Effects of herbivory on arctic and alpine vegetation Åsa Lindgren

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1 Effects of herbivory on arctic and alpine vegetation Åsa Lindgren Stockholm University

2 Åsa Lindgren, Stockholm 2007 Cover illustration: a curious reindeer in Svalbard Photo: Åsa Lindgren ISSN pp Printed in Sweden by Universitetsservice, US-AB, Stockholm 2007 Distributor: Department of Botany, Stockholm University 2

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5 Doctoral dissertation Åsa Lindgren Department of Botany Stockholm University SE Stockholm Sweden Effects of herbivory on arctic and alpine vegetation Abstract - The distribution of plant species and functional traits in alpine and arctic environments are determined by abiotic conditions, but also by biotic interactions. In this thesis, I investigate interactions among plants and herbivory effects on plant community composition and plant functional traits in three different regions: Swedish Lapland, Beringia (USA/Russia) and Finnmark (Norway). Reindeer grazing was found to be extensive in southern Lapland and had limited effects on plant community composition and seedling germination. However, reindeer presence was found to influence plant functional traits, particularly in the subalpine birch forest. Tall herbs were lower and had lower SLA when reindeer were present, while small herbs showed an opposite pattern. The contrasting effects on the two herb groups are probably explained by a competitive release for small herbs when the tall herbs are suppressed by reindeer. Rodents had the largest relative impact on plant community composition in southern Lapland and this is consistent with the study from Finnmark, where rodents heavily affected dwarf shrubs on predator-free islands. With no predators present, vole densities increased profoundly and almost depleted some dwarf shrub species. These results support the idea that small mammals in arctic and alpine tundra are controlled by predators (i.e. topdown). However, a decrease in the nutritional quality in a sedge after defoliation gives support for the idea that small mammals are regulated by plant quality (i.e. bottom-up). In Beringia, small and large herbivores differed in the relation to plant community composition, since large herbivores were related to species richness and small herbivores were related to plant abundance. Plant functional traits were related only to large herbivores and standing crop of vascular plants. Keywords herbivory, reindeer, rodents, functional traits, plant species composition, arctic, alpine, tundra, seed limitation, Carex bigelowii 5

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7 List of papers The thesis is based on five papers, which are referred to in the text by their Roman numerals: I II Lindgren, Å., O. Eriksson and J. Moen. The impact of disturbance and seed availability on germination in alpine vegetation in the Scandinavian mountains. Arctic, Antarctic and Alpine Vegetation. In press. Lindgren, Å., J. Moen and O. Eriksson. The effect of different herbivore groups on the vegetation in subalpine birch forests and alpine heaths. Manuscript. III Lindgren, Å., J. Ehrlen, R. Bergström, K. Danell, G. Ericsson and C. Skarpe. Herbivory and plant biodiversity in an arctic environment. Manuscript. IV V Lindgren, Å., J. Klint and J. Moen. Defense mechanisms against grazing: a study of trypsin inhibitor responses to simulated grazing by the sedge Carex bigelowii. Accepted in Oikos. Hambäck, P.A., L. Oksanen, P. Ekerholm, Å. Lindgren, T. Oksanen and M. Schneider Predators indirectly protect tundra plants by reducing herbivore abundance. Oikos 106: My contributions to the papers were: Planning, field work, data analysis and writing in papers I-IV. For paper V, I was involved in the data analysis, the writing of the paper and the fieldwork. Previously printed and accepted papers are printed in this thesis with the kind permission from the copyright holder. 7

8 Contents Introduction...9 Biotic interactions within a framework of alpine and arctic abiotic conditions...9 Aim of the thesis...12 Methods...13 Results and discussion...18 Concluding remarks...22 Acknowledgement...23 References...23 Svensk sammanfattning...32 Tack!...36 Fieldwork recommendations

9 Introduction Biotic interactions within a framework of alpine and arctic abiotic conditions Common characteristics for arctic and alpine habitats in northern regions are low temperatures, short growing seasons, and a relatively low productivity (Grime 1977). Although the abiotic conditions are very crucial, they are not necessarily overwhelming the importance of biotic interactions. Biotic interactions include plant plant interactions, such as competition and facilitation, and interactions between herbivores and plants. The biotic interactions could either work directly or through abiotic factors (Mulder 1999), altering the physical conditions of the environment (Hyvärinen et al. 2002). Interactions among plants have been suggested to be dominated by facilitation rather than competition in harsh environments (Callaway et al. 2002) because of the amelioration of extreme conditions (Rixen and Mulder 2005). For example, Körner (1999) showed that cushion plants could have a micro-climate profoundly differing from outside temperature, wind velocity and relative humidity. However, Olofsson et al. (1999) suggested that positive and negative interactions could work simultaneously even in harsh environments, and that experimental studies are needed to assess the net effect of interactions. Herbivory is generally negative for a grazed plant, but could be positive for plant species richness and plant community processes. Herbivory might affect plant interactions, e.g. prevent competitive exclusion or influence abiotic factors, e.g. increased soil temperatures due to the reduction of the isolating moss layer (Brooker and van der Wal 2003; Olofsson et al. 2004a; van der Wal and Brooker 2004) and changed nutrient cycling (Olofsson and Oksanen 2002; Stark et al. 2002). The net effect of herbivory on plant species richness and traits 9

