ISSN 1211-3026
Cas. Slez. Muz. Opava (A), 57: 37-44.2008
Proposal of ecological classification of centipede, millipede
and terrestrial isopod faunas for evaluation of habitat
quality in Czech Republic
IvanH. T u f -Jana T u f o v a
Proposal of ecological classification of centipede, millipede and terrestrial isopod faunas for
evaluation of habitat quality in Czech Republic. - Cas. Slez. Muz. Opava (A), 57: 37-44,
2008.
A b S t r a c t : Terrestrial invertebrates are frequently used for evaluation of habitat quality.
Centipedes, millipedes and terrestrial isopods can be used for this purpose as well, due to
their life history parameters and sufficient number of representatives of our fauna (in total
188 species for the Czech Republic). The proposed scheme divides all species into three
categories after their habitat requirements: relic (restricted to natural, undisturbed habitats),
adaptable (able to colonise both undisturbed and moderately disturbed habitats), and eurytopic (colonising different biotopes include heavily anthropically disturbed sites). Proportion
of species of individual categories at locality is possible to use for evaluation of its human
disturbance. Possible application is demonstrated using known faunistic data from six different areas differing in level of naturalness and in size respectively.
K e y w o r d s : habitat quality, Chilopoda, Diplopoda, Isopoda, Oniscidea
Biodiversity depletion is only one possible evident result of changes in natural condition caused
by human beings. The reduction of number of species is the most evident; nevertheless, replacement of rare species by other common species is very frequent too. Several groups of soil invertebrates have been used for bioindication of environmental changes (Dufrgne & Baguette 1990,
van Straalen 1998, Bohac 1999, Frouz 1999, Lobry de Bruyn 1999, Marc et al. 1999, Paoletti
1999, Allegro & Sciaki 2003). In the Czech Republic, ground beetles (Coleoptera: Carabidae)
and spiders (Arachnida: Araneae) are used as the most popular indicators. The representatives
of both these groups were classified according to their ecological valences (Hhrka et al. 1996,
Buchar 1983). Two reasons for use of these taxa for evaluation of habitat quality can be listed:
Vast popularity of the given groups among professional and amateur zoologists, and high numbers of species known from the Czech Republic (circa 570 and 800 respectively). Centipedes
(Chilopoda), millipedes (Diplopoda) and terrestrial isopods (Isopoda: Oniscidea) represent in our
fauna smaller invertebrate groups generally left out these evaluation approaches, although there
have been trials to use them for assessing habitat quality as well (Bilton 1996, Paoletti & Hassall
1999, Souty-Grosset et al. 2005). Representatives of these soil invertebrates are relatively common; they inhabit all types of terrestrial habitats in the Czech Republic from lowlands to mountain tops. Hence they are useful for evaluation of environmental conditions. Their propriety for
environmental studies is based on their limited dispersal capabilities -they are wingless and they
move relatively slowly. Furthermore, besides individual collecting or soil samples heat-extracting,
there is a simple sampling method of their communities, e.g. they are easily caught by pitfall trapping. All three groups are studied frequently together because of similar life style, comparable
densities, similar activity pattern during the year and other characteristics.
The fauna of the Czech centipedes, millipedes and terrestrial isopods is relatively well known.
The check-list of centipedes of the Czech Republic was published by Tajovski (2001a) and
actualized by Tuf and LaSka (2005), and Tuf et al. (2008, in prep.). Altogether, 66 centipede
species are known from the Czech Republic. The check-list of millipedes was also published
by Tajovskg (2001~);several new species of millipedes were added by Kocourek (2001, 2004),
Tajovsky and Mlejnek (2007) and Tufovl et al. (in prep.). So far, 80 species of millipedes in total
are known from the Czech Republic. The fauna of the Czech terrestrial isopods has been studied for a long period by Flasarovh (2000). There are 42 isopod species known from the Czech
Republic.
