Clone Diversity of Eiseniella Tetraedra (Oligochaeta: Lumbricidae) Along Regulated and Free-ﬂowing Boreal Rivers

ECOGRAPHY 25: 714–720, 2002

Clone diversity of Eiseniella tetraedra (Oligochaeta: Lumbricidae) along regulated and free-ﬂowing boreal rivers

Juhani Terhivuo, Elisabeth Lundqvist and Anssi Saura

Terhivuo, J., Lundqvist, E. and Saura, A. 2002. Clone diversity of Eiseniella tetraedra (Oligochaeta: Lumbricidae) along regulated and free-ﬂowing boreal rivers. – Ecogra- phy 25: 714–720.

We have sampled populations of the parthenogenetic and polyploid earthworm Eiseniella tetraedra along the Ume, Vindel and Sa¨var Rivers in northern Sweden. The Vindel River is one of the last free-flowing large rivers in NW Europe, while the Ume River, which flows parallel to it, is harnessed with twenty major dams. Clones were identified on the basis of overall enzyme phenotypes that were detected using starch gel electrophoresis. We found that clone pool diversity is higher along the Vindel River than along the Ume River and the clone pool similarity is, in a similar fashion, higher along the free-flowing river. Evidently the dams stop effectively clone dispersal along the Ume River. Clone diversity is highest at the river mouth. The small free-running Sa¨var River had also high clone diversity at the lower course of the river. Clone turnover between years is high. We found no evidence for parallel adaptation of clones along the two rivers.

J. Terhi6uo ( juhani.terhi6uo@helsinki.ﬁ), Finnish Museum of Natural History, Zoolog- ical Museum, FIN-00014 Uni6. of Helsinki, Finland.—E. Lundq6ist and A. Saura, Di6. of Genetics, Dept of Molecular Biology, Umea˚Uni6., SE-901 87 Umea˚, Sweden.

Rivers transport animals and plants across ecosystems. ecosystems. An ideal test situation would include a The diversity of plants and animals is high in the river number of parallel rivers. biotopes (including the shorelines and nearest area) in A river represents a transect through varying terrain. comparison with the surrounding environment. At the A sexually reproducing organism may respond to same time the rivers are unpredictable habitats. They changing environment through a cline in allele frequen- exhibit large natural seasonal fluctuations in water flow cies, while a clonal organism should show ecotypic and water level, which on a local scale may cause a high differentiation. Given that the pattern of diversity does degree of disturbance. Studying the flora and fauna not show evidence for adaptation, the pattern of diver- along rivers increases our understanding of the pro- sity may be used to trace the migration history of the cesses that affect the diversity and dispersal of organ- organism. Here we study clone diversity of the clonal isms. The flow of most large rivers is, however, earthworm Eiseniella tetraedra (Sav.). Rivers are self- regulated with dams and relatively few free-flowing evident corridors for these worms to spread. rivers remain (Dynesius and Nilsson 1994). It would be We have chosen to study the Ume and Vindel Rivers most desirable to get data that show how this regula- in Sweden. These rivers flow to the Gulf of Bothnia but tion affects the pattern of biological diversity. One way originate in the Scandes Mountain chain. The Vindel to get these data is to compare a regulated river with a River is one of the few free-flowing major rivers in NW free-flowing one next to it or to follow a number of Europe. The Ume River flows parallel to the Vindel but rivers before, under and after regulation. In Sweden the its flow has been regulated with dams and impound- northern rivers run in parallel through broadly similar ments in the course of the past 50 yr. The two rivers

