Endozoochorous seed dispersal by martens (Martes foina, M. martes) in two woodland habitats

Flora (2002) 197, 370–378 http://www.urbanfischer.de/journals/flora

Endozoochorous seed dispersal by martens (Martes foina, M. martes) in two woodland habitats Friederike Schaumann & Thilo Heinken* Institute of Biology, Systematic Botany and Plant Geography, Free University Berlin, Altensteinstr. 6, D-14195 Berlin, Germany * e-mail corresponding author: [email protected] Received: Mar 28, 2002 · Accepted: Jun 20, 2002

Summary Endozoochorous seed dispersal by stone and/or pine martens (Martes foina, M. martes) was investigated throughout the main fruiting period (July through October) in two contrasting forest areas (acid soil and mesic) in Brandenburg, Germany. The amount of seeds dispersed by martens was determined by counting the seeds per scat, and seed dispersal was related to plant abundance in the study areas. In addition, the germinability of dispersed seeds was tested. For the three most commonly dispersed seeds percent germination of ingested and uningested seeds was compared. In the acid-soil forest, ten species and more than 4,000 seeds per 10 g of dry mass faeces were recovered, whereas the faeces from the mesic forest yielded only seven species and less than 500 seeds per 10 g. Almost all endozoochorous seeds were from fleshy-fruited species growing in the forest stands; very few seeds were transported from adjacent settlements into the woodlands. Seeds of Vaccinium myrtillus predominated in faeces from the acid-soil forest where it was one of the most abundant herb layer species, followed by Rubus idaeus. In the mesic forest, Rubus caesius/fruticosus agg. and Vaccinium myrtillus seeds were most abundant in marten scats, while Liliaceae species with toxic berries lacked endozoochorous transport by martens despite being abundant in the study area. Ten of the 12 dispersed species germinated from scat samples. In contrast to seeds of Rubus idaeus and Rubus caesius/fruticosus agg., those of Vaccinium myrtillus showed a germination enhancement after having passed through the digestive tracts of martens, possibly due to abrasion of their soft seed coat. Both martens are considered to be important dispersal vectors for fleshy-fruited plants inhabiting the understorey of Central European forests. Key words: dispersal, frugivory, germination, martens, NE Germany, temperate woodland

Introduction In temperate forests and shrublands, high percentages of plant species are adapted for endozoochorous seed dispersal by vertebrates (Jordano 2000). Numerous studies have evaluated endozoochorous dispersal of fleshy-fruited plants, but most studies dealt with birds as dispersal agents (e.g. Clergeau 1992; Jordano & Schupp 2000). With the exception of migrating individuals, birds are mainly short-range dispersers (Kollmann 1994 ; Godoy & Jordano 2001), since they have a short retention time of less than 1.5 hours, often regurgitate seeds and move relatively short distances during digestion (Jordano 2000). In contrast, omnivorous mammals of the order Carnivora (subsequently termed carnivorous mammals) have seldom been studied as seed dispersers, although it is well-known that they also consume large quantities of fleshy fruits (e.g. Willson 1993; Clevenger 1994). 370

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Data on seed dispersal by carnivores from Central and western Europe are lacking, except for the red fox (Vulpes vulpes) (Müller 1938; Turek 1967; Kollmann 1994). However, some studies on seed dispersal by carnivorous mammals were carried out in southern Europe (Debussche & Isenmann 1989; Herrera 1989; Pigozzi 1992), Chile (Bustamante et al. 1992) and Alaska (Hickey et al. 1999). These, and earlier investigations (see Ridley 1930) showed that carnivorous mammals are efficient and legitimate seed dispersers. In addition, to date in Central Europe only the effect of digestion by birds on seed germination has been investigated systematically (Traveset 1998). We studied the dispersal of seeds by Martes foina and/or M. martes in an acid-soil, mixed forest and in a mesic, deciduous forest in Germany. Data were collected over four months during the main period of fleshy fruit dissemination. Additionally, we test the legitimacy, i.e. occurrence of apparently undamaged seeds 0367-2530/02/197/05-370 $ 15.00/0

in the faeces (cf. Herrera 1989) of Martes foina and/or M. martes as seed dispersers, and the effect of ingestion on seed germination by comparing the germination proportion in defecated versus control seeds. We have concentrated on the following aspects: 1) How many seeds and species are transported? 2) Do martens contribute to dispersal of forest plants? 3) Are there any differences in seed dispersal between the investigated forests? 4) What effect does the passage through the gut of martens have on germination?

