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Terrestrial isopods and millipedes, members of the invertebrate macro-decomposer guild, were collected through pitfall traps in three Swiss cities (Zurich, Lucerne, Lugano). A total of 7, 198 individuals of 17 isopod species (7093 ind.), and 10 millipede species (105 ind.) were captured. Besides the Alpine endemic isopod (Trichoniscus alemannicus) and millipede (Cylindroiulus verhoeffi), urban assemblages were mainly composed of widespread, native European and even cosmopolitan species, which are frequent in anthropogenic areas. Overall species richness (isopods and millipedes combined) was similar in Zurich (17 species) and Lucerne (16), while only 13 species were sampled in Lugano. According to the Sørensen index of similarity, species composition of Zurich and Lucerne were more alike, while the one of Lugano was more distinct from the other two cities. This result can be explained by the spatial proximity of Zurich and Lucerne in the north of the Alps compared to Lugano, which is located more distantly and in the south of the Alps. Dominant isopods and millipedes in Zurich and Lucerne were found to be widespread synanthropic species in temperate Europe(Porcellio scaber, Trachelipus rathkii and Ophyiulus pilosus) while the dominant isopod in Lugano (Trachelipus razzautii) is a species with a north-eastern Mediterranean distribution. Our study reveals that the urban millipede and isopod fauna in Swiss cities mainly consists of widespread species, but species of narrower distribution (e.g. Trichoniscus alemannicus, Cylindroiulus verhoeffi) may also find suitable habitats in cities. Despite some signs of biotic homogenization, our study also found compositional differences of millipede and isopod assemblages between northern and southern cities that suggest geographical effects of the regional species pool.
Decomposers, urbanization, woodlice, urban biodiversity, arthropods
As one of the major factors of global change, urbanization and its effects on biodiversity have attracted great scientific attention in the past decade (e.g.
Urban soil meso- and macro-arthropods have received less attention (but see
Soil macro- meso- and micro-invertebrates contribute in the decomposition cascade by either fragmenting, or further mineralizing dead plant matter (
Millipedes and isopods are known to inhabit European urban habitats, mainly by cosmopolitan and Holarctic species (
Urban assemblages of soil invertebrates show controversial patterns of species composition: some studies suggest that species compositions differ along urbanization gradients (
The study took place in three Swiss cities, namely Zurich (371, 000 inhabitants /92 km2), Lucerne (59, 000 /24 km2) and Lugano (49, 000/ 26 km2), which represent small to medium sized cities in central Europe. The cities studied lay on a north to south gradient (approx. 200 km, with Lugano south of the Alps) and all are bordered by a lake and mountains > 800 m. Originally, 36 sampling sites were selected in each city but at the end only 106 could be used for the analyses: 36 in Zurich and Lugano, 34 in Lucerne.
The three cities share common features such as historical centres, residential areas, business quarters, public green areas, parks and cemeteries, and former industrial areas. The cities are characterized by moderate temperature (North: average January temperature 1°C, July 17°C; South: January 3°C, July 20°C) with an annual precipitation of 1000 mm for Zurich, 1150 mm for Lucerne and 1600 mm for Lugano.
Within each of the three cities sampling points were selected along a continuous urbanization gradient, which was measured as the fraction of sealed and built area in the 50 m radius around the sampling points. The selection of the individual sampling points followed a reasoned choice sampling strategy to cover the entire urbanisation gradient (3% to 92% sealed and built area). We included a wide range of urban habitat types (private gardens, semi-public spaces of apartment buildings, public parks and courtyards of industrial buildings) into the study. Mean distance between study sites was 388 m (± 21 m SE). A minimal distance of 250 metres was kept between sampling sites and the city fringe. Precise locations of the study sites are given in
Isopods and millipedes were sampled through pitfall traps, consisting of 3 plastic cups (opening diameter 75 mm) per trap site recessed into the soil and arranged in an isosceles triangle with a distance of one meter. Transparent roofs installed approximately 8 cm above the cups provided protection from rain. Traps were emptied weekly during 7 weeks from June 13th to August 3rd 2006 (
Identification of millipedes was based on
We used species richness (number of species) as the most common measure to quantify biodiversity (
The similarity between the millipede and isopod species assemblages combined sampled in the three cities was assessed using the Sørensen index (
Overall, 17 species of isopods (7015 individuals) and 8 species millipedes (98 ind.) were identified in the three studied Swiss cities; one isopod could only be identified at genus level, while two millipedes only at family level.
