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Woodlice of the green houses at Ghent Botanical Garden and Botanic Garden Meise with two new exotic species for Belgium (Isopoda: Oniscidae)

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Abstract

In countries with a mild climate, greenhouses are often the only places, where exotic species can survive outside their native range. This is certainly the case for woodlice, of which the greenhouse fauna is relatively well studied in neighbouring countries. In Belgium, inventories of woodlice in greenhouses are very scarce. Here we report woodlouse inventories in Ghent Botanical Garden and Botanic Garden Meise during 2015-2017, resulting in fourteen species of which five are exotic. Two species are mentioned for the first time in Belgium being Nagurus cristatus (Dollfus, 1889) and Reductoniscus costulatus Kesselyák, 1930. An overview of woodlouse inventories in greenhouses in Belgium is given. Verwarmde kassen zijn, door hun constant en warmer klimaat, vaak de enige plaatsen waar exotische soorten kunnen overleven buiten hun natuurlijk verspreidingsgebied. Dit is ook zo voor pissebedden, waarvan de fauna van verwarmde kassen vrij goed bestudeerd is in onze buurlanden. In België zijn deze inventarissen schaars. In dit artikel rapporteren we enkele inventarisaties van pissebedden in de plantentuin in Gent en Meise gedurende 2015-2017. Dit resulteerde in veertien soorten waarvan vijf uitheems zijn. Twee soorten werden voor de eerste keer in België waargenomen nl. Nagurus cristatus (Dollfus, 1889) en Reductoniscus costulatus Kesselyák, 1930. Een overzicht van inventarisaties van pissebedden in verwarmde kassen in België is weergegeven. Résumé Les serres sont, en raison de leurs températures élevées, souvent les seuls endroits dans les pays à climat doux, où des espèces exotiques peuvent survivre car elles y trouvent des conditions similaires à celles de leur pays d'origine. C'est le cas en effet pour les cloportes exotiques. La faune des serres est relativement bien étudiée dans les pays voisins. En Belgique, les cloportes exotiques sont rares. Lors d'un inventaire aux jardins botaniques de Gand et de Meise effectué en 2015-2017, quatorze espèces de cloportes dont cinq exotiques ont été trouvées. Parmi ces dernières, deux espèces sont mentionnées pour la première fois de Belgique : Nagurus cristatus (Dollfus, 1889) et Reductoniscus costulatus Kesselyák, 1930. Nous donnons aussi un aperçu des cloportes des serres en Belgique.
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Bulletin de la Société royale belge d’Entomologie/Bulletin van de Koninklijke Belgische Vereniging voor Entomologie, 153 (2017): 109–112
Woodlice of the green houses at Ghent Botanical Garden and
Botanic Garden Meise with two new exotic species for Belgium
(Isopoda: Oniscidae)
Pallieter DE SMEDT1,2, Gert ARIJS2, Stijn SEGERS2 & Pepijn BOERAEVE²
1 Forest & Nature Lab, Ghent University, Geraardsbergsesteenweg 267, B-9090 Melle (Gontrode), Belgium
(Corresponding author, e-mail: Pallieter.desmedt@ugent.be)
2 SPINICORNIS, Mispeldonk 2, B-2820 Bonheiden, Belgium (e-mail: info@spinicornis.be)
Abstract
In countries with a mild climate, greenhouses are often the only places, where exotic species can
survive outside their native range. This is certainly the case for woodlice, of which the greenhouse
fauna is relatively well studied in neighbouring countries. In Belgium, inventories of woodlice in
greenhouses are very scarce. Here we report woodlouse inventories in Ghent Botanical Garden and
Botanic Garden Meise during 2015-2017, resulting in fourteen species of which five are exotic. Two
species are mentioned for the first time in Belgium being Nagurus cristatus (Dollfus, 1889) and
Reductoniscus costulatus Kesselyák, 1930. An overview of woodlouse inventories in greenhouses in
Belgium is given.