714 ECOGRAPHY 25:6 (2002) flow together before reaching the Gulf of Bothnia. Both rivers are relatively unpolluted (Jansson et al. 2000). The two rivers represent two parallel transects through roughly similar overall terrain. Evidence for differences in adaptation among clones should be reflected along sets of similar ecological gradients. We have also sampled worms from the lower course close to the mouth of a small free-running river, the Sa¨var. We pose the following questions: what is the amount of clone diversity and how is it distributed along a major river? Has the mouth of a large river with wide catchment area higher clone diversity in comparison with a small one? Do dams affect dispersal and diversity of clones? Is there any evidence for parallel adaptation of clones Fig. 2. A profile of the collection localities along the Ume and along the two rivers? Vindel Rivers. Note that the unregulated Vindel River flows smoothly in contrast to the regulated Ume River. m.a.s.l.=altitude expressed as meter above the sea level. Material and methods with a catchment area of 1165 km2. Water discharge at The rivers its mouth ranges annually between 1 and 160 m3 s−1 The Vindel and Ume Rivers (Fig. 1) are of the same (Nilsson et al. 1991). length (both 450 km from the mountains in Norway down to the point of confluence at Va¨nna¨s). Both have a catchment area of ca 13 000 km2. Water discharge of The worms the Vindel River is subject to extensive differences from Eiseniella tetraedra is tetraploid and parthenogenetic in a minimum mean of 15 m3 s−1 to a maximum mean of northern Europe (Terhivuo et al. 1994). The species 1660 m3 s−1 at the confluence with the Ume River. The reproduces through an automictic (meiotic) partheno- natural discharge for Ume River at this confluence genesis, but the chromosome set is doubled before varied from 72 m3 s−1 up to 1800 m3 s−1. After meiosis (Omodeo 1957). regulation Ume River consists of a stair-stepped series Eiseniella tetraedra is a remarkably stenotopic inhab- of storage reservoirs and run-of-river impoundments itant of waterlogged habitats such as shores of lakes (Fig. 2). In total there are 20 major dams. The regu- and rivers and the brackish water of the Baltic Sea lated discharge in Ume River varies between 0 and 918 (Terhivuo 1988). The species is in general sluggish and m3 s−1. The upper reaches of the Ume River had stationary but may swim by wriggling its body when before regulation few major lakes, whereas the Vindel disturbed. This small earthworm reproduces through River has only one. The Sa¨var River is 145 km long laying resistant cocoons that can be carried by water (Schwert and Dance 1979). It is short-lived, attaining at most an age of one and a half years (Sims and Gerard 1985).

Sampling We sampled the following localities in August of 1999. Figure 1 shows the localities situated along the rivers. V1. Sorsele, Ammarna¨s, 540 m a.s.l. Lake Tjultra¨sk, a1–1.5 m wide brook ﬂowing from a mountain to the lake that drains to the Vindel River. The worms were found under stones and among gravel. V2. Sorsele, Ja¨rnforsen, 395 m a.s.l. A mountain brook running to the Vindel River. Under stones and among liverworts in the brook. V3. Lycksele, Holmforsen, 275 m a.s.l. Under stones at the water line of the Vindel River. Fig. 1. A map of a section of northern Sweden and Norway UV1. Va¨nna¨s, 77 m a.s.l. A steep river bank at the that shows the sampling localities of E. tetraedra in 1999– conﬂuence of the Ume and Vindel Rivers. The worms 2000. were under stones and plant detritus at the water line.