10 depends on a combination of factors, e.g. the composition of the vegetation and the growth forms of plants (Chapin 1980; van der Wal et al. 2001) and the productivity (Moen and Oksanen 1998; Proulx and Mazumder 1998; Bardgett and Wardle 2003). Other factors of importance are the grazing history of the area and the types of herbivores involved (Virtanen et al. 1997; 2002; Hartley and Jones 2003; McIntire and Hik 2002; 2005; Olofsson et al. 2004b) and the grazing intensity (Olofsson et al. 2001). For instance, reindeer have been found to cause vegetation shifts between different vegetation states in some studies (e.g. from mosses to graminoids) (van der Wal and Brooker 2004; van der Wal 2006; Eskelinen and Oksanen 2006). High grazing intensities is required to change the vegetation from one state to another and this change is not always reversible. Thus, abandoned summer grazing areas do not always return to an un-grazed vegetation state, at least not during a short time-scale (Olofsson 2006). Herbivores moving over large distances can play an important role as seed dispersers and thus, enhance the colonization of vascular plants, but there is also indications of that arctic seed banks can be depleted through intense grazing (Kuijper et al. 2006). Trampling and digging by herbivores at intermediate intensities might also enhance colonisation and establishment of vascular plants by creating suitable microsites in closed vegetation, by trampling and digging (Cairns and Moen 2004). Thus, herbivore activity can lead to increased vascular plant species diversity in arctic and alpine areas, since many vascular plants are limited by both seed and microsite availability (Eriksson and Ehrlén 1992; Jakobsson and Eriksson 2000; Eskelinen and Virtanen 2005; Gough 2006). The primary production is of importance determining the net effects of interactions and processes in alpine and arctic tundra. In more productive environments, there is generally a hump-shaped relationship between productivity and species richness (Grime 1979; Grace 1999), while this pattern is not always the case in alpine and arctic tundra (Fox 1985; Waide et al. 1999; Grytnes and Birks 2003). Productivity is not easily measured and a common method to estimate productivity is by sampling biomass or standing crop (see e.g. Krebs et al. 2003). However, biomass or standing crop is not always easily interpreted into productivity, particularly not in habitats with only plants and herbivores (Oksanen 1983; Oksanen et al. 1992; Oksanen and Oksanen 2000). In systems, like tundra heaths, with no, or only transient preda- 10

11 tors, herbivores are assumed to be resource-limited. Thus, plants are kept below their carrying capacity and standing crop is not correlated to productivity or to herbivore numbers (Rosenzweig 1971, but see van de Koppel et al. 1996; Wegener and Odasz-Albrigtsen 1998). However, biomass or standing crop might still be a qualitative estimate of the competitive situation experienced by the plants. The composition of plant functional traits may determine the competitive ability of a plant individual, the ability to grow in extreme conditions and the ability to cope with herbivory. High plant height can be an important competitive character, but prostrate growth can be an advantage both to avoid herbivory and to adapt to a harsh climate (Diaz et al. 2001; 2007; Oksanen 1990; Körner 1999). Nutrient availability will be of great importance for the functional traits developed by a plant since there is a positive correlation between productivity, specific leaf area, leaf palatability and digestibility (Williams and Rastetter 1999; Lavorel and Garnier 2002; Cornelissen et al. 2006). Plants growing in low productive areas are presumed to have low N contents due to a limited nutrient availability, while carbon is abundant, resulting in low palatability and digestibility. Nitrogen-based defence substances, working more specifically (e.g. trypsin inhibitors; Seldal et al. 1994), are suggested to be more common in productive habitats (Mattson 1980; Bryant et al. 1983; 1989). There are studies indicating that grazing leads to increased levels of nitrogen (Beaulieu et al. 1996; Olofsson et al. 2004a) in arctic and alpine environments. Increased levels of nitrogen imply an improved litter quality (Olofsson and Oksanen 2002), further enhancing the rate of nutrient cycling as a result of herbivory. In this thesis, three different regions are investigated and there are regional differences in the compositions of plant communities. The arctic tundra around Beringia is characterized by more herb species than the tundra in Lapland and Finnmark in the Fennoscandian mountain region. During the last Pleistocene, Beringia was largely unglaciated (Brubaker et al. 2005; Gualtieri et al. 2005), while other parts of Arctic were covered by ice, and those differences have had a major impact on the recent evolutionary history of Arctic species (Flagstad and Roed 2003). The herbivorous fauna (both present and historical; Zimov et al. 1995) differ between the regions with more species both in terms of large and small herbivores in Beringia. 11

12 Aim of the thesis In this thesis, I investigated effects of herbivory on arctic and alpine tundra vegetation and interactions among plants, with a focus on effects on plant species richness, abundance, biomass production and plant functional traits related to competition and herbivory. More specifically, I addressed the following questions: Are vascular plant distributions in alpine and subalpine environments limited by seed availability and/or suitable microsites, and could the presence of reindeer influence germination rates by creating microsites? (paper I) How do reindeer, rodents and insects affect plant species composition and biomass production in alpine heaths and subalpine birch forests? Are vascular plant functional traits in the heath and in the birch forest related to reindeer grazing? (paper II) Are densities of small and large herbivores and vascular plant standing crop in Beringia correlated to plant species richness, abundance and functional traits? (paper III) Do food quality and trypsin inhibitors in the common sedge Carex bigelowii vary with different grazing intensities, and do the response to defoliation vary over time and with productivity of the habitat? (paper IV) Do predators regulate the population dynamics of rodents, and thus the standing crop of plants via a trophic cascade? (paper V) 12

