Top-down and bottom-up effects in a Fennoscandian tundra community
Doris Grellmann
Umeå 2001
Department of Ecology and Environmental Science Umeå University
S E -9 0 1 87 Umeå Sweden
AKADEMISK AVHANDLING
Som med vederbörligt tillstånd av rektorsämbetet vid Umeå universitet för erhållande av filosofie doktorsexamen i ekologi
kommer att offentligen försvaras fredagen den 4 maj 2001, kl. 10.00
i stora hörsalen, KBC.
Examinator: Prof. Lars Ericson, Umeå University, Umeå, Sweden
Opponent: Prof. Richard Inouye, Idaho State University, Pocatello, USA
Organisation
Department of Ecology and Environmental Science Umeå University
SE — 90187 Umeå, Sweden April 2001
Document name Doctoral dissertation Date of issue
Author: Doris Grellmann
Title: Top-down and bottom-up effects in a Fennoscandian tundra plant community
Abstract: The objective of this thesis was to investigate the effects of mammalian grazers, such as microtine rodents and reindeer, (top-down effects) and nutrient availability (bottom- up effects) on the plant community of a tundra heath.
I conducted a large-scale fertilization experiment and studied the impact of grazers using exclosures. I measured the effects of fertilization and grazing on soil microbial activity and nutrient cycling. I investigated the responses to fertilization of the invertebrate community, I studied the effects on the quality of bilberry as food for mammalian herbivores, and I looked at how concentrations of nutrients and carbon-based secondary defences against herbivory fluctuated between seasons in unfertilized and fertilized treatments.
The results of my thesis show that the plant community investigated is exposed to a strong top-down control by mammalian herbivores. On the fertilized and grazed areas the aboveground biomass of the vascular plant community did not increase compared to unfertilized areas. However, the productivity of the plant community was clearly nutrient- limited. During the eight years of the experiment, on the fertilized areas plant biomass was significantly increased inside the herbivore exclosures
In my study mammalian herbivores at comparatively low densities and grazing outside the growing season were sufficient to control the biomass of a heterogeneous plant community. Microtine rodents (Norwegian lemmings and grey-sided voles) preferred the fertilized areas for overwintering. The food plant quality of bilberry for grey-sided voles was improved on the fertilized areas throughout the year. Grazing decreased the nitrogen storage in the aboveground plant biomass. Reindeer and rodents had also important indirect effects on the plant community by decelerating soil nutrient cycling and soil microbial activity. This effect may be accelerated by the impact of herbivore on plant species composition.
Graminoids, which contained the highest nitrogen concentrations in their tissues, increased rapidly on the fertilized areas, but their abundance was significantly lower on grazed fertilized areas.
The invertebrate community was detritus-based and received their energy indirectly from the litter via soil microbes and detritivores. Fertilization increased the biomass of invertebrate carnivores, but had no effect on the biomass of invertebrate herbivores.
Apparent competition between detritivores and invertebrate herbivores, mediated by carnivorous invertebrates predating on both of them, is supposed to keep the densities and grazing pressure of invertebrate herbivores low. Grazing damage by invertebrates was very low and only 0.021 % of the total vascular plant biomass was removed.
Key words: consumer-resource interactions, exclosures, food web dynamics, grey-sided voles, lemmings, NPK-fertilization, plant defences, reindeer, soil microbes, vertebrate grazing.
Language: English ISBN: 91-7305-032-6 No. of pages: 24 + 6 app.
Sign J Date: 31 March 2001
To my mother, who,
during the short time we had together, shared with me
her fascination for nature.
Description of the front page
Main picture: A view across the highland tundra study area, from the north to the south, showing three of the study plots (two fertilised, one unfertilised) (photo by Michael Schneider).
Above: Norwegian lemming {Lemmus lemmus), subadult female, on one of the fertilised study plots (photo by Michael Schneider).
Below: Flowering bilberry ( Vaccinium myrtillus) (photo by Doris
Grellmann).
Contents
List of papers... 5
Introduction... 6
Bottom-up effects: nutrient availability... 6
Top-down effects: trophic interactions... 7
Aims of the thesis... 8
Study site... 9
M ethods... 10
Summary of the papers... 11
Effects of improved nutrient availability... 11
The impact of vertebrate herbivores on tundra heaths... 12
Effects of mammalian herbivory on nutrient cycling and soil microbial activity... 13
Invertebrate responses to nutrient enrichment... 15
Effects of season and nutrient enrichment on food plant quality... 16
Conclusions... 17
Acknowledgements... 18
References... 18
Finally... 23
Appendices: I - VI
List o f papers
This thesis is a summary and discussion of the following papers that will be referred to in the text by their Roman numerals.
I. Grellmann, D. Is the plant biomass of a European tundra community limited by nutrients? A fertilization experiment. - Manuscript.
II. Grellmann, D. Plant responses to fertilization and exclusions of grazers on an arctic tundra heath. - Manuscript.
III. Grellmann, D., Schneider, M. F. & Oksanen, L. Top-down control of heterogeneous tundra vegetation. - Submitted manuscript
IV. Stark, S. & Grellmann, D. Soif microbial responses to mammalian herbivory in an arctic tundra heath at two levels of nutrient availability. - Submitted manuscript
V. Schneider, M. F. & Grellmann, D. Multitrophic interactions in an invertebrate tundra food web. - Submitted manuscript
VI. Grellmann, D. & Hjältén, J. Seasonal variation in bilberry chemistry
following fertilization: a test of current theories of phenolic
allocation. - Submitted manuscript.