ECOGRAPHY 25:6 (2002) 715 UV2A. Umea˚, Holmen, at sea level, a bay in the Table 1. The numbers of worms sampled, clones and local northern part of the Holmen Island in the estuary of clones (found only in one locality). N=sample size, C=number of clones. the Ume River. The worms were found under stones, pieces of board etc. and among plant detritus at the LocalityN C Local clones water line. S. Umea˚, The Sa¨var River, 3 m a.s.l. Under stones and among gravel at the water line. This is V1 25 10 4 V2 25 8 2 identical to locality 1 in Terhivuo and Saura (1999). V3 55 10 4 In August of 2000 we sampled: U1. Norway, Rana, U135 5 4 Umbukta, 535 m a.s.l. At the mouth of a brook flowing U2 27 7 6 U320 4 2 from the watershed to an impoundment of the Ume U4 30 4 3 River. Under stones and among plant detritus. U2. UV1 20 11 8 Storuman, Klippen, 460 m a.s.l. A brook running to UV2A 3018 9 UV2B31 24 17 the Ume River. Among stones and plant detritus. U3. S181325 Storuman, Forsba¨ck, 440 m a.s.l. A brook flowing to the Ume River at the Forsba¨ck impoundment. Under stones and among gravel and liverworts. U4. Lycksele, individuals in the two areas compared simultaneously Norrlunda, 212 m a.s.l. A boggy bank of an impound- (e.g. Wallwork 1970). ment of the Ume River. Under water line among mosses and drifting plant detritus. UV2B. Identical to UV2A sampled in 1999. Results The worms were taken alive to the laboratory, where they were weighed. The first anterior segments were The laboratory experiment involving 12 adults and stored in deep freeze at −70°C; the rest of the worm their offspring showed that in each case the enzyme was stored in alcohol for morphometric measuring. phenotype of the offspring was identical with its parent. They represented different phenotypes in all the enzyme systems that we use here. The result shows that the worms reproduce clonally and transmit the enzyme Laboratory procedures phenotype intact to their offspring. Four enzyme systems were assayed with starch gel electrophoresis: esterase (Est), leucine aminopeptidase Diversity of clone pools (Lap), peptidase (Pep) and phosphoglucose isomerase (Pgi). The methods are identical to the ones described Table 1 shows that the two river mouths (Ume: UV2A earlier for Eiseniella (see e.g. Pecsenye and To´thme´resz and UV2B and Sa¨var: S) have more clones than the 1994, Terhivuo and Saura 1999). Electrophoretic vari- populations along the river. The Vindel River localities ants of these enzyme systems were indicated with let- (V1 through V3) have more clones than the ones along ters. The total enzyme phenotype of a worm was a the Ume River (U1 through U4). Moreover, the locali- combination of these letters. ties along the Vindel River have less local clones (36%) In 1999 we took 12 adult worms to the laboratory than the ones along the Ume River (75%). We have not from different populations of the Vindel and Sa¨var included the Va¨nna¨s locality (UV1) at the confluence of Rivers and let them lay cocoons in plastic vials. The the Ume and Vindel Rivers to these calculations. This enzyme phenotype of the offspring was compared with locality is under influence from both rivers and can that of the parent worm for each of the four enzyme neither be classified as a free-flowing nor a regulated systems that we have used here. locality. It has as many (73%) local clones as the Ume River populations. The samples from the Ume River mouth (UV2A and UV2B) and the sample from the Morphometrics and statistics Sa¨var River mouth (S) had 62% and 72% local clones, respectively. Fresh body weight and posterior body length, including Figure 3 shows clone diversity calculated according clitellum, were measured for each adult worm. The to distribution-free rarefaction method. The expected localities were compared according to the Kruskal-Wal- number of clones is given for two sample sizes: 15 and lis test in these respects. 20 individuals. Note that standard deviations could not Clone pool diversity was calculated according to the be calculated for two samples of 20 individuals. As in distribution-free rarefaction method (Simberloff 1979). Table 1, the river mouths have greatest clone diversity The method allows comparisons between samples with and the localities along the Vindel River are more different numbers of individuals. Clone pool similarities diverse than the ones on Ume River. In the small Sa¨var are based on the Renkonen formula, which takes into River the diversity at the downstream locality is as account both the number of clones and the number of extensive as in the case of the large river.