13 Methods The field work of this thesis was performed in three different study areas shown in Figure 1 and 2: Ammarnäs in southern Lapland (Sweden), Joatkanjavrit research area in Finnmark (Norway) and the regions around Bering Strait (Russia/USA). Ammarnäs - The study sites in paper I, II and IV were situated in the vicinity of Ammarnäs, Southern Lappland, Sweden. The sites in the alpine heath were located above the tree line at an altitude of m.a.s.l., and the sites in the subalpine birch forest were located at an altitude of m.a.s.l. The heath sites were dominated by mosses, lichens, dwarf shrubs, grasses and sedges. The sites in the birch forest were situated in humid slopes where tall herbs dominated. Mosses, liverworts, Vaccinum myrtillus, graminoids and small herbs were also significant constituents of the field layer. In one birch forest site, the vegetation consisted of patches of more dry heath-like birch forest with grasses, herbs and mosses. All sites were inhabited by free ranging reindeer (Rangifer tarandus) during the summer season. Finnmark - The study area in paper V was situated in the Joatkanjávrit research area on Finnmarksvidda in northernmost Norway. Three islands in the large tundra lake Iesjaure were used as predatorfree areas and two sites at mainland approximately 10 km from the lake were used as reference areas. The vegetation consisted of produc- 13

14 tive, low arctic scrublands or barren lowland tundra heaths with patches of scrubland. Beringia - The fieldwork in paper III was conducted during a polar expedition to Beringia in The areas visited were Kamtjatka, Chukotka and Wrangel Island in Russia and Alaska in the United States. The 9 sites were of a drier type of tundra on alpine slopes with a vegetation cover consisting of Dwarf Shrub Types described by Hansson (1953). Herbivore composition differed between the sites and was divided into small and large herbivores. Chukotka sites Alaska sites Kamchatka sites Wrangel Island site Figure 2. Nine sites were investigated in the Beringia region: Esso, Karaginski and Mysnotski in Kamchatka, Penkigney Bay, Yan Rakinot and Lavrentiya in Chukotka, Wrangel Island and Salmon lake and Tisuk river in Alaska (map from 14

15 Paper I: impact of seed limitation and seed availability on germination Six species were selected based on their different functional traits, e.g. life span, seed size, dispersal mode, and occurrence. Inside reindeer exclosures (1000m 2 ) and in adjacent control areas, a factorial experiment with four different treatments was performed: seeds added/not added combined with plots disturbed/not disturbed. The disturbance treatment consisted of the removal of all aboveground biomass. Forty cm-plots (ten replicates of each treatment) were used in each reindeer exclosure and control area with two replicates in the alpine heath and two replicates in the subalpine birch forest. Seedlings emerging in the plots were recorded at the end of July for three years ( ). Paper II: effects of different herbivore groups (reindeer, rodents and insects) A split-plot design was used to investigate the effects of different herbivore groups (reindeer, rodents and insects) on the vegetation. The experiment was based on reindeer exclosures (1000 m 2 ), rodent exclosures (16 m 2 ) and insecticide treatments (16 m 2 ) with three replicates in the alpine heath and three replicates in the subalpine birch forest. Estimations of reindeer densities were done by sampling all reindeer faeces along a transect (100 m 1 m) in each control area in both habitats. Rodent densities were estimated by the sampling of rodent faeces from ten 1 m 2 plots in reindeer exclosure and control area at each site. Additionally, rodents were also monitored by trap lines with snap traps twice a year along a transect situated approximately in the middle of the study area. Insect densities were recorded by traps consisting of four pit-fall traps in each treatment. All insects were examined but only herbivorous insects were used in the analyses. Plant species abundance was sampled using a frame (50 50 cm) divided into smaller squares (5 5 cm in the alpine heath and cm in the birch forest), where all species of vascular plants were recorded. Mosses, liverworts and lichens were determined to species level if possible, otherwise to genus. During , the vegetation change in biomass due to reindeer presence was monitored each year by biomass samples from 0.25 m 2. In 2003, biomass samples were taken from 4 dm 2 within each of the different treatments. All aboveground biomass was sampled, sorted into species or genus, dried and weighed. The amount of litter was measured by 5 samples of 1 dm 2 of 15

16 litter from each treatment that were collected in the end of August 2003, dried and weighed. Vegetation height was measured by 9 points in each treatment, where the highest photosynthetic plant part was measured in the field layer (i.e. not trees). Plant functional traits were sampled from ten individuals of each species within reindeer exclosures and in control areas in both habitats using a standardized method by Cornelissen et al. (2003). The sampled traits were plant height, specific leaf area (SLA), and the amount of nitrogen in the plant. Paper III: effects of herbivores and standing crop on plant species and trait composition The data on herbivore activities at each site was collected from triangle transects (Lindén and Helle 1996), where each triangle leg was 1000 meters (with a few exceptions). When walking along the transect, the vegetation type and every contact with mammals, some birds and visible insect attacks were noted. A contact could be trampling, faeces, carcass remains, nests, grazed plants and visible animals or warning calls. The signs of herbivore activities were divided into two classes related to small and large herbivores, respectively. The group of large herbivores included muskoxen, reindeer, moose and bears, and the group of small herbivores included pikas, ground squirrels, lemmings, voles, ptarmigan, grouse, geese, and caterpillars. Standing crop of vascular plants was sampled in five cm-square per site, dried and weighed. Plant species diversity and abundance were sampled using five frames (50 50 cm) per site. Each frame consisted of twenty five cm squares, and all plants present in the small squares were recorded. Vascular plants were examined to the species level, in a few cases only to family, while graminoids, mosses and lichens were generally grouped into genera or family. The abundance of a plant group, e.g. herbs, was then calculated as the sum of all the abundance of all occurring herb species within the frame. Plant functional traits were measured for ten samples of all herb species present in the frames. We investigated six traits; maximum photosynthetic tissue height, mean photosynthetic tissue height, height of flowers, specific leaf area (SLA; leaf area per unit leaf mass), C/N-ratio and individual mass, using methods developed by Cornelissen et al. (2003). Paper IV: nutritional quality of a common sedge after defoliation The nutritional quality of a common sedge Carex bigelowii was investigated in three habitats with differing productivity in the alpine heath. 16