Keywords: Belgium, Distribution, Greenhouse fauna, Nagurus cristatus, Reductoniscus costulatus,
Woodlouse
Samenvatting
Verwarmde kassen zijn, door hun constant en warmer klimaat, vaak de enige plaatsen waar exotische
soorten kunnen overleven buiten hun natuurlijk verspreidingsgebied. Dit is ook zo voor pissebedden,
waarvan de fauna van verwarmde kassen vrij goed bestudeerd is in onze buurlanden. In België zijn
deze inventarissen schaars. In dit artikel rapporteren we enkele inventarisaties van pissebedden in de
plantentuin in Gent en Meise gedurende 2015-2017. Dit resulteerde in veertien soorten waarvan vijf
uitheems zijn. Twee soorten werden voor de eerste keer in België waargenomen nl. Nagurus cristatus
(Dollfus, 1889) en Reductoniscus costulatus Kesselyák, 1930. Een overzicht van inventarisaties van
pissebedden in verwarmde kassen in België is weergegeven.
Résumé
Les serres sont, en raison de leurs températures élevées, souvent les seuls endroits dans les pays à
climat doux, où des espèces exotiques peuvent survivre car elles y trouvent des conditions similaires à
celles de leur pays d’origine. C'est le cas en effet pour les cloportes exotiques. La faune des serres est
relativement bien étudiée dans les pays voisins. En Belgique, les cloportes exotiques sont rares. Lors
d’un inventaire aux jardins botaniques de Gand et de Meise effectué en 2015-2017, quatorze espèces
de cloportes dont cinq exotiques ont été trouvées. Parmi ces dernières, deux espèces sont mentionnées
pour la première fois de Belgique : Nagurus cristatus (Dollfus, 1889) et Reductoniscus costulatus
Kesselyák, 1930. Nous donnons aussi un aperçu des cloportes des serres en Belgique.
Introduction
Greenhouses are very often the only places where exotic species can survive in temperate regions.
Many species are introduced via the import of exotic plants and can often establish viable populations
inside the greenhouses. Although many species are not able to survive outside greenhouses it sounds
reasonable that they might be able to do this once the outside climate gets more suitable. Therefore, it
110
is interesting to know which species occur in greenhouses to evaluate the change that they will
establish populations in the wild. Woodlice in greenhouses and heated environments in e.g. zoos are
studied relatively well in the Netherlands (BERG et al., 2008) with eight species that are restricted to
greenhouses. Studies from Belgium are however extremely scarce. In Belgium, only two species are
known to exclusively occur in greenhouses being Cordioniscus stebbingii (Patience, 1907) and
Trichorina tomentosa (Budde-Lund, 1893) while some others were first reported from greenhouses
but appeared to be native with the discovery of wild populations e.g. Trichoniscus pygmaeus Sars,
1898, Haplophthalmus danicus Budde-Lund, 1880 and Armadillidium nasatum Budde-Lund, 1885
(BAGNALL, 1907). The last note on woodlice from greenhouses in Belgium dates back to 1973
(KERSMAEKERS, 1973), while the last reported inventory was done in 1956 (POLK & VAN OYE, 1956).
Therefore, an update on woodlice in Belgian greenhouses could be interesting more than 60 years after
the last inventory. This was the reason to undertake some short visits to the greenhouses of Ghent
Botanical Garden and Botanic Garden Meise in 2015-2017 to evaluate the presence of woodlouse
species in greenhouses.
Surveys
During four inventories between 2015 and 2017 to Ghent botanical garden and one to Botanic Garden
Meise, we found a total of fourteen woodlouse species mostly underneath stones and flowerpots
(Table 1). Five out of fourteen species can be considered as exotic, of which two species and one
genus mentioned for the first time in Belgium. These are Nagurus cristatus (Dollfus, 1889),
Reductoniscus costulatus Kesselyák, 1930 and Synarmadillo spec. A visit to Botanic Garden Meise in
May 2016 did not result in additional species but resulted in a second location for N. cristatus. The
two new species and new genus are shortly discussed below. The collected specimens are deposited in
the private collection of Pallieter De Smedt.
Table 1. Species reported from greenhouses in Belgium by BAGNALL (1907, 1908), POLK & VAN OYE (1956)
and this study. KERSMAEKERS (1973) reported again T. tomentosa from the botanical gardens of Ghent but this
single observation was not reported in the table. X: presence of the species, (X) species of which BAGNALL
(1907) did not report if it was collected in Brussels or Antwerp, X* specimens collected at Ghent botanical
garden in Juli 1949 that were stored at the Natural History Museum in Leiden (the Netherlands) and re-identified
by POLK & VAN OYE (1956). POLK & VAN OYE (1956) reports a woodlouse of the genus Rhyscotus. He
mentions that the specimen was send to Prof. Vandel in Toulouse but after this, there has been no report of the
species anymore. Therefore, we did not include it in the list.
