Grazing and the geographical range of seaweeds
The introduced Fucus evanescens and the newly described Fucus radicans
Licentiate thesis by
Helena Forslund
Supervisors:
Lena Kautsky and Ove Eriksson
Plants & Ecology
Plant Ecology 2009/5
Department of Botany
Stockholm University
Plants & Ecology Plant Ecology
Department of Botany Stockholm University S-106 91 Stockholm Sweden
© Plant Ecology ISSN 1651-9248
Printed by Solna Printcenter
Cover: Fucus species. Photo by Helena Forslund
3 Summary
Along the coast of temperate oceans brown algae of the genus Fucus form dense stands on rocky shores and are keystone species of the coastal ecosystem. These large seaweeds are perennial and function as substrate for many sessile marine organisms, provide shelter for fauna and juvenile fish, and are food source. A number of abiotic (e.g. wave-exposure, salinity and substrate) and biotic (e.g. herbivory and competition) factors structures these communities and determines the abundance and composition of fucoids at each specific site.
Earlier studies have shown that herbivores may reduce growth of fucoids, thus affecting their distribution, and at high densities eliminate the species from previously occupied sites. In my thesis I focused on investigating herbivore-seaweed interactions and whether such interactions could influence the geographical range limits of Fucus species. A set of laboratory bioassays and a field survey were conducted (1) to investigate the resistance to grazing by a generalist gastropod between introduced (to Sweden) and native (Iceland) Fucus evanescens (Paper I), (2) to study the distribution pattern of F. radicans and F. vesiculosus along the Swedish coast and specifically the southern limit of F. radicans, (3) to examine the abundance of herbivores in these two species, and (4) to test the hypothesis that Idotea baltica may contribute to restrict F. radicans to the Bothnian Sea (objective 2-4; Paper II). Fucus evanescens, a species that was introduced to the Swedish coast about 100 years ago, was found to be more resistant to grazing by L. littorea compared to F. evanescens from the native Icelandic populations. It was also shown to contain a higher amount of phlorotannins; a putative chemical defence to herbivory. This indicates that development of resistance to herbivory could be important for a successful introduction and survival in a new range. No gradual change in the proportion, measured as % cover of either F. radicans or F. vesiculosus was found inside the range of F.
radicans and its southernmost limit was abrupt without any corresponding abrupt change in any abiotic factor, e.g. salinity. Herbivores, i.e. Idotea spp., Gammarus spp. and Theodoxus fluviatils were found to be more abundant in F. radicans than in F. vesiculosus thalli indicating a habitat preference for F. radicans. Further, Idotea baltica, whose range only overlaps with that of F. radicans in the south, was shown to prefer F. radicans over F.
vesiculosus, possibly due to its lower content of phlorotannins. Based on these findings I propose that Idotea species may contribute in restricting the southern range of F. radicans, although further experiments, especially regarding competition with the larger F. vesiculosus need to be performed. In conclusion, biotic interactions e.g. the ability of to resist herbivore grazing by e.g. high phlorotannin content or having a structure less attractive as habitat to herbivores may be of importance in determining the geographic range of fucoids.
4 Sammanfattning
Längs kusterna i de tempererade haven bildar brunalger av släktet Fucus täta bestånd på klippiga stränder och är ofta nyckelarter i kustekosystemen. Dessa tångarter är fleråriga och utgör substrat för många fastsittande organismer, ger skydd åt små rörliga djur och fiskyngel, samt utgör föda för betare så som gastropoder, amphipoder och isopoder. Faktorer som vågexponering, bottentyp, salthalt, näringshalter, bete och konkurrens strukturerar tångsamhällen och avgör hur vanlig varje tångart är på en viss lokal. I min avhandling har jag fokuserat på interaktionen mellan betare och tång, samt hur viktig denna interaktion är för att avgöra den geografiska utbredningen av tångarter. Tidigare studier har visat att betare kan minska tillväxten hos tång och på så sätt påverka dess utbredning. I höga densiteter kan de beta ner hela bestånd av tång så att den försvinner från lokaler där de tidigare vuxit. Resistens mot bete hos Fucus evanescens, ishavstång, som är introducerad till Skagerrak, Kattegat och sydvästra Östersjön och inhemsk i norra Atlanten och norra Stilla Havet undersöktes i betesförsök (Artikel I). En betare, generalisten Littorina littorea, strandsnäcka, som är inhemsk i Sverige, dit F. evanescens har introducerats, föredrog att äta F. evanescens från Island där den är inhemsk, framför F. evanescens från Sverige. Det här skulle kunna tyda på att ett välutvecklat försvar är viktigt för att alger som blir introducerade till nya områden ska kunna etablera sig i det nya området. Jag undersökte även utbredningen av den nyligen beskrivna tångarten Fucus radicans, smaltång (Artikel II). Resistensen mot betare hos F.
radicans jämfördes med resistensen mot bete hos F. vesiculosus, blåstång, som växer tillsammans med F. radicans, genom att undersöka preferensen mellan de två arterna hos Idotea baltica, tånggråsugga (Artikel II). Det fanns ingen gradient i förekomsten av F.
radicans eller F. vesiculosus inom F. radicans utbredningsområde. Istället observerades en ganska abrupt gräns för utbredningen av F. radicans i söder. Eftersom I. baltica, vars utbredning överlappar F. radicans utbredning i söder, föredrog att äta F. radicans framför F.
vesiculosus, skulle F. radicans utbredning kunna påverkas av I. baltica. Både I. baltica och två andra betare, Gammarus spp. och Theodoxus fluviatilis, var vanligare i F. radicans än i F.
vesiculosus i plantor insamlade i fält. Det innebär att de vanligaste betarna, även i fält, föredrar att uppehålla sig i F. radicans och antagligen konsumerar mer av F. radicans.
Slutsatsen från de båda studierna är att betare och tångens försvar mot bete har potentialen att påverka utbredning av olika tångarter.
5 List of papers
The thesis is based in the following papers, referred to by their roman numerals:
I. Forslund, A. H., Pavia, H. and Wikström, S. A., Higher resistance to herbivory in introduced compared to native populations of the seaweed Fucus evanescens.
Manuscript
II. Forslund, A. H., Eriksson, O. and Kautsky L., Grazing and the geographic range of the recently described Fucus radicans (Phaeopyceae). Manuscript
6 Introduction
The brown seaweeds in the genus Fucus are perennial with a broad thallus and can grow up to a meter in length. They commonly form dense stands in the intertidal zone of most rocky temperate coasts (Lüning 1990; Graham & Wilcox 2000). These seaweed communities play an important role in costal ecosystems by providing substrate and shelter for many organisms as well as being a food source for others (Carr 1989; Arrontes 1999; Wikström & Kautsky 2007).
The distribution of seaweeds is commonly thought to mainly depend on abiotic factors, the most important factors being temperature and the availability of hard bottom substrate (Lüning 1990). Salinity also affects the range of many seaweed species since sexual reproduction is negatively affected by low salinities (Khfaji & Norton 1979; Malm et al.
2001; Wikström et al. 2002). On a local scale, biotic interactions can play a role in determining the distribution of seaweeds i.e. which species that are present at which sites in a region (Engkvist et al. 2000; Jonsson et al. 2006) and grazing, on kelp by sea urchins, have been found to affect distribution at large scales (Chapman & Johnson 1990; Sivertsen 2006).
