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Fluctuations of carabid populations inhabiting an ancient woodland (Coleoptera, Carabidae)
ARTICLE IN PRESS Pedobiologia 48 (2004) 159–164
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Fluctuations of carabid populations inhabiting an ancient woodland (Coleoptera, Carabidae) . Jens Gunther*, Thorsten Assmann . . Institute of Ecology and Environmental Chemistry, University of Luneburg, Scharnhorststr. 1, Luneburg D-21335, Germany Received 20 February 2003; accepted 6 November 2003
KEYWORDS Fluctuation pattern; Ancient woodland; Carabid beetles; Long-term investigation
Summary The changes in population size of carabid beetles inhabiting an ancient woodland were analysed in a long-term investigation covering a period of nine years (1994–2002). The amplitude of fluctuations of the relative density of these species was estimated and compared with those of carabid beetles inhabiting recent woodlands and more unstable habitats in open landscapes. To analyse this, 8 pitfall traps were set in an . ancient beech and oak woodland in the nature reserve ‘‘Luneburger Heide’’ in northern Germany and were emptied every fortnight the whole year round. Catching rates for some species (e.g. Carabus problematicus and Abax parallelepipedus) fluctuated only slightly, whereas those of other species (e.g. C. violaceus and C. auronitens) varied as much as ten-fold. Comparison of these results with those of other long-term investigations of recent woodlands and also of more open habitats showed that in each of the three habitat types some species varied very little in abundance and others, very widely. So it seems that the amplitude of fluctuations in abundance is a feature of each single species rather than a special attribute of their habitats. & 2004 Elsevier GmbH. All rights reserved.
Introduction During the Middle Ages and in early modern times woodlands in the lowlands of northwestern Germany were reduced to small remnants. In the past 200 years, woodland areas have considerably increased due to modern forestry (Hesmer and Schroeder, 1963). Adopting a definition of Peterken (1993) ‘‘ancient woodlands’’ are areas which have been wooded continuously, at least since the end of the
18th Century. This is indicated by historical and topographical maps as well as historical documents. Recent woodlands occupy areas that were re-forested after the end of the 18th century. The high habitat continuity of ancient woodlands over several hundreds or thousands of years could in principle have affected the population biology of woodland-inhabiting species. Two of the population-biological parameters that influence the longterm persistence of species are the reproduction
*Corresponding author. E-mail address: [email protected] (J. Gu. nther). 0031-4056/$ - see front matter & 2004 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2003.11.002
ARTICLE IN PRESS 160
rate and the fluctuation in abundance. To estimate the extent of such fluctuations long-term investigations with samples taken in consecutive years are needed. Long-term studies describing year-to-year variability in the catch of each carabid species are rare, and some of the longer studies do not show the number of individuals caught per year and location separately. In open sandy habitats in the Netherlands Den Boer (1981) found a wide range of net reproduction rate as well as the relative density of carabid beetles, which varied by a factor of over one hundred within 20 years. In more stable habitats such as recent woodlands, Althoff et al. (1992) detected a much smaller variation in population size of a woodland-inhabiting carabid beetle in the Westphalian lowlands (Germany). But nothing is known about the fluctuations in abundance of several woodland-inhabiting carabid beetles of ancient woodlands. To obtain this information it is necessary either to estimate the absolute density or to obtain a whole year catch with pitfall traps for several consecutive years. Pimm and Redfearn (1988) concluded that in the case of insects a period of at least 8 years may be necessary to describe the extent of fluctuations in this taxon. Over shorter periods the standard deviations of the logarithms of annual density (and other measures) increase with time. The long-term investigation in an ancient woodland area of northwestern Germany presented here for the first time has covered a period of 9 years (1994– 2002). The aim of this study is to estimate the amplitude of fluctuations of the relative density of carabid species in an ancient woodland. These fluctuations are then compared with those of carabid species inhabiting other habitats.
J. Gu ¨nther, T. Assmann
The numbers of ground-dwelling arthropods caught in pitfall traps are influenced by various biotic and abiotic factors (Heydemann, 1955, 1957; Luff, 1975; Franke et al., 1988). Baars (1979) detected a strong relationship between the relative density measured with pitfall traps and the absolute density (measured in enclosures) of two carabid beetles in the Netherlands and concluded that continuous pitfall sampling is a reliable relative measure of the sizes of carabid populations (for further data, see also Den Boer, 1979a). For the analysis of the fluctuations of the relative density we chose 7 typical woodland species (cf. Den Boer, 1977; Lindroth, 1985, 1986; Turin, 2000) which were caught in comparatively large numbers in all 9 years (see Table 1). Additionally, 3 more eurytopic but likewise frequently caught species (Pterostichus niger, Nebria brevicollis, C. nemoralis) were incorporated into this analysis. To describe the year-to-year fluctuations in relative density the variance of the estimated net reproduction rate (R) ¼ total number in year cycle i/total number in year cycle i 1 was used (Den Boer, 1990). The range between the highest and lowest relative density recorded in the investigation period is expressed as logarithmic-range (LR) ¼ ln(highest density)ln(lowest density) (see also Den Boer, 1971). Average ln R, the natural logarithms of net reproduction ( ¼ the logarithm of the geometric mean of R), estimates the overall trend of the relative density (Den Boer, 1991). Average ln R-values below zero indicate a decrease and values of average ln R above zero indicate an increase in numbers of a given species during the investigation period. To find out whether these trends were significantly correlated with time we used the sign-trend-test according to Cox and Stuart (cf. Sachs, 1999).
