254 10.873
5.594 0.597 2.742 47.068
0.025 0.447 0.109 <0.001
4.464 1.748 1.037 5.339
11.177 8.692 2.267 23.114
0.002 0.007 0.144 <0.001
10.783 5.429 12.343 6.237
C/N-ratio and lignin content were used as covariants. Significant results in bold, SS sums of squares.
any litter species. Unexpectedly, consumption by the other isopod species was apparently significantly higher in those litter species with higher lignin contents (Table 2). However, as the statistical sums of squares show, except for T. ratzeburgii, the effects of C/N or lignin content were lower than that of as yet unexplained factors (Error SS in Table 2). 4. Discussion In previous feeding experiments with litter of different tree species, oak and beech litter were among the least consumed leaf litter or – in a freshly fallen state – were not accepted at all by isopods (Dunger, 1958; Loginova and Busargina, 2005; Neuhauser and Hartenstein, 1978; Pobozsny, 1978). Due to their relatively high C/N-ratios, lignin and polyphenol contents, oak and beech litter are generally qualitatively inferior nutrient resources for the detritivore macrofauna than other litter species (Loranger-Merciris et al., 2008). In the present experiments, the beech and oak litter were readily accepted by the studied isopod species, possibly because no alternatives were offered. More palatable litter species were not tested, since in the forests in question primarily native beech and oak trees occur and are being replaced by Mediterranean oak species. Various studies on the food-resource preferences of isopods and the causes of these preferences have taken place in the past (i.e., Dunger, 1958; Nair, 1994; Neuhauser and Hartenstein, 1978; Pobozsny, 1978; Rushton and Hassall, 1983a). Especially chemical and partly also physical characteristics have been identified as potential factors for the palatability of leaf litter by detritivore macrofaunal species (Caseiro et al., 2000; David et al., 2001; Loranger-Merciris et al., 2008; McNeill and Southwood, 1978; Van Wensem et al., 1993). In preference experiments with Armadillidium vulgare, Abelho and Molles (2009) found a relationship
between consumption and the litter’s C/N-ratio, whereby nonnative leaf litter with a low C/N-ratio was more readily consumed. Cotrufo et al. (1998) found palatability differences in oak litter that had grown under different CO2 concentrations. In their study O. asellus exhibited reduced consumption of litter originating from high CO2 conditions, which possessed a higher C/N-ratio and lignin content. In the present study, the different isopods species exhibited different preferences for the various litter species. However, these preferences were apparently only partly influenced by the C/Nratios or the lignin contents of the litter. Only P. scaber and T. ratzeburgii preferred litter species with the lowest C/N-ratios, in accord with other studies (Abelho and Molles, 2009; Cotrufo et al., 1998). Interestingly, in contradiction to Cotrufo et al. (1998), all the presently studied isopods species exhibiting significant preferences favoured litter with higher lignin contents. Therefore, the lignin content seems to have no inhibitory influence on the consumption by isopods of these litter species. However, the absolute differences in lignin content among the studied litter species were minor. Furthermore, the data variability explained by C/N-ratios or lignin content were in most cases much smaller than the unexplained variability (Error SS in the covariance analyses). This indicates that factors other than C/N-ratio or lignin content were responsible for the species-specific differences in litter palatability. Besides nitrogen or lignin content, especially polyphenolic substances have been indicated as factors influencing palatability especially of harder litter species (Herlitzius and Herlitzius, 1977; King and Heath, 1967; Loranger-Merciris et al., 2008). On the other hand, in experiments with 25 different litter species, Neuhauser and Hartenstein (1978) could find no relationship between palatability and chemical litter composition. Other authors (e.g., Dunger, 1958; Pobozsny, 1978) could also not find any clear relationship between chemical properties of
Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006
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the litter and consumption by isopods. Especially in experiments with pre-decomposed (e.g., overwintered) litter, which is clearly favoured by isopods (Gere, 1956; Gunnarsson, 1987; Hassall and Rushton, 1984; Hassall et al., 1987; Stöckli, 1990; Van Wensem et al., 1993), differences in consumption among different litter species were much less than in freshly fallen litter and were generally independent from C/N-ratios (Dunger, 1958). The sequence of litter preference ascertained by Dunger (1958) corresponded with the order in which the litter had been decomposed by microorganisms (without faunal influence). This indicates that isopod palatability especially of litter in later stages of decomposition are influenced less by properties of the litter