Plant Ecology 133: 101106, 1997. c 1997 Kluwer Academic Publishers. Printed in Belgium.

101

Effects of altitude and seed size on germination and seedling survival of heathland plants in north Spain
M. L. Vera
Departamento de Biologa de Organismos y Sistemas, Universidad de Oviedo, 33071 Oviedo, Spain i
Received 9 October 1996; accepted in revised form 20 July 1997

Key words: Germination, Elevation effect, Ericaceae species, North Spain, Seed size

Abstract The effects of altitude and seed size on germination and seedling survival were studied in Calluna vulgaris, Erica cinerea and Erica vagans. Experiments were carried out in the laboratory over a one year period. Seeds collected from heathlands of different altitudes were divided in two size classes. They were sowed on moist lter paper inside Petri dishes which were placed in chambers at 20 C and a photoperiod of 12 h light/12 h darkeness. The seeds of Calluna vulgaris were the rst to begin germination and had the highest rate and percentage of germination. The germination of Erica vagans was moderate, while seeds of Erica cinerea germinated later and the germination was very low. Seeds of Calluna vulgaris and E. cinerea collected at the highest altitudes had the highest germination percentages. Seed size in Calluna vulgaris and E. cinerea did not affect germination. However, large seeds of Erica vagans had higher germination rates and percentages than small seeds. The large seed size of Calluna vulgaris contributes to a better survival and growth of its seedlings. Introduction Calluna vulgaris (L.) Hull (hereafter referred to as Calluna), Erica vagans L. and Erica cinerea L. are three heathland plants common in Asturias (North Spain), but Calluna has a wider altitudinal range than the other two heaths, being spread from sea level to over 2000 m (Vera 1983). These dwarf shrubs grow in sites frequently disturbed. The recolonization of heaths in disturbed areas can occur by seedling establishment or by vegetative methods (Hobbs et al. 1984; Mallik & Gimingham 1985; Clement & Touffet 1990). The three species studied use both mechanisms of regeneration, but the emergence of seedlings is more frequent in Calluna and E. cinerea than in E. vagans (Vera 1994; Vera & Obeso 1995; Obeso & Vera 1996). However, E. vagans shows a higher sprouting ability than the other two species. Calluna and Erica cinerea maintain persistent seed banks (Miller & Cummins 1987; Mallik et al. 1984). The presence of a seed bank in soils of heathland vegetation and their capacity for germination and seedling establishment could partly determine the regeneration of the heathland. Seedling regeneration could be limited by low germination or high seedling mortality. Variations in germination of different species had been observed in relation to altitude (Miller & Cummins 1987; Lavorel 1987; Holm 1994).Thus, this factor could have an inuence on germination. An estimate of germination capacity is important determining sexual reproductive efciency, which could vary with altitude and between species. Seedling regeneration takes place even at high altitudes, where establishment and growth of plants occur in a brief period. Several studies suggest that some species can be maintained by rapid germination during less severe climatic periods (Archibold 1989). The percentage of germination and survival of seedlings could be inuenced by the seed size (Harper 1977; Tripathi & Khan 1990; Lusk 1995). Therefore, a comparison of the germination capacity of seeds from different altitudes and the effect of seed size on germination and seedling survival is necessary in studies on reproductive efciency of the species mentioned above. Data from seed regeneration at different altitudes are necessary to understand the mechanisms of colonization of disturbed areas, and they also are

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Table 1. Locality and site descriptions Calluma vulgaris Cabo Pe as. n Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. Pto. San Isidro. 100 m. 800 m. 800 m. 1200 m. 1200 m. 1510 m. 1620 m. 1680 m. 2020 m. 2090 m. Quartzite. Limestone. Quartzite. Quartzite. Shale. Shale. Shale. Limestone. Quartzite. Quartzite. Soil pH: 3.9 Soil pH: 6.8 Soil pH: 4.9 Soil pH: 4.7 Soil pH: 4.8 Soil pH: 5.2 Soil pH: 3.7 Soil pH: 5.1 Soil pH: 3.6 Soil pH: 3.7 Erica vagans Erica cinerea

       

   

  

Cabo Cape; Pto. Mountain pass. Table 2. Number of months required for seeds to reach 90% germination (t90 ) in large and small seeds of Calluna vulgaris, Erica cinerea and E. vagans obtained from different altitudinal locations. Species Altitude (m) 100 810

1200

1510

1620

1680

2020

2090

a) Large seeds Calluna vulgaris Erica vagans Erica cinerea

3 5 11

3 6 12

4 6 10

3 4

b) Small seeds Calluna vulgaris Erica vagans Erica cinerea

4 7 11

7 10 12

3 7 11

4 6

important in order to know the distribution patterns of different plants.