Materials and methods Results In June 1994, 8 pitfall traps containing a mixture of ethanol (40%), water (30%), glycerol (20%) and acetic acid (10%) (cf. Renner, 1980) were set in an ancient beech and oak woodland on acid ground . (Periclymeno-Fagetum). This area ‘‘Hofgeholz Mo. hr’’ is marked as woodland in historical maps like the ‘‘Kurhannoveranische Landesaufnahme’’ (1774–1786). This ancient woodland is located in . the nature reserve ‘‘Luneburger Heide’’ in northern Germany (91500 east, 531060 north). All pitfalls were emptied every fortnight throughout the year so that we were able to analyse the catch for 9 years in the case of the summer-breeding species and the catch for 8 years in that of the spring breeders.
In the years 1994–2002 a total of 11,617 individuals belonging to 47 species were caught (Table 1). The numbers of species caught per year ranged from 15 (1994) to 31 (1998), showing no trend over time. Out of the 11 typical woodland species 8 were caught in every year. The total number of individuals varied from 545 (1995) to 2244 (1998) with no significant trend over time. The results show that some species (e.g. C. problematicus and A. parallelepipedus) fluctuate only slightly in their catching rates in the . ‘‘Luneburger Heide’’ whereas the catching rates of other species (e.g. C. violaceus and C. auronitens)
ARTICLE IN PRESS Carabid populations inhabiting an ancient woodland
161
Table 1. Total year catch of all species in the years 1994–2002 1994
1995
1996
1997
1998
1999
2000
2001
2002
Woodland species Carabus auronitens Carabus problematicus Carabus violaceus Pterostichus oblongopunctatus Abax parallelepipedus Leistus rufomarginatus Notiophilus biguttatus Cychrus caraboides Carabus convexus Harpalus quadripunctatus Carabus glabratus
117 45 129 168 193 19 26 1 1 . .
47 43 33 149 63 17 24 1 1 . .
17 40 52 190 89 18 93 1 1 . .
130 43 208 773 178 18 39 1 . 2 1
119 36 482 497 130 4 75 9 3 5 2
58 52 400 444 257 2 51 5 1 10 .
72 18 351 261 109 6 40 9 . 4 .
23 14 450 63 67 3 2 6 1 . .
32 15 305 199 106 1 24 3 . . .
Other species Pterostichus niger Nebria brevicollis Carabus nemoralis Trechus obtusus Asaphidion curtum Bembidion lampros Poecilus versicolor Pseudoophonus rufipes Pterostichus melanarius Pterostichus minor Amara consularis Bembidion properans Bembidion quadrimaculatum Bembidion tetracolum Carabus arvensis Nebria salina Notiophilus palustris Pterostichus strenuus Loricera pilicornis Amara similata Amara plebeja Synuchus vivalis Agonum sexpunctatum Anisodactylus binotatus Pterostichus nigrita Amara familiaris Pterostichus rhaeticus Agonum fuliginosum Poecilus cupreus Dromius quadrinotatus Harpalus latus Amara municipalis Carabus granulatus Amara tibialis Limodromus assimilis Bradycellus ruficollis
185 73 8 2 . . . 1 . . . . . . . . . . 1 . . . . . . . . . . . . . . . . .
61 80 11 1 1 10 . . . . . . . . . . . . 3 . . . . . . . . . . . . . . . . .
142 16 8 11 3 55 . . . . . . . . . 1 . . . . . . . . . . . . . . . . . . . .
306 20 21 . 4 22 5 1 1 . 1 . . 1 . . 1 1 . 1 1 1 1 2 . . . . . . . . . . . .
658 34 93 2 16 58 1 1 6 1 . 1 . . 1 . 1 . 1 . . . . 2 1 1 2 1 1 . . . . . . .
652 35 22 2 9 11 2 34 3 . . . 1 1 . 1 . 4 2 . . . . 2 . . 1 1 . 1 8 . . . . .
255 22 20 6 . . . 3 1 . . . . . . . . . . . . . . . . . 1 . . . 1 1 . . . .