Descriptions of ecological categories
In order to evaluate habitat, species ecological valence related to its habitat allegiance is the
most important characteristic (Zimmer et al. 2000). It seems to be more important than rarity of
individual species because there are some rarely introduced species which are opportunist in their
homeland and adapt frequently to different conditions in new areas. Proposed classification is
applicable mainly to the Czech Republic because ecological requirements of species can differ in
their distribution range (Souty-Grosset et al. 1988, Lardies & Bozinovic 2006). All species of the
Czech fauna were split up into three ecological categories; affiliation of individual species to the
respective category is presented in tables 1-3.
Table 1: List of species of centipedes (Chilopoda) known from the Czech Republic (66 species) and their affiliation to ecological categories. R, A, E - see the text.
E
R
R
R
A
A
A
R
A
R
A
A
E
R
R
E
E
R
A
R
R
R
R
A
E
A
E
LITHOBIOMORPHA
Henicopidae
Lomyctes emarginatus Newport, 1844
Lithobiidae
Eupolybothrus grossipes (C.L.Koch, 1847 )
Eupolybothrus tridentinus (Fanzago, 1874)
Harpolithobius anodus (Latzel, 1880)
Lithobius aeruginosus L.Koch, 1862
Lithobius agilis L.Koch, 1847
Lithobius austriacus Verhoeff, 1937
Lithobius biunguiculatus Loksa, 1947
Lithobius borealis Meinert, 1868
Lithobius burzenlandicus Verhoeff, 1934
Lithobius calcaratus C.L.Koch, 1844
Lithobius crassipes L.Koch, 1862
Lithobius curtipes C.L.Koch, 1847
Lithobius cyrtopus Latzel, 1880
Lithobius dentatus C.L.Koch, 1844
Lithobius erythrocephalus CL.Koch, 1847
Lithobiusforficatus Linnaeus, 1758
Lithobius lapadensis Verhoeff, 1900
Lithobius lapidicola Meinert, 1872
Lithobius latro Meinert, 1872
Lithobius lucifugus L.Koch, 1862
Lithobius lusitanus Verhoeff, 1925
Lithobius luteus Loksa, 1947
Lithohius macilentus L.Koch, 1862
Lithobius melanops Newport, l845
Lithobius micropodus (Matic, 1980)
Lithobius microps Meinert, 1868
SCUTIGEROMORPHA
Scutigeridae
A Scutigera coleoptrata (Linnaeus, 1758)
R
A
E
A
R
R
A
E
A
R
A
R
A
A
R
A
R
R
A
A
A
GEOPHILOMORPHA
Schendylidae
Schendyla monoeci Brolemann, 1904
Schendyla montana (Attems, 18%)
Schendyla nemorensis (C.L.Koch, 1836)
Geophilidae
Clinopodesflavidus C.L.Koch, 1847
Folkmanovius paralellus Dobromka, 1957
Geophilus carpophagus Leach, 1814
Geophilus electricus (Linnaeus, 1758)
Geophilusflavus (DeGeer, 1778)
Geophilus insculptus Attems, 1895
Geophilus oligopus (Attems, 1895)
Geophilus osquidatum Brijlemann, 1909
Geophilus proximus C.L.Koch, 1847
Geophilus pygrnaeus Latzel, 1880
Geophilus truncorum Bergsoe & Meinert, 1866
Photophilus griseus Follunanovfi, 1928
Pachymerium ferrugineum (C.L.Koch, 1835)
Stenotaenia linearis (C.L.Koch, 1835)
Dignathodontidae
Dignathodon microcephalus (Lucas, 1846)
Henia brevis (Silvestri, 1896)
Henia illyrica (Meinert, 1870)
Henia vesuviana (Newport, 1845)
E
A
R
R
A
R
R
R
A
R
Lithobius mutabilis L.Koch, l862
Lirhobius muticus C.L.Koch, 1847
Lithobius nodulipes Latzel, 1880
Lithobius pelidnus Haase, 1880
Lithobius piceus L.Koch, 1862
Lithobius punctulatus C.L.Koch, 1847
Lithobius salicis Verhoeff, 1925
Lithobius schuleri Verhoeff, 1925
Lirhobius tenebrosus Meinert, 1872
Lithobius tricuspis Meinert, 1872
Linotaeniidae
E Strigamia acuminata (Leach, 1814)
A Strigamia crassipes (C.L.Koch, 1835)
A Strigamia transsilvanica (Verhoeff, 1928)
Himantariidae
A Srigmatogaster subterranea (Shaw, 1789)
SCOLOPENDROMORPHA
Cryptopidae
A Cryptops anomalans Newport, 1844
A Cryptops hortensis (Donovan, 1810)
A Cryptops parisi Brolemann, 1920
Table 2: List of species of millipedes (Diplopoda) known from the Czech Republic (80 species) and their affliation to ecological categories. R, A, E - see the text.