17 Different intensities of grazing were simulated by clipping at three different levels in the end of July In order to study the kinetics of the inhibitor response, ramets were harvested at three different times after the clipping experiment. The response to simulated grazing by both vegetative and reproducing ramets of C. bigelowii was measured by the activity of trypsin inhibitors (TIA), the amount of total soluble protein in the ramet (SPP), and the ratio TIA/SPP. Paper V: predators regulate herbivore densities and thus, indirectly protect plants Grey-sided voles were introduced to predator-free islands in a large tundra lake at densities representing the densities on mainland areas (35 voles per ha) in Thereafter, vole densities were monitored both in mainland areas and in the islands by live-trapping two times each year, early July and late August. Plant cover was estimated in open plots and in vole exclosures (approximately 1 m 2 ) using a modified intercept method. Shoot mortality due to herbivory was assessed by marking of bilberry shoots. 240 shoots were marked in 12 plots in each site and checked every spring and autumn. 17

18 Results and discussion Vascular plants in alpine and subalpine vegetation seemed not only to be limited by abiotic factors, but also by seed availability (paper I). To some extent, plants were also favoured by removal of aboveground biomass in both habitats, while the effect of reindeer presence was negligible except for negative effects on germination of Trollius europeus in the birch forest. All of the investigated herbivore groups (reindeer, rodents and insects) had some effects on the vegetation in the exclosure experiment (paper II), and if evaluating the relative importance, rodents have the largest impact on the vegetation in this study. In the subalpine birch forest, the biomass of herb species was higher inside rodent exclosures, while in the alpine heath, biomass of dwarf shrub species was favoured by the exclusion of rodents. In a similar exclusion study of reindeer and rodents, Olofsson et al. (2004b) found the largest relative effects on the abundance of some common plant species, both in the forest and in the open heath. Large local effects of rodent herbivory was also found in the predator-free islands in Iesjaure, where grey-sided voles had strong negative effects on some plants, especially dwarf shrubs (paper V). In contrast, small herbivores in Beringia were positively related to the abundance of dwarf shrubs in alpine tundra (paper III). This positive relationship could be due to a negative relationship between the density of small herbivores and the abundances of graminoids and mosses. A decrease in mosses might benefit vascular plants (Virtanen et al. 1997; van der Wal and Brooker 2004). The relationship between the density of small herbivore activities and different plant groups could also be explained by small-scale habitat selection by the rodents, i.e. the rodents in this study avoid areas rich in graminoids and mosses, while preferring dwarf shrub heaths. The different effects on the vegetation by rodents among the regions, i.e. Beringia and Fennoscandia and between habitats in Ammarnäs, might be explained by a different rodent (and plant) species composition and thus, different food preferences. The most common rodent species in the study areas are listed in Table 1 and there are differences in food preferences, resulting in different effects on the vegetation. Reindeer had limited effects on plant community composition in the exclosure experiment, but had significant effects on plant functional 18

19 Table 1. The vole and lemming species found in the three study areas and their primary food preferences (Watson 1956; Siivonen 1976; Angerbjörn et al. 2005) Species Common name Swedish name Food preferences Presence in the study regions Chlethrionomys glareolus bank vole skogssork herbs, seeds, insects Ammarnäs Chlethrionomys rufocanus grey-sided vole gråsiding herbs, dwarf shrubs Ammarnäs, Finnmark Dicrostonyx groenlandicus collared lemming halsbandslämmel dwarf shrubs, (graminoids) Beringia Lemmus lemmus Norwegian lemming fjällämmel mosses, graminoids Ammarnäs Lemmus trimucronatus brown lemming brun lämmel graminoids, mosses Beringia Microtus agrestis field vole åkersork grasses, herbs, dwarf shrubs Ammarnäs Microtus oeconomus root vole mellansork grasses, herbs (dwarf shrubs) Beringia Myopus schisticolor wood lemming skogslämmel mosses, graminoids Ammarnäs 19

20 traits (paper II). In order to investigate more detailed effects of reindeer (in paper II) and of small and large herbivores (in paper III) on the vegetation, some selected plant functional traits were examined: plant height, specific leaf area (SLA) and nitrogen content. The data on plant functional traits are used in two ways in paper II. Firstly, a site specific estimation of the value of a special trait was obtained using the species abundances of vascular plants in each frame as weights and then calculating a weighted average for each of the three traits. The results indicated that plant nitrogen content was higher where reindeer were present in the alpine heath (paper II), which is in concordance with other studies indicating that grazing leads to increased levels of nitrogen (Beaulieu et al. 1996; Olofsson et al. 2004a). This site specific approach was also used in Beringia (paper III) and similarly, there was a negative relation between the density of large herbivores and the C/N-ratio, indicating higher nitrogen concentrations at high densities of large herbivores. The density of large herbivores in Beringia was also negatively related to mean green plant height, flower height and SLA. The SLA is related to the re-growth capacity of the plant, leaf palatability and digestibility (Diaz et al. 2001; Williams and Rastetter 1999; Lavorel and Garnier 2002; Hoffmann et al. 2005; Cornelissen et al. 2006). Thus, low plant heights and low SLA might be advantageous in order to avoid defoliation. Secondly, the data in paper II was used to assess intraspecific variations in herbs due to reindeer presence. We sampled ten individuals of all herbs present both inside and outside reindeer exclosures. Although other studies have shown that at least some of the traits are relatively consistent within species, both temporarily and spatially (Garnier et al. 2001, Tolvanen et al. 2004), we found intraspecific variation in plant height and specific leaf area. Tall, dominating herbs in the subalpine birch forest were taller and had higher SLA inside reindeer exclosures. However, the pattern was the opposite for low herbs, which could be explained by a competitive release when the dominant tall herbs were suppressed by reindeer. Rodents are shown to have relatively large impacts on plant community composition in this thesis (paper II, III and V). Simultaneously, they constitute a crucial food resource for many predators (Ims and Fuglei 2005). Thus, their population dynamics have been in focus and several studies have tried to evaluate both causes and consequences of the dynamics of small mammals in arctic and alpine ecosystems (e.g. Elton 1924; Boonstra et al. 1998; Turchin et al. 2000; Butet and Spitz 20