itself and more by the microbial colonization or activity on the litter (Zimmer and Topp, 1997). Microorganisms apparently increase the quality of litter as a nutrient resource (Hassall and Rushton, 1984) and are most likely a nutrient resource themselves (Gunnarsson and Tunlid, 1986; Ihnen and Zimmer, 2008; Ullrich et al., 1991; Zimmer and Topp, 1998). In experiments with P. scaber, Ihnen and Zimmer (2008) observed that especially low-quality food resources (pure cellulose) became much more attractive after microbial colonization. This isopod species particularly preferred litter colonized by fungi and fungal biomass is clearly reduced by isopod consumption (Hanlon and Anderson, 1980; Kayang et al., 1996). In the present study, a differential microbial colonization or “conditioning” of the litter is a possible further cause for the different litter preferences of the studied isopod species. The microbial activity is dependent on the litter properties (especially C/N-ratio), but more importantly on moisture and temperature (Beyer, 1992; Van Gestel et al., 1993). It is possible that different microclimatic conditions existed among the different litter species during the 6month exposition period prior to the experiments. It can therefore not be ruled out that the observed preferences were more influenced by microclimatic conditions during exposition and especially resulting microbial factors – which may not have been counteracted by air drying – than by the chemical properties of the litter itself. Besides the different preferences of the studied isopods species, different total amounts of consumption among the isopod species were also observed, with P. scaber and T. ratzeburgii showing the highest total consumption. This is in contrast to the study of Dunger (1958), in which the investigated species T. rathkii, P. scaber and O. asellus showed smaller differences in the total consumption of beech and oak litter. The determined different consumption of the species could be influenced by the size or weight of individual use in experiments. Smaller individuals consume relatively more than larger individuals, whereby the differences are much larger after calculating consumption per gram animal weight (cf. Dunger, 1958). The present study partly controlled for this by using very similarly sized individuals of the same species in the experiments. However, the different isopod species differed considerably in size (mass), with T. ratzeburgii and P. scaber weighing on average 30–50% less than T. rathkii or O. asellus. The observed differences in total consumption could thus simply be partly a factor of species size. Independent from the determined consumption rates or the possible causes for nutrient-resource preferences, the results of the present study show that the litter of introduced southern European oak species (Q. pubescens, Q. frainetto, Q. ilex) are clearly accepted by native isopod species. In almost all cases, the beech litter was less consumed than that of the oak species. Among the oak species, the pre-decomposed introduced Mediterranean litter was generally consumed in fairly equivalent amounts as the pre-decomposed local litter. Two species (P. scaber, T. ratzeburgii) even exhibited higher preferences for the introduced Q. ilex. Only with O. asellus (and partly P. scaber) was local oak litter considerably more consumed than introduced species. Compared to native beech or oak litter, litter from introduced tree species thus apparently do not
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influence the consumption rates of or primary decomposition by isopods. Therefore, a negative influence on faunal decomposition caused by introducing foreign oak species into German forests is not indicated by these experiments. At most, increased decomposition rates could be possible with the introduction of Q. ilex. Future studies must investigate further reactions of isopod species to the changing conditions caused by the litter of introduced tree species. For instance, the present study did not consider a differential litter influence on population parameters. Especially food quality and thus the assimilability of nutrients can affect growth and reproduction of isopods (Kautz et al., 2000; Rushton and Hassall, 1983b; Sousa et al., 1998). Furthermore, the reactions of faunal primary decomposers to changing environmental and climatic conditions (being the reasons for introducing Mediterranean tree species in Germany) must be studied (cf. David and Gillon, 2009; Dias et al., 2012; Hassall et al., 2010; Kight, 2009). For instance, Römbke et al. (2011) could show increased mortality of P. scaber due to increasing temperatures. Besides changes in leaf litter composition, such climatic effects may also influence primary decomposition processes. However, these have to date only been identified in laboratory tests. The actual influence of climatic changes (especially soil moisture) on saprophagous organism communities and their ecological functions under semi-field or field conditions still requires further research.