430 9 2 . . . . . 1 . . . . . . . . . 3 . . . . . . . . . . . . . 1 1 . .
282 23 11 . 2 . . 1 . . . . . . . . . 3 . . 1 . . . . . . . 1 . . . . . 1 1
Total
969
545
737
1783
2244
2072
1180
1076
1011
vary up to a factor of ten (Fig. 1). The Var R-values and the logarithmic-range for C. problematicus and A. parallelepipedus are much lower than the
respective values for C. violaceus, C. auronitens, C. nemoralis, Notiophilus biguttatus and P. oblongopunctatus (Table 2). The other species
ARTICLE IN PRESS 162
J. Gu ¨nther, T. Assmann
10000
Individuals
1000
100
Carabus problematicus Carabus violaceus Carabus auronitens Abax parallelepipedus total
10
1 1994
1995
1996
1997
1998
1999
2000
2001
2002
year
Figure 1. Total year catch, mean and standard deviation (logarithmic scale) of Carabus problematicus, Carabus violaceus, Carabus auronitens, Abax parallelepipedus and all individuals caught (total). Table 2. Ascending sorted variance of the net reproduction rate. (Var R), the logarithmic range (LR), the average logarithmic range of R; the standard deviation (SD) of ln R, the number of R-values (nR), mean number of . individuals7SD and the number of individuals (n) of woodland inhabiting ground beetles in the Luneburger Heide
Carabus problematicus Abax parallelepipedus Nebria brevicollis Pterostichus niger Leistus rufomarginatus Carabus violaceus Pterostichus oblongopunctatus Carabus nemoralis Carabus auronitens Notiophilus biguttatus
Var R
LR
Average ln R
SD ln R
nR
Mean n7SD
n
0.10 0.43 0.57 0.70 0.79 1.43 2.15 4.67 6.90 18.06
1.31 1.4 2.19 2.38 2.89 2.68 2.51 3.84 2.03 3.62
0.14 0.07 0.14 0.05 0.37 0.11 0.04 0.00 0.05 0.00
0.42 0.62 0.82 0.8 0.81 0.83 0.99 1.5 1.09 1.75
8 7 8 8 8 8 7 7 7 7
34714 125765 35725 3307212 1078 2687169 3227234 24729 62743 44729
306 999 312 2971 88 2410 2576 188 498 348
under investigation (N. brevicollis, P. niger and Leistus rufomarginatus) showed low Var R-values but relatively high LR-values. The average ln R indicates the overall trend of the relative density during the investigation period. Within some species this value was near zero, whereas C. violaceus had the highest positive value and L. rufomarginatus the lowest negative value. But none of these decreases or increases were significantly correlated over time.
Discussion The fluctuations of some woodland species inhabit. Mo. hr’’ were low, indicated by ing the ‘‘Hofgeholz
low Var R and LR-values (e.g. C. problematicus, A. parallelepipedus). C. problematicus seems to have more unstable populations in the Netherlands (Var R: 1.42; LR: 1.69, Den Boer, 1990). The reason could be that the habitats investigated there consist of young and open woodland types and adjacent heathlands (Den Boer and van Dijk, 1994). Nothing is known about the fluctuations of C. problematicus populations in beech and oak woodlands in the Netherlands. Abax parallelepipedus is a similar case. In a 40-year-old birch stand in the Ruhr Valley in Western Germany, Schwerk and Abs (2002) detected high fluctuations in the total year catch during 6 years of investigation (Var R: 6.88; LR: 2.83). Loreau (1990) found no long-term changes in the yearly maximum mean density of this species within 10 years in enclosures in a
ARTICLE IN PRESS Carabid populations inhabiting an ancient woodland
beechwood in Lembeek (Belgium) (6 years of investigation). The reasons for the differences of the amplitude are still unknown. A decision is impossible if the different ages of the habitats are important determinants due to the fact that data for long-term fluctuations of this species are only known from three investigation areas. The year-to-year change in the relative densities (Var R) of more eurytopic species like N. brevicollis and P. niger were also relatively low, but with a high range of relative density during the whole investigation period (LR) in the ‘‘Hofgeho. lz Mo. hr’’. In an oak–birch stand in the Netherlands (Den Boer, 1979a), and also in an agricultural field in the UK (Luff, 2001), N. brevicollis showed comparable fluctuations in density (Var R: 1.34, 1.4; LR: 2.07, 3.04). In the study of Schwerk and Abs (2002), this species had lower fluctuations (Var R: 