Material and methods The study was carried out in Asturias (North Spain) along a 75 km north-south section from the coast (Cape Pe as) to the central range of the Cantabrian Mountains n (San Isidro Mountain Pass). Seeds capsules were collected in November 1994 from ve individuals of each species at each altitude. Characteristics of the samples sites are given in Table 1. Seed size Seeds were divided in two classes according their length and width. They were measured with a micrometer under a stereoscopic microscope. Calluna vul-

garis: Small seeds ( 0:7  0:5 mm) and large seeds ( 0:7  0:5 mm); Erica vagans: Small seeds ( 0:6  0:5 mm) and large seeds ( 0:6  0:5 mm); Erica cinerea: Small seeds ( 0:8  0:6 mm) and large seeds ( 0:8  0:6 mm). Seed germination The two seed size classes selected for each species were stored dry at 5 C for 6 weeks under darkness. In January, 50 ripe seeds of each size and species were sown in a Petri dish. The Petri dishes were kept in a chamber at 20 C with a photoperiod of 12 h light/12 h darkness. Six replicates for each seed size, species and collection site were used. Seeds were regularly watered with tap water. The study of seed germination lasted 12 months and counts were made every 14 days during the rst 6 months and every month during the last 6 months.

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Table 3. Seedling survival and mean weight from each seed size in different altitudes of Calluna vulgaris at the end of 3th month. Locality Seedling survival (%) Large seeds Small seeds 100 m. 810 m. 1200 m. 1620 m. 1680 m. 2020 m. 2090 m. 84 82 70 90 74 96 90 64 36 36 70 58 86 64 Mean seedling weight (mg) Large seeds Small seeds 0.35 0.31 0.37 0.33 0.41 0.37 0.32 0.25 0.21 0.27 0.27 0.31 0.28 0.28

Cabo Pe as, n Pto. San Isidro, Pto. San Isidro, Pto. San Isidro, Pto. San Isidro, Pto. San Isidro, Pto. San Isidro,

Germination rate (t90 ) was determined, as the time in months required to reach 90% of nal germination percentage. Survival and weight of seedlings Germinated seeds of Calluna from both seed sizes originating in each altitude (except from 1510 m, due to scarce germination during the rst month) were removed to other Petri dishes in February 1995. Two replicates of 25 germinated seeds were carried out. The dishes were placed in the same chamber where the study of germination was realized. The survival of seedlings and the dry weight of the livings ones was determined three months later. This study was only performed in Calluna, because it was the species which had the highest seedling production. Statistical analyses The statistical analysis of germination was carried out with one way ANOVAs. The germination percentage data were arc-transformed for Calluna and a squareroot-transformation of low germination percentage was carried out in Erica cinerea.

from higher altitudes had the highest germination percentage (Figure 1) and the shortest t90 (Table 2). Seed size in Calluna did not affect germination, only large seeds germinated slightly better in the rst month than small seeds (p 0:01). The percentage of germination of Erica vagans was lower than in Calluna (mean 76%) at the end of the experiment. The altitude did not seem to have an effect on total germination, although the percentage of germination was higher in the four rst months in seed 0:001). There were from the highest altitudes (p signicant differences in the germination among seed size in E. vagans (p 0:0001), showing the large seeds higher germination percentages (Figure 1) and reaching the 90% of germination in a shorter time compared to the smaller seeds (Table 2). Germination of Erica cinerea was very low (mean 23%), although the seeds collected from the highest altitude had a higher percentage of germination than those from lower altitudes (p 0:0001), with an average germination of 51% at the end of 12 months. There were no signicant differences in the rate and the percentage of germination between the two E. cinerea seed size classes. The highest t90 values in the studied heathland plants was obtained in E. cinerea which was the species with the lowest germination percentages. Effect of seed size on seedling survival and weight The larger seeds of Calluna produced the seedlings with the highest survival rate, compared with smaller seeds (p 0:01; Table 3). These seedlings were also heavier (00 31 to 00 41 mg) than those derived from the small seeds (00 21 to 00 31 mg) (p 0:001; Table 3). Seedlings from large seeds, collected at the highest altitudes, showed the highest survival rate (Table 3).

Results Effect of altitude and seed size on germination The seeds of Calluna vulgaris had the highest germination percentage (mean 88%) twelve months after sowing and it was the rst species to begin germination. There were signicant differences between Calluna 0:0001), at each seeds from different altitudes (p month until the end of the experiment. Seeds collected

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Figure 1. Percentage of cumulative germination during twelve months after sowing in relation to seed size from different altitudes. Seeds were incubated at a 12 h light/12 h darkness daily photoperiod at 20 C.