BAGNALL
1907, 1908
POLK & VAN OYE
1956
This study
2015-2017
Brussel Antwerp Ghent Antwerp Ghent Meise
Androniscus dentiger Verhoeff, 1908 X X X* X X
Armadillidium nasatum Budde-Lund, 1885 X X X X X
Armadillidium vulgare Latreille, 1804 X
Cordioniscus stebbingi (Patience, 1907) X X* X
Cylisticus convexus (De Geer, 1778) (X) (X)
Haplophthalmus danicus Budde-Lund, 1880 X X X
Haplophthalmus mengii (Zaddach, 1844) X
Nagurus cristatus (Dollfus, 1889) X X
Oniscus asellus Linnaeus, 1758 (X) (X) X X
Philoscia muscorum (Scopoli, 1763) (X) (X) X
Platyarthrus hoffmannsseggii Brandt, 1833 X
Porcellio dilatatus Brandt, 1833 X X X
Porcellio scaber Latreille, 1804 (X) (X) X* X X X
Porcellio spinicornis Say, 1818 X X
Porcellionides pruinosus (Brandt, 1833) (X) (X) X
Reductoniscus costulatus Kesselyák, 1930 X
Synarmadillo spec. X
Trichorina tomentosa (Budde-Lund, 1893) X X X
Trichoniscus pusillus s.l. (X) (X)
Trichoniscus pygmaeus Sars, 1898 X X X
111
Fig. 1. Nagurus cristatus (photograph: Gert Arijs). Fig. 2. Reductoniscus costulatus (photograph: Walte
r
P. Pflieger).
Nagurus cristatus (Dollfus, 1889) Belg. sp. nov.
MATERIAL: Ghent, greenhouse, 31UES5053, 5.II.2015, 2ƂƂ, leg. & det. Pallieter De Smedt ʊ
10.VII.2015, 2ƂƂ, leg. & det. Pallieter De Smedt ʊ 18.XII.2015, 50 ex., det. Pallieter De Smedt ʊ
17.III.2017, 10 ex., det. Pallieter De Smedt ʊ Meise, greenhouse, 31UES9342, 1.V.2016, 1Ƃ, det.
Gert Arijs.
The species (Fig. 1) is pantropical and occurs in greenhouses in temperate regions (SCHMALFUSS,
2003). Nagurus cristatus was very common in the subtropical greenhouses where it mostly occurred
underneath flowerpots on concrete. All collected specimens were females. Males are very rare and the
species reproduces asexual (BERG & WIJNHOVEN, 1997). The species was also found in greenhouses
at Botanic Garden Meise. See GREGORY (2014) for drawings of the species.
Reductoniscus costulatus Kesselyák, 1930 Belg. sp. nov.
MATERIAL: Ghent, greenhouse, 31UES5053, 5.II.2015, 1ex., leg. & det. Pallieter De Smedt.
The species (Fig. 2) is known form the Seychelles, Mauritius, Malaysia and Hawaiian Islands but also
occurs in greenhouses in Europe (SCHMALFUSS, 2003). Only one specimen was found underneath a
stone on humid soil in the tropical greenhouse. The habitat corresponds to sightings in greenhouses in
the Netherlands where this species is found under humid conditions (BERG et al., 2008). See
GREGORY (2014) for drawings of the species.
Synarmadillo spec.
MATERIAL: Ghent, greenhouse, 31UES5053, 5.II.2015, 1ex., det. Pallieter De Smedt. (The specimen
got lost for further identification.)
A single individual of the genus Synarmadillo was found in the tropical greenhouse at Ghent botanical
garden. After collection, the specimen got lost. Therefore, it was not possible to identify the individual
to species level. In a Dutch greenhouse Synarmadillo pallidus Arcangeli, 1950 has been reported.
A species originally described from Zaïre (SCHMALFUSS, 2003). In the Netherlands, this species has
been found in only one greenhouse and is absent from Germany and the UK (BERG et al., 2008).
Therefore, it is not certain if the specimen at Ghent botanical gardens is the same species.