Isopod species richness was highest in Lucerne (14 species) and lowest in Lugano (10 species), with 11 species in Zurich (Table 1). One third (6 species) of all Isopoda species occurred in all three cities. Five additional species were captured in both Lucerne and Zurich but not in Lugano (Table 1). Three isopod species were dominant in the three cities (Fig. 1), i.e. the cosmopolitan Porcellio scaber Latreille, 1804 in Zurich (1216 individuals, 32% relative abundance); the widespread European Trachelipus rathkii (Brandt, 1833)in Zurich (1934, 33%) and Lucerne (1234, 72%), and the Mediterranean Trachelipus razzautii (Arcangeli, 1913) in Lugano (307, 52.3%).
Incidence of isopod and millipede species in sampling sites in the cities of Zurich, Lucerne, and Lugano.
Species | Species occurrences in traps | ||
---|---|---|---|
Zurich (n=36) | Lucerne (n=34) | Lugano (n=36) | |
Androniscus dentiger Verhoeff, 1908 | + | + | 0 |
Armadillidium nasatum Budde-Lund, 1885 | + | + | + |
Armadillidium vulgare (Latreille, 1804) | + | + | + |
Cylisticus convexus (De Geer, 1778) | + | + | 0 |
Haplophthalmus danicus Budde-Lund, 1880 | 0 | 0 | + |
Hyloniscus riparius (C. Koch, 1838) | +! | +! | + |
Ligidium hypnorum (Cuvier, 1792) | 0 | + | 0 |
Oniscus asellus Linnaeus, 1758 | +! | +! | 0 |
Orthometopon planum (Budde-Lund, 1885) | 0 | 0 | + |
Philoscia muscorum (Scopoli, 1763) | + | +! | 0 |
Platyarthrus hoffmannseggii (Budde-Lund, 1893)* | + | + | + |
Porcellio scaber Latreille, 1704 | +! | +! | + |
Porcellionides pruinosus (Brandt, 1833) | + | 0 | 0 |
Trachelipus rathkii (Brandt, 1833) | +! | +! | + |
Trachelipus razzautii (Arcangeli, 1913) | 0 | 0 | +! |
Trichoniscus alemannicus Verhoeff, 1917 | + | + | 0 |
Trichoniscus pusillus Brandt, 1833 | 0 | + | 0 |
Trichoniscus sp. | 0 | + | + |
Isopod species | 11 | 13 | 9 |
Isopod specimens | 3738 | 2690 | 587 |
Brachydesmus superus Latzel, 1884 | + | 0 | + |
Cylindroiulus caeruleocinctus (Wood, 1864) | + | 0 | 0 |
Cylindroiulus verhoeffi (Brolemann, 1896) | 0 | 0 | + |
Nemasoma varicorne C. L. Koch, 1847 | + | 0 | 0 |
Ophyiulus pilosus (Newport, 1842) | + | + | +! |
Oxidus gracilis (C. L. Koch, 1847) | 0 | + | + |
Polydesmus angustus Latzel, 1884 | 0 | + | 0 |
Propolydesmus testaceus (C. L. Koch, 1847) | + | 0 | 0 |
Chordeumatidae sp. | 0 | + | 0 |
Craspedosomatidae sp. | 0 | 0 | + |
indet + | + | 0 | 0 |
Millipede species | 5 | 3 | 4 |
Millipede specimens | 32 | 27 | 46 |
Legend: 0: species absent; +: species present; +!: species present at > 25% of sites per city; * taxa identified as a myrmecophilous species (ubiquitous in ant nests); number of specimens were not counted, see text for explanation
Abundances of isopods and millipedes in Zurich, Lucerne and Lugano in logarithmic scale. Dashed line separates isopods (on the left) from millipedes. Black bars represent abundances, white circles show the species’ incidences per all sites per city.