Top-down and bottom-up effects in a Fennoscandian tundra plant community
Introduction
Earlier studies on tundra plant communities focused mainly on the physiological ecology of plants (Billings 1974, Billings and Mooney 1968, Bliss 1971,). The harsh environment in the arctic with long winters, short growing seasons and low temperatures was seen as the main challenge for the physiological capabilities of plants and their ability to survive under these conditions (Billings and Mooney 1968, Walter 1973). Still today, the impacts of the physical environment are commonly assumed to be the most relevant factors structuring arctic plant communities, while impacts by trophic interactions such as grazing are considered to be small or even unimportant (cf. Chapin et al. 1992, Jefferies et al. 1994, Jonasson and Shaver 1999). However, it has been shown that herbivores are able to influence plant communities fundamentally by changing species composition, diversity, total biomass and productivity in a variety of ecosystems (Huntly 1991). In recent years, the development of theoretical food chain models investigating the importance of consumptive processes (top-down effects) and resource limitation (bottom-up effects) for the population dynamics on various trophic levels (plants, herbivores, carnivores), has made progress (Persson 1999). However, attempts to test the ideas of food chain theory on entire terrestrial plant communities have been scarce.
Bottom-up effects: nutrient availability
Physiological processes in arctic plants are well adapted to the physical environment and appear not to be very sensitive to the low temperatures during the growing season (Crawford 1989, Körner 1999). Therefore growth is not directly influenced by the cold, but more indirectly by the low rate at which resources become available (Chapin 1993). Low temperatures influence decomposition rates, chemical weathering, and hence nutrient availability for plants (Billings 1987, Billings and Mooney 1968, Callaghan 1989, Callaghan and Emanuelsson 1985, Hobbie and Chapin 1998, Jonasson 1983). Therefore, nutrient limitation by nitrogen is seen as the main factor that determines the low productivity of arctic plant communities (Chapin et al. 1995, Chapin and Shaver 1996, Jonasson 1992, Shaver and Chapin 1980). In these plant communities fertilization is thus predicted to have large effects on primary productivity and biomass patterns.
Several studies have tried to understand the nature of nutrient limitation in tundra plant communities by fertilization and by raising temperatures (Chapin et al. 1995, Chapin and Shaver 1996, Jonasson 1992, Jonasson et al. 1996, McKendrick et al.
1978, Parsons et al. 1994, Press et al. 1998, Shaver et al. 1998). Although fertilization caused increased growth rates in the dominant plant species, this was not always reflected in an increase in plant biomass at the plant community level (Chapin et al. 1995, Parson et al. 1994, Press et al. 1998). There have been several attempts to explain these contradictory results. Parson et al. (1994) argued that in
long living dwarf shrubs the large amount of biomass accumulated in years prior to the fertilization event diluted the fertilizer response on the community level. Positive responses of one set of plant species, such as deciduous shrubs might be offset by negative responses of other, mainly evergreen, species to fertilization (Chapin and Shaver 1985). However, except competition for nutrients between faster-growing deciduous shrubs and slower-growing evergreen plants, there have been no attempts to involve other biotic interactions, such as herbivory, to explain the results of the fertilization experiments. In general, the impact of vertebrate herbivores on arctic tundra communities is considered to be small, because it is suggested that herbivores consume only a small fraction of the biomass produced during the growing season (Jefferies et al. 1994, Jonasson and Shaver 1999).
Top-down effects: trophic interactions
There is an ongoing debate on to which extent terrestrial plant communities can be structured by nutrient limitation or by herbivory (Hunter and Price 1992, Persson
1999, Polis 1999, Polis and Strong 1996, Power 1992, Strong 1992,). Especially the capacity o f herbivores to limit the standing crop of entire and diverse terrestrial plant communities as one important prerequisite for the occurrence of trophic cascades (i.e. mutual interactions between non-adjacent levels) are intensely discussed (Chase 2000, Chase et al. 2000, Oksanen and Oksanen 2000, Paine 2000, Polis 1999, Polis et al. 2000, Schmitz et al. 2000, Strong 1992).
According to food chain theory, the importance of herbivores for the plant community depends on the number of trophic levels in the system. A hypothesis developed for terrestrial systems by Oksanen et al. (1981) and Oksanen and Oksanen (2000) proposed that the numbers of trophic levels depend on primary productivity. According to this view, productive terrestrial systems are consisting of three trophic levels (plants, herbivores and predators) and are called three-link systems. In moderately productive systems, such as tundra heaths, primary productivity is not sufficient to maintain a viable predator population feeding on herbivores and, therefore, such systems consist of two trophic levels only (two-link systems). In very unproductive systems, such as arctic deserts, the productivity is supposed to be not even sufficient to maintain a viable grazer population, and plant communities are regulated by their resources (one-link systems). This concept makes important predictions for the regulation of plant communities. In productive systems, predators control herbivore populations and have indirect positive effects on the plants because predators efficiently decrease herbivore pressure upon the vegetation. In consequence, in productive systems plant biomass is primarily limited by nutrient availability. In moderately productive systems, on the other hand, herbivore populations are supposed to be controlled by the availability of their food resources and, the plant biomass should be primarily controlled by herbivores (Oksanen and Oksanen 2000). Therefore, nutrient enrichment of relatively unproductive two-level systems should cause an increase in herbivore densities while plant biomass should remain constant (Oksanen and Oksanen 2000).