Herbivores that graze seaweeds can affect the abundance and distribution of seaweeds both directly by grazing and indirectly by altering the competitive outcome between seaweed species in the community (Schaffelke et al. 1995; Engkvist et al. 2004; Sivertsen 2006). In many terrestrial habitats herbivores are believed to affect the introduction of plants either by the specialized herbivores failing to recognise them as suitable host (i.e. the Enemy Release Hypothesis, e.g. Keane & Crawley 2002) or through generalist grazers preferring the introduced species since they lack an effective defence to herbivores in the new range (Colautti et al. 2004). Selective grazing by generalist herbivores of brown algae are correlated to the concentration of phlorotannins (Geiselman & McConnell 1981; Denton & Chapman 1991; Wikström et al. 2006), a group of chemicals that are unique to this group (Ragan &
Glombitza 1986). However, the function of phlorotannins as herbivore defence is disputed, and phlorotannins have also been shown to have many other functions (reviewed by Amsler
& Fairhead 2006). The structure of the seaweed may also determine herbivore preference, since herbivores would choose a habitat that provides protection, e.g. by a complex and branched structure. Further, if the herbivores are generalists they are likely to consume the seaweed in which they live.
7
The Swedish coast has a strong salinity gradient, with salinities varying between 30-20 psu on the west coast, rapidly decreasing below 15 psu at the entrance to the Baltic Sea, 10-5 psu in the Baltic Proper, 5-3 psu in the Bothnian Sea and as low as 2 psu in the Bothnian Bay. At the west coast of Sweden (Paper I) the tide is approximately 0.2 m and often obscured by water level fluctuations caused by air pressure. These weather driven changes in water level can be in the magnitude of 1 meter and last for several weeks causing the intertidal area to be highly variable. In the atidal Bothnian Sea (Paper II) these water level changes, in combination with ice scour and lack of other competitors, cause F. radicans and F.
vesiculosus to grow submerged at 0.5-10 m depth, with highest densities at 1-4.5 m depth (Paper II). While on the west coast the fucoid community occupies a narrow belt close to the surface and might be exposed during long periods of low water levels.
Fucus evanescens is circumpolar in the arctic seas (Powell 1957), where it usually forms dense stands in the intertidal. It was introduced to the North Sea in the last century, with the first record in Oslofjorden, Norway, in the end of the 1900th century (Simmons 1989) and the first record on the Swedish west coast in 1924 (Hylmö 1933). Lately it has spread south into the south-western parts of the Baltic Sea (Schueller & Peters 1994). In some parts F.
evanescens has become abundant (Bokn et al. 1992), but in most places it is restricted to habitats such as harbours where other fucoids are scarce (Wikström et al. 2002). It has been previously shown that F. evanescens hosts a less abundant and less diverse community of epiphytic algae than the native fucoids and thus a less diverse and abundant community of free-living invertebrates such as amphipods, isopods and gastropods (Wikström & Kautsky 2004). Previous studies have also revealed that F. evanescens is grazed less than the co- occurring fucoids in the new range, while it is the preferred food choice in the native range corresponding to phlorotannin levels (Wikström et al. 2006).
In large areas of the Baltic Sea F. vesiculosus (L.) is the only fucoid. In the northern parts, in the Bothnian Sea, Wærn (1952) described two morphs of F. vesiculosus; the common morph and a smaller, bushier morph with many branches, lacking the vesicles that are typical for F.
vesiculosus. The dwarf morph was believed to be caused by salinity stress, that commonly cause dwarfism (Remane 1971; Kautsky et al. 1990), but it has also been suggested that genetic studies are needed to settle the taxonomic status of this morph (Luther 1981). Studies of the morphological and genetic differences between the two morphs, found growing in mixed stands, lead to the description of the dwarf morph as a separate species, Fucus radicans
8
(Bergström et al. 2005). In Sweden, F. radicans has so far only been reported from the coast of the Bothnian Sea, although it can grow in the slightly higher salinities of the Baltic proper (pers. obs. from keeping F. radicans in ambient seawater from Askö, at 6-6.5 psu, Paper II).
Further little is known about the ecology of F. radicans, e.g. grazing resistance and interactions with associated flora and fauna, (Råberg & Kautsky 2007) and studies are thus highly needed to understand what mechanisms are involved in regulating the distribution of F.
radicans.
Aims
The overall aim of my thesis is to examine the importance of herbivores and resistance of seaweeds to herbivory for the distribution of seaweeds. This has been done in two systems, one with an introduced seaweed and one with a recently described seaweed species, where little is known about the ecology and herbivore interaction. The aims for the two studies were:
Paper I:
-To test whether the reluctance to consume F. evanescens in the new range depended on resistance to herbivory of F. evanescens or the failure of herbivores to recognize it as suitable food because of its novelty.
Paper II:
-To examine the geographic range and abundance of F. radicans, in comparisons to F.
vesiculosus.
-To study the abundance of herbivores in the field on F. radicans and F. vesiculosus.
-To compare the palatability of F. radicans to that of F. vesiculosus.
-To study whether the range of F. radicans could be affected by selective grazing of herbivores.
Material and Methods
Study sites
Material for the bioassays with F. evanescens (Paper I) were collected from two sites in Iceland, where F. evanescens is native and two sites on the Swedish west coast where it has been introduced (Wikström et al. 2002). The bioassays were performed at Tjärnö Marine
9
Biological Laboratory (N 65°37.07; E 12°31.22); close to the collection sites (Fig. 1). For the bioassay with F. radicans and F. vesiculosus (Paper II) material were collected in Öregrund (southern Bothnian Sea, site 3 in Fig. 6), and then brought to the Askö Laboratory (N 58°
49.4’; E 017° 38.2) (Fig. 1). The survey of F. radicans and F. vesiculosus (Paper II) was performed at 16 sites on the Swedish Baltic Sea coast, with two sites south of F. radicans range and the northernmost site comprising one of the northernmost populations of fucoids known in Sweden (Pekkari 1973; Lüning 1990; Fig. 6).
Study species
Fucus evanescens
The morphology of F. evanescens is variable, but the species is described as being large with broad fronds, midrib indistinct in the apical parts of the fronds and receptacles flattened and broad, clearly separated from the rest of the thallus, with the shape of the receptacles as the best characteristic (Powell 1957). Fucus evanescens is monoecious and self-fertile (Quatrano 1980), with both male and female gametes released from the same individual. Thus, only one
N
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B
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500 0 500 Kilometers
A
189 8
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See Figure 6
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Figure 1. Northern Europe with A) the area in Iceland, the native range, where F. evanescens was collected (Paper I), B) the Tjärnö Marine Biology Laboratory in Sweden, the new range, where F. evanescens was collected (Paper I), and C) the Askö Laboratory where bioassays with F. radicans and F.
vesiculosus were performed (Paper II). The square is shown in more detail in Fig 6, with the sites of the survey of F. radicans and F. vesiculosus marked (Paper II).
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plant is necessary to produce offspring and establish a new population upon introduction. The north Atlantic, north Pacific and Arctic oceans are the native range of F. evanescens (Powell 1957). Reproduction fails in salinities lower than 12 psu and germlings cannot grow in lower salinities (Wikström et al. 2002). Epiphytic seaweeds in the new range are less common and less diverse on F. evanescens than on the native F. vesiculosus (Wikström & Kautsky 2004).
Co-occurring fucoid species in the new and native range of F. evanescens are F. vesiculosus, F. serratus (L.), F. spiralis (L.) and Ascophyllum nodosum (Le Jol.). In the native range F.
ceranoides (L.) is also present (Lüning 1990).