POLYXENIDA
Polyxenidae
A Polyxenus lagurus (Linnaeus, 1758)
POLYZONIIDA
Polyzoniidae
A Polyzonium germanicum Brandt, 1831
R
R
A
A
R
R
R
R
A
R
R
R
E
R
R
R
E
A
A
A
A
A
CHORDEUMATLDA
Brachychaeteumatidae
Brachychaeteuma bradeae (Bmlemann &
Brade-Birks, 1917)
Mastigophorophyllidae
Haploporatia eremita (Verhoeff, 1909)
Masrigona bosniensis (Verhoeff, 1897)
Mastigona mutabilis (Latzel, 1884)
Mastigona vihorlarica (Attems, 1899)
Mastigophorophyllon alpivagum bohemicum
Attems, 1900
Mastigophorophyllon saronicum Verhoeff, 1910
Haaseidae
Haasea flavescens (Latzel, 1884)
Haasea germanica (Verhoeff, 1901)
Haasea pinivaga (Verhoeff, 190 1)
Craspedosomatidae
Craspedosoma alemannicum Verhoeff, 1910
Craspedosoma germanicum (Verhoeff, 1910)
Craspedosoma rawlinsii Leach, l 8 15
Cras~edosomaslavum Anems, 1929
Craspedosoma transsilvanicum (Verhoeff, 1897)
Listrocheiritium septentrionale GuliEka, 1965
Ochogona caroli (Rothenbiihler, 1900)
Chordeumatidae
Melogona broelemanni (Verhoeff, 1897)
Melogona gallica (Latzel, 1884)
Melogona voigti (Verhoeff, 1899)
Mycogona g e m n i c a (Verhoeff, 1892)
Verhoffiidae
Haplogona oculodistincta (Verhoeff, 1893)
E
E
E
E
A
A
A
R
R
A
A
A
A
R
A
A
A
A
A
E
R
R
A
R
R
A
E
A
E
A
E
E
R
A
JULIDA
Nemasomatidae
Nemasoma varicorne C.L.Koch, 1847
Blaniulidae
Blaniulus guttulatus (Fabricius, 1798)
Choneiulus palmatus (Ngmec, 1895)
Nopoiulus kochii (Gervais, 1847)
Proteroiulusfuscus (Am Stein, 1857)
Julidae
Allajulus nitidus (Verhoeff, 1891)
Brachyiulus bagnalli (Curtis, 1845)
Brachyiulus lusitanus Verhoeff, 1898
Cylindroiulus arborum Verhoeff, 1928
Cylindroiulus brirannicus (Verhoeff, 1891)
Cylindroiulus boleti (C.L.Koch, 1847)
Cylindroiulus caeruleocinctus (Wood, 1864)
Cylindroiulus latestriatus (Curtis, 1845)
Cylindroiulus luridus (C.L.Koch, 1847)
Cylindroiulus parisiorum (Brolemann &
Verhoeff, 1896)
Cylindroiulus punctatus (Leach, 1815)
Cylindroiulus truncorum (Silvestri, 1896)
Cylindroiulus vulnerarius (Berlese, 1888)
Enantiulus nanus (Latzel, 1884)
Julus scandinavius Latzel, 1884
Julus scanicus Lohmander, 1925
Julus rerrestris Linnaeus, 1758
Kryphioiulus occultus (C.L.Koch, 1847)
Leutoiulus cibdellus (Chamberlin, 1921)
Leptoiulus montivagus (Latzel. 1884)
Leptoiulus noricus Verhoeff, 1913
Leptoiulus proximus (Ngmec, 1896)
Leptoiulus trilobatus (Verhoeff, 1894)
Megaphyllum projectum (Verhoeff, 1894)
Megaphyllum unilineatum (C.L.Koch, 1838)
Ommatoiulus sabulosus (Linnaeus, 1758)
Ophyiulus pilosus (Newport, 1842)
Pachypodoiulus eurypus (Attems, 1895)
Rossiulus vilnensis (Jawlowski, 1925)
R
A
A
A
E
A
E
E
E
R
A
POLYDESMIDA
Macrosternodesmidae
Macrosternodesmus palicola (Brijlemann, 1908)
Oniscodesmidae
Amphitomeus attemsi (Schubart 1934)
Paradoxosomatidae
Oxidus gracilis (C.L.Koch, 1847)
Strongylosoma stigmatosum (Eichwald, 1830)
Polydesmidae
Brachydesmus superus Latzel, 1884
Polydesmus angustus Latzel, 1884