Studies on trophic interactions testing the predictions of food chain theory have mostly been done in aquatic environments and often included entire lake systems (Brett and Goldman 1996, 1997, Carpenter et al. 1985, 1987, Hansson & Carpenter
1993, Persson et al. 1992). Most of the terrestrial studies, on the other hand, only involved community subsets and arthropod food chains (Altlegrim 1989, Fraser and Grime 1998, Schmitz 1993, Schmitz et al. 1997, 2000, Spillerand Schoener 1990).
Although the results of these studies supported the ideas of food chain theory, the applicability of the trophic level concept on entire terrestrial communities is questioned, mainly because of the heterogeneity within trophic levels (Strong 1992, Persson 1999, Polis 1999). Because of a variety of defence mechanisms in plants against herbivory, herbivores are not supposed to be able to control an entire plant community in a given system (Hunter and Price 1992, Murdoch 1966). It has been argued that growth responses by plant species that are inferior competitors, but more resistant to herbivory, may cause positive correlations between the biomass of the two trophic levels after nutrient enrichment of unproductive systems (Hunter and Price 1992, Leibold 1989, Leibold et al. 1997, Polis and Strong 1996,).
A im s o f the thesis
The main aim of my thesis was to investigate to what extent vertebrate herbivores such as microtine rodents and reindeer are able to alter the responses o f a tundra plant community to nutrient enrichment. The specific questions addressed were:
1. Is the investigated plant community nutrient-limited, and does fertilization increase its productivity and biomass? How does plant species composition change after fertilization? (Papers I and II)
2. Are mammalian herbivores able to control the biomass of a heterogeneous plant community consisting of palatable and unpalatable species? Are herbivores able to keep plant biomass at a constant level after fertilization, as predicted by food chain theory? (Papers I, II and III)
3. How does fertilization, grazing by mammalian herbivores, and the interaction of both factors influence soil microbes and nutrient cycling in the soil? Does grazing have accelerating or decelerating effects on nutrient cycling and, consequently, on nutrient availability for the plants? (Paper IV)
4. How does fertilization affect the invertebrate community? Are green plants the primary energy resource for the invertebrate food web as predicted by classical food chain theory, or is the food web detritus-based, as proposed by Oksanen et al. (1997)? Are omnivorous birds as top predators dynamically important in controlling the invertebrate community? (Paper V)
5. How does fertilization affect the quality of plants as food for mammalian herbivores? How do carbon, nitrogen and carbon-based secondary defences against herbivory fluctuate between seasons? (Paper VI)
Finally, I discuss how all these factors (fertilization, grazing, plant species composition, soil microbial activity, invertebrate community, omnivorous birds, and food plant quality) act in combination in the regulation of the investigated plant community.
Study site
I conducted my field studies in the Joatka Research Area on Finnmarksvidda in North Norway. The Joatka Research Area has a long tradition of research on the interactions of voles and lemmings with their food resources and their predators.
The study area has been described in detail by Oksanen et al. (1996, 1997). My study area is situated about 150 m above the tree line on a highland plateau (69°45’N, 23°58’E) at an altitude of 520-540 m above sea level. Due to its northern location and altitude, the study area belongs to the tundra proper where no tall shrubs occur. The vegetation of the study area corresponds to the arctic Empetrum- Vaccinium type described by Oksanen and Virtanen (1995), a mossy dwarf shrub heath dominated by dwarf-birch (Betula nana), crowberry (Empetrum nigrum spp.
hermaphroditum), and bilberry ( Vaccinium myrtillus). For further descriptions concerning the species composition o f the plant community see papers I and II. The nomenclature of the plant species follows Lid (1985). The growing season starts at the end of June and lasts for about 70 days. The climate is continental with an average annual precipitation of 354 mm (Oksanen and Virtanen 1995). The greatest thickness of the snow cover (about 100 cm) is usually reached in late March or early April. The organic soil layer is shallow, averages 2.8 cm on the unfertilized and 3.8 cm on the fertilized areas, and is underlain by hard and nutrient-poor rocks (Lindström 1987). The aboveground biomass o f vascular plants was about 250 g m“2 (dry weight), the aboveground productivity (measured in 1999 was 20 - 40 gm"2, and the average vegetation height was 5 cm on unfertilized and unfenced areas.
The main mammalian herbivores in the study area are Norwegian lemmings (Lemmus lemmus L.) and grey-sided voles (Clethrionomys rufocanus Sundevall). In the Joatka Research Area, studies on the population dynamics o f microtine rodents have been carried out since 1977. Lemmings had population outbreaks in 1978 and 1988 and the voles had peak years in 1983, 1987 and 1993 (Oksanen and Oksanen 1992, Oksanen et al. 1996). Another herbivorous mammal in the system is the mountain hare (Lepus timidus L.), occasionally moving up to my study site from the mountain birch forest on a nearby mountain slope.