We found seven millipede species in Zurich, four in Lugano, and three in Lucerne. Ophyiulus pilosus (Newport, 1842) occurred in all three cities, but was dominant in Zurich (62.5%) and Lugano (42.5%), while Polydesmus angustus Latzel, 1884 was dominant in Lucerne (85%) (Fig. 1). Two other species [Brachydesmus superus Latzel, 1884 and Oxydus gracilis (C. L. Koch, 1847)] were exclusively found in Zurich and Lucerne (Table 1).
Millipedes show a different occurrence pattern than isopods, for the latter the differences among the three cities seem to be greater. Overall, 50% of all millipede and isopod species were observed in only one city. The mean number of individuals for isopods and millipedes per site varied substantially in the three cities, i.e. Lucerne [mean 159.7 (SE: 75.3)], Lugano [mean 45 (SE: 12.56)], and Zurich [mean 221.7 (SE: 77.22)]. Sørensen similarity index of species compositions (isopods and millipedes combined) was highest between Zurich and Lucerne (0.67) and lowest between Zurich and Lugano (0.40), with an intermediate value of 0.58 between Lucerne and Lugano.
Species incidenceIncidences of isopod and millipede species per city were generally low, i.e. below 10% of the total number of traps (Figure 1). For isopods, the most abundant species were also the most frequent ones. The most widespread isopod in Zurich was Porcellio scaber (55.6% of 36 traps), while in Lucerne it was Trachelipus rathkii (58.8% of 34 traps), and in Lugano Trachelipus razzautii (44.4% of 36 traps). Lucerne and Zurich, cities located north of the Alps, shared four isopod species [Hyloniscus riparius (C. Koch, 1838), Porcellio scaber, Oniscus asellus Linnaeus, 1758, and Trachelipus rathkii] out of the five most frequently sampled (> 25%). The only millipede with an incidence over 25% (out of 36 traps) was Ophyiulus pilosus in Lugano, while the rest of millipede species of our study occurred with incidences < 10% (Figure 1).
There were also examples where higher relative abundances paired with relatively low incidences (<10% occurrence per all sites or per all city) which suggest an aggregated distribution of some species. This was the case for Trachelipus rathkii (relative abundance 20%; incidence 6%) and Armadillidium vulgare (Latreille, 1804) in Lugano (14%; 6%), and Armadillidium nasatum Budde-Lund, 1885 in Zurich (30%; 6%).
Discussion Faunistic resultsNext to many taxonomic and faunistic studies on European isopods (
Our results reveal that the observed cities harbour mostly species widespread in Europe. Regarding isopods, six species are known as widespread in temperate and northern Europe, occupying both urbanized and rural areas: Armadillidium vulgare, Oniscus asellus, Philoscia muscorum (Scopoli, 1763), Porcellio scaber, Trachelipus rathkii, Trichoniscus pusillus Brandt, 1833 (e.g.
Among millipedes, seven species are widely distributed across Europe (
One isopod (Trichoniscus alemannicus Verhoeff, 1917) and one millipede(Cylindroiulus verhoeffi) species are known to be restricted to the Alps (
The isopod Platyarthrus hoffmannseggii (Budde-Lund, 1893), a depigmented and blind myrmecophilous species, ubiquitous in ant nests, was frequently sampled in Lucerne. The distribution pattern of such isopods may follow the distribution of their ant hosts.
The intra-European alien (Cochard et al. 2011) Armadillidium nasatum is commonly introduced to greenhouses across Europe (
Our survey in three Swiss cities resulted in a relatively high species richness and abundance of isopods, while millipedes were captured in lower number of species and individuals.