Materials and methods Study areas The study was carried out in the “Krämer forest” (13°04 E, 52°40 N) and the “Brieselang forest” (13°05 E, 52°35 N) in the state of Brandenburg, northeastern Germany. Mean annual precipitation is about 500 mm; mean temperature in July is 17.9°C, and mean temperature in January –0.8°C (Deutscher Wetterdienst 1997/98). The woodland areas are approximately 5 km apart. They are surrounded by agricultural land, and settlements with gardens are close by. The Krämer forest (3,200 ha) is characterized by sandy and acidic soils on inland dunes; scots pine (Pinus sylvestris) forests and mixed oak (Quercus petraea, Q. robur) forests predominate. In this forest, acidity indicators (e.g. Agrostis capillaris, Carex pilulifera, Deschampsia flexuosa, Vaccinium myrtillus) dominate the herb layer. The Brieselang forest (650 ha) is mainly characterized by more or less moist, meso- to eutrophic soils with species-rich mixed oak-hornbeam forests where Carpinus betulus, Fraxinus excelsior, Quercus robur and Tilia cordata prevail. The herb layer is dominated by species which require a moderate to good nutrient supply (e.g. Anemone nemorosa, Lamium galeobdolon, Milium effusum, Paris quadrifolia, Ranunculus ficaria, Stellaria holostea). Only a small portion of woodland is found on acidic soils, and here mixed oak forests dominate. For abundance of fleshy-fruited plants in both forest areas see Table 3. While investigations were carried out in the complete Brieselang forest, we selected a representative section of 800 ha in the southern part of the Krämer forest for our investigations. Probably both, stone marten (Martes foina Erxleben) and pine marten (Martes martes L.), occur in the Krämer forest as well as in the Brieselang forest (Dolch 1995). The stone marten, the second-most abundant carnivorous mammal in the region following the red fox (Vulpes vulpes L.) (Dolch 1995), inhabits nearly exclusively settlements, but the foraging territories also include large forest areas. The rarer pine marten inhabits exclusively woodland areas.

Collection of faeces and scat analysis We collected marten scats once a week from July through October 1999 in both woodland areas. At the beginning the whole study areas were searched for marten scats. Localities

where scats were found revealed preferred movement routes of martens. These were checked from August onwards. Since it is impossible to distinguish scats of the two marten species in the field (Goszczyski 1976), the scats were combined into a single sample for analysis. All samples from one month were pooled. Scats were dried at 20–25°C for one week, weighed and then stored in a refrigerator (day: 6°C, night: 0°C) for further analysis. The dry mass (DM) of all scats was calculated from the mean of 12 randomly selected scats which were dried for 24 h at 105°C. These scats were not used for further analysis. The amount of seeds dispersed by martens was determined by counting the seeds per scat. The Mann-Whitney U-test was used to compare the seed content per scat mass of marten faeces in the two different study areas. We compared the proportion of scats containing seeds between the study areas using the χ2-test (Sachs 1992).

Vegetation survey To assess the role of dispersal by martens in the studied forests, we recorded the phanerogam vegetation by 43 sample plots (20 m × 20 m) in the Krämer forest, and 76 sample plots in the Brieselang forest, respectively. Plots were evenly distributed within the forest stands (one in each of the 43 investigated forest compartments of the Krämer forest, and two in each of the 38 forest compartments of the Brieselang forest, which has more heterogenous site conditions and vegetation). In each plot the cover of all phanerogam species was estimated. Additionally, presence of fruits was checked in each sample plot during the dissemination period. Nomenclature of plant species follows Wisskirchen & Haeupler (1998). For both forest areas, the mean cover within all sample plots of all species with fleshy fruits was determined.