716 ECOGRAPHY 25:6 (2002) which again shares clones with the next one downstream (V3). Locality V1 also has clones in common with locality V3. The Vindel River also contributes clones to the Va¨nna¨s locality (UV1) at the confluence of the Vindel and Ume Rivers; while the Ume River does not share any clones with locality UV1. Evidently the clones spread downstream the Vindel River. The flow of the Ume River is regulated with impoundments. The localities along this river do not share Fig. 3. Clone diversity according to the rarefaction method. The expected numbers of clones are calculated for sample sizes any clones with each other. They share, however, some of 15 and 20 individuals. Standard deviation bars indicate91 clones with the Sa¨var River, (which is not connected SD. with the Ume and Vindel Rivers) and again with the Holmen locality at the estuary. In contrast to the Turnover of clones Vindel River, there is hardly any evidence of clones spreading downstream the Ume River. The Holmen locality (UV2A and UV2B) is the only one, from which we have material from 1999 and 2000. The Renkonen similarity index showed rather low simi- Morphometrics larity: 16.1% between years, which may mean a rapid turnover of clones sampled in identical fashion at the Table 3 shows body weight and posterior body length same site. Heavy rains caused a flooding of rivers over for the adult worms in localities sampled in 1999 and much of Sweden in late August 2000. Water levels were 2000. The populations sampled are significantly hetero- ca 1–1.5 m above the sample sites of 1999. We did not geneous in these traits as shown by the Kruskal-Wallis get a sample from Va¨nna¨s and, despite efforts, a few test applied. At the same time, there are no trends worms only from the Sa¨var River. associated with an area or river. The mountain brooks had large worms (V2 and U1) as well as small ones (V1 and U2) and differed from each other. The two samples from the Ume River mouth (UV2A and UV2B) were Dispersal of clones also clearly different from each other. Table 2 shows the clone pool similarities according to the Renkonen index. The Holmen locality (UV2 in Fig. 1) is at the estuary of the Ume River. This locality Discussion shares clones with all other localities except locality U1, Genetic diversity which is situated on the watershed area on the Scandes Mountains in Norway. The free-flowing Vindel River The clone pool diversity values that we report here are contributed more clones (10 clones) than the regulated of the same order of magnitude than the ones that we Ume River (3 clones) to the Holmen (UV2) estuary have found before for E. tetraedra (Terhivuo and Saura population. 1997, 1999). We had previously (Terhivuo and Saura Populations along the Vindel River (V1, V2 and V3) 1997) found evidence for a more or less even distribu- have more clones in common than populations along tion of clones across northern Europe. Evidently, E. the Ume River (U1 through U4). tetraedra must have an effective mechanism of passive Along the Vindel River a stepwise pattern can be dispersal. Many other clonal and flightless invertebrates seen (Table 2). The locality highest upstream (V1) show much the same pattern (e.g. Stenberg et al. 1997, shares clones with the next one downstream (V2), 2000).

Table 2. Clone pool similarities among E. tetraedra populations based on the Renkonen index. The values are given in per cent similarity; 100% means complete similarity and 0 means a complete lack of similarity. UV2AB represents the combination of samples of the years 1999 and 2000 from the Holmen locality.

V1 V2 V3 U1 U2 U3 U4 UV1 UV2AB S

V1 – 8.0 8.0 0 0 0 0 17.0 12.2 4.0 V2 – 5.5 0 0 0 0 5.0 8.9 4.0 V3 – 0 3.6 0 3.6 0 18.6 4.0 U1 – 0 0 0 0 0 2.9 U2 – 0 0 0 3.3 0 U3 – 0 0 1.6 4.0 U4 – 0 6.6 0 UV1 – 3.3 0 UV2AB – 1.6

ECOGRAPHY 25:6 (2002) 717 Table 3. Fresh body weight (g) and posterior body length (=incl. clitellum, mm in ethanol preserved specimens) in E. tetraedra adults from the Vindel (V1–V3), Ume (UV1, UV2A and B, U1–U4) and Sa¨var Rivers (sample S).

Locality N of ind. Fresh body weight Posterior body length

MeanSD Median Mean SD Median

V1 18 0.09 0.02 0.08 15.31 2.30 15.00 V2 16 0.12 0.020.12 19.66 2.23 19.00 V3 40 0.11 0.03 0.11 17.54 3.06 17.50 U1 22 0.12 0.03 0.11 21.14 3.48 21.20 U2 15 0.08 0.030.09 16.80 3.63 17.00 U3 12 0.110.03 0.12 19.96 1.66 19.70 U4 16 0.09 0.02 0.09 17.91 2.12 17.50 UV1 11 0.09 0.020.09 16.68 2.09 17.00 UV2A 19 0.07 0.03 0.06 15.472.92 15.00 UV2B 23 0.12 0.03 0.12 18.24 3.02 19.00 S 20 0.10 0.030.11 16.80 2.30 17.00 Kruskal-Wallis: *** ***