The overall number of millipede species revealed in the three cities is relatively low (8.7%) compared with the known millipede fauna of Switzerland (127 species;
Reports on urban isopod and millipede fauna show relatively high species richness in temperate cities as compared to known native, local faunas. Such reports are, however, hardly comparable due to differences in sampled habitats, sampling effort and methodology. Pitfall trapping in parks of the city Debrecen (Hungary) resulted to a 19% (14 species) of the known millipede fauna of Hungary (
Pooled abundances of isopods and millipedes were well over 1000 individuals in each of the above mentioned studies (90 to 120 operating traps for 6 to 9 months). As the number of millipedes in our study was less than 100 individuals, the question arises why abundances were so low in the three Swiss cities? In his review
The only alien isopod captured, Armadillidium nasatum, also known as the “greenhouse pillbug”, was among the dominating species in Zurich, but it only occurred in 5.7% of the sampling sites (out of the total 36), turning to be one of the rarest species in the city. Similarly, the alien millipede Oxidus gracilis (
The three millipedes (Ophyiulus pilosus, Brachydesmus superus, Oxidus gracilis) occurring in two or more cities are widespread in Europe and occupy rural as well as urban settlements (
Pitfall trapping, as the sampling method employed in this study, is a passive sampling method that has been developed to catch specimens active on the soil and litter surface. It has proven to efficiently represent species richness and activity density data of several arthropod groups (e.g. Araneae, Coleoptera) (
As with many other invertebrate taxa (e.g. Lepidoptera and Mollusca in IUCN 2011 European Red List), geographic patterns of European isopods and millipedes show a decrease in species richness from southern biodiversity hot-spots to the north. The available literature on millipede and isopod faunas suggests species diversity to decrease roughly by half from Southern Europe to Central Europe, and it further halves towards Fennoscandia (e.g. isopods: Italy:
Similarities between species compositions hint at the impact of geographical location and distance between cities: the two northern cities (Zurich and Lucerne), which share more species than any other combination of two cities, are only 60 km apart. Lugano is located 170 km south of Lucerne and 210 km south of Zurich, from which it is additionally separated by the Alps. Lugano is already under the influence of Mediterranean climate, which affects the regional flora and fauna.
The common temperate European isopod species (Trachelipus rathkii, Porcellio scaber, Oniscus asellus, Philoscia muscorum) are among the most common synanthropic species (i.e. species live near humans and benefit from their association with humans and anthropogenous habitats). Common Mediterranean isopod species are also common in urban sites. Besides Armadillidium nasatum, several other species, such as Agabiformius lentus (Budde-Lund, 1885) and Chaetophiloscia cellaria (Dollfus, 1884), occur further to the north from their natural range and can survive outdoors (e.g.
Biotic homogenization in cities has been described earlier (e.g.
In our study we recorded 16 species mentioned in this list, i.e. 11 isopod species (64.7% of the 17 species found in this study) and 5 millipede species (62.5% of 8). The proportion of widespread isopod and millipede species contributing to homogenization was highest in the largest city, Zurich (81.5% of all 25 species), and lowest in the smaller cities, Lugano (70%) and Lucerne (69%).
ConclusionOur study showed that urban millipede and isopod assemblages in Switzerland mainly consist of species with wide distribution in Europe. We also showed that cities offer suitable habitats for native and non-native species, with both wide and narrow ecological requirements. Cities under temperate climate showed remarkable differences in their species compositions from the one under Mediterranean influence. This suggests that biogeography plays an important role in shaping isopod and millipede assemblages in the cities.
Our thanks go to V. Albin, F. Bontadina, P. Duelli, B. Fecker, F. Fibbioli, R. Home, W. Kastenholz, M. Cooke Kindermann, L. Milani, A. Niederer, M. K. Obrist, M. Ryf, A. Schulz, R. Siegwart, R. Tester, and P. Wirz who helped in the field, in the lab or with the organization of the data collection. The study (‘BiodiverCity’; www.biodivercity.ch) was funded by the Swiss National Science Foundation as a project of NRP54 ‘Sustainable development of the built environment’ (www.nrp54.ch). We are thankful to Zoltán Korsós for his help in millipede identifications and Stefano Taiti for the revision of Trichoniscus alemannicus specimens. The authors would like to thank the three anonymous referees for their invaluable comments.