0.56; LR: 0.98). C. violaceus, C. auronitens, P. oblongopunctatus, C. nemoralis, and N. biguttatus showed high fluctuations in the number of individuals caught per year in the present study. In the Netherlands P. oblongopunctatus is a species with a low fluctuation in numbers as described in the study of Den Boer (1979a) mentioned above, and also in a 90year-old oak-forest near Baarn during 9 years of investigation (Brunsting, 1981) (Var R: 0.17, 0.16; LR: 0.81, 1.57). Comparably high fluctuation patterns were found with C. nemoralis (Var R: 8.13; LR: 2.93), and N. biguttatus (Var R: 4.96; LR: 4.11) in the study of Schwerk and Abs (2002). In each of the described habitats species with very low fluctuations in abundance and others with very high fluctuations were found. Even in our fairly stable habitat, like large and ancient woodlands, no dominance by species with a low fluctuation in population density was observed. On the contrary, in this study the fluctuations of species of stable habitats are in most cases as high as those of species of younger woodlands and more open and dynamic habitats. During the study period the amplitude of fluctuations in abundance seemed to be mainly a feature of each single species (and perhaps also differences at the population level) rather than a special component of their habitats. Den Boer (1979b) compared the life tactics of different carabid species of oak–birch forests (stable habitat) and recently abandoned agricultural fields (unstable habitat) in the Netherlands. Although much of the data were only provisional, he concluded that among these carabid species no specific combination of traits has co-evolved to maximize survival in either a stable or an unstable habitat. Therefore, it does not seem very probable that only certain assemblages of traits will always
163
be found together as optimal strategies (cf. Stearns, 1992). Furthermore, habitat stability does not necessarily mean the same predictable environment for different species, e.g., for a winterbreeding ground beetle like Trichocellus placidus woodlands represent unstable habitats because of the highly unpredictable weather conditions in winter during critical phases of the life cycle (Den Boer et al., 1980).
Acknowledgements . This study was supported by the Alfred Topfer . Naturschutz, NNA. We are grateful to Akademie fur . Johannes Pruter for organization and Ludger Schmidt and others for checking the pitfall traps. J.G. was supported by a grant from the Federal Agency for Nature Conservation (Bonn, Germany). We wish to thank Christine Hoefer, Andrea Matern and Ann Thorson for correcting the English and one anonymous referee for valuable comments on the manuscript.
References Althoff, G.-H., Ewig, M., Hemmer, J., Hockmann, P., Klenner, M., Niehues, F.-J., Schulte, R., Weber, F., 1992. Ergebnisse eines Zehn-Jahres-Zensus an einer . Carabus auronitens Subpopulation im Munsterland (Westf.). Abh. Westfa. lischen Museums Naturkunde 54–4, 3–64. Baars, M.A., 1979. Catches in pitfall traps in relation to mean densities of carabid beetles. Oecologia 41, 25–46. Brunsting, A.M.H., 1981. Distribution patterns, life cycle and phenology of Pterostichus oblongopunctatus F. (Col., Carabidae) and Philonthus decorus Grav. (Col., Staphylinidae). Neth. J. Zool. 31, 418–452. Den Boer, P.J., 1971. Stabilization of animal numbers and the heterogeneity of the environment: the problem of the persistence of sparse populations. In: Den Boer, P.J., Gradwell, G.R. (Eds.), Dynamics of Populations. Pudoc, Wageningen, pp. 77–97. Den Boer, P.J., 1977. Dispersal power and survivalFcarabids in a cultivated countryside. Miscellaneous Papers Landbouwhogeschool, Wageningen, Vol. 14, pp. 1–189. Den Boer, P.J., 1979a. The individual behaviour and population dynamics of some carabid beetles of forests. In: Den Boer, P.J., Thiele, H.U., Weber, F. (Eds.), On the Evolution of Behaviour in Carabid Beetles, Vol. 18. Miscellaneous Papers Landbouwhogeschool, Wageningen, pp. 151–166. Den Boer, P.J., 1979b. Some remarks in retrospect. In: Den Boer, P.J., Thiele, H.U., Weber, F. (Eds.), On the Evolution of Behaviour in Carabid Beetles, Vol. 18.