Acknowledgements The present study was financially supported by the research program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research and the Arts. The authors thank the members of the Department of Soil Zoology of the Senckenberg Museum of Natural History Görlitz for helpful comments during the experiments. Furthermore the Palmengarten and Botanical Garden in Frankfurt on the Main, Hesse, as well as the Botanical Garden in Tharandt, Saxony, are expressly thanked for access to litter material.
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Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter A. Gerlach a,b , D.J. Russell b,∗ , B. Jaeschke a,b , J. Römbke c a b c
Biodiversity and Climate Research Centre Frankfurt, Senckenberganlage 25, 60325 Frankfurt am Main, Germany Senckenberg Museum of Natural History, am Museum 1, 02826 Görlitz, Germany ECT Oekotoxikologie GmbH, 65439 Flörsheim/Main, Germany
a r t i c l e
i n f o
Article history: Received 5 February 2013 Received in revised form 7 February 2014 Accepted 11 February 2014 Keywords: Feeding activity Primary leaf litter decomposition Introduced leaf litter Isopoda Laboratory choice tests
a b s t r a c t Due to current predictions for Central Europe that forecast higher frequencies of hot and dry summers, Mediterranean drought-tolerant oak species are being evaluated as future forest trees for German forest sites that are becoming increasingly damaged by water deficit. As a result of planting foreign tree species, the leaf litter composition and thus the food resources of native saprophagous macroarthropods will change, possibly altering primary decomposition processes. Therefore, experiments concerning the acceptance and palatability of introduced versus native litter for native isopods were undertaken. Consumption rates of four native isopod species (Porcellio scaber, Oniscus asellus, Trachelipus rathkii, Trachelipus ratzeburgii) were investigated in laboratory choice tests with introduced (Quercus pubescens, Quercus frainetto, Quercus ilex) and comparable native (Fagus sylvatica, Quercus robur) leaf litter. Litter was characterized by measurement of C/N-ratios and lignin content. Although species-specific preferences of isopods could be observed in the experiments, Mediterranean oak litter was consumed by all investigated species. Furthermore, two isopod species even preferred the leaf litter of the introduced Q. ilex. Compared to native beech or oak litter, litter from these introduced tree species thus apparently do not negatively influence the consumption rates of terrestrial isopods. Possible reasons for the determined preferences are discussed. © 2014 Published by Elsevier B.V.
1. Introduction Current climate models predict a scenario for Central Europe that implies an increasing frequency of hot and dry summers as well as a raise of the average summer temperature of approximately 4 ◦ C within the next 50–100 years (Schär et al., 2004). As a long-term consequence of the altered climate, a change in the composition of native forest ecosystems can be expected (Kölling and Zimmermann, 2007; Pompe et al., 2009). The impact of increasing drought stress can already be observed in some forest sites in southern Hesse, Germany, where native tree species such as Fagus sylvatica and Quercus robur show strong water-deficit damage, intensified by human-induced groundwater drawdown (pers. comm.: Forestry Office Hesse). To prevent further forest degradation and to maintain sustainable forest ecosystems, a long-term study is ongoing to evaluate the potential of more drought tolerant Mediterranean oak species such as Quercus pubescens, Quercus
∗ Corresponding author. Tel.: +49 358147605502. E-mail address: [email protected] (D.J. Russell).