Polydesmus complanatus (Linnaeus, 1761)
Polydesmus denticulatus C.L.Koch, 1847
Polydesmus inconstans Latzel, 1884
Propolydesmus germanicus (Verhoeff, 1896)
Propolydesmus testaceus (C.L. Koch, 1847)
A Tachypodoiulus niger (Leach, 1815)
E Uncigerfoetidus (C.L.Koch. 1838)
A Unciger transsilvanicus (Verhoeff, 1899)
R
A
A
A
A
A
R
R
GLOMERIDA
Glomeridae
Geoglomeris subterranea Verhoeff, 1908
Glomeris connexa C .L .Koch, l847
Glomeris hexasticha Brandt, 1833
Glomeris klugii Brandt, 1833
Glomeris pustulata Latreille, 1804
Glomeris tetrasticha Brandt, 1833
Doderiidae
Trachysphaera costata (Waga, 1857)
Trachysphaera gibbula (Latzel, 1884)
Table 3: List of species of terrestrial isopods (Isopoda: Oniscidea) known from the Czech Republic (42 species) and their affiliation to ecological categories. R, A, E - see the text.
R
E
R
A
A
A
R
E
A
R
R
R
R
E
A
A
E
A
E
A
ISOPODA: ONISCIDEA
Ligiidae
Ligidium germanicum Verhoeff, 1901
Ligidium hypnorum (Cuvier, 1792)
Trichoniscidae
Androniscus dentiger Verhoeff, 1908
Androniscus roseus (C. Koch, 1838)
Haplophthalmus danicus Budde-Lund, 1880
Haplophthalmus mengii (Zaddach, 1844)
Hyloniscus mariae Verhoeff, 1908
Hyloniscus riparius (C. Koch, 1838)
Metatrichoniscoides leydigi (Weber, 1880)
Trichoniscoides helveticus (Carl, 1908)
Trichoniscus crassipes Verhoeff, 1939
Trichoniscus noricus Verhoeff, 1917
Trichoniscus provisorius Rakovitza, 1908
Trichoniscus pusillus Brandt, 1833
Trichoniscus pygmaeus Sars, 1898
Buddelundiellidae
Buddelundiella cataractae (Verhoeff, 1930)
Platyarthridae
Platyarthrus hoffmannseggi Brandt, 1833
Philosciidae
Lepidoniscus minutus (C. Koch, 1838)
Oniscidae
Oniscus asellus Linnaeus, 1758
Cylisticidae
Cylisticus convexus (De Geer, 1778)
R
A
R
A
E
A
A
A
A
A
E
A
E
A
A
A
R
R
A
E
R
A
Trachelipodidae
Protracheoniscus major (Dollfus, 1903)
Protracheoniscuspolitus (C. Koch, 1841)
Trachelipus difjicilis (Radu, 1950)
Trachelipus nodulosus (C. Koch, 1838)
Trachelipus rathkii (Brandt, 1833)
Trachelipus ratzeburgii (Brandt, 1833)
Porcellium collicola (Verhoeff, 1907)
Porcellium conspersum (C. Koch, l84 1)
Porcellionidae
Porcellionides pruinosus (Brandt, 1833)
Porcellio dilatatus Brandt, 1833
Porcellio laevis Latreille, 1804
Porcellio montanus Budde-Lund, 1885
Porcellio scaber Latreille, 1804
Porcellio spinicornis Say, l 8 l 8
Armadillidiidae
Armadillidium nasatum Budde-Lund, 1885
A r d i l l i d i u m opacum (C. Koch, 1841)
Armadillidium pictum Brandt, 1833
Armadillidium pulchellum (Zenker, 1798)
Armadillidium versicolor Stein, 1859
Armadillidium vulgare (Latreille, 1804)
Armadillidium zenckeri Brandt, 1833
Paraschizidium roubali Frankenberger, 1940
Relic species ( R )-In this category, the most stenotopic species are included. These species inhab-
it exclusively undisturbed habitats with low impact of human activities, e.g. the nature-closest
forests, rests of steppes, caves, stony debris, or mountain habitats.