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Miscellaneous Papers Landbouwhogeschool, Wageningen, pp. 213–222. Den Boer, P.J., 1981. On the survival of populations in a heterogeneous and variable environment. Oecologia 50, 39–53. Den Boer, P.J., 1990. Density limits and survival of local populations in 64 carabid species with different powers of dispersal. J. Evol. Biol. 3, 19–48. Den Boer, P.J., 1991. Seeing the trees for the wood: random walks or bounded fluctuations of population size? Oecologia 86, 484–491. Den Boer, P.J., Van Huizen, T.H.P., Den Boer-Daanje, W., Aukema, B., Den Bieman, C.F.M., 1980. Wing polymorphism and dimorphism in ground beetles as stages in an evolutionary process (Coleoptera: Carabidae). Entomol. Generalis 6, 107–134. Den Boer, P.J., Van Dijk, Th.S., 1994. Carabid beetles in a changing environment. Wageningen Agricultural University Papers, Vol. 94–6, pp. 1–30. Franke, U., Friebe, B., Beck, L., 1988. Methodisches zur Erfassung der Siedlungsdichte von Bodentieren aus Quadratproben und Bodenfallen. Pedobiologia 32, 253–264. Hesmer, H., Schroeder, F.G., 1963. Waldzusammensetzung und Waldbehandlung im Niedersa. chsischen Tief. land westlich der Weser und der Munsterschen Bucht bis zum Ende des 18. Jahrhunderts. Decheniana Beiheft 11, 1–304. Heydemann, B., 1955. Carabiden der Kulturfelder als . okologische Indikatoren. Berichte der 7. Wanderversammlung Deutscher Entomologen, Berlin, pp. 172–185. Heydemann, B., 1957. Die Biotopstruktur als Raumwider. fur . die Tierwelt. Verh. Deutschen stand und Raumfulle Zool. Gesellschaft 1956, 332–347.
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Lindroth, C.H., 1985. The Carabidae (Coleoptera) of Fennoskandia and Denmark. Fauna Entomologica Scandinavica. Vol. 15, Scandinavian Science Press, Leiden, part 1. Lindroth, C.H., 1986. The Carabidae (Coleoptera) of Fennoskandia and Denmark. Fauna Entomologica Scandinavica. Vol. 15, Scandinavian Science Press, Leiden, part 2. Loreau, M., 1990. Competition in a carabid community: a field experiment. Oikos 58, 25–38. Luff, M.L., 1975. Some features influencing the efficiency of pitfall traps. Oecologia 19, 345–357. Luff, M.L., 2001. Temporal stability of carabidae in an agricultural habitat. Russ. Entomol. J. 10, 205–212. Peterken, G.F., 1993. Woodland Conservation and Management. Chapman & Hall, London. Pimm, S.L., Redfearn, A., 1988. The variability of population densities. Nature 334, 613–614. . Renner, K., 1980. Faunistisch-okologische Untersuchungen der Ka. ferfauna pflanzensoziologisch unterschiedlicher Biotope im Evessell-Bruch bei Bielefeld-Sennestadt. Ber. Naturwiss. Ver. Bielefeld, Sonderheft 2, 145–176. Sachs, L., 1999. Angewandte Statistik. Springer, Berlin. Schwerk, A., Abs, M., 2002. The carabid fauna (Coleoptera: Carabidae) of forest stands on colliery spoil heaps. Baltic J. Coleopterol. 2, 15–24. Stearns, S.C., 1992. The Evolution of Life Histories. Oxford University Press, New York. Turin, H., 2000. De Nederlandse loopkeevers, verspreiding en oecologie (Coleoptera: Carabidae). Nederlands Fauna 3, National Natuurhistorisch Museum Naturalis, Leiden.
www.elsevier-deutschland.de/pedobi
Fluctuations of carabid populations inhabiting an ancient woodland (Coleoptera, Carabidae) . Jens Gunther*, Thorsten Assmann . . Institute of Ecology and Environmental Chemistry, University of Luneburg, Scharnhorststr. 1, Luneburg D-21335, Germany Received 20 February 2003; accepted 6 November 2003
KEYWORDS Fluctuation pattern; Ancient woodland; Carabid beetles; Long-term investigation
Summary The changes in population size of carabid beetles inhabiting an ancient woodland were analysed in a long-term investigation covering a period of nine years (1994–2002). The amplitude of fluctuations of the relative density of these species was estimated and compared with those of carabid beetles inhabiting recent woodlands and more unstable habitats in open landscapes. To analyse this, 8 pitfall traps were set in an . ancient beech and oak woodland in the nature reserve ‘‘Luneburger Heide’’ in northern Germany and were emptied every fortnight the whole year round. Catching rates for some species (e.g. Carabus problematicus and Abax parallelepipedus) fluctuated only slightly, whereas those of other species (e.g. C. violaceus and C. auronitens) varied as much as ten-fold. Comparison of these results with those of other long-term investigations of recent woodlands and also of more open habitats showed that in each of the three habitat types some species varied very little in abundance and others, very widely. So it seems that the amplitude of fluctuations in abundance is a feature of each single species rather than a special attribute of their habitats. & 2004 Elsevier GmbH. All rights reserved.