Germination assays To assess the efficiency of endozoochorous dispersal by martens, we investigated percentage of germination of all seed species detected in the faeces. Seeds were removed from the faeces and washed in a sieve under running water. The experimental design varied with the availability of ingested seeds and the different stratification requirements of the species. Max. 50 seeds of Betula pendula, Malus sylvestris, Ribes uvacrispa, Vaccinium myrtillus and Vitis vinifera were set in Petri dishes (9 cm diameter), on filter paper with 5 ml distilled water, under an illumination of two 15 W fluorescent tubes from 7:00 a.m. – 7:00 p.m. and with a temperature regime of 20°C (day) and 14°C (night). Since the seeds of Ribes uvacrispa and Vitis vinifera require a cold treatment of 130 and 60 days, respectively (Grime et al. 1988; Baskin & Baskin 1998), they were first stratified in a refrigerator (day: 6°C, night: 0°C). No fungicide was used to protect seeds against mould. Three times a week, dishes were examined: germinated seeds were counted and removed to reduce their possible effect on ungerminated seeds. Germination was defined as the emergence of the radicle from the seed. FLORA (2002) 197

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Table 1. Dry mass, number (n) of marten scats and number of seed-containing scats collected in both study areas per month. Kr: Krämer forest; Br: Brieselang forest. July

Dry mass of scats [g] Mean dry mass per scat [g] ± SD n scats n scats with seeds

August

September

October

Total

Kr

Br

Kr

Br

Kr

Br

Kr

Br

Kr

Br

47.9 1.65 ±1.23 29 23

36.5 1.22 ±0.89 30 6

30.9 2.21 ±1.16 14 9

20.2 1.84 ±1.06 11 7

30.2 2.15 ±1.21 14 10

24.6 1.89 ±1.13 13 6

27.9 1.86 ±1.66 15 2

18.5 1.43 ±0.54 13 2

136.9 1.90 ±1.31 72 44

99.8 1.49 ±0.94 67 21

Seeds of Carpinus betulus, Prunus spp., Rubus spp., Sorbus aucuparia and Taxus baccata require one long or two shorter periods of cold stratification (Schopmeyer 1974; Grime et al. 1988; Baskin & Baskin 1998). Max. 500 seeds of these species were set in soil-filled plastic pots (12 cm diameter), covered with 0.5 cm of soil and over-wintered outside for two years from November until May. Pots were covered with a 1-cm mesh lid during outdoor stratification to prevent seed predation by rodents. Over the vegetational period germinability was tested in a greenhouse (day: 20°C, night: 16°C). Germination was identified by the emergence of cotyledons. All seedlings were removed twice a week. In most cases, all seeds from one scat were put in one Petri dish or pot. The range of seed numbers per pot is listed in Table 4. Only scats containing more than the above mentioned number of seeds were split into equal portions. Three and four replicates, respectively, with 50 seeds each were used for Vaccinium myrtillus seeds. Additionally, we compared percentage of germination of the most commonly dispersed seeds (Vaccinium myrtillus, Rubus caesius/fruticosus agg. and R. idaeus) with those of non-ingested seeds. Seeds were collected from at least ten different individuals in the same month in the forest areas where the scats were found. After the pulp was manually removed from the seeds on the day of collection, they were stored similarly to, and put in germination conditions the same day as, the defecated seeds. Defecated and non-ingested seeds of Vaccinium myrtillus were used for the germination tests within two weeks after sampling. Before the germination tests the seeds were rinsed in a sieve under running water for 10 min. For two years defecated and collected seeds of the Rubus spp. were separately cold stratified in the above mentioned soil-filled

pots under field conditions. The mean cumulative germination percentages were calculated and the significance of any difference between the treatments and the control in each series, and for each tested plant species, was determined by the Mann-Whitney U-test. Seed coats of ten ingested and uningested seeds of Rubus idaeus and Vaccinium myrtillus were randomly chosen for scanning electron microscope (SEM) examination. These were gold-coated in vacuum, photographed, and the seed-coat sculptures compared.