We have before surveyed morphometric and genetic tunistic i.e. it often occupies unstable waterlogged habi- variation in north European parthenogenetic earth- tats. Lundqvist and Andersson (2001) studied the worms (Terhivuo and Saura 1990, 1993a, b, 1996). genetic evidence of dispersal of plants with different Eurytopic lumbricids (e.g. Dendrobaena octaedra) have propagule types along the upper reaches of the Vindel a high clonal diversity (Terhivuo et al. 1987, Terhivuo River. They found that the dispersal ability and breed- and Saura 1990, 1997), irrespective of habitat. Again, at ing strategy are reflected in the genetic population least some commensals of culture have low diversity, so structure. Bistorta 6i6ipara (Polygonaceae) reproduces that, Octolasion cyaneum spreading with human culture through bulbils that in contrast to the cocoons of E. is in general represented by a single or only few clones tetraedra sink rapidly in water. Populations along the at almost any locality (Terhivuo and Saura 1993a, b). Vindel River share only a few clones, and evidently the Parthenogenetic earthworms that live close to the soil clones cannot disperse over long distances. We have no surface, the so-called epigeics, including E. tetraedra turnover data for B. 6i6ipara, but these plants are have higher clone diversity than endogeics, i.e. worms long-lived (Law et al. 1983). Perhaps there are old and that burrow into the soil (Terhivuo and Saura 1997). permanent clone assemblages of Bistorta along the Eiseniella tetraedra has a high clonal diversity on the Ume River, irrespective of the effect of dams that Swedish mainland, with ca 24 different clones among restrict clone flow. 50 individuals sampled. The diversity falls towards the The amount of clone diversity at the mouth of the east, so that on the A,land Islands between Sweden and Sa¨var River was about the same order of magnitude as Finland the corresponding number of clones is ca 16 at the mouth of the Ume River. These two localities and on the Finnish mainland ca 12.5. shared, however, just one clone. This means that these We have also followed the clone diversity along the two populations do not represent samples of a large lower course of the Sa¨var River and on the islands at homogeneous coastal clone pool. In fact, the previous the mouth of it in the vicinity of the town of Umea˚ for results (Terhivuo and Saura 1997) on coastal popula- three years (Terhivuo and Saura 1999). The rate of tions on the Baltic sea show much lower diversity isostatic land upheaval is high at this area: ca 1 cm (about half of that at locality S and UV2) on non-river yr−1, so that all the islands off Umea˚ are geologically mouth sea shore. very young (Ericson and Wallentinus 1979). Clones We have tried to assess whether the extensive regula- present along the river were also found at the river tion of the Ume River has an effect on clone diversity mouth as well as on the islands off the river mouth. in comparison with the free-flowing Vindel River. Clone diversity was highest along the river and fell Firstly, we found that the Ume River has lower clone towards the open sea on the islands. The islands had diversity than the Vindel River. Secondly, clones can few clones but high clone similarity, that is, the same effectively disperse along the Vindel River but not clones had colonized the islands. There is considerable along the Ume River. Presumably, the cocoons seldom turnover of clones between years along the Sa¨var River pass the dams. Likewise, the Vindel River contributed and on the islands. This is seen in the turnover values much more to the high clone diversity than the Ume calculated from the data of Terhivuo and Saura (1999). River at the river mouth common to the both rivers. We have also observed a rapid turnover among E. Andersson et al. (2000) have, using floating diaspore tetraedra clones at the Holmen locality (UV2). This mimics, directly observed that diaspores do not pass the may be associated with the circumstance that the dams of the Ume River. The diaspore mimics did not worms are short-lived and that E. tetraedra is oppor- pass the Storvindeln Lake on the Vindel River either,