105 Discussion Effect of altitude and seed size on germination The high percentage and rate of germination of Calluna seeds is in agreement with previous studies (Gimingham 1960; Mallik & Gimingham 1985; Pons 1989; Gonz lez-Rabanal & Casal 1995). The results from the a seeds of E. vagans are also similar to those obtained in previous experiments (Obeso & Vera 1996). The seeds of E. cinerea, which failed to germinate in other studies (Mallik & Gimingham 1985), yield the lowest germination percentage and the slowest germination rate of all three species. This indicates that the highest t90 values correspond to species with the lowest germination percentages (Gonz lez- Rabanal & Casal 1995). a The results from the seeds of Calluna and E. vagans suggest that part of the physiological dormancy of the seeds has been broken. Although freshly ripened seeds of Calluna and Erica have a high degree of dormancy (Pons 1989; Bruggink 1993). The effects of the dry storage at 5 C could have induced the physiological changes to break the innate dormancy (Baskin & Baskin 1989; Probert 1992). Germination percentage and rate could be inuenced by the altitude at which seed were collected. In this study, seeds of Calluna and E. cinerea collected at the highest sites reached higher and quicker germination than those from the lower ones. Chilling represents a natural dormancy breaking mechanism in many species followed by favourable temperatures (Baker 1989; Probert 1992). Seeds collected by us at the higher altitudes might have started the stratication period earlier than seeds from lower sites due to the reduction of temperature as altitude increases. It may explain why Calluna and E. cinerea seeds from the highest populations, subjected to low temperatures, showed higher germination percentages. The germination of E. vagans was not inuenced by altitude. This suggests that its seeds are less affected by the lower temperatures at high altitudes. In Southern France, Lavorel (1987) reported similar results and conclusions for Calluna , showing that seeds from high sites (Ecrins, C vennes, e and Pyrenees) germinated better than those collected in low sites (Montpellier). However, Miller & Cummins (1987) obtained different results for Calluna in the Scottish mountains. This could be due to the fact that those experiments were done with seeds collected at lower altitudes, (between 300 and 750 m) than ours. However, the compensatory effect between latitude and altitude between the mountains of Scotland and Asturias has to be taken in account. Different responses in the seed germinability of birches along an altitudinal gradient were described by Holm (1994). This author found that seed germinability decreased or increased with altitude according to species and between years. An alternative explanation is that the intensity of dormancy could vary in Calluna and E. cinerea according to altitude, being lower in the higher populations. This may partly be explained by an earlier and higher germination of seeds from these zones when subjected to optimal temperatures for germination during a brief growing season. An earlier germination would facilitate the emergence and survival of seedlings in the rst phases of the life cycle in the mountain site (McGraw & Vavrek 1989). However, low seedling densities of Calluna have been observed above 2000 m (pers. observ.). This might be due to the low moisture content of sandy soils developed on quartzites (when there is no snow cover), which affects germination and survival of seedlings. The absence of seedlings could also be the result of the difculty to survive the harsh winter conditions of high mountains (Bruggink 1993). The variations in the percentage and rate of germination among the studied species could be a consequence of differences in the degree of dormancy. The data show that seeds of E. cinerea present a higher degree of dormancy than those of Calluna and E. vagans. The seed size only had a signicant effect on the germination of Erica vagans, showing the large seeds higher germination percentages and rates. In Calluna only large seeds germinated slightly better than small seeds only during the rst month. Heavy seeds germinated earlier and showed better germination, which can be due to bigger storage reserves of these seeds (Gross 1984; Tripathi & Khan 1990; Arista et al. 1992). Effect of seed size on seedling survival and weight The importance of seed size on seedling survival and weight of Calluna coincides with the results obtained before on other species. A better seedling survival and growth from large seeds, linked with bigger amounts of nutritive substances, is found by Harper (1977), Gross (1984), Tripathi & Khan (1990) and Reyes & Casal (1994). Large seeds from the highest altitudes showed the highest seedling survival. Large seeds reserves would improve the success of seedlings in a harsh environment (Holm 1994). However, the little occurrence of seedlings observed above 2000 m suggest that the