frainetto and Quercus ilex, among others, as future forest trees in these Central European sites (cf. Brüggemann et al., 2009; Holland and Brüggemann, 2011). Leaf litter decomposition is an important process in the nutrient cycle of forests (Chew, 1974; Swift and Anderson, 1989). The feeding activity of saprophagous macroarthropods, such as earthworms, diplopods and isopods, and the associated fragmentation of plant litter material plays an essential role in the incorporation of organic matter into soils. As a result of planting foreign tree species, the leaf litter composition and thus the food resources of the native soil macrofauna will change. To ensure that the introduction of foreign tree species into local forests does not affect primary decomposition processes, it is therefore necessary to assess how foreign leaf litter affects the feeding activity of the local macrofaunal decomposers. Results of a previous experiment, in which the consumption rate of local populations of the abundant diplopod species Glomeris marginata (Villers, 1789) from the experimental forest sites in southern Hesse was measured, indicate that consumption of introduced Mediterranean-oak leaf litter takes place at equivalent or even higher rates than that of domestic leaf species (Gerlach
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et al., 2012). It could thus been shown that this diplopod species does feed on the introduced leaf litter, at least in the absence of other food resources. These first results gave rise to the question how other native decomposer species respond to the changed nutrient resources caused by the altered litter sources. Terrestrial isopods also feed predominantly on fallen leaf litter and soft, decaying plant material (Gruner, 1966) and are also abundant in the forest study sites in question. Additionally their selective feeding behaviour (Hassall and Rushton, 1984; Ihnen and Zimmer, 2008; Loureiro et al., 2006; Zimmer et al., 2002) and sensitivity towards changes in diet (Caseiro et al., 2000; Farkas et al., 1996; Hornung et al., 1998) render isopods suitable test organisms for such experiments. The aim of the study was therefore to determine whether local isopod populations will feed on Mediterranean leaf litter, which litter species is preferred when given the choice between leaf litter of introduced (Q. pubescens, Q. frainetto, Q. ilex) and comparable native (F. sylvatica, Q. robur) tree species, and whether isopod consumption of the various litter species differ. Fig. 1. Setup of the chambered containers used in the feeding preference experiments.
2. Material and methods Feeding-preference experiments were carried out with four isopod species obtained from forest sites in southern Hesse, Germany, where Mediterranean oak species are being introduced. Trachelipus rathkii (Brandt, 1833), Porcellio scaber Latreille, 1804 and Oniscus asellus Linnaeus, 1758 were collected from mixed forests near Rüsselsheim (N49◦ 57 16.5 , E8◦ 24 58.4 ) and Trachelipus ratzeburgii (Brandt, 1833) from deciduous forests near Lampertheim (N49◦ 35 7.2 , E8◦ 34 42.3 ). In the laboratory, the animals were kept species-specifically in round transparent containers (diameter: 14 cm; height: 7 cm) with a bottom coating of a plaster of paris and activated charcoal mixture (20:1; 1 cm layer) and above that a 1 cm high soil mixture (obtained from the same forest sites from which the animals were collected), which was moistened bi-weekly. deadwood, bark, mosses and especially moistened fieldcollected litter (Q. robur, F. sylvatica, Tilia cordata, Carpinus betulus, Acer platanoides and more rarely Q. rubra) were added to the containers as food resources as well as concealment possibilities. The litter was provided ad libitum. Maximally 30 individuals of single species were kept in one container. The containers with the animals were maintained in a climate chamber with a 13:11-h light:dark rhythm and a diurnal temperature regime of 12 ◦ C (nighttime) to maximally 20 ◦ C (daytime). For the experiments, freshly fallen litter of the tree species F. sylvatica, Q. frainetto, Q. robur and Q. pubescens was collected in October and November 2008 from the Palmengarten and Botanical Garden in Frankfurt am Main (Hesse) as well as the Botanical Garden in Tharandt (Saxony) and air dried. Due to the low leaf abscission of the evergreen Q. ilex and resulting lack of litter in Germany, litter of this species was collected from its natural distributional area in southern France. Freshly fallen litter is decidedly less consumed than microbially pre-decomposed litter (Bertrand and Lumaret, 1992; Dunger, 1958; Gerlach et al., 2012; Hassall and Rushton, 1984). The litter was therefore exposed in litterbags (mesh size: 5 mm) for six months in the same woodlands from which the animals were obtained. After this, the litter was returned to the laboratory, air dried and stored dried until use in the experiments. For the experiments, litter was then used that showed no macroscopic signs of advanced decomposition. Parallel studies on field decomposition showed a litter decomposition rate of, on average, ca. 15% after six months, with the Mediterranean species being somewhat more decomposed than the Central European species (unpubl. data).