Introduction During the Middle Ages and in early modern times woodlands in the lowlands of northwestern Germany were reduced to small remnants. In the past 200 years, woodland areas have considerably increased due to modern forestry (Hesmer and Schroeder, 1963). Adopting a definition of Peterken (1993) ‘‘ancient woodlands’’ are areas which have been wooded continuously, at least since the end of the
18th Century. This is indicated by historical and topographical maps as well as historical documents. Recent woodlands occupy areas that were re-forested after the end of the 18th century. The high habitat continuity of ancient woodlands over several hundreds or thousands of years could in principle have affected the population biology of woodland-inhabiting species. Two of the population-biological parameters that influence the longterm persistence of species are the reproduction
*Corresponding author. E-mail address: [email protected] (J. Gu. nther). 0031-4056/$ - see front matter & 2004 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2003.11.002
ARTICLE IN PRESS 160
rate and the fluctuation in abundance. To estimate the extent of such fluctuations long-term investigations with samples taken in consecutive years are needed. Long-term studies describing year-to-year variability in the catch of each carabid species are rare, and some of the longer studies do not show the number of individuals caught per year and location separately. In open sandy habitats in the Netherlands Den Boer (1981) found a wide range of net reproduction rate as well as the relative density of carabid beetles, which varied by a factor of over one hundred within 20 years. In more stable habitats such as recent woodlands, Althoff et al. (1992) detected a much smaller variation in population size of a woodland-inhabiting carabid beetle in the Westphalian lowlands (Germany). But nothing is known about the fluctuations in abundance of several woodland-inhabiting carabid beetles of ancient woodlands. To obtain this information it is necessary either to estimate the absolute density or to obtain a whole year catch with pitfall traps for several consecutive years. Pimm and Redfearn (1988) concluded that in the case of insects a period of at least 8 years may be necessary to describe the extent of fluctuations in this taxon. Over shorter periods the standard deviations of the logarithms of annual density (and other measures) increase with time. The long-term investigation in an ancient woodland area of northwestern Germany presented here for the first time has covered a period of 9 years (1994– 2002). The aim of this study is to estimate the amplitude of fluctuations of the relative density of carabid species in an ancient woodland. These fluctuations are then compared with those of carabid species inhabiting other habitats.
J. Gu ¨nther, T. Assmann
The numbers of ground-dwelling arthropods caught in pitfall traps are influenced by various biotic and abiotic factors (Heydemann, 1955, 1957; Luff, 1975; Franke et al., 1988). Baars (1979) detected a strong relationship between the relative density measured with pitfall traps and the absolute density (measured in enclosures) of two carabid beetles in the Netherlands and concluded that continuous pitfall sampling is a reliable relative measure of the sizes of carabid populations (for further data, see also Den Boer, 1979a). For the analysis of the fluctuations of the relative density we chose 7 typical woodland species (cf. Den Boer, 1977; Lindroth, 1985, 1986; Turin, 2000) which were caught in comparatively large numbers in all 9 years (see Table 1). Additionally, 3 more eurytopic but likewise frequently caught species (Pterostichus niger, Nebria brevicollis, C. nemoralis) were incorporated into this analysis. To describe the year-to-year fluctuations in relative density the variance of the estimated net reproduction rate (R) ¼ total number in year cycle i/total number in year cycle i 1 was used (Den Boer, 1990). The range between the highest and lowest relative density recorded in the investigation period is expressed as logarithmic-range (LR) ¼ ln(highest density)ln(lowest density) (see also Den Boer, 1971). Average ln R, the natural logarithms of net reproduction ( ¼ the logarithm of the geometric mean of R), estimates the overall trend of the relative density (Den Boer, 1991). Average ln R-values below zero indicate a decrease and values of average ln R above zero indicate an increase in numbers of a given species during the investigation period. To find out whether these trends were significantly correlated with time we used the sign-trend-test according to Cox and Stuart (cf. Sachs, 1999).
Materials and methods Results In June 1994, 8 pitfall traps containing a mixture of ethanol (40%), water (30%), glycerol (20%) and acetic acid (10%) (cf. Renner, 1980) were set in an ancient beech and oak woodland on acid ground . (Periclymeno-Fagetum). This area ‘‘Hofgeholz Mo. hr’’ is marked as woodland in historical maps like the ‘‘Kurhannoveranische Landesaufnahme’’ (1774–1786). This ancient woodland is located in . the nature reserve ‘‘Luneburger Heide’’ in northern Germany (91500 east, 531060 north). All pitfalls were emptied every fortnight throughout the year so that we were able to analyse the catch for 9 years in the case of the summer-breeding species and the catch for 8 years in that of the spring breeders.
In the years 1994–2002 a total of 11,617 individuals belonging to 47 species were caught (Table 1). The numbers of species caught per year ranged from 15 (1994) to 31 (1998), showing no trend over time. Out of the 11 typical woodland species 8 were caught in every year. The total number of individuals varied from 545 (1995) to 2244 (1998) with no significant trend over time. The results show that some species (e.g. C. problematicus and A. parallelepipedus) fluctuate only slightly in their catching rates in the . ‘‘Luneburger Heide’’ whereas the catching rates of other species (e.g. C. violaceus and C. auronitens)
ARTICLE IN PRESS Carabid populations inhabiting an ancient woodland
161
Table 1. Total year catch of all species in the years 1994–2002 1994
1995
1996
1997
1998
1999
2000
2001
2002
Woodland species Carabus auronitens Carabus problematicus Carabus violaceus Pterostichus oblongopunctatus Abax parallelepipedus Leistus rufomarginatus Notiophilus biguttatus Cychrus caraboides Carabus convexus Harpalus quadripunctatus Carabus glabratus
117 45 129 168 193 19 26 1 1 . .