21 2001; Kent et al. 2005). Some studies suggest that the population dynamics in small mammals are structured by the nutritional quality of their food resources (e.g. Seldal et al. 1994; Jensen and Doncaster 1999; Bråthen et al. 2004, but see Oksanen et al. 1987; Klemola et al. 2000). Other studies suggest that small mammals in arctic and alpine tundra are regulated by predators (Korpimäki and Norrdahl 1998; Ekerholm et al. 2004; Lima et al. 2006). In contrast to studies by e.g. Seldal et al. (1994) and Bråthen et al. (2004), an investigation of trypsin inhibitors in the common sedge Carex bigelowii did not support the idea of an induced defense in response of defoliation (paper IV). However, we did find a significant decrease of soluble plant protein (SPP) with an increased intensity of defoliation. This may have nutritional consequences for herbivores and thus might be of importance for an assumed bottom-up-regulation of rodents in this ecosystem. We also found support for a top-downregulation of voles in the study of predator-free islands in Finnmarksvidda (paper V). On islands without predators, the vegetation (dwarf shrubs in particular) was heavily grazed due to high vole densities, compared to mainland reference areas. The question whether the world is green (see Hairston et al. 1960) because of low nutritional quality of plants or because of predators reducing herbivore numbers may still need further investigations, but my suggestion is that a combination of factors is needed for a full explanation. 21

22 Concluding remarks It is of great importance to understand the processes going on in an ecosystem, when constructing management plans for a sustainable use of natural resources and when making plans for conserving biological diversity. The management of arctic and alpine areas might be a complicated assignment, since there are two strong parties with differing perspectives. On one side, there are opinions favouring the idea of the last wilderness area, primarily by people not living there. On the other side, there are opinions that arctic and alpine areas are cultural landscapes managed, for example by reindeer herding. In addition, there is a growing interest among tourists for the mountain areas, which may lead to increased damage of the vegetation along hiking paths during summer and increased snow mobile transports during winter, which could cause disturbances for both reindeer and other wildlife. In this context, all information we could get about the processes and mechanisms working in the alpine and arctic tundra, is of great importance. Small mammals are keystone species in the arctic and alpine tundra, and thus, knowledge gained about causes and consequences of their population dynamics is of importance. Small mammals are a crucial food resource for most predators in the arctic and alpine tundra, and some predator species are not even breeding during years with low rodent densities (e.g. polar fox and snowy owl). Small mammals may have a large impact on the vegetation, at least on a local scale, and the vegetation may also have an impact on small mammals through changes in nutritional quality or quantity. There have been discussions about whether the tundra ecosystem is driven by bottom-up processes or top-down processes. If the ecosystem is driven by bottom-up processes, the herbivores are regulated by their food resources, which mean that the population densities of herbivores decrease when available food plants or their nutritional quality decrease. If the ecosystem is driven by top-down processes, the predators play a crucial role in suppressing the densities of herbivores and changes in the predator fauna will indirectly have consequences for the vegetation through so called trophic cascades. We still lack information for fully understanding the mechanisms driving the population dynamics of as well plants as of herbivores and predators in arctic and alpine regions. 22

23 To summarize, the results suggest that small mammals are regulated by a combination of predators and plant nutritional quality (paper III and V). Small herbivores have relatively large impact on plant community composition, measured by biomass (paper II) and by plant group abundance (paper III). Reindeer do not have any profound effect on the species composition but do affect plant functional traits significantly (paper II). Large herbivores, however, are negatively related to dwarf shrub species richness in Beringia, while small herbivores are positively related to dwarf shrub abundance, further pointing out that the type of herbivore investigated is of great importance for the vegetation responses (paper III). An additional conclusion from this thesis is that plant species distributions in alpine tundra and subalpine birch forests are not only regulated by abiotic factors but also by a lack of suitable microsites and seed limitation. Acknowledgement I am grateful to Ove Eriksson, Jon Moen and Regina Lindborg for valuable comments on this manuscript. References Angerbjörn, A., Dalén, L., Dalerum, F., Henttonen, H., Fedorov, V. B. and Abramson, N Evolutionary consequences of the Pleistocene glacial cycles. In: Rickberg, S. (ed.) Yearbook 2005, Swedish Polar Research Secretariat. Bardgett, R. D. and D. A. Wardle Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84: Beaulieu, J., Gauthier, G., and Rochefort, L The growth response of graminoid plants to goose grazing in a High Arctic environment. Journal of Ecology 84: Boonstra, R., Krebs, C. J. and Stenseth, N. C Population cycles in small mammals: The problem of explaining the low phase. Ecology 79:

24 Brooker, R. and van der Wal, R Can soil temperature direct the composition of high arctic plant communities? Journal of Vegetation Science 14: Brubaker, L. B., Anderson, P. M., Edwards, M. E. and Lozhkin, A. V Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. Journal of Biogeography 32: Bryant, J. P., Chapin III, F. S. and Klein, D Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: Bryant, J. P., Kuropat, P. J., Cooper, S. M., Frisby, K. and Owen- Smith, N Resource availability hypothesis of plant antiherbivore defence tested in a South African savanna ecosystem. Nature 340: Butet, A. and Spitz, F Cyclic fluctuations of microtine populations: half a century of research. - Revue D Ecologie la Terre et la Vie 56: Bråthen, K. A., Agrell, J., Berteaux, D. and Jònsdòttir, I. S Intraclonal varation in defence substances and palatability: a study on Carex and lemmings. - Oikos 105: Cairns, D. M. and Moen, J Herbivory influences tree lines. Journal of Ecology 92: Callaway, R. M., Brooker, R. W., Choler, P., Kikvidze, Z., Lortie, C. J., Michalet, R., Paolini, L., Pugnaire, F. I., Newingham, B., Aschehoug, E. T., Armas, C., Kikodze, D. and Cook, B. J Positive interactions among alpine plants increase with stress. Nature 417: Chapin, F. S. III Nutrient allocation and responses to defoliation in tundra plants. Arctic and Alpine Research 12: Cornelissen, J. H. C., Lavorel, S., Garnier, E., Diaz, S., Buchmann, N., Gurvich, D. E., Reich, P. B., ter Steege, H., Morgan, H. D., van der 24

25 Heijden, M. G. A., Pausas, J. G. and Poorter, H A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: Cornelissen, J. H. C., Quested, H. M., van Logtestijn, R. S. P., Perez- Harguindeguy, N., Gwynn-Jones, D., Diaz, S., Callaghan, T. V., Press, M. C. and Aerts, R Foliar ph as a new trait: can it explain variation in foliar chemistry and carbon cycling processes among subarctic plant species and types? Oecologia 147: Diaz, S., Noy-Meir, I. and Cabido, M Can grazing response of herbaceous plants be predicted from simple vegetative traits? Journal of Applied Ecology 38: Diaz, S., Lavorel, S., McIntyre, S., Falczuk, V., Casanoves, F., Milchunas, D. G., Skarpe, C., Rusch, G., Sternberg, M., Noy-Meir, I., Landsberg, J., Zhang, W., Clark, H. and Campbell, B.D Plant trait responses to grazing a global synthesis. Global Change Biology 13: Ekerholm, P., Oksanen, L., Oksanen, T. and Schneider, M The impact of short-term predator removal on vole dynamics in an arcticalpine landscape. - Oikos 106: Elton, C. S Periodic fluctuations in the number of animals: their causes and effects. - British Journal of Experimental Biology 2: Eriksson, O. and Ehrlen, J Seed and microsite limitation of recruitment in plant populations. Oecologia 91: Eskelinen, A. and Virtanen, R Local and regional processes in low-productive mountain plant communities: the roles of seed and microsite limitation in relation to grazing. Oikos 110: Eskelinen, A. and Oksanen, J Changes in the abundance, composition and species richness of mountain vegetation in relation to summer grazing by reindeer. Journal of Vegetation Science 17:

26 Flagstad, O. and Roed, R. H Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences. Evolution 57: Fox, J. F Plant diversity in relation to plant production and disturbance by voles in Alaskan tundra communities. Arctic and Alpine Research 17: Garnier, E., Laurent, G., Bellmann, A., Debain, S., Berthelier, P., Ducout, B., Roumet, C. and Navas, M.-L Consistency of species ranking based on functional leaf traits. New Phytologist 152: Gough, L Neighbour effects on germination, survival, and growth in two arctic tundra plant communities. Ecography 29: Grace, J. B The factors controlling species density in herbaceous plant communities: an assessment. Perspectives in Plant Ecology, Evolution and Systematics 2: Grime, J. P Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111: Grime, J. P Plant Strategies and Vegetation Processes. John Wiley and Sons., New York, NY. Grytnes, J. A. and Birks, H. J. B The influence of scale and species pool on the relationship between vascular plant species richness and cover in an alpine area in Norway. Plant Ecology 169: Gualtieri, L., Vartayan, S. L., Brigham-Grette, J. and Anderson, P. M Evidence for an ice-free Wrangel Island, northeast Siberia during the Last Glacial Maximum. Boreas 34: Hairston, N. G., Smith, F. E. and Slobodkin, L. B Community structure, population control, and competition. American Naturalist 149:

27 Hansson, H. C Vegetation Types in Northwestern Alaska and Comparisons with Communities in Other Arctic Regions. Ecology 34: Hartley, S. E. and T. H. Jones Plant diversity and insect herbivores: effects of environmental change in contrasting model systems. Oikos 101: Hoffman, W. A., Franco, A. C., Moreira, M. Z. and Haridasan, M Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Functional Ecology 19: Hyvärinen, M., Walter, B. and Koopmann, R Secondary metabolites in Cladina stellaris in relation to reindeer grazing and thallus nutrient content. Oikos 96: Ims, R. A. and Fuglei, E Trophic interaction cycles in tundra ecosystems and the impact of climate change. - Bioscience 55: Jakobsson, A. and Eriksson, O A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88: 494:502. Kent, A., Jensen, S. P. and Doncaster, C. P Model of microtine cycles caused by lethal toxins in non-preferred food plants. - Journal of Theoretical Biology 234: Klemola, T., Norrdahl, K. and Korpimäki, E Do delayed effects of overgrazing explain population cycles in voles? - Oikos 90: Van de Koppel, J., Huisman, J., van der Wal, R. and Olff, H Patterns of Herbivory Along a Productivity Gradient: An Empirical and Theoretical Investigation. Ecology 77: Korpimäki, E. and Norrdahl, K Experimental reduction of predators reverses the crash phase of small-rodent cycles. - Ecology 79: Krebs, C. J., Danell, K., Angerbjörn, A., Agrell, J., Berteaux, D., Bråthen, K. A., Danell, Ö., Erlinge, J., Fedorov, V., Fredga, K., 27