Studies on the interaction between habitat structure and the occurrence of rodents and their specialist predators weasel {Mustela nivalis L.) and stoat {Mustela erminea L.) have shown that mammalian predators are virtually absent from my study site (Oksanen et al. 1992, 1996, 1999). Avian predators of rodents were scarce during the study period, except one pair o f long-tailed skuas {Stercorarius longicaudus Vieillot) that have been nesting near the study site. However, long-tailed skuas are no rodent specialists, and they have been seen to eat plant parts, invertebrate prey, and carrion (Schneider unpubl.). Other insectivorous bird species are plovers {Charadrius morinellus L., Pluvialis apricaria L.), wheatears {Oenanlhe oenanthe L.), and meadow pipits {Anthus pratensis L.) (see Paper V).
Reindeer {Rangifer tararandus L.) migrate through the area to their winter grazing sites in autumn (October) and to their summer grazing sites in the north during spring (April, May). Reindeer are not allowed to remain in the Joatka area during the growing season, but some individuals were grazing on the study area in early summer 1995.
The study site
Highland i
O *
1 km
10 m
An experimental area n Bogs, lichen heaths, moss-bilberry heaths, open meadows
■ Bilberry heaths, moist woodlands, scrubby habitats
■ Lakes — Rivers *3 Bare rock
o Unfertilized area • Fertilized area
Fig. 1. The study site with the experimental areas within the Joatka Research area on Finnmarksvidda in northern Norway. Each area is subdivided by a 10 m x 10 m grid.
The sites for the rodent live trapping are situated at the intercepts. On the plots marked by X four open plots, four reindeer exclosures, and four reindeer plus rodents exclosures were established randomly on each experimental area.
Methods
In order to investigate the responses of rodent populations to nutrient enrichment rather than the behavioural responses of individuals that concentrate foraging on smaller nutrient-rich areas within their home ranges, I chose rather large areas (0.25 ha each) as study plots. The size of these plots was larger than an average home range of a vole or lemming in this area (cf. Oksanen et al. 1999). In 1991 I established eight circular study plots, each covering 0.25 ha. I fertilized once during July 1991 with an N-P-K fertilizer (80 gmf2; 13.7 % N, 6.0 % P, 15.7 % K), and after observing that the primary productivity on the fertilized areas eased off, fertilization was repeated in the beginning of July 1997.
The impact o f mammalian herbivores on the plant community was investigated by using two types o f exclosures, one that excluded reindeer only, and another one that excluded both reindeer and rodents. The exclosures had a size of 1 m2 and were made of galvanised net (mesh size 1.2 x 1.2 cm2). When constructing the exclosures for both reindeer and rodents, the net was dug into the soil to a depth of 20 cm. To build exclosures that excluded reindeer only, the net was fastened to wooden sticks at a height of about 15 cm above ground, allowing free access for the rodents (Paper II and III). I did not observe any effects of fences on temperature or snow packing patterns during winter. There was no accumulation of snow inside the fences or
outside along the lee side, indicating that the wind flow was not significantly influenced.
The densities of microtine rodents were estimated by live trapping using Ugglan special multiple capture live traps (Schneider 2000) (Papers II, III and VI). In addition to this, the winter nests of the rodents were counted on each area, and the areas heavily grazed by rodents during winter were mapped shortly after snow melt.
(Papers I and II). The vegetation was analysed by harvesting aboveground biomass (Papers I and III) and by studying changes in plant species abundance on permanent plots using a point frequency method (Paper II). The invertebrate community was studied using emergence traps. These traps consist of a funnel tent with a collecting jar at the top and a pitfall trap dug into the ground inside the tent. Birds were excluded by using large plastic nets (100 m2) having a mesh size of 3 cm. The nets efficiently excluded the smallest bird species present, but invertebrates were not hindered to fly through the mesh. For details of the chemical soil and plant analyses done see Papers IV and VI.
Summary of the papers
Effects of improved nutrient availability
In general, tundra plants are supposed to be strongly nutrient limited and therefore improvement of the resource supply by fertilization should have profound effects on the productivity, biomass and species composition of the plant community (Chapin et al. 1995, Jonasson 1992, Shaver and Chapin 1980,).
In earlier fertilization studies of tundra plant communities, graminoids showed the fastest response to fertilization and increased significantly in abundance (Chapin et al. 1995, Chapin and Shaver 1985, Jonasson 1992, Parssons et al. 1994, Press et al. 1998). Considering the responses of the most abundant dwarf shrubs, different studies gave contrasting results. In a study in Alaska (Chapin et al. 1995, Chapin and Shaver 1985), deciduous plants such as Betula nana increased tremendously on fertilized areas. However, in fertilization studies in Fennoscandia the biomass of deciduous plants such as Vaccinium myrtillus and B. ncma remained constant, although the productivity of these species increased (Graglia et al. 1997, Parssons et al. 1994, Press et al. 1998). Evergreen dwarf shrubs are supposed to react more slowly to fertilization because of slower growth rates compared to deciduous plants (Chapin and Shaver 1985). However, different studies yielded various results. While evergreen plants decreased in Alaska (Chapin et al. 1995), Fennoscandian studies showed decreased, increased, or unchanged biomasses/abundance of evergreen plants on fertilized plots (Jonasson 1992, Parsson et al. 1994, Press et al. 1998).
In my study the investigated plant community was nutrient limited because fertilization significantly increased the aboveground net primary production.
Although fertilization caused increased plant productivity, this did not result in an increase in standing plant biomass on on the grazed areas (Papers I and III).