SCHMALFUSS (2003) reports more than 20 species within the genus Synarmadillo.
The nine native species (Table 1) recorded in the greenhouses from Ghent and Meise are all very
common or common in Belgium. Armadillidium vulgare and Platyarthrus hoffmannsseggii are
recorded for the first time inside greenhouses in Belgium.
112
Discussion
Twenty woodlouse species have been recorded in Belgian greenhouses up to date of which five can be
considered as exotic. Four of these species are widespread in greenhouses across the Netherlands
(BERG et al., 2008) and the rest of Europe (SCHMALFUSS 2003) and are easily transported via
horticultural trade. Therefore, they can be expected to occur in many greenhouses in Belgium as well.
Only the status of the Synarmadillo species remains somewhat unclear. Hopefully, a second specimen
can be found in the near future to identify the species. Furthermore, there are three other species
recorded in Dutch greenhouses (BERG et al., 2008) and no less than 17 species are known from
greenhouses in the UK (GREGORY, 2014). Inventories in Belgian greenhouses can probably extend
table 1 with some of these species. Alongside the exotic species, also some native species are
frequently found in greenhouses like P. scaber, H. danicus, T. pygmaeus, A. dentiger and A. nasatum.
The latter two occur, outside greenhouses, mostly on anthropogenic disturbed areas like graveyards in
the northern part of the country. In the southern part of Belgium, they are not anthropogenic. The other
three species are common in most areas in Belgium.
We hope that this article can encourage people to have a closer look at woodlice in Belgian
greenhouses, both botanical greenhouses and in zoos. In Belgium, there is no report of woodlouse
inventories in zoos while there is evidence that zoos can harbour some interesting species (BERG et al.,
2008).
References
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stebbingi Patience. Annales de la Société royale de Zoologie et de Malacologie de Belgique, 43: 127–129.
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... Studies on woodlice in heated greenhouses are not abundant worldwide. Some relevant examples are those of Bagnall (1909) in Ireland, Holthuis (1945) in the Netherlands, Holthuis (1947Holthuis ( , 1948 in the United Kingdom, and more recently of De Smedt et al. (2017) in Belgium and Carpio-Díaz et al. (2018) in Colombia. In Switzerland, only Holzapfel (1932) examined woodlice in the heated greenhouses of the Botanical Garden of Bern and reported the occurrence of nine species: Androniscus dentiger Verhoeff, 1908a, Armadillidium nasatum Budde-Lund, 1885, Haplophthalmus danicus Budde-Lund, 1880, Haplophthalmus mengii (Zaddach, 1844, Hyloniscus riparius (C.L. Koch, 1838), Oniscus asellus Linnaeus, 1758, Porcellio scaber Latreille, 1804, Trachelipus rathkii (Brandt, 1833) and Trichoniscus pygmaeus Sars, 1898. ...
... Abbreviations of the greenhouse names as in Table 1. Remarks: This species has been recorded in Seychelles, Mauritius, Malaysia and Hawaii, as well as in greenhouses of Belgium, France, Germany, Hungary, the Netherlands, and in the United Kingdom (Bagnall, 1909;Kesselyák, 1930;Holthuis, 1945Holthuis, , 1947Holthuis, , 1948Gruner, 1966;Berg, 1997;Soesbergen, 2003;Kontschán, 2004;Berg et al., 2008;Vilisics & Hornung, 2009;Cochard et al., 2010;Gregory, 2009Gregory, , 2014Séchet & Noël, 2015;De Smedt et al., 2017, 2018. This is the fi rst record for Switzerland. ...
... This has also contributed to its dispersal. In Europe, the species can be found in greenhouses of many countries: Austria, Belgium, Czech Republic, Denmark, France, Germany, Hungary, Ireland, the Netherlands, Norway, Poland, United Kingdom, and Switzerland (Dollfus, 1896;Foster, 1911;Pack-Beresford & Foster, 1913;Meinertz, 1934Meinertz, , 1936Holthuis, 1945Holthuis, , 1948Holthuis, , 1956Polk, 1959;Jędryczkowski, 1979Jędryczkowski, , 1981Olsen, 1995;Berg, 1997;Wouters et al., 2000;Korsós et al., 2002;Soesbergen, 2003;Farkas, 2007;Berg et al., 2008;Vilisics & Hornung, 2009;Cochard et al., 2010;Farkas & Vilisics, 2013;Gregory, 2009Gregory, , 2014Séchet & Noël, 2015;De Smedt et al., 2017, 2018Jaskul et al., 2019). ...