The feeding-preference experiments were carried out under the same climatic conditions in plastic containers of the same size and treated as mentioned above (however, without added organic material). For each of the four isopod species, six replicates (=containers) with isopods and six replicates without isopods (=controls) were studied (24 replicates + 24 controls total). The mass of the isopod individuals was, on average, 44.4 ± 13.0 mg (O. asellus), 23.9 ± 5.9 mg (P. scaber), 31.9 ± 10.8 mg (T. rathkii), and 20.0 ± 11.4 mg (T. ratzeburgii). In each replicated container, 400 mg ± 2 mg air-dried litter of each tree species, which was steeped in water for 24 h before beginning the experiments, and five previously weighed individuals of the respective isopod species (absent in the controls) was added. The interior space of the containers was divided into five chambers (Fig. 1), which ensured that the different litter species did not become mixed. To determine the initial dry weight of the litter, a portion (ca. 100 mg) of the airdried litter of each species was dried at 60 ◦ C to constant mass and weighed. All experiments continued for 10 days. After this period, the remaining litter was collected species-specifically, dried at 60 ◦ C to constant mass and weighed. The calculation of consumption by isopods (=mass loss) was performed according to the formula of David (1998):
C=
Wi − Wi D − Wf
D=
(SQRT(1 − D)) Wi − Wf
Wi
whereby C is the consumed litter in mg, Wi the initial dry weight of the litter sample before soaking in water, Wf the dry weight of the litter sample after the experiment and D the respective mass loss of the litter in the controls without animals. Consumption was calculated as per day values and was based on the total mass of the isopod individuals in the respective container. Since the palatability of the different litter species was expected to be limited by more indigestible components, the C/N-ratio and lignin content was quantified for each litter species used in the experiments. For this characterization, a portion of the litter exposed in the field for six months was first dried at 60 ◦ C and ground to a particle size of <1 mm. For each litter species, 6–7 mg of ground litter was sealed airtight in zinc capsules (8 replicates per species) and the total carbon and nitrogen contents measured in a vario PYRO cube element analyzer (Elementar Analysensysteme
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GmbH). The C/N-ratio of each litter species was calculated from these values (averages of the replicates). The least decomposable carbohydrates (acid-insoluble lignin = “Klason-lignin”) of each litter species was quantified via a two-step acid hydrolysis (cf. Hatfield et al., 1994; Hatfield and Fukushima, 2005). For this, 2 ml of 72% sulfuric acid (H2 SO4 ) was added to 200 mg of the dried and ground litter material (8 replicates of each litter species), homogenized and the mixture placed in a shaker for 60 min. at 30 ◦ C. Subsequently, 56 ml distilled water was added, resulting in a 2.5% H2 SO4 concentration. This mixture was then placed in an autoclave at 120 ◦ C for 60 min. to ensure a total hydrolysis. After allowing the mixture to cool, it was passed through a fibreglass filter (GF 92), rinsed six times with boiling distilled water until acid-free and subsequently dried at 105 ◦ C for 24 h. The mass of the remaining material was weighed and this “lignin” content calculated with the formula KLi =
(mLi × 100%) mEi
whereby KLi is the acid-insoluble lignin content of the litter sample in percent, mLi the mass of the remaining material (lignin) after the acid hydrolysis and mEi the mass of the original sample before hydrolysis (ca. 200 mg). To test for significant differences in the consumption of the different litter species, for each isopod species the data (consumed litter mass) was submitted to a variance analysis with leaf litter species as the main factor. Significance was tested using a nonparametric one-way ANOVA for multiple observations (=samples) per cell (=leaf litter species) (modified Friedman test; Zar, 1999). This ANOVA is based on ranked per sample data for each leaf litter species, on the r 2 rather than the F distribution and can easily handle unbalanced sampling designs (e.g., resulting from missing replicates caused by two exceptional cases of mortality during the experiments). A post hoc Tukey-like multiple comparison procedure for this non-parametric ANOVA (Zar, 1999) tested for significant differences of consumption between leaf litter species. The modified Friedman test was also used to test for significant differences in total consumption among the different isopod species as well as in the C/N-ratios and lignin content of the various litter species. To test for significant influences of C/N-ratio or lignin content of the litter, a covariance analysis (GLM Function of Statistica V. 10, StatSoft) was performed for each isopod species with the litter consumption (data of all litter species together) as the dependant variable and C/N-ratio and lignin content as covariables. For this analysis, all data were (ln + 1)-transformed. 3. Results 3.1. Chemical characterization of the litter species The largest C/N-ratios were measured in the litter of F. sylvatica (Table 1). Significantly lower values (r 2 = 27.040) were found in the litter of Q. robur (p < 0.05) and Q. ilex (p < 0.001). Little difference was found in the C/N-ratios of the deciduous oak species. Among the southern European oak litter, significant differences were found between Q. ilex and Q. pubescens (p < 0.01) as well as Q. frainetto (p < 0.05). Detected differences in the “lignin” contents of the oak species were not large (Table 1). The lowest lignin contents were found in the beech litter, which were significantly lower (r 2 = 14.010) than that of Q. robur as well as Q. ilex (p < 0.05). 3.2. Preferential consumption experiments The different isopod species used in the experiments exhibited significantly different total rates of litter consumption
Fig. 2. Consumption rates of the tested isopod species on total litter. Different letters denote significant differences in consumption. LW live weight.