Fertilization increased the productivity of both deciduous plants and graminoids, while evergreen plants, as a group did not react (Papers I and II). One attempt to generalise plant responses to fertilization was to assign the different plant species to
functional groups according to their growth forms, including deciduous and evergreen plants, graminoids, and herbs (Chapin et al. 1996). Deciduous plants and graminoids are assumed to respond positively to fertilization, while evergreen plants are supposed to respond negatively (Chapin et al. 1996). However, in my study evergreen plants did not respond uniformly. Fertilization affected the aboveground biomass of Vaccinimi vitis-idaea and Phyllodoce caerulea negatively, while the biomass of Empetrum nigrum ssp. hermaphroditum increased on the fertilized areas.
(Paper III).
Deciduous plant biomass did not increase on the fertilized areas, and the biomass increase of graminoids was not sufficient to significantly rise total plant biomass after fertilization. Considering the changes in abundance measured by the point frequency method, vascular plants as well as deciduous plants increased slightly in abundance on the fertilized plots (Paper III). As the productivity o f deciduous plants was higher on the fertilized areas (resulting in an increased leaf area and, consequently, in a higher cover and deciduous plants), the point frequency method used in paper II yielded positive responses of total vascular plant abundance and deciduous plants on the fertilized areas.
In a nutrient limited tundra heath community where herbivores are excluded, I predict that both the productivity and the biomass accumulation of graminoids and deciduous plants will be higher on fertilized plots. Evergreen plants react more slowly and at a longer time scale probably will be outcompeted by faster growing deciduous plants. Papers I, II and III discuss these questions.
The impact of vertebrate herbivores on tundra heaths
According to Oksanen and Oksanen (2000), the tundra plant communities of cold and unproductive areas are supposed to be two link-systems and should therefore be under intense grazing pressure by mammalian herbivores. Arctic plant biomass patterns with constant, not increasing plant biomass over large intervals of productivity (Oksanen 1993, Oksanen and Oksanen 2000) and the nature of the population dynamics of lemmings (Ekerholm et al. 2001) suggest that mammalian herbivores grazing in tundra habitats are locked in tight, coupled predator-prey interactions with the vegetation. The population fluctuations of lemmings show long periods of low numbers and sudden, sharp peaks, which is a time trajectory more characteristic for consumer than for a prey populations (Turchin et al. 2000).
Enrichment of such systems should lead to increased herbivore biomass while the plant biomass should remain constant (Rosenzweig 1971, Oksanen and Oksanen 2000). The applicability of this prediction to heterogeneous plant communities has been debated (Polis 1999, Polis et al. 2000, Polis and Strong 1996). In heterogeneous plant communities, plant biomass will remain constant after fertilization, and herbivore biomass will increase only if (i) herbivory is more important for the determination of plant community composition than competition for limited nutrients, and if (ii) competitive plants are more edible than the slower- growing species of inferior competitive ability (Oksanen 1990, Rosemond 1996).
These conditions can be met in unproductive tundra communities, where, in general, graminoids and deciduous shrubs have a higher palatability and higher growth rates than evergreen plants, which have relatively low growth rates but well developed mechanisms of carbon-based defences (Bryant et al. 1983, Coley et al. 1985). I
investigated the effects of reindeer and rodents in an unfertilized and a fertilized plant community with the help of exclosures as described in Paper II and III.
On the fertilized areas the aboveground vascular plant biomass was significantly higher inside the exclosures, while the plant biomass was not significantly increased on grazed fertilized plots when compared to grazed but unfertilized plots (Paper III).
This shows that herbivores are able to consume a considerable part of the increased plant productivity on the fertilized areas. The extent of the herbivore impact depends on the time scale o f the investigation. During a single growing season the impact of herbivores can be negligible, partly because plants are able to compensate for the losses, but mainly because the density o f herbivores during summer is quite low (Paper III). However, in my study rodents preferred the fertilized areas during winter (Papers I, II, III). When looking at a longer time period that also included winter herbivory, the plant biomass remained constant on grazed areas despite nutrient enrichment, which is in accordance with the prediction o f Rosenzweig (1971) and Oksanen and Oksanen (2000). This was the case although the density of rodents was relatively low during my study period. During 1993 - 1994 one minor peak year occurred, but the densities o f rodents were about 10 times lower compared to the densities of the peak years 1977 and 1988. Nevertheless, during the winter 1993 - 1994 the rodents devastated on average 27 % o f the surface of the fertilized areas, with 90 % of all vascular biomass clipped on the grazed parts (Papers I, III).
Considering that during four years only about 25 % of the formerly removed plant biomass had regrown on the fertilized areas (and even less on the unfertilized areas, Paper I), repeated rodent peaks can heavily influence the plant community.
Contrary to the ideas of Polis and Strong (1996), Polis (1999) and Polis et al.
(2000), mammalian herbivores limited the biomass o f a heterogeneous plant community consisting of plant species o f different growth patterns and herbivore preference in my study. Graminoids showed the largest response to fertilization, but herbivores were successful in controlling the abundance o f grasses on the fertilized areas. Deciduous plants as a group responded positively to fertilization, but showed a marginal tendency of increase inside herbivore exclosures. Here B. nana increased significantly on the fertilized areas, but was not preferred by herbivores. On the other hand, V. myrtillus, which is highly preferred by overwintering grey-sided voles, increased in the exclosures but showed only a slight response to fertilization.
This is in contrast to the general assumption that deciduous plants of nutrient-limited sites will react positively to fertilization and are more palatable for herbivores than evergreen plants (Bryant et al. 1983, Coley et al. 1985).