718 ECOGRAPHY 25:6 (2002) but otherwise they floated downstream unimpeded Acknowledgements – We thank Astrid Ho¨glund and Kerstin along the Vindel River. Kristiansson for skillful technical assistance and Vladimir There were no clear-cut regional trends in the mor- Tolchkov for a keen pair of eyes and enthusiasm in collecting the worms. This study was financially supported by a grant phometric measures done on the worms. This agrees from the Swedish Natural Science Research Council (NFR). with our previous observations (Terhivuo et al. 1994, Terhivuo and Saura 1997, 1999) on morphology: we have found only local differences but we have failed to correlate them with genetic differences. References Andersson, E., Nilsson, C. and Johansson, M. E. 2000. Effects of river fragmentation on plant dispersal and riparian flora. – Reg. Riv. Res. Manage. 16: 83–89. Deterministic versus random patterns Asker, S. E. and Jerling, L. 1992. Apomixis in plants. – CRC Press, Boca Raton, Florida. Species of animals cannot share the same niche. The Christensen, B. and Jelnes, J. 1976. Sibling species in the definition of a species is based on the concept of oligochaete worm Lumbricillus ri6alis (Enchytraeidae) re- reproductive isolation. Clonal organisms are reproduc- vealed by enzyme polymorphisms and breeding experi- tively isolated from each other and behave like sexually ments. – Hereditas 83: 237–244. Christensen, B., Berg, U. and Jelnes, J. 1976. A comparative reproducing species in this respect. Clones of a clonal study on enzyme polymorphism in sympatric diploid and ‘‘species’’ seem to share, however, the same niche (Suo- triploid forms of Lumbricillus lineatus (Enchytraeidae, malainen et al. 1987, Asker and Jerling 1992). Oligochaeta). – Hereditas 84: 41–48. We have here two rivers that run in parallel from the Dynesius, M. and Nilsson, C. 1994. Fragmentation and flow regulation of river systems in the northern third of the same range of mountains. This can be taken to repre- world. – Science 266: 753–762. sent a test of clone adaptation. If the clones were Ericson, L. and Wallentinus, H.-G. 1979. Sea-shore vegetation adapted to an ecological parameter, say altitude, we around the gulf of Bothnia. Guide for the International should expect to find the same clones in succession Society for Vegetation Science. – Wahlenbergia 5: 1–142. Jaenike, J. and Selander, J. 1979. Evolution and ecology of along the two rivers. When we go downstream the parthenogenesis in earthworms. – Am. Zool. 19: 729–737. Vindel River we observe a smooth pattern of clone Jaenike, J. and Selander, J. 1985. On the coexistence of replacement. Localities along the Ume River do not, ecologically similar clones of parthenogenetic earthworms. however, share clones, i.e. there is no such pattern – Oikos 44: 512–514. Jansson, R. et al. 2000. Effects of river regulation on river- whatsoever. However, the two rivers share a single margin vegetation: a comparison of eight boreal rivers. – clone between the localities V3 and U4 close to each Ecol. Appl. 10: 203–224. other and a single clone between V3 and U2. Moreover, Law, R., Cook, R. E. D. and Manlove, R. J. 1983. The the locality U1, high up on the mountains, shares a ecology of flower and bulbil production in Polygonum 6i6iparum. – Nord. J. Bot. 3: 559–565. clone with the Sa¨var River mouth. Clone flow, that is Lundqvist, E. and Andersson, E. 2001. Genetic diversity in migration downstream the river, seems to explain the populations of plants with different breeding and dispersal smooth replacement of clones along the Vindel River. strategies in a free-flowing boreal river system. – Hereditas Christensen et al. (1976) as well as Christensen and 135: 75–83. Nilsson, C. et al. 1991. Small rivers behave like large rivers – Jelnes (1976) have, however, found evidence for differ- effects of postglacial history on plant-species richness along ential adaptation among the clones of the Lumbricillus riverbanks. – J. Biogeogr. 18: 533–541. (Enchytraeidae) on the shores of the North Sea and the Omodeo, P. 1957. Lumbricidae and Lumbriculidae of Green- Danish fjords. In addition, the distribution of the major land. – Medd. Gro¨nland 124: 1–27. Pecsenye, K. and To´thme´resz, B. 1994. Linkage disequilibrium clones of the weevil Otiorhynchus scaber in northern in Hungarian populations of Drosophila melanogaster. – Europe to the east and west of the Baltic Sea is Hereditas 121: 301–306. correlated with the biotic zonation, which can be taken Saura, A. et al. 1976. Genetic polymorphism and evolution in as evidence for differential adaptation (Saura et al. parthenogenetic animals. III. Tetraploid Otiorrhyncus scaber (Coleoptera: Curculionidae). – Hereditas 82: 79– 1976, Stenberg et al. 1997, 2000). 100. Jaenike and Selander (1979, 1985) have offered three Schwert, D. P. and Dance, K. W. 1979. Earthworms cocoons hypotheses to explain the apparently complete niche as a drift component in a southern Ontario stream. – Can. overlap of earthworm clones, viz. differential adapta- Field-Nat. 93: 180–183. Simberloff, D. 1979. Rarefaction as a distribution free method tion, transient overlap with replacement and clonal of expressing and estimating diversity. – In: Grassle, R. W. drift. They mean that the frequencies of clones seem to et al. (eds), Ecological diversity in theory and practice. be subject to random events. Our results support the Fairland, Maryland, pp. 159–176. clonal drift hypothesis. Sims, R. W. and Gerard, B. M. 1985. Earthworms. – Synopsis of the British Fauna (New Ser.) 31: 1–71. An ecological theatre that would allow testing adap- Stenberg, P. et al. 1997. Clone diversity of tetraploid Otiorhyn- tive differences among clones is made up of the parallel cus scaber in northern Europe. – Hereditas 126: 169–172. small brooks that flow from the mountains to the lakes Stenberg, P. et al. 2000. Clone diversity in the polyploid weevil below: here the altitudinal difference is great along a Otiorhyncus scaber. – Hereditas 132: 137–142. Suomalainen, E., Saura, A. and Lokki, J. 1987. Cytology and short stretch and the headwaters of the brooks close to evolution in parthenogenesis. – CRC Press, Boca Raton, each other Florida.