Results Endozoochorous seeds in marten faeces In both forest areas, faeces with seeds occurred in all months studied. The number and mass of collected faeces per month and the proportion of faeces containing seeds are summarized in Table 1. The proportion of faeces containing seeds varied between 13% and 79% and was high from July through September, but low in October. Overall, faeces from the Krämer forest contained significantly more seeds than faeces from the Krämer forest (χ2-test: χ2 = 7.11; df = 1; p < 0.01). In the Krämer forest, faeces contained 4,087 seeds per 10 g DM, whereas faeces collected in the Brieselang forest yielded only 478 seeds per 10 g DM (Table 2). Hence, compared to the Brieselang forest, scats from the Krämer forest contained significantly more seeds with respect to scat mass (Mann-Whitney U-test: n1 = 72,

Table 2. Seed content of the three dominant species in the marten scats for each month and both study areas. All values are given as number of seeds per 10 g of dry mass. Kr: Krämer forest; Br: Brieselang forest. July

August

October

Total

Kr

Br

Kr

Br

Kr

Kr

Br

Kr

Vaccinium myrtillus Rubus caesius/fruticosus agg. Rubus idaeus Other species

9,017.8 – 9,744.3 9, 28.8

528.8 233.2 7.9 13.2

2,791.6 – 2, 14.2 881.2 – – 2, 6.1 0.5

– – – 117.6

– 26.0 – 19.9

– – – 1.4

– – – 9.7

3,785.3 193.4 2, 3.2 270.0 2,260.4 2.9 2, 37.7 11.6

All species

9,790.9

783.1

2,811.9 881.7

117.6

45.9

1.4

9.7

4,086.6 477.9

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Br

September

Br

Table 3. Proportion of seed species in marten faeces collected in the Krämer forest (n = 4,087 seeds) and in the Brieselang forest (n = 487), and abundance of all species with fleshy fruits in the forest areas. MC, mean cover related to all sample plots; Prop., mean cover proportion of fleshy-fruited species. For tree and shrub species which do not set fruit in the herb layer only occurrences in the tree and/or shrub layer are listed. 1) after Müller-Schneider (1986) and own observations. w: presentation of fruits for the whole winter period (“Wintersteher”). 2) after Frohne & Pfänder (1997). * with toxic seeds. 3) cultivated in gardens within settlements. 4) species without fleshy fruits. Species

Fruiting period 1)

Toxicity of fruit pulps2)

Krämer forest

Brieselang forest

Prop. in faeces

Prop. in faeces

Abundance in vegetation

[%]

MC [%]

Prop. [%]

[%]

Abundance in vegetation MC [%]

Prop. [%]

Species present in the study areas Vaccinium myrtillus Rubus caesius/fruticosus agg. Rubus idaeus3) Betula pendula Sorbus aucuparia Prunus serotina Carpinus betulus

VII–IX VII–IX VII–IX VIII–Xw VIII–Xw VII–IX IX–Xw

non-toxic non-toxic non-toxic – 4) toxic non-toxic* – 4)

92.6 0.1 6.4 0.1 0.5 0.1 <0.1

16.6 0.4 0.7 2.9 1.7 1.3 3.5

70.0 1.7 3.0 () 7.2 5.5 ()

40.5 56.5 0.6 <0.1 – – –

1.8 0.8 0.2 2.4 0.4 – 19.7

14.3 6.3 1.6 () 3.2 – ()