Effects of mammalian herbivory on nutrient cycling and soil microbial activity
Herbivores do not only have direct effects through grazing, but have also indirect effects on nutrient cycling and, consequently, on nutrient availability for plants.
Urine and faecal deposition have been shown to have a positive influence on nutrient cycling in the soil (Frank and Groffman 1998, McKendrick et al. 1980, Ruess and McNaughton 1987). Selective foraging by herbivores alters plant species composition, which indirectly affects nutrient cycling. In nutrient-limited plant communities, herbivores are supposed to shift the species composition towards less palatable plants with high amounts o f fiber and carbon based defences by preferring
more palatable plants with relatively high contents of nutrients. This has negative impacts on overall litter quality and reduces decomposition rates and the quality of soil organic matter (Pastor et al. 1988, 1993, Ritchie et al. 1998). This indirect effect on plant composition is supposed to have a decelerating effect on the rate of nutrient cycling. Conversely, on sites richer in nutrients, herbivores can have an accelerating effect on nutrient cycling by increasing the biomass of palatable and nitrogen-rich plant species responding to grazing by high growth rates (McNaughton 1979, Ruess and McNaughton 1987). The increased abundance of these plant species causes improved overall litter quality, which accelerates litter decomposition and stimulates nutrient cycling (Frank and Groffman 1998, Taylor et al. 1989).
Several studies have shown that grazing by reindeer and rodents increases the proportion o f graminoids in relation to dwarf shrubs in arctic plant communities (Chapin et al. 1986, McKendrick et al. 1980, Olofsson et al. 2001, Post and Klein 1996). An increased abundance of graminoids increased the amount of nitrogen in the soil and in soil microbes and enhanced soil respiration and microbial activity (Olofsson et al. 2001).
In Paper IV 1 investigated, together with Sari Stark, the role of reindeer and rodent herbivory on soil microbial processes, soil nutrient levels, and nutrient levels in the plant community on both unfertilized and fertilized areas. Grazing by mammalian herbivores had a decelerating effect on soil nutrient cycling and reduced soil respiration on both unfertilized and fertilized areas. Fertilization increased the carbon and nitrogen storage in the aboveground plant biomass, mainly because of the increase of graminoids, which contained the highest concentrations of nitrogen and carbon. However, grazing decreased the abundance of graminoids and, consequently, reduced the litter quality outside the exclosures. In spite of fertilization, soil nutrient availability was obviously not high enough to enable graminoids growth responses sufficiently high to compensate for grazing losses. The supposed positive effects of urine and faecal deposition did not outweigh the negative impacts of grazing on nutrient cycling. This may be because grazing mainly occurred outside the growing season. Another reason may be that a substantial amount of nutrients were transported elsewhere by migrating reindeer and migratory birds (cf. Paper V).
Both fertilization and herbivory decreased the amount of microbial carbon in the soil organic matter, which indicates that the soil microbes were primarily limited by organic carbon. This result is in contrast to earlier tundra fertilization studies, where the microbial biomass remained constant but soil respiration increased on the fertilized areas (Jonasson et al. 1996, Michelsen et al. 1999, Schmidt et al. 2000).
However, in this study the soil organic layer was quite thin which indicates a low level o f organic matter accumulation, which is uncommon for tundra sites. We suppose that the decrease of total plant biomass by herbivores had negative effects on microbial population size in soils with low carbon availability, whereas in areas with high organic matter accumulation the soil carbon reserve may act as buffer against microbial carbon deficiency.
Summing up it can be concluded that herbivore exclosures had positive effects on soil microbial biomass and nutrient cycling mainly by favouring graminoids, which resulted in litter of higher quality and quantity.
Invertebrate responses to nutrient enrichment
Originally, the hypothesis of exploitation ecosystems was developed for endothermie herbivores (Oksanen et al. 1981). Nevertheless, the idea of cascading effects in food chains has been tested with subsets of invertebrate communities (Fraser and Grime 1997, 1998, Schmitz et al. 2000). Applying food chain theory on invertebrate communities as a whole causes some problems. Plants are the primary energy source in terrestrial systems, and the energy is transferred through successive trophic levels via consumptive processes (Oksanen et al, 1981). However, not all of the energy fixed in plants is consumed directly by herbivores, and in many systems a major part of the plant biomass becomes litter. This plant litter is the base of the detritus food chain (Polis and Strong 1996). In invertebrates, the detritus-based and the plant-based chains are tightly intertwined, because consumers of the higher trophic levels, such as carnivorous invertebrates and insectivorous birds, ignore the feeding history of their resources (Cousins 1987). Oksanen et al. (1997) proposed that invertebrate food webs in unproductive areas are characterised by a strong detritus-based energy shunt rather than being based on living plants. According to Oksanen et al. (1997), the availability of detritus-based prey increases the biomass of carnivorous invertebrates, and consequently, the population density of omnivorous birds such as passerines and waders. The resulting high predation pressure on invertebrate herbivores is supposed to be the reason why these are rare in such systems.