Fucus radicans
The morphology of F. radicans is similar to that of F. vesiculosus, the only co-occurring fucoid, but it is smaller and always lacks vesicles. The fronds are rarely wider than 5 mm and thallus usually shorter than 26 cm. It has few chryptostomata and is richly branched with many adventitious branches (Wærn 1952; Bergström et al. 2005). These adventitious branches can reattach and is the mode of asexual reproduction. Since F. radicans has the, for fucoids, rare capacity to reproduce asexually, it is largely clonal, with one genotype making up approximately 80 % of the sampled fronds at the two studied sites in Tatarenkov et al. (2005) that corresponds to site 3 and 16 in Paper II. However, F. radicans is dioic and has sexual organs too, and preliminary results (pers. Obs. H. Forslund) show that they are capable of producing viable offspring. It has so far not been found outside the Baltic Sea, and might be endemic to the Baltic Sea. In a recent study Pereyra et al. (2009) suggests that F. radicans has evolved in the Baltic Sea and as a species probably is less than 1000 years old (Pereyra et al.
2009). Only one previous study has looked at the ecological interactions of F. radicans. This study shows that F. radicans supports a more diverse and abundant community of associated fauna than filamentous algae (Råberg & Kautsky 2007).
Fucus vesiculosus
Fucus vesiculosus is common on temperate shores throughout the northern Atlantic and occupies the midsection of the fucoid zone. It is one of the most tolerant fucoid species, extending its range into the high temperature of northern Africa and to the low salinities of the Baltic Sea (Lüning 1990). The morphology of F. vesiculosus is very variable, depending on factors such as wave exposure and salinity. For example the vesicles that are typical of F.
vesiculosus are lacking in large parts of the Baltic Sea, and at wave exposed sites, while in sheltered bays they might have many vesicles between dichotomies instead of one pair
11
(Burrows & Lodge 1951; Wærn 1952). The gametes and the reproductive success of the diocious F. vesiculosus is negatively affected by reduced salinities (Serrão et al. 1996) as are the growth rate (Nygård & Dring 2008 and references therein).
Herbivores in bioassays
Both Littorina littorea (L.) and Idotea baltica (Pallas) are native Swedish generalist grazers, known to consume fucoids in such large quantities that they effectively decrease growth (Engkvist et al. 2000; Toth et al. 2007). Since L. littorea is absent from Iceland, and thus has no evolutionary history with F. evanescens it was chosen to test the preference of a generalist grazer (Paper I). In the Baltic Sea Idotea baltica, that prefers fucoids over other seaweeds (Jormalainen et al. 2001), is the major grazer of fucoids since the major grazers in temperate marine communities, such as L. littorea, are not able to survive at the low salinity of the region. Thus I. baltica was used as grazer in the bioassay with F. radicans and F. vesiculosus (Paper II). Both herbivore species were collected in natural Fucus stands close to the field stations where the respective bioassays were run.
Bioassays
In both papers, bioassays with a paired designed was used to test for herbivore preference.
One tip from one thallus was used in the control and another tip from the same thallus was used in the grazing treatment, and paired with tips from a fucoid from the other population / species. The bioassays with F. evanescens (Paper I) had an experimental setup with separate containers for the control and the grazing treatment with five L. littorea. The containers had running ambient water (for temperatures and salinities see paper I) in a constant temperature room. In the 2005 10 replicates were run for 3 days and in 2006 12 replicates were run for 13 days (se material and methods in paper I for a discussion of the different running times). An additional bioassay with pulverized F. evanescens incorporated in agar (Paper I) was also run, to eliminate morphology as a possible cause for herbivore preference. The bioassay with F.
radicans and F. vesiculosus (Paper II) had an experimental setup with one container separated by a fine mesh into two compartments, one containing the control algae, and one containing four I. baltica and algae for the grazing treatment. Each compartment had two mesh
“windows” to allow water circulations as the containers were hung at 0.5-1.5 m depth from a floating dock placed over a fucoid belt. The experiment was left in the field for five days and five replicates were used.
12 Phlorotannin quantification
Pieces of F. evanescens, F. radicans and F. vesiculosus from the bioassays were analyzed for phlorotannin content. Approximately 0.1 g wet weight were removed and frozen. The pieces used came from the young thallus; midribs and damaged tissue were excluded. The frozen algal parts were then freeze-dried and pulverized. The phlorotannins were extracted with 60%
acetone for an hour in room temperature. After the extraction, the samples were centrifuged and evaporated in vacuo to remove the acetone, leaving an aqueous solution. Samples were then filtered and diluted to a known volume and analyzed colorimetrically with the Folin- Ciocalteus analysis (Van Alstyne 1995). Phloroglucinol (Merck art 7069) was used as standard.
Inventory of the distribution of fucoids and number of associated herbivores (Paper II)
At 16 sites along the Swedish Baltic coast (Fig. 1) 15 randomly placed 1m2 square were surveyed. The squares were placed within the fucoid belt (defined as the depths where coverage was 25% or higher) at 1.1±0.1 m to 4.5±0.3m depth (average depth ± SE; n=9). In each square the percentage cover of F. radicans, F. vesiculosus, and filamentous algae were recorded. At each site a water sample was collected to measure the salinity. To collect and record the abundance of herbivores three Fucus thallus of each species were collected and the number of individuals of Idotea spp, Gammarus spp, Theodoxus fluviatilis (L.), was counted and the wet weight of the fucoids was measured. Idotea spp. is mainly I. baltica but probably a few I. viridis (Slabber) and Gammarus spp. probably mainly G. oceanicus (Segerstråle) and G. zaddachi (Sexton), but likely a few other species too.
Statistical methods
Difference in grazing in the bioassays was tested for with a paired t-test according to the method described by Peterson and Renaud (1989). Spearman’s rank correlation was used to test for a gradient in cover for Paper II. Data on the abundance of herbivores were transformed appropriately when necessary and then analyzed in a nested ANOVA, with site as the error term. In Paper I a two-way ANOVA with region of origin (Sweden/Iceland) as fixed, and year, as random factor was used to test for differences in phlorotannins between populations, while in Paper II a t-test was used to test for differences in phlorotannin concentrations between species. In Paper I STATISTICA 6.0 was used for statistical test and in Paper II R 2.6.2 was used.
13 -0.5 -0.4 -0.3 -0.2 -0.1 0.0 0.1 0.2
Grazing Control
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Change in wet weight (g) 2005
Results and discussion
Paper I
The generalist herbivore, L. littorea, showed a clear preference for algae from the native region (Iceland) in the bioassay in 2005 (t9 = -6.380; p < 0.001; Fig. 2), but no significant preference for algae from either region in 2006 (t11=-1.920; p = 0.0811; Fig. 2). However, in the bioassay with agar, in 2006, L. littorea showed a preference for agar pieces containing algal material from the native region (t19= -3.177; p = 0.005). This confirms that the generalist grazer, L. littorea, in the new range of F. evanescens willingly consumes the introduced species. Thus, as expected since the community is dominated by generalist herbivores, the Enemy Release Hypothesis (Keane & Crawley 2002) is not applicable to this system. The preference instead correlates to a chemical propriety of the algae, as shown in the bioassay with agar. The preference of the generalist grazer is for algae from the range with low levels of phlorotannins (Table 1, Fig. 3). However, I cannot rule out that some property that correlates with phlorotannins, e.g. nutrient content, or other chemical compounds, is the trait that causes the herbivore preference, since no direct test of the effect of phlorotannins was made.