(r 2 = 17.340, p < 0.001; Fig. 2). P. scaber (p < 0.05) and T. ratzeburgii (p < 0.01) both consumed more than double as much litter in total than O. asellus or T. rathkii. Clear differences in the preference for specific litter species could be determined for some of the studied isopod species (Fig. 3). O. asellus clearly preferred the native oak litter. The litter of the Mediterranean species was somewhat less consumed and no significant difference in the preference of the species could be determined. The beech litter was most strongly avoided and was significantly less consumed than the other central European species, Q. robur (r 2 = 11.370, p < 0.01). P. scaber preferred litter from Q. ilex and Q. robur, whereby the other three litter species were considerably less consumed. The average consumption of Q. ilex was significantly more (r 2 = 21.230) than that of F. sylvatica (p < 0.05), Q. pubescens (p < 0.01) or Q. frainetto (p < 0.01). Differences to Q. robur were generally not significant, with only Q. pubescens being less consumed than Q. robur (p < 0.05). The litter of the central European Q. robur and the Mediterranean Q. pubescens were utilized the most by T. rathkii, although no significant difference in consumption and thus no preference for any litter species could be detected (r 2 = 9.030, p = 0.06). T. ratzeburgii clearly preferred litter from Q. ilex, the consumption of which was significantly more (r 2 = 19.730) than that of F. sylvatica (p < 0.05), Q. robur (p < 0.001) or Q. pubescens (p < 0.01). No significant differences in the consumption of the litter of the deciduous tree species were detected. The central European Q. robur was the least preferred litter species. An effect of litter chemical parameters on consumption could be detected with some of the isopod species. A significant relationship between C/N-ratio and litter consumption was only found with O. asellus and T. ratzeburgii (Table 2), whereby as expected consumption was higher in litter with lower C/N-ratios. A significant effect of litter lignin content on consumption was detected with all isopod species except T. rathkii, which had showed no preference for
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Table 1 C/N-ratios and acid-insoluble “lignin” content (in %) of the litter species used in the experiments. Different letters represent significant differences between the litter species.
C/N-ratio “Lignin“
F. sylvatica
Q. robur
Q. pubescens
Q. frainetto
Q. ilex
43.01 ± 2.98 (a) 29.16 ± 2.44 (a)
33.51 ± 3.01 (b,c) 33.49 ± 2.80 (b)
36.77 ± 6.37 (a,b) 30.03 ± 3.63 (a,b)
36.09 ± 4.00 (a,b) 30.24 ± 2.40 (a,b)
24.62 ± 1.91 (c) 33.21 ± 2.07 (b)
Fig. 3. Consumption rates of the various isopod species on the five tested litter species. Different letters denote significant differences in consumption by the respective isopod species. LW live weight.
Table 2 Results of the covariance analyses of litter consumption by the tested isopod species (influence of litter parameters on consumption). C/N
O. asellus P. scaber T. rathkii T. ratzeburgii
Lignin
Error SS
SS
F
p
SS
F
p
2.234 0.120 1.254 10.873
5.594 0.597 2.742 47.068
0.025 0.447 0.109 <0.001
4.464 1.748 1.037 5.339
11.177 8.692 2.267 23.114
0.002 0.007 0.144 <0.001
10.783 5.429 12.343 6.237
C/N-ratio and lignin content were used as covariants. Significant results in bold, SS sums of squares.