In paper V I investigated, together with Michael Schneider, the effects o f nutrient enrichment on an invertebrate community during two summers. We applied fertilization, litter removal and bird exclusion as factorial treatments. We assigned the food web to four trophic levels: plants and litter on the basic level, herbivores and detritivores on the second level, invertebrate carnivores preying upon both herbivores and detritivores on the third level, and on the top level birds feeding on invertebrates irrespective of trophic position. We assumed that fertilization increased the detritus resource and consequently the amount of carnivorous invertebrates, while litter removal decreased the detritus resource. If birds are dynamically unimportant for the invertebrate community we predicted a higher biomass of carnivorous invertebrates on the fertilized areas, while herbivores and detritivores should not respond. On the other hand, if birds are important, carnivores should not respond where birds have access, but they should increase on areas where birds have been excluded.
The biomass o f carnivorous invertebrates was significantly increased on the fertilized areas. The invertebrate food chain appeared to be strongly detritus-based.
Consumption of plant biomass by invertebrates was very low (0.021 % of the total aboveground biomass) and even lower on the fertilized areas, while fertilization had no effect on the biomass of herbivores. The amount of litter produced during one year was significantly higher on the fertilized areas and supposedly improved the energy resources of the detrital chain. Consequently, the biomass the invertebrate predators increased. As the herbivores were obviously not food limited, their biomass was supposedly kept down by predation by invertebrate carnivores. Litter removal had no effect on the invertebrate community.
The two study years were very different with respect to temperature and precipitation, which caused differences in size distribution, number, species abundance and biomasses of invertebrates between study years. During the first year, when the biomass of carnivorous invertebrates was higher, birds were dynamically important on the fertilized areas, where the biomass o f invertebrates was increased. The exclusion of birds significantly increased the biomass of invertebrate carnivores on the fertilized areas, but not on unfertilized ones.
Effects of season and nutrient enrichment on food plant quality
Carbon-based secondary compounds such as phenolics and condensed tannins are believed to play a major role in the defence of plants against herbivores in nutrient- limited plant communities (Coley et al. 1985). In tundra areas, where rodents are forced to make a living on food of comparatively low quality, food quality is crucial for the habitat choice of the rodents. Rodents have been shown to prefer plants with low fiber and phenolic but high nitrogen concentrations (Bergeron and Jodoin 1987, Hartley et al. 1995, Hjältén and Palo 1992, Lindroth 1988). In fertilization experiments the quality of plants as food for herbivores is improved, because fertilized plants have in general a higher nitrogen concentration than unfertilized ones (Shaver and Chapin 1980, Chapin and Shaver 1996, Paper IV). There are several theories predicting the changes of carbon-based secondary defence compounds in a given plant species after fertilization (Bryant et al. 1983, Herms and Mattson 1992, Jones and Hartley 1999). Common for all these theories is that they predict lower levels of total phenolics and condensed tannins after fertilization.
In my studies, rodents preferred the fertilized areas (Papers I, II and III ), and their densities showed clear annual fluctuations with high population densities during fall and low population densities during spring (Oksanen et al. 1999). The most abundant rodent overwintering on the study site are grey-sided voles (C.
rufocanus). Bilberry (V. myrtillus) is an important food plant for them, especially during winter (Kalela 1957, Hansson 1985, Hambäck and Ekerholm 1997). Arctic deciduous plants, investing in winter storage of nutrients and carbon, show large seasonal variations in nutrient and carbohydrate concentrations and, consequently, in food quality (Chapin et al. 1980). However, to my knowledge there are no studies that investigated seasonal variations of carbon-based secondary defence compounds including all seasons, and how this variation might affect the habitat choice of rodents. In Paper VI I analysed, together with Joakim Hjältén, the effects of fertilization on carbon, nitrogen, fiber, total phenolics and condensed tannin concentrations in bilberry, and how these chemical compounds interact and fluctuate during a whole year.
Fertilization improved the food quality of bilberry. The concentrations of total phenolics and condensed tannins in both leaves and stems were significantly lower, while nitrogen concentrations were significantly higher on the fertilized areas throughout the year. We found a very strong negative correlation between nitrogen concentrations and the amount of total phenolics in both leaves and stems. The allocation of carbon into total phenolics did not change during the year, but was highly dependent on nitrogen concentrations in the plant tissue, which showed considerable seasonal variations with high plant nitrogen contents during spring and the lowest contents during autumn. However, there was only a weak relationship
between carbon concentrations and the amount of total phenolics in leaves and stems. Although higher nitrogen concentrations decreased C/N ratios and phenolic concentrations as predicted by the carbon nutrient balance hypothesis (Bryant et al.
1983), it was primarily nitrogen availability that determined the amount o f carbon- based secondary compounds produced. This is consistent with the predictions of the protein competition model by Jones and Hartley (1999), assuming a phenylalanine substrate limitation for phenolic synthesis. Phenylalanine is an important precursor for the synthesis of both protein and phenolics and, according to this model, an increased availability of nitrogen favours the synthesis of proteins instead of phenolics.
Bilberry shoots had the lowest food quality, with high concentrations of phenolics and fiber but low nitrogen concentrations, during autumn and winter, i.e.
at times of high energetic requirements o f overwintering voles (Hammond and Wunder 1991). However, during spring, when vole densities were generally low, bilberry was of high food quality because of high nutrient contents and low concentrations of digestible fiber, phenolics and tannins. The low food quality during autumn and winter probably contributed to the low winter survival of voles on the study area (Oksanen et al. 1999).
Herbivores may indirectly affect the quality of their food plants by their effects on soil nutrient mineralisation rates and, consequently, on plant nutrient availability.