VII–VIII VIII–X VIII–X – VIII–XII

non-toxic non-toxic non-toxic* non-toxic non-toxic*

0.2 <0.1 <0.1 – –

– – – – –

– – – – –

1.0 – – 1.4 <0.1

– – – – –

– – – – –

– – – – – – – – – – – – –

1.2 0.1 0.1 1.1 0.2 0.2 0.1 – – – – – –

5.1 0.4 0.4 4.6 0.8 0.8 0.4 – – – – – –

– – – – – – – – – – – – –

2.4 3.7 1.0 0.5 0.2 – – 1.0 0.2 0.2 0.2 <0.1 <0.1

19.0 29.4 7.9 4.0 1.6 – – 7.9 1.6 1.6 1.6 <0.1 <0.1

99.9

23.7

<100

12.6

100

Species not present in the study areas Ribes uva-crispa3) Malus domestica3) Prunus domestica s.l.3) Vitis vinifera Taxus baccata3)

Species with fleshy fruits lacking endozoochorous transport Maianthemum bifolium Convallaria majalis Polygonatum multiflorum Frangula alnus Crataegus monogyna/laevigata Rubus saxatilis Vaccinium vitis-idaea Paris quadrifolia Malus sylvestris Euonymus europaeus Rhamnus cathartica Fragaria vesca Cornus sanguinea

IX–XII VIII–XI IX–XII VIII–IX IX–Xw VII–IX IX–X VII–IX VIII–X X–XI VIII–IXw VI–IX IXw

toxic toxic toxic toxic non-toxic non-toxic non-toxic toxic non-toxic toxic toxic non-toxic non-toxic

Σ species with fleshy fruits

n2 = 67, Z = – 3.5, p < 0.001). In both study areas, the total seed content reached a maximum in July and August, the fruiting period of the dominating species (cf. Table 3), and declined towards September and October. Whereas in the Krämer forest seeds of Vaccinium myrtillus were quantitatively of major importance, followed by Rubus idaeus; seeds of Rubus caesius/fruticosus agg. and Vaccinium myrtillus predominated in the Brieselang forest (Table 2, 3). Overall, seeds from twelve plant species were recovered from the marten faeces, ten in the Krämer forest

100

and seven in the Brieselang forest (Table 3). Nearly all seeds dispersed were from fleshy-fruited plants producing berries, drupes or functionally analogous fruits; rarely nuts of Carpinus betulus and Betula pendula were also ingested. Most seeds recovered were from wild plants growing in the study areas (Krämer forest: 70% of species, >99% of seed number; Brieselang forest: 57%, 98%, respectively). The prevailing species were abundant or even dominating in the respective forest vegetation (Table 3). Exceptions were Prunus domestica s.l., Ribes uva-crispa, Taxus baccata and Malus FLORA (2002) 197

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domestica which were cultivated in gardens near the forest areas, and Vitis vinifera which is only found in organic waste. Altogether, in the Krämer area five of the twelve fleshy-fruited species (42%) of the forest vegetation were dispersed by martens, while in the Brieselang area only three of fifteen fleshy-fruited species (20%) occurring in the forest vegetation were dispersed endozoochorously. Moreover, the dispersed species constituted 87% of the vegetation cover by species with fruit pulp in the Krämer forest, but only 25% in the Brieselang forest (Table 3). These differences result essentially from the absence of Liliaceae fruits in the faeces, i.e. Convallaria majalis, Maianthemum bifolium, Paris quadrifolia and Polygonatum multiflorum which are toxic to humans and probably other mammals (Frohne & Pfänder 1997). Liliaceae were abundant especially in the Brieselang forest (mean cover proportion : Brieselang 64%, Krämer 6%) and fruited during the study period. Altogether, only one of the six abundant toxic fruit species (Sorbus aucupa-

ria), but all four abundant non-toxic species (Rubus spp., Prunus serotina, Vaccinium myrtillus) were detected in the faeces.