The results of this study is supported by previous studies that have shown that F. evanescens is preferred over co-occurring fucoids in the native range (Barker & Chapman 1990; Denton
& Chapman 1991; Wikström et al. 2006) while in the new range it is less preferred compared to the native fucoids (Schaffelke et al. 1995; Wikström et al. 2006). Wikström et al. (2006) Figure 2. The change in wet weight (g) of the new (Sweden) and native (Iceland) region of F.
evanescens during 3 days in 2005 (n=10) and 13 days in 2006 (n=12)(Paper I). Error bars show SE.
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also showed that F. evanescens in the new range had higher defence levels than the co- occurring fucoids, while in the native range it has the lowest levels of defence. For seaweeds that are introduced to communities dominated by generalist enemies it is probably vital to be well defended or to be able to increase the defence to establish and be successful, since it has been shown that generalist grazers can affect the growth and fitness of seaweeds (Engkvist et al. 2000; Toth et al. 2007, Jormalainen & Ramsay 2009). Whether the increase in defence of F. evanescens in the new range compared to the native range is induced by grazing (Toth &
Pavia 2007), or some other factor e.g. by nutrient levels, by salinity, or selected for either by grazing or by some abiotic factor is not clear. My study also shows that traits, such as resistance to herbivory, dispersal, and growth, which might be important when trying to estimate which seaweeds that could be successfully introduced, can differ between the native and new range. Thus, it is important to look at how variable and plastic these traits are, when predicting which seaweeds could be successfully introduced to new ranges.
0 2 4 6 8 10 12 14 16
2005 2006
Phlorotannin sas % of dry weight
Iceland Sweden
Figure 3. Phlorotannin concentrations as % of dry weight of F. evanescens from the native (Iceland) and new (Sweden) region (n=19) (Paper I). Error bars show SE.
df MS F p
Region 1 621.031 188.163 <0.0001
Year 1 5.366 1.626 0.206
Region x Year 1 92.260 27.953 <0.0001
Error 72 3.300
Table 1. ANOVA table of the phlorotannin levels of F. evanescens from the native and new region in 2005 and 2006 (Paper I).
15 Paper II
I was able to show that F. radicans was preferred as food compared to F. vesiculosus in a bioassay with the common herbivore I. baltica (t = 6.92, df = 4, p-value = 0.002; Fig. 4).
Fucus radicans (7.7 ± 0.3 SE % dry weight) also had significantly lower levels of phlorotannins compared to F. vesiculosus (9.9 ± 0.4 SE % dry weight; t = -4.15, df = 28, p <
0.001).
In the survey Idotea baltica was more abundant in F. radicans than in F. vesiculosus (p<0.001), as were the two other most common grazers Gammarus spp. (p= 0.041) and T.
fluivatilis (p=0.012, Fig. 5). Previous studies have shown that herbivores can affect the fitness and growth of seaweeds (Engkvist et al. 2000; Toth et al. 2007) and affect the competitive outcome between fucoid species (Schaffelke et al. 1995; Engkvist et al. 2004). Since the geographic range of I. baltica only overlaps with the southern range of F. radicans (Fig. 5A), the preference of I. baltica in combination with increasing competition from F. vesiculosus that grows faster in higher salinities (Nygård & Dring 2008) could limit the southern range of F. radicans. The other two herbivores have ranges that overlap completely with F. radicans (Fig. 5 B-C) so it is not likely that they limit the southern range of F. radicans. On the other hand they may locally affect the two Fucus species by selective grazing. Within the geographical range of F. radicans there was no gradient in cover of either F. radicans (p=0.84, n= 14), or the co-occurring F. vesiculosus (p=0.66, n=14), or filamentous algae (p=0.86, n=16; see Paper II). Instead it seems to be a rather abrupt limit to the southern range of F. radicans, as abundance at each site is varying independent of salinity and north-south gradient. This suggests that factors other than grazing might be involved in limiting the
-0.06 -0.05 -0.04 -0.03 -0.02 -0.01 0 0.01 0.02
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weight change per day ( g ww)
F. vesiculosus F. radicans
Figure 4. Weight change (g wet weight) in a bioassay with F. radicans and F. vesiculosus with the grazer I. baltica, run for five days (n=5) (Paper II). Error bars shows SE.
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southern range of F. radicans. One such factor may be reproduction. Since F. radicans is clonal with a female dominance (Serrão et al. 1999; Tatarenkov et al. 2005) sexual reproduction is not likely as a mean for dispersal. Asexual reproduction is the most likely mean for dispersal. Thus more information about factors that affect the asexual reproduction is needed to understand what limits the southward dispersal of F. radicans.
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F. vesiculosus F. radicans
Figure 5. The average number of A) Idotea spp., B) Gammarus spp. and C) Theodoxus fluviatilis per g wet weight algae. Error bars shows SE.
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Densities of I. baltica at site 3 and 4 are in the range of 80 animals per 100 g wet weight seaweed, the densities that in the study by Engkvist et al. (2000) reduced the biomass of F.
vesiculosus by 50% in 15 days. Even at lower densities, I. baltica, e.g. the ~20 animals per 100 g ww found at site 5-7, could prevent increase in biomass according to Engkvist et al.
(2000). Thus I propose that since selective grazing by I. baltica of F. radicans was observed Figure 6. The 16 sites investigated in the survey in the
Bothnian Sea. Circles shows the percentage cover of F.
radicans (black) and F. vesiculosus (white) as percent of total Fucus cover. Numbers at circles refers to site number as referred to elsewhere. Numbers at each site indicate the salinity in psu. Site 3 and 4 both had a salinity of 4.9 psu.
Stars indicate sites where no fucoids were found. The location of the Bothnian Sea is indicated by the square in Fig 1.
18
in the bioassay, grazing could affect the population negatively and could contribute to limiting the southern range of F. radicans. Gammarus spp. were even more abundant than I. baltica in the survey, and they were also found in higher numbers on F. radicans than F. vesiculosus.
Preliminary results show that Gammarus spp. also prefer to graze F. radicans (pers. obs.), and further studies will be necessary to understand the impact of Gammarus spp. on the range of F. radicans. It is also possible that T. fluviatilis may affect the competitive relation between F. radicans and F. vesiculosus trough selective grazing. However T. fluviatilis only has an effect on juvenile fucoids smaller than 1 mm (Malm et al. 1999), and it is not known whether they too have a preference for F. radicans. Since F. radicans relies on asexual reproduction, with adventitious branches that commonly are several mm in size, I suggest that the dispersal of F. radicans may be less affected by T. fluviatilis than by I. baltica and Gammarus species.
Conclusions and further studies
In both studies the herbivores showed a preference for the species (Paper II) or population (Paper I) that had the lowest levels of defence, measured as concentration of phlorotannins.
Previous studies have shown that grazers can affect the distribution of seaweeds at smaller scales trough grazing (Schaffelke et al. 1995; Engkvist et al. 2000; Jonsson et al. 2006). Based on the fact that grazing is known to affect seaweeds negatively and the results presented in Paper II, I propose that the geographic range of seaweeds may also be affected by grazing, especially if the herbivores are generalists. To investigate the effect of herbivores and other biotic interactions, transplant studies where e.g. F. radicans are moved and placed in the field, outside of its present range, should be performed. If herbivory are limiting the southern range of F. radicans, as is suggested by the results presented here, the transplanted seaweeds would be grazed down and eventually die if moved outside the present range. If competition from the larger F. vesiculosus, trough shading and whip-lashing effects, similar as shown for e.g.
filamentous algae by Kiirikki (1996) is contributing to limit the southern range, F. radicans transplanted into F. vesiculosus stands would be eliminated faster than if they were transplanted to areas where F. vesiculosus has been removed.