In the study area the herbivores significantly decreased the concentration of nitrogen in the plants (Paper IV). By this, vertebrate herbivores may indirectly cause a response of increased phenolic concentration and thereby decrease the quality of their food plants.
Conclusions
The results of my thesis show that the plant community investigated is exposed to a strong top-down control by mammalian herbivores. On the fertilized and grazed areas the aboveground biomass of the vascular plant community did not increase compared to unfertilized areas. However, the productivity of the plant community was clearly nutrient-limited. During the eight years of the experiment, on the fertilized areas plant biomass continued to increase inside the herbivore exclosures, indicating that the plant community still not had reached equilibrium when the experiment was terminated, and that the difference in plant biomass between the grazing treatments may be even more pronounced in a few years. These results are in agreement with the predictions by Oksanen et al. (1981) made for moderately productive two-link systems.
In my study a comparatively low density of mammalian herbivores that grazed outside the growing season was sufficient to control the biomass of a heterogeneous plant community. Reindeer and rodents had also important indirect effects for the plant community by decelerating soil nutrient cycling and soil microbial activity.
Grazing decreased the nitrogen storage in the aboveground plant biomass. As the amount of carbon-based secondary defence compounds in bilberry increased with decreasing nitrogen concentrations in the plant tissues, grazing might indirectly increase the amount of carbon-based secondary defence compounds in the plants,
resulting in litter of low quality, which decreases nutrient cycling. This effect may be accelerated by the herbivore impact on plant species composition. Graminoids, which contained the highest nitrogen concentrations in their tissues, increased rapidly on the fertilized areas, but their abundance was significantly where herbivores had access. Both plants and soil microbes are nutrient-limited, but because soil microbes appeared to be carbon-limited as well, plants are superior competitors for the available nutrients
Classic linear food chains, built of plants, herbivores and carnivores, are not applicable to explain invertebrate food webs. Invertebrate carnivores were detritus- based and received their energy indirectly from the litter via soil microbes and detritivores. Apparent competition between detritivores and invertebrate herbivores, mediated by carnivorous invertebrates predating on both of them, is supposed to keep the densities and grazing pressure of herbivores low. Grazing damage by invertebrates was not dynamically important for the plant community.
In essence, it can be said that the physical environment is not the only factor that has to be taken into account for understanding responses in arctic tundra plant communities to environmental changes. Mammalian herbivores can be an important factor in structuring tundra plant communities, although their densities are comparatively low and although grazing occurs mainly outside the growing season.
Mammalian herbivores affect the plant community not only directly, but may also have important indirect effects, limiting even more the nutrient availability for plants in this harsh environments.
Acknowledgements
I thank Lars Ericson, Jon Moen and Michael Schneider for their valuable comments on this summary. This thesis was funded by Ruth and Gunnar Björkmans Minnesfond, Lars Hiertas Minnes Stipendiefond, Ebba and Sven Schwartz Stiftelse, JC Kempes Minnes Stipendiefond and the Schwedish Natural Science Research Council (to L. Oksanen).
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Finally...
When I was an undergraduate student in Würzburg I dreamed about working in the tropics and planned to do my PhD-thesis in Africa. However, the journeys through life take sometimes very unpredictable ways. Instead of moving to the warm tropical South, I started my thesis in the cold far North. I do not regret it! Working in Joatka was very exciting too, and the millions of mosquitoes have one big advantage, they do not spread malaria. There are many people who have made my time in Joatka and Umeå pleasant, interesting and unforgettable. I am grateful to all of you!
First of all I want to thank my supervisors Lars Ericson and Lauri Oksanen. Lasse for making it possible to start my PhD work in Umeå and for all his support and fruitful discussions during the years. Lauri for offering me such an interesting topic to work on and for giving me the freedom to follow up my own ideas and projects.
His unending supply of visions, theories and ideas has been very inspiring.
I am indebted to Jon Moen for all his scientific and mental support. I am not sure if I ever would have finished my thesis without him. Thank you to the Joatka group:
Tarja, Peter, Pere, Maano, Johan, Oliar and Jonas for your discussions, and your help in Joatka whenever it was needed.
Thank you Sari for getting interested in the soil microbes on my study area, and Jocke Hjältén for sharing your knowledge about the chemical plant analyses with me.
All the fieldwork would not have been possible without all the field assistants from Sweden, Germany and Estonia during the summers. Thank you to all of you!
Several students from Würzburg chose to carry out their practical part of an ecology course in Joatka and helped me during my fieldwork. Thanks to all of them, and to their supervisor Dieter Mahsberg for helping me to organise this.
Without the sporty action of Torgny L. and Peter E. I do not know how we would have managed to bring all the equipment for the insect project up to my field site.
Maarja and Kristjaan helped me taking plant samples during several years. The tireless assistance of Patrik J., Åsa G. and late-riser Jonas R. enabled me during my last field season to finish several projects.
I owe many thanks to Helge and Brita Romsdal and their family for the support and hospitality in Joatka. Oskar Eriksen played an important role with his technical support and in helping me with the transport of all that fertilizer.
I am indebted to the technicians at the department, the late Gunnar Borgström and Stickan for constructing the traps for the insect project. I thank Gun-Britt, Yngve, Sussi and Ylva for their professional help with all practical and bureaucratic questions.
And of course thank you to all my botanical and zoological colleagues in Umeå:
Lennart P. for reading and giving comments on my manuscripts although I am not