Germinability of dispersed seeds Except for Carpinus betulus and Taxus baccata, all other endozoochorously dispersed seed species germinated after defecation (Table 4). Percent germination varied between 1.4% (Prunus serotina) and 81% (Vaccinium myrtillus). The ingested seeds of Carpinus betulus and Taxus baccata were intact, but since only three seeds were recovered, generalizations about their germination capacity are not possible (see also Malus domestica). Comparing the germination success of ingested seeds of Vaccinium myrtillus with an untreated control results in an enhanced germination of ingested seeds, the difference was highly significant (Mann-Whitney U-test: n1 = 14, n2 = 17, Z = –4.5, p < 0.001, Table 5). By con-

Table 4. Germination percentage of endozoochorously dispersed seeds. For each species the number of tested seeds, the number of faeces from which the seeds were taken, the minimum and maximum number of seeds per faeces and the proportion of germinated seeds (percent germination) are given. ( ) = not calculated; * one seed germinated, ** three replicates with 50 seeds each (twice four replicates). species

n tested seeds

Betula pendula Carpinus betulus Malus domestica Prunus domestica s.l. Prunus serotina Ribes uva-crispa Rubus caesius/fruticosus agg. Rubus idaeus Sorbus aucuparia Taxus baccata Vaccinium myrtillus Vitis vinifera

2,27 2,2 2,2 2,14 2,69 2,135 2,409 3,304 2,241 2,1 2,700** 2,66

n tested faeces 7 2 7 6 2 14 4 2 1 3 3

seeds per faeces (range)

percent germination [%]

1–19 2 1 1–3 2–24 48–87 2–545 17–2,032 101–194 1 16–7,225 4–45

14.8 () ( )* 50.0 1.4 25.9 6.5 23.9 13.7 () 80.7 42.4

Table 5. Effect of seed passage through the gut of martens on germination percentage of Rubus spp. and Vaccinium myrtillus taken from marten scats from both study areas (see Table 4) (x ± SD; Mann-Whitney U-test; ***, p < 0.001; ns, p > 0.05). ingested seeds n tested seeds Rubus caesius/fruticosus agg. 2,409 Rubus idaeus 3,304 Vaccinium myrtillus 3,700 374

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non-ingested seeds

significance

n replicates

percent germination

n tested seeds

n replicates

percent germination [%]

16 6 14

6.5 ± 8.9 23.9 ± 14.8 80.7 ± 11.1

200 400 850

4 5 17

1.0 ± 2.0 17.8 ± 16.9 36.2 ± 19.4

ns ns ***

Fig. 1. SEM micrographs of testa surfaces of a non-ingested Vaccinium myrtillus seed with intact cell walls (above), and a seed taken from a marten scat from the Krämer forest with damaged cell walls (below).

trast, ingestion of the seeds of Rubus idaeus and Rubus caesius/fruticosus agg. had no significant influence on germination capacity (Mann-Whitney U-test: n1 = 6, n2 = 5, U = 10, p > 0.05 ; n1 = 16, n2 = 4, U = 14, p > 0.05 ; Table 5). While the testa of uningested seeds of Vaccinium myrtillus were intact and the cell walls were evident, the coat of a seed that has passed through a marten gut displayed various damage to its cell walls (Fig. 1). For the drupes of Rubus idaeus no such difference could be detected.

Discussion Seed dispersal by martens Martens ate fruits during the whole study period from July to October. Previous investigations in different parts of Europe also indicate that fruits are a major com-