Adaptable species (A) - These species are grouped in communities in nature-close habitats such
as.different types of forests or meadows. However, they are able to inhabit artificial and manmade habitats as well. It is possible to meet for example typical forests inhabiting species in older
parks, abandoned gardens, graveyards etc. with more stable environmental conditions. Introduced
species are involved in this category too; although they can be rare in Czech Republic, their distribution is typically connected with human made sites (greenhouses, parks etc.)
Eurytopic species (E) - Species in this category have the widest ecological valence. They are frequently found for example in both forests and non-forested biotopes and also in many humanmade biotopes (fields, brown-fields, etc.). Synantropical species inhabiting wide spectrum of
man-made localities are also involved in this category although they can miss in communities at
natural biotopes (e.g. Porcellio scaber).
According to this categorization, 40% of species of the Czech centipede fauna can be classified as relic, 45 % as adaptable and 15 % as eurytopic. Similarly, within the millipedes known
from the Czech Republic, 31 % we categorize as relic, 49% as adaptable and 20 % as eurytopic. For the Czech terrestrial isopods this ratio is 29% relic, 50% adaptable and 21 % eurytopic
species. At the family level, the relic ones are the millipede families Brachychueteumidae and
Macrosternodesmidue with cave species and the endogeic family Doderiidae. The high proportion
of relic species (50% or more) is typical for the families Mastigophorophyllidae, Haaseidae, and
Craspedosomatidue (Diplopoda), Lithobiidae (Chilopoda), and Trichoniscidae (Oniscidea).
Based on the classification of known species and determination of portion of proposed ecological categories we can evaluate habitat quality. Undisturbed, nature-close habitats are inhabited mainly by relic and adaptable species. The moderately influenced sites, e.g. planted forests,
are mainly inhabited by adaptable species with the low proportion of relic species. Human-made
biotopes, such as residential areas etc., are mainly inhabited by adaptable species with higher proportion of eurytopic species, too. The usefulness of categorization of species according to their
Table 4: Comparison of species number and assemblages structure based on the ecological groups (proportion in %) in six different areas. Sources: ' - Tajovse 2002; - Tajovskf 2001d;' - Tufova & Tuf in litt.,
Strichelovi in
- Tajovskf 1998;5- Tajovsky 2001b, Voienillcovi in Mt.; - Navratil in litt. R, A, E - see
the text.
iofin Primeval
Forest NNR1
Chilopoda
species
R
A
E
Diplopoda
species
R
A
E
Oniscidea
species
R
A
E
together
species
R
A
E
BflB Karpaty
Labskt
colliery
heapsspoil Olomouc City6
(forest parts piskovce PLA4 new sokolov5
19
41
17
21
15
19
31.6
52.6
15.8
29.3
51.2
19.5
29 A
35.3
35.3
19.0
42.9
38.1
6.7
40.0
53.3
5.3
57.9
36.8
14
33
21.2
42.4
36.4
20
17
15
16
10.0
65 .O
25 O
.
11.8
41.2
47.1
0O
.
33.3
66.7
0O
.
68.7
31.3
21.4
42.9
35.7
7
14
11
28.6
57.1
14.3
7.1
50.O
42.9
9O
.