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Woodlice (Isopoda: Oniscidea) represents a group of arthropods that has been neglected in Switzerland. The last comprehensive review on Swiss woodlice was published more than a cent ury ago. In the present work, we update the checklist of woodlice in Switzerland and provide information on the distribution of each species as well as further remarks. We considered information on recent records of woodlice from different regions and habitats of Switzerland and present new species records, which are mainly based on a survey of heated reenhouses in nine botanical gardens and other institutions across Switzerland and a fi eld survey in the Swiss National Park. Altogether, we found six new species for Switzerland. Five of them are exotic species, captured so far exclusively in heated greenhouses: Reductoniscus costulatus Kesselyák, 1930, Venezillo parvus (Budde-Lund, 1885), Chaetophiloscia cellaria (Dollfus, 1884), Nagurus cristatus (Dollfus, 1889), Buddelundiella cataractae Verhoeff, 1930b, and Miktoniscus linearis (Patience, 1908). Thus, the updated checklist of terrestrial woodlice in Switzerland comprises 50 species.
... Certain exotic species are in Belgium only recorded from greenhouses and do not have free-living populations. These species are discussed in a recent paper dedicated to greenhouse species in Belgium (De Smedt et al. 2017a) and only briefly in a separate section of this discussion as they are not considered as part of the Belgian fauna. ...
... Bibliography: Moniez (1886), Preudhomme de Borre (1886b), Lameere (1897), Maitland (1897), Bagnall (1907Bagnall ( , 1908, Vandel (1933), Leruth (1936aLeruth ( ,b,c,d,e, 1937b, Lameere (1938), Leruth (1939), Capart (1942, Delhez and Houssa (1969), , Delhez and Kersmaekers (1973), Gilson and Hubart (1973), Kersmaekers and Deroeck (1973), Holthuis (1983), Tavernier andWouters (1989, 1991), Boon et al. (1993), Delhez et al. (1999), Wouters et al. (2000), Dethier and Hubart (2010), Segers (2015), De Smedt et al. (2017a). ...
... Bibliography: Bagnall (1907Bagnall ( , 1908, Polk and Van Oye (1956), , Kersmaekers (1974), Tavernier andWouters (1989,1991), Boon et al. (1993), Wouters et al. (2000), Lock (2007), Segers (2015), De Smedt et al. (2016cSmedt et al. ( , 2017a. ...
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Humans strongly affect landscapes via land-use changes. Forests have been profoundly fragmented around the world due to land conversion for agriculture. Hence, many landscapes consist of small, isolated forest fragments embedded in an agricultural matrix, which puts severe pressure on the forests’ biodiversity and the multiple ecosystem services they can provide. Within the European Union, no less than 40% of the forest habitat lies within 100 m of other land use types and can thus be regarded as forest edge. Small forest fragments suffer from strong edge effects because of their large edge-to-interior ratio. Forest edges differ from forest interiors in abiotic conditions. Forest edges are characterised by higher light levels, wind speeds, air and soil temperatures, lower air humidity and soil moisture and increased soil pH. Forest edges also receive higher nutrient inputs through higher litter fall quantity and quality, via spill-over from adjacent land-use types such as agricultural fields and through higher atmospheric deposition. These environmental differences between forest edge and interior impact the distribution of biota which is relatively well studied for plants, birds, or above-ground invertebrates, but have remained poorly explored for the soil fauna community. Despite its extreme diversity, soil associated taxa are poorly studied. A good knowledge on taxonomy is essential to understand and study species-specific distribution patterns; therefore, we start with contributing taxonomical knowledge of woodlice (a dominant letter-dwelling arthropod taxa) in Belgium in Chapter 2. We compiled a new checklist and assessed the status of occurrence of all Belgian species, contributing to the current knowledge on a large share of the Western-European woodlice fauna. This was done based on a review of 142 papers on Belgian woodlice, re-identifying museum collections and performing extensive field surveys. We added nine species (25%) to the Belgian checklist and assessed for the first time the state of occurrence of all Belgian species. Based on good taxonomical knowledge we studied species-specific distribution patterns of woodlice and millipedes along forest edge to interior gradients in six forest stands in Northern Belgium (Chapter 3). Woodlice abundance strongly decreased from the forest edge towards the forest interior, while millipede abundance only decreased after a few meters inside the forest along the same gradient. The patterns strongly differed per species and could be linked to species’ desiccation resistance as well as to some key environmental factors such as litter quality, leaf area index, pH and soil nutrients. Abundance along forest edge to interior