any litter species. Unexpectedly, consumption by the other isopod species was apparently significantly higher in those litter species with higher lignin contents (Table 2). However, as the statistical sums of squares show, except for T. ratzeburgii, the effects of C/N or lignin content were lower than that of as yet unexplained factors (Error SS in Table 2). 4. Discussion In previous feeding experiments with litter of different tree species, oak and beech litter were among the least consumed leaf litter or – in a freshly fallen state – were not accepted at all by isopods (Dunger, 1958; Loginova and Busargina, 2005; Neuhauser and Hartenstein, 1978; Pobozsny, 1978). Due to their relatively high C/N-ratios, lignin and polyphenol contents, oak and beech litter are generally qualitatively inferior nutrient resources for the detritivore macrofauna than other litter species (Loranger-Merciris et al., 2008). In the present experiments, the beech and oak litter were readily accepted by the studied isopod species, possibly because no alternatives were offered. More palatable litter species were not tested, since in the forests in question primarily native beech and oak trees occur and are being replaced by Mediterranean oak species. Various studies on the food-resource preferences of isopods and the causes of these preferences have taken place in the past (i.e., Dunger, 1958; Nair, 1994; Neuhauser and Hartenstein, 1978; Pobozsny, 1978; Rushton and Hassall, 1983a). Especially chemical and partly also physical characteristics have been identified as potential factors for the palatability of leaf litter by detritivore macrofaunal species (Caseiro et al., 2000; David et al., 2001; Loranger-Merciris et al., 2008; McNeill and Southwood, 1978; Van Wensem et al., 1993). In preference experiments with Armadillidium vulgare, Abelho and Molles (2009) found a relationship
between consumption and the litter’s C/N-ratio, whereby nonnative leaf litter with a low C/N-ratio was more readily consumed. Cotrufo et al. (1998) found palatability differences in oak litter that had grown under different CO2 concentrations. In their study O. asellus exhibited reduced consumption of litter originating from high CO2 conditions, which possessed a higher C/N-ratio and lignin content. In the present study, the different isopods species exhibited different preferences for the various litter species. However, these preferences were apparently only partly influenced by the C/Nratios or the lignin contents of the litter. Only P. scaber and T. ratzeburgii preferred litter species with the lowest C/N-ratios, in accord with other studies (Abelho and Molles, 2009; Cotrufo et al., 1998). Interestingly, in contradiction to Cotrufo et al. (1998), all the presently studied isopods species exhibiting significant preferences favoured litter with higher lignin contents. Therefore, the lignin content seems to have no inhibitory influence on the consumption by isopods of these litter species. However, the absolute differences in lignin content among the studied litter species were minor. Furthermore, the data variability explained by C/N-ratios or lignin content were in most cases much smaller than the unexplained variability (Error SS in the covariance analyses). This indicates that factors other than C/N-ratio or lignin content were responsible for the species-specific differences in litter palatability. Besides nitrogen or lignin content, especially polyphenolic substances have been indicated as factors influencing palatability especially of harder litter species (Herlitzius and Herlitzius, 1977; King and Heath, 1967; Loranger-Merciris et al., 2008). On the other hand, in experiments with 25 different litter species, Neuhauser and Hartenstein (1978) could find no relationship between palatability and chemical litter composition. Other authors (e.g., Dunger, 1958; Pobozsny, 1978) could also not find any clear relationship between chemical properties of
Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006
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the litter and consumption by isopods. Especially in experiments with pre-decomposed (e.g., overwintered) litter, which is clearly favoured by isopods (Gere, 1956; Gunnarsson, 1987; Hassall and Rushton, 1984; Hassall et al., 1987; Stöckli, 1990; Van Wensem et al., 1993), differences in consumption among different litter species were much less than in freshly fallen litter and were generally independent from C/N-ratios (Dunger, 1958). The sequence of litter preference ascertained by Dunger (1958) corresponded with the order in which the litter had been decomposed by microorganisms (without faunal influence). This indicates that isopod palatability especially of litter in later stages of decomposition are influenced less by properties of the litter itself and more by the microbial colonization or activity on the litter (Zimmer and Topp, 1997). Microorganisms apparently increase the quality of litter as a nutrient resource (Hassall and Rushton, 1984) and are most likely a nutrient resource themselves (Gunnarsson and Tunlid, 1986; Ihnen and Zimmer, 2008; Ullrich et al., 1991; Zimmer and Topp, 1998). In experiments with P. scaber, Ihnen and Zimmer (2008) observed that especially low-quality food resources (pure cellulose) became much more attractive after microbial colonization. This