47 43 33 149 63 17 24 1 1 . .
17 40 52 190 89 18 93 1 1 . .
130 43 208 773 178 18 39 1 . 2 1
119 36 482 497 130 4 75 9 3 5 2
58 52 400 444 257 2 51 5 1 10 .
72 18 351 261 109 6 40 9 . 4 .
23 14 450 63 67 3 2 6 1 . .
32 15 305 199 106 1 24 3 . . .
Other species Pterostichus niger Nebria brevicollis Carabus nemoralis Trechus obtusus Asaphidion curtum Bembidion lampros Poecilus versicolor Pseudoophonus rufipes Pterostichus melanarius Pterostichus minor Amara consularis Bembidion properans Bembidion quadrimaculatum Bembidion tetracolum Carabus arvensis Nebria salina Notiophilus palustris Pterostichus strenuus Loricera pilicornis Amara similata Amara plebeja Synuchus vivalis Agonum sexpunctatum Anisodactylus binotatus Pterostichus nigrita Amara familiaris Pterostichus rhaeticus Agonum fuliginosum Poecilus cupreus Dromius quadrinotatus Harpalus latus Amara municipalis Carabus granulatus Amara tibialis Limodromus assimilis Bradycellus ruficollis
185 73 8 2 . . . 1 . . . . . . . . . . 1 . . . . . . . . . . . . . . . . .
61 80 11 1 1 10 . . . . . . . . . . . . 3 . . . . . . . . . . . . . . . . .
142 16 8 11 3 55 . . . . . . . . . 1 . . . . . . . . . . . . . . . . . . . .
306 20 21 . 4 22 5 1 1 . 1 . . 1 . . 1 1 . 1 1 1 1 2 . . . . . . . . . . . .
658 34 93 2 16 58 1 1 6 1 . 1 . . 1 . 1 . 1 . . . . 2 1 1 2 1 1 . . . . . . .
652 35 22 2 9 11 2 34 3 . . . 1 1 . 1 . 4 2 . . . . 2 . . 1 1 . 1 8 . . . . .
255 22 20 6 . . . 3 1 . . . . . . . . . . . . . . . . . 1 . . . 1 1 . . . .
430 9 2 . . . . . 1 . . . . . . . . . 3 . . . . . . . . . . . . . 1 1 . .
282 23 11 . 2 . . 1 . . . . . . . . . 3 . . 1 . . . . . . . 1 . . . . . 1 1
Total
969
545
737
1783
2244
2072
1180
1076
1011
vary up to a factor of ten (Fig. 1). The Var R-values and the logarithmic-range for C. problematicus and A. parallelepipedus are much lower than the
respective values for C. violaceus, C. auronitens, C. nemoralis, Notiophilus biguttatus and P. oblongopunctatus (Table 2). The other species
ARTICLE IN PRESS 162
J. Gu ¨nther, T. Assmann
10000
Individuals
1000
100
Carabus problematicus Carabus violaceus Carabus auronitens Abax parallelepipedus total
10
1 1994
1995
1996
1997
1998
1999
2000
2001
2002
year
Figure 1. Total year catch, mean and standard deviation (logarithmic scale) of Carabus problematicus, Carabus violaceus, Carabus auronitens, Abax parallelepipedus and all individuals caught (total). Table 2. Ascending sorted variance of the net reproduction rate. (Var R), the logarithmic range (LR), the average logarithmic range of R; the standard deviation (SD) of ln R, the number of R-values (nR), mean number of . individuals7SD and the number of individuals (n) of woodland inhabiting ground beetles in the Luneburger Heide
Carabus problematicus Abax parallelepipedus Nebria brevicollis Pterostichus niger Leistus rufomarginatus Carabus violaceus Pterostichus oblongopunctatus Carabus nemoralis Carabus auronitens Notiophilus biguttatus
Var R
LR
Average ln R
SD ln R
nR
Mean n7SD
n
0.10 0.43 0.57 0.70 0.79 1.43 2.15 4.67 6.90 18.06
1.31 1.4 2.19 2.38 2.89 2.68 2.51 3.84 2.03 3.62
0.14 0.07 0.14 0.05 0.37 0.11 0.04 0.00 0.05 0.00
0.42 0.62 0.82 0.8 0.81 0.83 0.99 1.5 1.09 1.75
8 7 8 8 8 8 7 7 7 7
34714 125765 35725 3307212 1078 2687169 3227234 24729 62743 44729
306 999 312 2971 88 2410 2576 188 498 348
under investigation (N. brevicollis, P. niger and Leistus rufomarginatus) showed low Var R-values but relatively high LR-values. The average ln R indicates the overall trend of the relative density during the investigation period. Within some species this value was near zero, whereas C. violaceus had the highest positive value and L. rufomarginatus the lowest negative value. But none of these decreases or increases were significantly correlated over time.