gradients across all species were independent from forest stand or dominating tree species, while dominating tree species strongly influenced species composition. We hypothesized that species-specific distribution along forest edge-to-interior gradients could be predicted based on species’ desiccation resistance because of the strong differences in temperature and soil moisture content between forest edges and forest interiors. We tested this for woodlice distribution across 10 landscapes in Europe covering 160 forest patches (Chapter 4). We saw that drought sensitive species reduce their activity-density in forest edges while drought resistant species flourish. Resulting in higher overall activity-density in forest edges. To disentangle the importance of increased temperature and reduced moisture for macro-detritvore functioning in the forest ecosystem we performed a full-factorial field experiment in a deciduous forest fragment in Northern Belgium (Chapter 5). We installed microcosms with four detritivore treatments (woodlice, millipedes, both woodlice and millipedes and a control) under four environmental treatments being a reduced moisture treatment (using a rainout shelter above the microcosms), an increased temperature treatment (using open top chambers), a combination of both treatments and a control. We added low and high quality litter to test for litter breakdown by macro-detritivores under the different treatments. We found mainly moisture availability to be a limiting factor for litter breakdown of high quality litter, not for low quality litter. Macro-detritivore identity proved to be important for the breakdown of low quality litter, not for high quality litter. Relative consumption rates of macro-detritivores were not influenced by any environmental treatment but depended on macro-detritivore identity for low quality litter. Woodlice were more efficient for the breakdown of low quality litter compared to millipedes. The next step was to identify drivers of macro-detritivore distribution across spatial scales. In 224 forest patches in 14 landscapes in Western Europe, we explored woodlice and millipede distribution at within-fragment level (forest edge vs forest interior), fragment level and landscape level (Chapter 6). Distribution of woodlice and millipedes was mainly affected by differences between forest edges and interiors and the landscape disturbance intensity. Forest edges had higher activity-density of woodlice and millipedes. Forest fragments located in high disturbance landscapes (high land use intensity) had higher activity-density compared to forests located in lower disturbance landscapes. In high disturbance landscapes, macro-detritivores probably profit from higher atmospheric nitrogen input and spill over of fertilizers from adjacent fields in forest edges embedded in high disturbance landscapes. We investigated forest edge-to-interior distribution patterns for multiple litter-dwelling arthropod taxa in 192 forest patches in 12 landscapes in Western Europe (Chapter 7). Next to woodlice and millipedes, also spiders are more abundant in forest edges compared to forest interiors, while there was no difference for carabid beetles, harvestmen and centipedes. Older forests showed stronger edge effects when the distance between forest edge and interior increased, while the strength of the edge effect did not increase in recent forests. Species composition differed more with increasing distance between edge and interiors in older forests and southern forest edges while there was no effect in recent forests and northern forest edges. Edges bordering more structural continuous habitat (i.e. grasslands) showed stronger edge effects for carabid beetles and spiders compared to higher edge contrast (i.e. edges bordered by croplands). In conclusion, edge effects strongly influence abundance and species composition of litter-dwelling arthropods in small forest fragments in Europe (1). Species-specific desiccation resistance, which we identified as a key response trait, can explain litter-dwelling arthropod distribution patterns (2). Forest edges filter species based on their response traits, resulting in a different community composition between forest edges and interiors with associated differences in species effect traits (e.g. feeding rate). This so-called response-and-effecttrait framework gives us a powerful tool to understand litter-dwelling arthropod distribution and predict the effects on ecosystem functioning (via effect traits) such as nutrient cycling, carbon sequestration etc.
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Woodlice (Isopoda: Oniscidea) from the Eden project, Cornwall, with descriptions of species new to Britain and poorly known British species
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On some terrestrial Isopod Crustacea new to the Fauna of Belgium
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On the occurrence in Belgium of a recently described terrestrial Isopod
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