Similarly, reciprocal transplant experiments would be needed to further investigate the development and consequence of herbivore resistance for the successful introduction of F.
evanescence. However, transplant experiments are not possible because of the risk of introducing new fucoid species or populations with different genetic setup, or associated flora
19
and fauna. Thus, mesocosm experiments where natural conditions and communities are mimicked would be the next step in understanding the importance of the herbivore-seaweed interaction. Further, studies that actually proves that phlorotannins, and not other factors, e.g.
galactolipids (Deal et al. 2003) or another unknown component (Kubanek et al. 2004) that usually correlate with them, would be useful to analyse to confirmation the present theories.
In conclusion the two studies presented here shows that, in addition to abiotic factors, biotic interactions can be important in determining the large scale geographical ranges of seaweeds.
These interactions thus need more attention, since so far, the distributions of seaweeds are mainly explained by abiotic factors such as temperature and salinities.
20 Acknowledgments
First of all I would like to thank my supervisors, Lena Kautsky for sharing love for seaweeds and an amazing amount of knowledge about fucoids with me, and Ove Eriksson for friendly support and enthusiasm for science. I would also like to thank Sofia Wikström who always helps me to remember how interesting my research is and who always let me think for myself.
I would like to thank the following persons who has somehow helped me in my work: Henrik Pavia and Gunilla Toth for welcoming me to Tjärnö and teaching me about phlorotannins.
Swantje Enge and everyone else on Tjärnö for making my time there fun and not so lonely.
Jessica Honkakangas and Tomas Meijer who made the survey fun and fast. Annika Lindström for friendship and help with field and laboratory work. Peter Hambäck for statistical advice.
The staff at Askö, not only for all the help I have gotten, but also for being so friendly and always having time for a few words. Without you and other researchers at Askö I would have gone crazy. PhD students and others at Botan, I thank you for fun discussions about statistics, ecology and life.
I would also like to thank my family: Kerstin Juneberg, my mother, you always believe in me, no matter what strange directions I have chosen, and you support me in every way; ranging from dinner when I have a lot of work, making me run, or coming to Askö with me to clean Fucus. I think I have my dad, Eric Forslund, to thank for my interest in natural science and the curiosity that drives research, you introduced me to the world of research trough playful snail experiments at an early age – and now this is part of my work! Tomas, I want to thank you, but can’t really come up with any description that could fit in a few sentences so I thank you simply for taking part in every aspect of my life and for help in keeping dreams alive.
21 References
Amsler C.D. & Fairhead V.A. (2006). Defensive and sensory chemical ecology of brown algae. In: Advances in Botanical Research, 43:1-91.
Arrontes J. (1999). On the Evolution of Interactions between Marine Mesoherbivores and Algae. Botanica Marina, 42:137-155.
Barker K.M. & Chapman A.R.O. (1990). Feeding preferences of periwinkles among 4 species of Fucus. Marine Biology, 106:113-118.
Bergström L., Tatarenkov A., Johannesson K., Jönsson R.B. & Kautsky L. (2005). Genetic and morphological identification of Fucus radicans sp Nov (Fucales, Phaeophyceae) in the brackish Baltic Sea. Journal of Phycology, 41:1025-1038.
Bokn T.L., Murray S.N., Moy F.E. & Magnusson J.B. (1992). Changes in fucoid distributions and abundances in the inner Oslofjord, Norway: 1974-80 versus 1988-90. Acta Phytogeographica Suecica, 78:117-124.
Burrows E.M. & Lodge S. (1951). Autecology and the species problem in Fucus. Journal of the Marine Biological Association of the United Kingdom, 30:161-176.
Carr M.H. (1989). Effects of macroalgal assemblages on the recruitment of temperate zone reef fishes. Journal of Experimental Marine Biology and Ecology, 126:59-76.
Colautti R.I., Ricciardi A., Grigorovich I.A. & MacIsaac H.J. (2004). Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7:721-733.
Chapman A.R.O. & Johnson C.R. (1990). Disturbance and organization of macroalgal assemblages in the Northwest Atlantic. Hydrobiologia, 192:77-121.
Denton A.B. & Chapman A.R.O. (1991). Feeding preferences of gammarid amphipods among four species of Fucus. Marine Biology, 109:503-506.
Engkvist R., Malm T. & Nilsson J. (2004). Interaction between isopod grazing and wave action: a structuring force in macroalgal communities in the southern Baltic Sea.
Aquatic Ecology, 38:403-413.
Engkvist R., Malm T. & Tobiasson S. (2000). Density dependent grazing effects of the isopod Idotea baltica Pallas on Fucus vesiculosus L in the Baltic Sea. Aquatic Ecology, 34:253-260.
Geiselman J.A. & McConnell O.J. (1981). Polyphenols in brown algae Fucus vesiculosus and Ascophyllum nodosum: Chemical defenses against the marine herbivorous snail, Littorina littorea. Journal of Chemical Ecology, 7:1115-1133.
Graham L.E. & Wilcox L.W. (2000). Algae. Prentice-Hall Inc., Upper Saddle River.
Hylmö D.E. (1933). Algenimmigration nach der schwedischen Westküste. Botaniska Notiser, 1933:377-390.
Jonsson P.R., Granhag L., Moschella P.S., Aberg P., Hawkins S.J. & Thompson R.C. (2006).
Interactions between wave action and grazing control the distribution of intertidal macroalgae. Ecology, 87:1169-1178.
Jormalainen V., Honkanen T. & Heikkilä N. (2001). Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Marine Ecology Progress Series, 220:219-230.
Jormalainen V. & Ramsay T., (2009). Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos, in press.
Kautsky N., Johannesson K., & Tedengren M. (1990). Genotypic and phenotypic differences between Baltic and North Sea populations of Mytilus edulis evaluated trough reciprocal transplantations. I. Growth and morphology. Marine Ecology Progress Series, 59:203-210.
Keane R.M. & Crawley M.J. (2002). Exotic plant invasions and the enemy release hypothesis.
Trends in Ecology & Evolution, 17:164-170.
22
Khfaji A.K. & Norton T.A. (1979). The effects of salinity on the distribution of Fucus ceranoides. Estuarine and Coastal Marine Science, 8:433-439.
Kiirikki, M. 1996. Experimental evidence that Fucus vesiculosus (Phaeophyta) controls filamentous algae by means of the whip-lash effect. European Journal of Phycology, 31:61-66.
Lüning K. (1990). Seaweeds: Their environment, Biogeography, and Ecophysiology. John Wiley New York, NY.
Luther, H., 1981. Occurrence and ecological requirements of Fucus vesiculosus in semi- enclosed inlets of the Archeplago Sea, SW Finland. Annales Botanici Fennici, 18:187- 200.
Malm T., Engkvist R. & Kautsky L. (1999). Grazing effects of two freshwater snails on juvenile Fucus vesiculosus in the Baltic Sea. Marine Ecology-Progress Series, 188:63- 71.