isopod species particularly preferred litter colonized by fungi and fungal biomass is clearly reduced by isopod consumption (Hanlon and Anderson, 1980; Kayang et al., 1996). In the present study, a differential microbial colonization or “conditioning” of the litter is a possible further cause for the different litter preferences of the studied isopod species. The microbial activity is dependent on the litter properties (especially C/N-ratio), but more importantly on moisture and temperature (Beyer, 1992; Van Gestel et al., 1993). It is possible that different microclimatic conditions existed among the different litter species during the 6month exposition period prior to the experiments. It can therefore not be ruled out that the observed preferences were more influenced by microclimatic conditions during exposition and especially resulting microbial factors – which may not have been counteracted by air drying – than by the chemical properties of the litter itself. Besides the different preferences of the studied isopods species, different total amounts of consumption among the isopod species were also observed, with P. scaber and T. ratzeburgii showing the highest total consumption. This is in contrast to the study of Dunger (1958), in which the investigated species T. rathkii, P. scaber and O. asellus showed smaller differences in the total consumption of beech and oak litter. The determined different consumption of the species could be influenced by the size or weight of individual use in experiments. Smaller individuals consume relatively more than larger individuals, whereby the differences are much larger after calculating consumption per gram animal weight (cf. Dunger, 1958). The present study partly controlled for this by using very similarly sized individuals of the same species in the experiments. However, the different isopod species differed considerably in size (mass), with T. ratzeburgii and P. scaber weighing on average 30–50% less than T. rathkii or O. asellus. The observed differences in total consumption could thus simply be partly a factor of species size. Independent from the determined consumption rates or the possible causes for nutrient-resource preferences, the results of the present study show that the litter of introduced southern European oak species (Q. pubescens, Q. frainetto, Q. ilex) are clearly accepted by native isopod species. In almost all cases, the beech litter was less consumed than that of the oak species. Among the oak species, the pre-decomposed introduced Mediterranean litter was generally consumed in fairly equivalent amounts as the pre-decomposed local litter. Two species (P. scaber, T. ratzeburgii) even exhibited higher preferences for the introduced Q. ilex. Only with O. asellus (and partly P. scaber) was local oak litter considerably more consumed than introduced species. Compared to native beech or oak litter, litter from introduced tree species thus apparently do not
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influence the consumption rates of or primary decomposition by isopods. Therefore, a negative influence on faunal decomposition caused by introducing foreign oak species into German forests is not indicated by these experiments. At most, increased decomposition rates could be possible with the introduction of Q. ilex. Future studies must investigate further reactions of isopod species to the changing conditions caused by the litter of introduced tree species. For instance, the present study did not consider a differential litter influence on population parameters. Especially food quality and thus the assimilability of nutrients can affect growth and reproduction of isopods (Kautz et al., 2000; Rushton and Hassall, 1983b; Sousa et al., 1998). Furthermore, the reactions of faunal primary decomposers to changing environmental and climatic conditions (being the reasons for introducing Mediterranean tree species in Germany) must be studied (cf. David and Gillon, 2009; Dias et al., 2012; Hassall et al., 2010; Kight, 2009). For instance, Römbke et al. (2011) could show increased mortality of P. scaber due to increasing temperatures. Besides changes in leaf litter composition, such climatic effects may also influence primary decomposition processes. However, these have to date only been identified in laboratory tests. The actual influence of climatic changes (especially soil moisture) on saprophagous organism communities and their ecological functions under semi-field or field conditions still requires further research.
Acknowledgements The present study was financially supported by the research program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research and the Arts. The authors thank the members of the Department of Soil Zoology of the Senckenberg Museum of Natural History Görlitz for helpful comments during the experiments. Furthermore the Palmengarten and Botanical Garden in Frankfurt on the Main, Hesse, as well as the Botanical Garden in Tharandt, Saxony, are expressly thanked for access to litter material.
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Please cite this article in press as: Gerlach, A., et al., Feeding preferences of native terrestrial isopod species (Oniscoidea, Isopoda) for native and introduced leaf litter. Appl. Soil Ecol. (2014), http://dx.doi.org/10.1016/j.apsoil.2014.02.006