ponent of the diet of martens (e.g. Clevenger 1993, 1994; Helldin 1999). For Martes foina, fruits account for 30–54% of total yearly food biomass (Tester 1986; Marchesi et al. 1989), and for Martes martes also high levels of fruit consumption have been reported (Lockie 1961; Marchesi & Mermod 1989; Jedrzejewski et al. 1993). Fruits contribute a major part of biomass to the martens’ diet in summer and fall (e.g. Clevenger 1993; Jedrzejewski et al. 1993; Gurnell et al. 1994; Nitze 1998) reflecting the seasonal patterns of fruit availability (Jordano 2000). However, frugivory occurs consistently throughout the year (e.g. Tester 1986; Marchesi & Mermod 1989; Marchesi et al. 1989). In the forest areas studied, seed contents in the faeces were maximal in July and August because the preferred plant species set fruit mainly in this period. The higher seed contents in the faeces from the Krämer forest in comparison to those from the Brieselang forest may be caused by the higher abundance of edible fruits – especially Vaccinium myrtillus – in the more acidic soil Krämer forest (cf. Table 3). The comparison of plant coverage and proportion of seeds in scats does not allow an exact assertion regarding fruit preference of martens, as they are not based upon the seed frequency in the study areas. Seed frequency is not only dependent on the abundance of the respective plant species, but also on the fruit setting and the relation of seed number to fruit mass. Moreover, some species with late-ripening or persistent fruits (Table 3) may be underrepresented because martens diet in winter was not studied. Nevertheless, the comparison elucidates that the presence of seeds in the faeces corresponds, to some extent, with the forest vegetation. The dominant endozoochorous plant species (Vaccinium myrtillus, Rubus spp.) are both abundant in the study areas, and contain ca. 25–35 seeds per fruit (Ehrlén & Eriksson 1993). In contrast, Sorbus aucuparia and Prunus serotina yield only three and one seed per fruit, respectively. With the exception of Paris quadrifolia, the abundant Liliaceae species of the study areas also contain low numbers (3–4 on average) of seeds per berry (Ehrlén & Eriksson 1993), and fruit setting of the clonal species is relatively low. However, their complete absence in the faeces suggests an extensive exclusion of Liliaceae species from marten’s dispersal. Besides diaspores with fruit pulp, martens dispersed some diaspores of Betula pendula and Carpinus betulus (cf. Jedrzejewski et al. 1993); perhaps these were ingested unintentionally together with other food items. The results correspond to previous investigations in Central Europe and North America: while, in particular Vaccinium myrtillus and Rubus spp. are dispersed by several mammal species in Central Europe – e.g. red fox (Vulpes vulpes L.), badger (Meles meles L.), red squirrel (Sciurus vulgaris L.) and dormice (Eliomys quercinus FLORA (2002) 197

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L., Glis glis L.); mammalian dispersers are largely unknown for the Liliaceae species of the study areas (cf. Müller-Schneider 1986). Their content of toxic substances, i.e. saponins and glycosids (Frohne & Pfänder 1997) may reduce attraction to mammalian dispersers (cf. Ehrlén & Eriksson 1993). Also, in North America the respective Liliaceae genera (Convallaria, Maianthemum, Polygonatum) are not consumed, while Vaccinium species and various Rosaceae genera are noteworthy for their high frequency of appearance in records of mammalian diets (Willson 1993).

Effect of seed passage through martens’ gut on germination Martens are legitimate dispersers of the fruit seeds eaten in the study region, as they disperse viable seeds. The results show that it is beneficial, at least for Vaccinium myrtillus seeds, to be ingested by martens, as the percentage of germination was higher. At least for Rubus spp. seeds, ingestion by martens had no negative effect on their viability. However, percent germination of Rubus caesius/fruticosus agg. both of ingested and non-ingested seeds was low compared to results of Clergeau (1992). Possibly the stratification treatment was not sufficient in our experiment. In the case of Vaccinium myrtillus, more successful germination after ingestion is probably due to a reduction of the seed coat by abrasion and chemical decomposition, thus increasing its permeability to water and possibly oxygen (cf. Krefting & Roe 1949; Izhaki & Safriel 1990 ; Barnea et al. 1992; Clergeau 1992). As suggested by Barnea et al. (1992), a relationship between germination success and the reduction of the seed coat may exist. According to the results of Clergeau (1992), species with a soft seed coat show an abrasion of the seed coat and consequently the highest differences in germination between ingested and control seeds. This can explain the observed differences in germination results between species: whereas Vaccinium myrtillus seeds showed a clearly visible abrasion and the highest range of germination success, there was no visible abrasion on the drupes of Rubus spp. A variation in seed germination after ingestion is related to the animal species that consumes the seed (Traveset 1998). Therefore, related plant species in temperate rain forests of Alaska showed a different germination response after ingestion by bears (Traveset & Willson 1997). Here, frugivory by bear (Ursus spp.) enhanced germination of Rubus spectabilis Pursh seeds, but did not affect germination of Vaccinium ovalifolium Sm. and V. alaskensis How. seeds. As the pas376

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sage through a bears gut lasts longer (up to one day, Traveset & Willson 1997), probably the effect on seeds especially with a hard seed coat (Rubus spectabilis) is greater.