Discussion The fluctuations of some woodland species inhabit. Mo. hr’’ were low, indicated by ing the ‘‘Hofgeholz
low Var R and LR-values (e.g. C. problematicus, A. parallelepipedus). C. problematicus seems to have more unstable populations in the Netherlands (Var R: 1.42; LR: 1.69, Den Boer, 1990). The reason could be that the habitats investigated there consist of young and open woodland types and adjacent heathlands (Den Boer and van Dijk, 1994). Nothing is known about the fluctuations of C. problematicus populations in beech and oak woodlands in the Netherlands. Abax parallelepipedus is a similar case. In a 40-year-old birch stand in the Ruhr Valley in Western Germany, Schwerk and Abs (2002) detected high fluctuations in the total year catch during 6 years of investigation (Var R: 6.88; LR: 2.83). Loreau (1990) found no long-term changes in the yearly maximum mean density of this species within 10 years in enclosures in a
ARTICLE IN PRESS Carabid populations inhabiting an ancient woodland
beechwood in Lembeek (Belgium) (6 years of investigation). The reasons for the differences of the amplitude are still unknown. A decision is impossible if the different ages of the habitats are important determinants due to the fact that data for long-term fluctuations of this species are only known from three investigation areas. The year-to-year change in the relative densities (Var R) of more eurytopic species like N. brevicollis and P. niger were also relatively low, but with a high range of relative density during the whole investigation period (LR) in the ‘‘Hofgeho. lz Mo. hr’’. In an oak–birch stand in the Netherlands (Den Boer, 1979a), and also in an agricultural field in the UK (Luff, 2001), N. brevicollis showed comparable fluctuations in density (Var R: 1.34, 1.4; LR: 2.07, 3.04). In the study of Schwerk and Abs (2002), this species had lower fluctuations (Var R: 0.56; LR: 0.98). C. violaceus, C. auronitens, P. oblongopunctatus, C. nemoralis, and N. biguttatus showed high fluctuations in the number of individuals caught per year in the present study. In the Netherlands P. oblongopunctatus is a species with a low fluctuation in numbers as described in the study of Den Boer (1979a) mentioned above, and also in a 90year-old oak-forest near Baarn during 9 years of investigation (Brunsting, 1981) (Var R: 0.17, 0.16; LR: 0.81, 1.57). Comparably high fluctuation patterns were found with C. nemoralis (Var R: 8.13; LR: 2.93), and N. biguttatus (Var R: 4.96; LR: 4.11) in the study of Schwerk and Abs (2002). In each of the described habitats species with very low fluctuations in abundance and others with very high fluctuations were found. Even in our fairly stable habitat, like large and ancient woodlands, no dominance by species with a low fluctuation in population density was observed. On the contrary, in this study the fluctuations of species of stable habitats are in most cases as high as those of species of younger woodlands and more open and dynamic habitats. During the study period the amplitude of fluctuations in abundance seemed to be mainly a feature of each single species (and perhaps also differences at the population level) rather than a special component of their habitats. Den Boer (1979b) compared the life tactics of different carabid species of oak–birch forests (stable habitat) and recently abandoned agricultural fields (unstable habitat) in the Netherlands. Although much of the data were only provisional, he concluded that among these carabid species no specific combination of traits has co-evolved to maximize survival in either a stable or an unstable habitat. Therefore, it does not seem very probable that only certain assemblages of traits will always
163
be found together as optimal strategies (cf. Stearns, 1992). Furthermore, habitat stability does not necessarily mean the same predictable environment for different species, e.g., for a winterbreeding ground beetle like Trichocellus placidus woodlands represent unstable habitats because of the highly unpredictable weather conditions in winter during critical phases of the life cycle (Den Boer et al., 1980).
Acknowledgements . This study was supported by the Alfred Topfer . Naturschutz, NNA. We are grateful to Akademie fur . Johannes Pruter for organization and Ludger Schmidt and others for checking the pitfall traps. J.G. was supported by a grant from the Federal Agency for Nature Conservation (Bonn, Germany). We wish to thank Christine Hoefer, Andrea Matern and Ann Thorson for correcting the English and one anonymous referee for valuable comments on the manuscript.
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