106 establishment of seedling is rare at high altitudes with severe winters (Miller & Cummins 1987; Bruggink 1993).
Holm, S. O. 1994. Reproductive patterns of Betula pendula and B. pubescens coll. along a regional altitudinal gradient in northern Sweden. Ecography 17: 6072. Lavorel, S. 1987. Etude de la plasticite phenotypique chez Calluna vulgaris (L.) Hull. Dipl me dEtudes Approfondies en Sciences o de lEvolution et Ecologie. Academie de Montpellier, Universit e des Sciences et Techniques du Languedoc, Montpellier, France. Lusk, C. H. 1995. Seed size, establishment sites and species coexistence in a Chilean rain forest. J. Veg. Sci. 6: 249256. Mallik, A. U., Hobbs, R. J. & Legg, C. J. 1984. Seed dynamics in Calluna-Arctostaphylos heath in North-Eastern Scotland. J. Ecol. 72: 855871. Mallik, A. U. & Gimingham, C. H. 1985. Ecological effects of heather burning. II. Effects on seed germination and vegetative regeneration. J. Ecol. 73: 767776. Miller, G. R. & Cummins, R. P. 1987. Role of buried viable seeds in the recolonization of disturbed ground by heather (Calluna vulgaris (L.) Hull) in the Cairngorm mountains, Scotland, U.K. Artic and Alpine Research. 19(4): 396401. Mcgraw, J. B. & Vavrek, M. C. 1989. The role of buried viable seeds in artic and alpine plant communities. In: Leck, M. A., Parker, V. T. & Simpson, R. L. (eds), Ecology of soil seed banks, Academic Press, San Diego. Obeso, J. R. & Vera, M. L. 1996. Resprouting after experimental re application and seed germination in Erica vagans. Orsis 11: 155163. Pons, T. L. 1989. Dormancy and germination of Calluna vulgaris (L.) Hull and Erica tetralix L. seeds. Acta Oecologica Oecol. Plant 10(1): 3543. Probert, R. J. 1992. The role of temperature in germination Ecophysiology. In: Fenner, M. (ed.), Seeds, The ecology of regeneration in plant communities, C.A.B., Wallingford. Reyes, O. & Casal, M. 1994. Reproductive behaviour of Quercus robur related to the size and damage state of the seed. Proc. 2nd. Int. Conf. Forest Fire Research. Vol. II (21): 10091018. Tripathi, R. S. & Khan, M. L. 1990. Effects of seed weight and microsite characterististics on germination and seedling tness in two species of Quercus in a subtropical wet hill forest. Oikos 57: 289296. Vera, M. L. 1983. Estudio de los pastizales de diente, matorrales, y su dinamismo, de la zona comprendida entre el Pto. de Ventana y el Pto. de Ventaniella (Asturias-Le n). Memoria Tesis Doctoral. o Universidad de Oviedo. Vera, M. L. 1994. Regeneraci n de un aulagar con Ulex europaeus o despu s de un incendio en el Norte de Espa a. Pirineos 143: e n 8798. Vera, M. L. & Obeso, J. R. 1995. Regeneraci n del brezal atl ntico o a de Cabo Pe as despu s de un incendio severo. Stvdia oecologica n e 12: 223236.

Acknowledgements This research was nanced by the University of Oviedo. I thank P. Alv rez-Ura for revising the Enga i lish version.

References
Archibold, O. W. 1989. Seed banks and vegetation processes in Coniferous forest. In: Leck, M. A., Parker, V. T. & Simpson, R. L. (eds), Ecology of soil seed banks, Academic Press, San Diego. Arista, M., Talavera, S. & Herrera, J. 1992. Viabilidad y germinacion de las semillas de Abies pinsapo Boiss. Acta Bot. Malacitana 17: 223228. Baker, G. H. 1989. Some aspects of the natural history of seed banks. In: Leck, M. A., Parker, V. T. & Simpson, R. L. (eds), Ecology of soil seed banks, Academic Press, San Diego. Baskin, J. M. & Baskin, C. C. 1989. Physiology of dormancy and germination in relation to seed bank ecology. In: Leck, M. A., Parker, V. T. & Simpson, R. L. (eds), Ecology of soil seed banks, Academic Press, San Diego. Bruggink, M. 1993. Seed bank, germination, and establishment of ericaceous and gramineous species in heathlands. In: Aerts, R. & Heil, G. W. (eds), Heathland: Patterns and Processes in a changing environment, Kluwer Academic Publishers, Dordrecht, Holland. Clement, B. & Touffet, J. 1990. Plant strategies and secondary succesion on Brittany heathlands after severe re. J. Veg. Sci. 1: 195202. Gimingham, C. H. 1960. Biological Flora of the British Isles. Calluna vulgaris (L.) Hull. J. Ecol. 48: 455483. Gonz` lez-Rabanal, F. & Casal, M. 1995. Effect of high temperatures a and ash on germination of ten species from gorse shrubland. Vegetatio 116: 123131. Gross, K. L. 1984. Effects of seed size and growth form on seedling establishment of six monocarpic perennial plants. J. Ecol. 72: 369387. Harper, J. L. 1977. Population Biology of Plants. Academic Press, London. Hobbs, R. J., Mallik, A. U. & Gimingham, C. H. 1984. Studies on re in Scottish heathland communities. III. Vital attributes of the species. J. Ecol. 72: 963976.

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