28 Hjältén, J., Högstedt, G., Jónsdóttir, I. S., Kenney, A. J., Kjellén, N., Nordin, T., Roininen, H., Svensson, M., Tannerfeldt, M. and Wiklund, C Terrestrial trophic dynamis in th Canadian Arctic. Canadian Journal of Zoology 81: Kuijper, D. P. J., Bakker, J. P., Cooper, E. J., Ubels, R., Jonsdottir, I. S. and Loonen, M. J. J. E Intensive grazing by Barnacle geese depletes High Arctic seed bank. Canadian Journal of Botany 84: Körner, C Alpine Plant Life. Functional Plant Ecology of High Mountain Ecosystems. Springer-Verlag Berlin. Lavorel, S. and Garnier, E Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology 16: Lima, M., Berryman, A. A. and Stenseth, N. C Feedback structures of northern small rodent populations. - Oikos 112: Mattson, W. J. Jr Herbivory in relation to plant nitrogen content. Annual Reviews of Ecology and Systematics 11: McIntire, E. J. B. and Hik, D. S Grazing history versus current grazing: leaf demography and compensatory growth of three alpine plants in response to a native herbivore (Ochotona collaris). Journal of Ecology 90: McIntire, E. J. B. and Hik, D. S Influences of chronic and current season grazing by collared pikas on above-ground biomass and species richness in subarctic alpine meadows. Oecologia 145: Moen, J. and Oksanen, L Long-term exclusion of folivorous mammals in two arctic-alpine plant communities: a test of the hypothesis of exploitation ecosystems. Oikos 82: Mulder, C. P. H Vertebrate herbivores and plants in the arctic and subarctic: effects on individuals, populations, communities and ecosystems. Perspectives in Plant Ecology, Evolution and Systematics 2:

29 Oksanen, L Trophic exploitation and Arctic phytomass patterns. American Naturalist 122: Oksanen, L., Oksanen, T., Lukkari, A. and Síren, S The role of phenol-based inducible defense in the interaction between tundra populations of the vole Clethrionomys rufocanus and the dwarf shrub Vaccinium myrtillus. - Oikos 50: Oksanen, L Predation, herbivory and plant strategies along gradients of primary productivity. In: D. Tilman and Grace, J., eds. Perspectives on plant competition. Academic Press, New York. Pp Oksanen, L., Moen, J., and Lundberg, P. A The time-scale problem in exploiter-victim models: does the solution lie in ratiodependent exploitation? American Naturalist 140: Oksanen, L. and Oksanen, T The logic and realism of the hypothesis of exploitation ecosystems. American Naturalist 155: Olofsson, J., Kitti, H., Rautiainen, P., Stark, S. and Oksanen, L Effects of summer grazing by reindeer on composition of vegetation, productivity and nitrogen cycling. Ecography 24: Olofsson, J. and Oksanen, L Role of litter decomposition for the increased primary production in areas heavily grazed by reindeer: a litterbag experiment. Oikos 96: Olofsson, J., Stark, S. and Oksanen, L. 2004a. Reindeer influence on ecosystem processes in the tundra. Oikos 105: Olofsson, J., Hulme, P. E., Oksanen, L. and Suominen O. 2004b. Importance of large and small mammalian herbivores for the plant community structure in the forest ecotone. Oikos 106: Olofsson, J Short- and long-term effects of changes in reindeer grazing pressure on tundra heath vegetation. Journal of Ecology 94:

30 Proulx, M. and Mazumder, A Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology: 79: Rixen, C. and Mulder, C. P. H Improved water retention links higher species richness with increased productivity in arctic tundra moss communities. Oecologia 146: Rosenzweig, M. L Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171: Seldal, T., Andersen, K. J. and Högstedt, G Grazing-induced proteinase-inhibitors a possible cause for lemming populationcycles. Oikos 70: Siivonen, L Nordeuropas däggdjur (Mammals of northern Europe). Norstedts, Stockholm, (in Swedish). Stark, S., Strömmer, R. and Tuomi, J Reindeer grazing and soil microbial processes in two suboceanicand two subcontinental tundra heaths. Oikos 97: Tolvanen, A., Alatalo, J. M. and Henry, G. H. R Resource allocation patterns in a forb and a sedge in two arctic environments short-term response to herbivory. Nordic Journal of Botany 22: Turchin, P., Oksanen, L., Ekerholm, P., Oksanen, T. and Henttonen, H Are lemmings prey or predators? - Nature 405: Waide, R. B., Willig, M. R., Mittelbach, G., Steiner, C., Gough, L., Dodson, S. I., Juday, G. P. and Parmenter, R The relationship between primary productivity and species richness. Annual Review of Ecology and Systematics 30: Van der Wal, R., Brooker, R., Cooper, E. and Langvatn, R Differential effect of reindeer on high Arctic lichens. Journal of Vegetation Science 12:

31 Van der Wal, R. and Brooker, R. W Mosses mediate grazer impact on grass abundance in arctic ecosystems. Functional Ecology 18: Van der Wal, R Do herbivores cause habitat degradation or vegetation state transition? Evidence from the tundra. Oikos 114: Watson, A Ecological Notes on the Lemmings Lemmus trimucronatus and Dicrostonyx groenlandicus in Baffin Island. The Journal of Animal Ecology 25: Wegener, C. and Odasz-Albrigtsen, A. M Do Svalbard reindeer regulate standing crop in the absence of predators? A test of the exploitation ecosystems model. Oecologia 116: Williams, M. and Rastetter, E. B Vegetation characteristics and primary productivity along an arctic transect: implications for scalingup. Journal of Ecology 87: Virtanen, R., Henttonen, H. and Laine, K Lemming grazing and structure of a snowbed plant community A long-term experiment at Kilpisjärvi, Finnish Lapland. Oikos 79: Virtanen, R., Parviainen, J. and Henttonen, H Winter grazing by the Norwegian lemming (Lemmus lemmus) at Kilpisjarvi (NW Finnish Lapland) during a moderate population peak. Annales Zoologici Fennici 39: Zimov, S., Chuprynin, V. I., Oreshko, F. S., Chapin III, F. S., Reynolds, J. F. and Chapin, M. C Steppe-tundra transition: a herbivore-driven biome shift at the end of the Pleistocene. American Naturalist 146:

32 Svensk sammanfattning Arktiska och alpina miljöer kännetecknas generellt av abiotiska miljöfaktorer som låga temperaturer, korta växtsäsonger och relativt låg produktivitet. Dessa faktorer är grundläggande för växters utbredning och funktionella egenskaper, men behöver inte överskugga betydelsen av andra faktorer, till exempel biotiska interaktioner. Biotiska interaktioner inkluderar dels interaktioner mellan olika växter (som kan vara både positiva och negativa) men även interaktioner mellan växter och djur. Fokus i den här avhandlingen är på effekter av betesdjur på sammansättningen av växtarter och växters funktionella egenskaper på den alpina och arktiska tundran. Beteseffekter är i regel negativa för den betade växten, men kan ha positiva effekter på växtsamhället, till exempel i form av ökad näringsomsättning. Aktiviteter av betande däggdjur kan även leda till att artdiversiteten bland växter ökar genom att djuren öppnar upp luckor i vegetationen. Detta kan till exempel vara av stor betydelse på fjällheden där markskiktet ofta är helt täckt av mossor och halvbuskar. Genom att större djur, till exempel renar, trampar och bökar öppnas det upp fläckar med bar jord där frön från kärlväxter kan gro. Även mindre djur, som gnagare, kan störa vegetationen och skapa så kallade microsites där groningsmöjligheterna för frön ökar. I alpina och arktiska tundramiljöer är många kärlväxter fröbegränsade eftersom det är svårt att upprätthålla en stabil fröproduktion i större omfattning under rådande miljöförhållanden och därför kan det vara av extra stor betydelse att befintliga frön lyckas etablera sig för att diversiteten bland kärlväxter ska bibehållas. Effekterna av bete på växters utbredning och egenskaper är beroende av flera faktorer. Bland annat spelar det stor roll vilken typ av herbivor det är som betar och vilken betesintensitet det är. Olika herbivorer föredrar olika födoväxter och beroende på vilka typer av växter det är som blir betade kan konsekvenserna skilja sig åt. Om det är dominanta arter som blir betade kan artdiversiteten öka genom att mindre dominanta växter får ökat utrymme ( competitive release ). Det är även skillnader i respons efter bete både mellan olika växtarter och inom en växtart, beroende på vilka egenskaper en individuell växt har och i detta sammanhang kan områdets produktivitet vara en viktig faktor. Näringstillgången kan påverka hur en växt kan återväxa efter att ha 32

33 blivit betad och även hur sannolikt det är att en växt blir betad. Egenskaperna hos en växt kan också vara avgörande för hur konkurrenskraftig växten är samt hur en växt klarar av att växa i extrema miljöer. En sådan funktionell egenskap kan till exempel vara höjden hos en växt. I områden med hög produktivitet och konkurrens om ljus är det bra att vara högre än sina grannar, men det är också en större risk för höga växter att bli betade. Genom ett krypande växtsätt kan en växt undvika att bli betad. Ett krypande växtsätt är även en bra egenskap för att klara miljöförhållandena (framförallt hård vind) på den öppna tundraheden. I relation till bete är även kapaciteten hos en växt att återväxa av stor betydelse för hur man tolererar att bli betad och denna kapacitet är till stor del beroende av näringstillgången. Tillväxt, och därmed även återväxtkapacitet, går att uppskatta genom att mäta en kvot mellan yta och torrvikt hos bladen (specific leaf area, SLA). SLA påverkar även risken att bli betad eftersom det finns en koppling mellan SLA, bladets smaklighet och nedbrytbarhet. Växter som växer i lågproduktiva områden kännetecknas generellt av låg SLA och låga kvävehalter. Eftersom ljustillgången inte är någon begränsande faktor på tundraheden, leder detta till höga kol/kväve-kvoter hos växterna, vilket resulterar i låg smaklighet och nedbrytbarhet. En strategi för att undvika bete är att producera försvarsubstanser och i områden med låg näringstillgång dominerar kolbaserade försvarsämnen som verkar genom att sänka smakligheten generellt hos växten. De kolbaserade försvarssubstanserna skiljer sig således från kvävebaserade försvar, där effekten ofta är specifik som till exempel de trypsin inhibitorer man har funnit i vissa halvgräs. Det finns studier som indikerar att försvarssubstanser och den näringsmässiga kvaliteten, tillsammans med mängden tillgänglig föda, kan vara av avgörande betydelse för hur populationsdynamiken hos de mindre däggdjuren styrs. Andra studier tyder på att de mindre däggdjuren, till exempel lämlar och sorkar, i första hand styrs av predatorer. Om predatorerna reglerar tätheterna av smågnagare, kan de indirekt styra växtligheten genom så kallade kaskadeffekter. För att få en något mer detaljerad bild av de biotiska interaktionerna i alpina miljöer och på den arktiska tundran genomfördes fyra olika studier där syftet var att dels kartlägga vilken betydelse olika herbivorgrupper har för växtsamhällets sammansättning av arter och egen- 33