Malm T., Kautsky L. & Engkvist R. (2001). Reproduction, recruitment and geographical distribution of Fucus serratus L. in the Baltic Sea. Botanica Marina, 44:101-108.
Nygård C.A. & Dring M.J. (2008). Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. European Journal of Phycology, 43:253- 262.
Pekkari S. (1973). Effects of sewage water on benthic vegetation. OIKOS, Supplement 15:185-188.
Pereyra R.T., Bergström L., Kautsky L. & Johannesson K. (2009). Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evolutionary Biology, in press.
Peterson C.H. & Renaud P.E. (1989). Analysis of feeding preference experiments. Oecologia, 80:82-86.
Powell H.T. (1957). Studies in the genus Fucus L. I. Fucus distichus L. emend. Powell.
Journal of the Marine Biological Association of the U.K, 36:407-432.
Quatrano R.S. (1980). Gamete release, fertilization and embryogenesis in the Fucales. In:
Handbook of phycological methods. Developmental and cytological methods (ed.
Gantt E). Cambridge University Press Cambridge, pp. 59-68.
Ragan M.A. & Glombitza K. (1986). Phlorotannins, brown algal Polyphenols. In: Progress in Phycological Research (eds. Round FE & Chapman DJ). Biopress Bristol, pp. 129- 241.
Råberg S. & Kautsky L. (2007). A comparative biodiversity study of the associated fauna of perennial fucoids and filamentous algae. Estuarine Coastal and Shelf Science, 73:249- 258.
Schaffelke B., Evers D. & Walhorn A. (1995). Selective grazing of the isopod Idotea baltica between Fucus evanescens and F. vesiculosus from Kiel Fjord (western Baltic).
Marine Biology, 124:215-218.
Schueller G.H. & Peters A.F. (1994). Arrival of Fucus evanescens (Phaeophyceae) in Kiel Bight (western Baltic). Botanica Marina, 37:471-477.
Serrão E.A., Brawley S.H., Hedman, J., Kautsky L. & Samuelsson, G. (1999). Reproductive success of Fucus vesiculosus (Phaeophyceae) in the Baltic Sea. Journal of Phycology 35:254-269.
Serrão E.A., Kautsky L. & Brawley S.H. (1996). Distributional success of the marine seaweed Fucus vesiculosus L in the brackish Baltic Sea correlates with osmotic capabilities of Baltic gametes. Oecologia, 107:1-12.
Simmons H.G. (1989). Algologiska notiser. II. Einige Algenfunde bei Drøbak. Botaniska Notiser, 117-123.
23
Sivertsen K. (2006). Overgrazing of kelp beds along the coast of Norway. Journal of Applied Phycology, 18:599-610.
Tatarenkov A., Bergström L., Jönsson R.B., Serrão E.A., Kautsky L. & Johannesson K.
(2005). Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Molecular Ecology, 14:647-651.
Toth G.B., Karlsson M. & Pavia H. (2007). Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia, 152:245-255.
Toth G.B. & Pavia H. (2007). Induced herbivore resistance in seaweeds: a meta-analysis.
Journal of Ecology, 95:425-434.
Van Alstyne K.L. (1995). Comparison of three methods for quantifying brown algal polyphenolic compounds. Journal of Chemical Ecology, 21:45-58.
Wærn M. (1952). Rocky-shore algae in the Öregrund archipelago. Acta Phytogeographica Suecica, 30:1-298.
Wikström S.A. & Kautsky L. (2004). Invasion of a Habitat-Forming Seaweed: Effects on Associated Biota. Biological Invasions, 6:141-150.
Wikström S.A. & Kautsky L. (2007). Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea.
Estuarine, Coastal and Shelf Science, 72:168-176.
Wikström S.A., Steinarsdottir M.B., Kautsky L. & Pavia H. (2006). Increased chemical resistance explains low herbivore colonization of introduced seaweed. Oecologia, 148:593-601.
Wikström S.A., von Wachenfeldt T. & Kautsky L. (2002). Establishment of the exotic species Fucus evanescens C. Ag. (Phaeophyceae) in Öresund, Southern Sweden. Botanica Marina, 45:510-517.
24
Serien Plants & Ecology (ISSN 1651-9248) har tidigare haft namnen "Meddelanden från Växtekologiska avdelningen, Botaniska institutionen, Stockholms Universitet" nummer 1978:1 – 1993:1 samt "Växtekologi". (ISSN 1400-9501) nummer 1994:1 – 2003:3.
Följande publikationer ingår i utgivningen:
1978:1 Liljelund, Lars-Erik: Kompendium i matematik för ekologer.
1978:2 Carlsson, Lars: Vegetationen på Littejåkkadeltat vid Sitasjaure, Lule Lappmark.
1978:3 Tapper, Per-Göran: Den maritima lövskogen i Stockholms skärgård.
1978:4: Forsse, Erik: Vegetationskartans användbarhet vid detaljplanering av fritidsbebyggelse.
1978:5 Bråvander, Lars-Gunnar och Engelmark, Thorbjörn: Botaniska studier vid Porjusselets och St. Lulevattens stränder i samband med regleringen 1974.
1979:1 Engström, Peter: Tillväxt, sulfatupptag och omsättning av cellmaterial hos pelagiska saltvattensbakterier.
1979:2 Eriksson, Sonja: Vegetationsutvecklingen i Husby-Långhundra de senaste tvåhundra åren.
1979:3 Bråvander, Lars-Gunnar: Vegetation och flora i övre Teusadalen och vid Auta- och Sitjasjaure; Norra Lule Lappmark. En översiktlig inventering med anledning av områdets exploatering för vattenkraftsändamål i Ritsemprojektet.
1979:4 Liljelund, Lars-Erik, Emanuelsson, Urban, Florgård, C. och Hofman-Bang, Vilhelm: Kunskapsöversikt och forskningsbehov rörande mekanisk påverkan på mark och vegetation.
1979:5 Reinhard, Ylva: Avloppsinfiltration - ett försök till konsekvensbeskrivning.
1980:1 Telenius, Anders och Torstensson, Peter: Populationsstudie på Spergularia marina och Spergularia media. I Frödimorfism och reproduktion.
1980:2 Hilding, Tuija: Populationsstudier på Spergularia marina och Spergularia media.
II Resursallokering och mortalitet.
1980:3 Eriksson, Ove: Reproduktion och vegetativ spridning hos Potentilla anserina L.
1981:1 Eriksson, Torsten: Aspekter på färgvariation hos Dactylorhiza sambucina.
1983:1 Blom, Göran: Undersökningar av lertäkter i Färentuna, Ekerö kommun.
1984:1 Jerling, Ingemar: Kalkning som motåtgärd till försurningen och dess effekter på blåbär, Vaccinium myrtillus.
1986:1 Svanberg, Kerstin: En studie av grusbräckans (Saxifraga tridactylites) demografi.
1986:2 Nyberg, Hans: Förändringar i träd- och buskskiktets sammansättning i ädellövskogen på Tullgarnsnäset 1960-1983.
1987:1 Edenholm, Krister: Undersökningar av vegetationspåverkan av vildsvinsbök i Tullgarnsområdet.
1987:2 Nilsson, Thomas: Variation i fröstorlek och tillväxthastighet inom släktet Veronica.
1988:1 Ehrlén, Johan: Fröproduktion hos vårärt (Lathyrus vernus L.). - Begränsningar och reglering.
1988:2 Dinnétz, Patrik: Local variation in degree of gynodioecy and protogyny in Plantago maritima.