ECOGRAPHY 25:6 (2002) 719 Terhivuo, J. 1988. The Finnish Lumbricidae fauna and its afﬁnities and morphometric differentiation of A,land popu- formation. – Ann. Zool. Fenn. 25: 229–247. lations. – Ecography 20: 185–196. Terhivuo, J. and Saura., A. 1990. Allozyme variation in Terhivuo, J and Saura, A. 1999. Island biogeography of a north parthenogenetic Dendrobaena octaedra (Oligochaeta, Lumb- European parthenogenetic earthworm: fugitive clones of ricidae) populations of eastern Fennoscandia. – Pedobiolo- Eiseniella tetraedra (Sav.) (Lumbricidae). – Pedobiologia 43: gia 34: 113–139. 481–486. Terhivuo, J. and Saura, A. 1993a. Genic and morphological Terhivuo, J. et al. 1987. Enzymic and morphometric variation variation of the parthenogenetic earthworm Aporrectodea of Dendrobaena octaedra (Sav.) (Oligochaeta:Lumbricidae) rosea in southern Finland. – Ann. Zool. Fenn. 30: 215–224. in eastern Fennoscandia – a preliminary report. – In: Terhivuo, J. and Saura, A. 1993b. Clonal and morphological Bonvicini Pagliai, A. M. and Omodeo, P. (eds), On earth- variation in marginal populations of parthenogenetic earthworms Octolasion tyrtaeum and O. cyaneum (Oligochaeta, worms. Selected Symp. and Monogr. U.Z.I., 2, Mucchi, Lumbricidae) from eastern Fennoscandia. – Boll. Zoll. 60: Modena, pp. 89–102. 87–96. Terhivuo, J., Saura, A. and Hongell, K. 1994. Genetic and Terhivuo, J. and Saura, A. 1996. Clone pool structure and morphological variation in the parthenogenetic earthworm morphometric variation in endogeic and epigeic north-Eu- Eiseniella tetraedra (Sav.) (Oligochaeta, Lumbricidae) from ropean parthenogenetic earthworms (Oligochaeta, Lumbri- south Finland and north Norway. – Pedobiologia 38: cidae). – Pedobiologia 40: 240–250. 81–96. Terhivuo, J. and Saura, A. 1997. Island biogeography of north Wallwork, J. A. 1970. Ecology of soil animals. – McGraw- European parthenogenetic Lumbricidae: I. Clone pool Hill.

720 ECOGRAPHY 25:6 (2002)