45.5
45.5
8
12.5
37.5
50O
.
8
0 .O
50.O
50 O
.
0 .O
56.2
43.8
40
88
22.7
47.7
29.6
48
16.7
50.0
33.3
46
15.2
41.3
43.5
38
2.6
39.5
57.9
2 .O
60.8
37.2
27.5
50.0
22.5
16
51
ecological valences for evaluation of habitat quality is demonstrated on the following comparison of assemblages from different areas (tab. 4). We used data obtained from papers of Tajovskf
(1998, 2001b, 2001d, 2002), unpublished master theses of VoZenflkovi (in litt.) and Navritil (in
litt.), and own data from inventory research (TufovB & Tuf in litt.). The proportion of relic species
corresponds well with naturalness of the area and consequently with level of locality protection.
Localities with the highest naturalness and protection level (National Nature Reserve and National
Park) are inhabited by assemblages with the highest portion of relic species (more than 20% in
millipedes, circa 30% in centipedes, about !4 in all groups together). To the contrary, relic species do not occur (millipedes, terrestrial isopods) or occur only rarely (centipedes) at human made
habitats (see colliery spoil heaps and the Olomouc City in tab. 4). High proportion of eurytopic
species is typical for primary succession on the colliery spoil heaps, whereas adaptable species are
typical mostly for the Olomouc City with the high diverse mosaic of different but often stabilized
biotopes.
Our analyses showed that evaluation of habitat does not depend on the size of assessed territory.
The same proportion of relic species of centipedes and millipedes were obtained from the &fin
Primeval Forest NNR as well as from the Podyji NP despite to hundred times larger area and
twice as higher number of species in the given national park.
Centipedes and millipedes seem to be more useful for the proposed purpose than terrestrial isopods because of different number of species in their communities. Typical community of terrestrial isopods in any forest habitat is created only by 4-7 species (see the ?o!nif
Primeval Forest NNR
in tab. 4). Presence or absence of l relic species in such community represents a big proportional
difference. Usage of terrestrial isopods for habitat quality evaluation together with other two presented myriapod groups is therefore highly recommended.
A c k n o W l e d g e m e n t s . We are grateful to Martin KonviEka who encouraged us to prepare classification of these species for habitat evaluation. We thank Karel Tajovskf, who introduced us to soil biology many
years ago, for a lot of information about individual species distribution during frequent consultations and for
many useful comments to this manuscript. Furthermore we would like to thank Dana BednGovi for improving of English. This study was supported by National Research Programme I1 (No. 2B 06101).
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Nhvrh ekologickk klasifikace stonoiek, mnohonoiek a suchozemsk$ch stejnonoicd pro hodnoceni kvality stanoviSt'v CR
SuchozemSti bezobratli jsou Easto pouiivini jako nistroj pro hodnoceni kvality stanoviSt'.
Stonoiky, mnohonoiky a suchozemSti stejnonoici mohou bft vyuiiti takt, d k y jejich biologii
(nelttavi iivoEichovt atp.) a dostateEnCmu poEtu druhi (v r h c i CR celkem 188 druhii). Zdstupci
3 kategorii podle jejich ekologickfch niiroki: reliktni (omezeny
vSech tii skupin byli rozdgleni do t
vfskytem na nenaruSen6 prost?edf), adaptabilni (schopnt kolonizovat ElovEkem EisteEnE
pietvoient prostfedf) a eurytopnl (kolonizujicl r h n t biotopy vEetnE siln6 ElovEkem postiienfch).
Zastoupeni jednotlivych kategorii ve spoleEenstvu dantho dzemi je moint vyuilt k hodnoceni
stupnk jeho zachovalosti. Moint pouiiti klasifikace je demonstrovino na phlladech z n h f c h
faunistickfch ddaji ze Sesti dzemnich celki IiSicich se stupnkm antropicktho ovlivnEni i vlastni
velikosti dzemi.
Authors' addresses: Ivan H. T U f & Jana T U f o v ,Department of Ecology and Environmental Science,
Faculty of Science,Palacky University, Svobody 26,77200 Olomouc, Czech Republic;
e-mail: [email protected],[email protected]