1988:3 Blom, Göran och Wincent, Helena: Effekter of kalkning på ängsvegetation.
1989:1 Eriksson, Pia: Täthetsreglering i Littoralvegetation.
1989:2 Kalvas, Arja: Jämförande studier av Fucus-populationer från Östersjön och västkusten.
1990:1 Kiviniemi, Katariina: Groddplantsetablering och spridning hos smultron, Fragaria vesca.
1990:2 Idestam-Almquist, Jerker: Transplantationsförsök med Borstnate.
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1992:1 Malm, Torleif: Allokemisk påverkan från mucus hos åtta bruna makroalger på epifytiska alger.
1992:2 Pontis, Cristina: Om groddknoppar och tandrötter. Funderingar kring en klonal växt: Dentaria bulbifera.
1992:3 Agartz, Susanne: Optimal utkorsning hos Primula farinosa.
1992:4 Berglund, Anita: Ekologiska effekter av en parasitsvamp - Uromyces lineolatus på Glaux maritima (Strandkrypa).
1992:5 Ehn, Maria: Distribution and tetrasporophytes in populations of Chondrus crispus Stackhouse (Gigartinaceae, Rhodophyta) on the west coast of Sweden.
1992:6 Peterson, Torbjörn: Mollusc herbivory.
1993:1 Klásterská-Hedenberg, Martina: The influence of pH, N:P ratio and zooplankton on the phytoplanctic composition in hypertrophic ponds in the Trebon-region, Czech Republic.
1994:1 Fröborg, Heléne: Pollination and seed set in Vaccinium and Andromeda.
1994:2 Eriksson, Åsa: Makrofossilanalys av förekomst och populationsdynamik hos Najas flexilis i Sörmland.
1994:3 Klee, Irene: Effekter av kvävetillförsel på 6 vanliga arter i gran- och tallskog.
1995:1 Holm, Martin: Beståndshistorik - vad 492 träd på Fagerön i Uppland kan berätta.
1995:2 Löfgren, Anders: Distribution patterns and population structure of an economically important Amazon palm, Jessenia bataua (Mart.) Burret ssp. bataua in Bolivia.
1995:3 Norberg, Ylva: Morphological variation in the reduced, free floating Fucus vesiculosus, in the Baltic Proper.
1995:4 Hylander, Kristoffer & Hylander, Eva: Mount Zuquala - an upland forest of Ethiopia. Floristic inventory and analysis of the state of conservation.
1996:1 Eriksson, Åsa: Plant species composition and diversity in semi-natural grasslands - with special emphasis on effects of mycorrhiza.
1996:2 Kalvas, Arja: Morphological variation and reproduction in Fucus vesiculosus L.
populations.
1996:3 Andersson, Regina: Fågelspridda frukter kemiska och morfologiska egenskaper i relation till fåglarnas val av frukter.
1996:4 Lindgren, Åsa: Restpopulationer, nykolonisation och diversitet hos växter i naturbetesmarker i sörmländsk skogsbygd.
1996:5 Kiviniemi, Katariina: The ecological and evolutionary significance of the early life cycle stages in plants, with special emphasis on seed dispersal.
1996:7 Franzén, Daniel: Fältskiktsförändringar i ädellövskog på Fagerön, Uppland, beroende på igenväxning av gran och skogsavverkning.
1997:1 Wicksell, Maria: Flowering synchronization in the Ericaceae and the Empetraceae.
1997:2 Bolmgren, Kjell: A study of asynchrony in phenology - with a little help from Frangula alnus.
1997:3 Kiviniemi, Katariina: A study of seed dispersal and recruitment of plants in a fragmented habitat.
1997:4 Jakobsson, Anna: Fecundity and abundance - a comparative study of grassland species.
1997:5 Löfgren, Per: Population dynamics and the influence of disturbance in the Carline Thistle, Carlina vulgaris.
1998:1 Mattsson, Birgitta: The stress concept, exemplified by low salinity and other stress factors in aquatic systems.
1998:2 Forsslund, Annika & Koffman, Anna: Species diversity of lichens on decaying wood - A comparison between old-growth and managed forest.
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1998:3 Eriksson, Åsa: Recruitment processes, site history and abundance patterns of plants in semi-natural grasslands.
1998:4 Fröborg, Heléne: Biotic interactions in the recruitment phase of forest field layer plants.
1998:5 Löfgren, Anders: Spatial and temporal structure of genetic variation in plants.
1998:6 Holmén Bränn, Kristina: Limitations of recruitment in Trifolium repens.
1999:1 Mattsson, Birgitta: Salinity effects on different life cycle stages in Baltic and North Sea Fucus vesiculosus L.
1999:2 Johannessen, Åse: Factors influencing vascular epiphyte composition in a lower montane rain forest in Ecuador. An inventory with aspects of altitudinal distribution, moisture, dispersal and pollination.
1999:3 Fröborg, Heléne: Seedling recruitment in forest field layer plants: seed production, herbivory and local species dynamics.
1999:4 Franzén, Daniel: Processes determining plant species richness at different scales - examplified by grassland studies.
1999:5 Malm, Torleif: Factors regulating distribution patterns of fucoid seaweeds. A comparison between marine tidal and brackish atidal environments.
1999:6 Iversen, Therese: Flowering dynamics of the tropical tree Jacquinia nervosa.
1999:7 Isæus, Martin: Structuring factors for Fucus vesiculosus L. in Stockholm south archipelago - a GIS application.
1999:8 Lannek, Joakim: Förändringar i vegetation och flora på öar i Norrtälje skärgård.
2000:1 Jakobsson, Anna: Explaining differences in geographic range size, with focus on dispersal and speciation.
2000:2 Jakobsson, Anna: Comparative studies of colonisation ability and abundance in semi-natural grassland and deciduous forest.
2000:3 Franzén, Daniel: Aspects of pattern, process and function of species richness in Swedish seminatural grasslands.
2000:4 Öster, Mathias: The effects of habitat fragmentation on reproduction and population structure in Ranunculus bulbosus.
2001:1 Lindborg, Regina: Projecting extinction risks in plants in a conservation context.
2001:2 Lindgren, Åsa: Herbivory effects at different levels of plant organisation; the individual and the community.
2001:3 Lindborg, Regina: Forecasting the fate of plant species exposed to land use change.
2001:4 Bertilsson, Maria: Effects of habitat fragmentation on fitness components.
2001:5 Ryberg, Britta: Sustainability aspects on Oleoresin extraction from Dipterocarpus alatus.
2001:6 Dahlgren, Stefan: Undersökning av fem havsvikar i Bergkvara skärgård, östra egentliga Östersjön.
2001:7 Moen, Jon; Angerbjörn, Anders; Dinnetz, Patrik & Eriksson Ove: Biodiversitet i fjällen ovan trädgränsen: Bakgrund och kunskapsläge.
2001:8 Vanhoenacker, Didrik: To be short or long. Floral and inflorescence traits of Bird`s eye primrose Primula farinose, and interactions with pollinators and a seed predator.
2001:9 Wikström, Sofia: Plant invasions: are they possible to predict?
2001:10 von Zeipel, Hugo: Metapopulations and plant fitness in a titrophic system – seed predation and population structure in Actaea spicata L. vary with population size.
2001:11 Forsén, Britt: Survival of Hordelymus europaéus and Bromus benekenii in a deciduous forest under influence of forest management.