Effectiveness of seed dispersal Seed disperser effectiveness does not only rely on the quantity of dispersed viable seeds, but also on the quality of deposition, i.e. dispersal distance and microsite selection (Schupp 1993). Martens are effective dispersers of fleshy-fruited plants, since they transport seeds over long distances and to suitable woodland habitats. A study by Hickey et al. (1999) showed that in southeast Alaska American martens (Martes americana Turton) dispersed seeds of Vaccinium alaskensis and V. ovalifolium reporting some of the longest distances found for vertebrates. For these seeds a median distance of 519 m was calculated; Rubus spectabilis seeds were estimated to be transported similar distances (Hickey et al. 1999). Likewise, Martes foina and M. martes probably disperse seeds over long distances (>>100 m) due to relatively long retention times (Martes americana: 4–5 hrs, Hickey et al. 1999) and large home ranges in northern and Central Europe (adults: approx. 0.5–12 km2 (lowland), 1.3–24 km2 (mountains); Skirnisson 1986; Schröpfer et al. 1989; Herrmann 1994). In our study, marten scats were commonly found on rotten logs, suggesting that martens take the seeds to non-random sites that are well-suited for establishment and growth especially for Vaccinium myrtillus. Investigations by Eriksson & Fröborg (1996) indicate that for Vaccinium myrtillus seeds, decaying wood is a favorable substrate for germination. A similar recruitment behavior can be assumed for other species, as in temperate and boreal forests recruitment on logs and stumps is common (e.g. Hytteborn et al. 1987). As stone marten territories include both forest and settlement habitats, several seeds of cultivated plant species were transported into the forest stands. Most of them (Malus domestica, Prunus domestica, Vitis vinifera) will not emerge, but several small plants of Ribes uva-crispa and Taxus baccata occurring in the investigated forest stands may originate from endozoic transportation by martens from settlements (cf. Seidling 1999). In our study areas, dispersal of woodland plant species by martens may occur above all within the large and rather homogenous woodland areas and thus to habitats of existing plant populations. However, in landscape sections with more marked vegetation dynamics and a more fragmented woodland distribution, dispersal by martens may contribute to colonization of isolated, new-

ly created forest patches by woodland species. Dispersal potential of woodland plant species affect actual distribution patterns in Central Europe: species with a high dispersal capacity are generally more successful in colonizing secondary woodlands on former arable land than are species with a low dispersal capacity which are therefore largely restricted to ancient woodlands (e.g. Hermy et al. 1999; cf. also Petersen & Philipp 2001). These distribution patterns correspond with the results of the current study: while in most regions of Central and Western Europe all wild fleshy-fruited plant species dispersed by martens are able to colonize secondary woodlands quickly, the Liliaceae species are reported to be ancient woodland indicators (e.g. Hermy et al. 1999). Also birds which may contribute to long-distance dispersal play a negligible role in dispersing the seeds of most toxic herbaceous species (Müller-Schneider 1986 ; Ehrlén & Eriksson 1993). Rodents consume seeds of Convallaria majalis and Paris quadrifolia but eat only a small proportion of the pulp (Ehrlén & Eriksson 1993). However, they only facilitate shortdistance dispersal. This emphasizes the importance of martens and presumably other carnivores like red fox and badger to facilitate long-distance dispersal also between isolated woodland habitats in Central Europe, which is essential both in the long-term viability of plant populations by maintaining migration between isolated habitats, and in the colonization of new potential habitats (cf. Poschlod et al. 1996).

Acknowledgements We wish to thank two anonymous referees, Rainer Altenkamp and Roger Mundry for valuable comments on the manuscript, and Christine Grüber für technical assistance.

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