2001:12 Hedin, Elisabeth: Bedömningsgrunder för restaurering av lövängsrester i Norrtälje kommun.
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2002:1 Dahlgren, Stefan & Kautsky, Lena: Distribution and recent changes in benthic macrovegetation in the Baltic Sea basins. – A literature review.
2002:2 Wikström, Sofia: Invasion history of Fucus evanescens C. Ag. in the Baltic Sea region and effects on the native biota.
2002:3 Janson, Emma: The effect of fragment size and isolation on the abundance of Viola tricolor in semi-natural grasslands.
2002:4 Bertilsson, Maria: Population persistance and individual fitness in Vicia pisiformis:
the effects of habitat quality, population size and isolation.
2002:5 Hedman, Irja: Hävdhistorik och artrikedom av kärlväxter i ängs- och hagmarker på Singö, Fogdö och norra Väddö.
2002:6 Karlsson, Ann: Analys av florans förändring under de senaste hundra åren, ett successionsförlopp i Norrtälje kommuns skärgård.
2002:7 Isæus, Martin: Factors affecting the large and small scale distribution of fucoids in the Baltic Sea.
2003:1 Anagrius, Malin: Plant distribution patterns in an urban environment, Södermalm, Stockholm.
2003:2 Persson, Christin: Artantal och abundans av lavar på askstammar – jämförelse mellan betade och igenvuxna lövängsrester.
2003:3 Isæus, Martin: Wave impact on macroalgal communities.
2003:4 Jansson-Ask, Kristina: Betydelsen av pollen, resurser och ljustillgång för reproduktiv framgång hos Storrams, Polygonatum multiflorum.
2003:5 Sundblad, Göran: Using GIS to simulate and examine effects of wave exposure on submerged macrophyte vegetation.
2004:1 Strindell, Magnus: Abundansförändringar hos kärlväxter i ädellövskog – en jämförelse av skötselåtgärder.
2004:2 Dahlgren, Johan P: Are metapopulation dynamics important for aquatic plants?
2004:3 Wahlstrand, Anna: Predicting the occurrence of Zostera marina in bays in the Stockholm archipelago,northern Baltic proper.
2004:4 Råberg, Sonja: Competition from filamentous algae on Fucus vesiculosus – negative effects and the implications on biodiversity of associated flora and fauna.
2004:5 Smaaland, John: Effects of phosphorous load by water run-off on submersed plant communities in shallow bays in the Stockholm archipelago.
2004:6 Ramula Satu: Covariation among life history traits: implications for plant population dynamics.
2004:7 Ramula, Satu: Population viability analysis for plants: Optimizing work effort and the precision of estimates.
2004:8 Niklasson, Camilla: Effects of nutrient content and polybrominated phenols on the reproduction of Idotea baltica and Gammarus ssp.
2004:9 Lönnberg, Karin: Flowering phenology and distribution in fleshy fruited plants.
2004:10 Almlöf, Anette: Miljöfaktorers inverkan på bladmossor i Fagersjöskogen, Farsta, Stockholm.
2005:1 Hult, Anna: Factors affecting plant species composition on shores - A study made in the Stockholm archipelago, Sweden.
2005:2 Vanhoenacker, Didrik: The evolutionary pollination ecology of Primula farinosa.
2005:3 von Zeipel, Hugo: The plant-animal interactions of Actea spicata in relation to spatial context.
2005:4 Arvanitis, Leena T.: Butterfly seed predation.
2005:5 Öster, Mathias: Landscape effects on plant species diversity – a case study of Antennaria dioica.
2005:6 Boalt, Elin: Ecosystem effects of large grazing herbivores: the role of nitrogen.
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2005:7 Ohlson, Helena: The influence of landscape history, connectivity and area on species diversity in semi-natural grasslands.
2005:8 Schmalholz, Martin: Patterns of variation in abundance and fecundity in the endangered grassland annual Euphrasia rostkovia ssp. Fennica.
2005:9 Knutsson, Linda: Do ants select for larger seeds in Melampyrum nemorosum?
2006:1 Forslund, Helena: A comparison of resistance to herbivory between one exotic and one native population of the brown alga Fucus evanescens.
2006:2 Nordqvist, Johanna: Effects of Ceratophyllum demersum L. on lake phytoplankton composition.
2006:3 Lönnberg, Karin: Recruitment patterns, community assembly, and the evolution of seed size.
2006:4 Mellbrand, Kajsa: Food webs across the waterline - Effects of marine subsidies on coastal predators and ecosystems.
2006:5 Enskog, Maria: Effects of eutrophication and marine subsidies on terrestrial invertebrates and plants.
2006:6 Dahlgren, Johan: Responses of forest herbs to the environment.
2006:7 Aggemyr, Elsa: The influence of landscape, field size and shape on plant species diversity in grazed former arable fields.
2006:8 Hedlund, Kristina: Flodkräftor (Astacus astacus) i Bornsjön, en omnivors påverkan på växter och snäckor.
2007:1 Eriksson, Ove: Naturbetesmarkernas växter- ekologi, artrikedom och bevarandebiologi.
2007:2 Schmalholz, Martin: The occurrence and ecological role of refugia at different spatial scales in a dynamic world.
2007:3 Vikström, Lina: Effects of local and regional variables on the flora in the former semi-natural grasslands on Wäsby Golf club’s course.
2007:4 Hansen, Joakim: The role of submersed angiosperms and charophytes for aquatic fauna communities.
2007:5 Johansson, Lena: Population dynamics of Gentianella campestris, effects of grassland management, soil conditions and the history of the landscape 2007:6 von Euler, Tove: Sex related colour polymorphism in Antennaria dioica.
2007:7 Mellbrand, Kajsa: Bechcombers, landlubbers and able seemen: Effects of marine subsidies on the roles of arthropod predators in coastal food webs.
2007:8 Hansen, Joakim: Distribution patterns of macroinvertebrates in vegetated, shallow, soft-bottom bays of the Baltic Sea.
2007:9 Axemar, Hanna: An experimental study of plant habitat choices by macroinvertebrates in brackish soft-bottom bays.
2007:10 Johnson, Samuel: The response of bryophytes to wildfire- to what extent do they survive in-situ?
2007:11 Kolb, Gundula: The effects of cormorants on population dynamics and food web structure on their nesting islands.
2007:12 Honkakangas, Jessica: Spring succession on shallow rocky shores in northern Baltic proper.
2008:1 Gunnarsson, Karl: Påverkas Fucus radicans utbredning av Idotea baltica?
2008:2 Fjäder, Mathilda: Anlagda våtmarker i odlingslandskap- Hur påverkas kärlväxternas diversitet?
2008:3 Schmalholz, Martin: Succession in boreal bryophyte communities – the role of microtopography and post-harvest bottlenecks.
2008:4 Jokinen, Kirsi: Recolonization patterns of boreal forest vegetation following a severe flash flood.
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2008:5 Sagerman, Josefin: Effects of macrophyte morphology on the invertebrate fauna in the Baltic Sea.
2009:1 Andersson, Petter: Quantitative aspects of plant-insect interaction in fragmented landscapes – the role of insect search behaviour.
2009:2 Kolb, Gundula: The effects of cormorants on the plant-arthropod food web on their nesting islands.
2009:3 Johansson, Veronika: Functional traits and remnant populations in abandoned semi-natural grasslands.
2009: 4 König, Malin: Phenotypic selection on flowering phenology and herbivory in Cardamine amara.
