Download Herbivory, phenotypic variation, and reproductive barriers in fucoids Helena Forslund

Herbivory, phenotypic variation, and
reproductive barriers in fucoids
Helena Forslund
©Helena Forslund, Stockholm University 2012
Cover illustration: Helena Forslund
ISBN 978-91-7447-538-8
Printed in Sweden by US-AB, Stockholm 2012
Distributor: Department of Botany, Stockholm University
Live your life filled with joy and wonder
Live your life filled with joy and thunder
- R.E.M.
Doctoral dissertation
Helena Forslund
Department of Botany
Stockholm University
SE-106 91 Stockholm
Sweden
Herbivory, phenotypic variation, and reproductive barriers in
fucoids
Abstract. Along the shores of the Northern hemisphere Fucus (Phaeophyceae) species
are a prominent presence, providing substrate, shelter, and food for many species. Fucus
evanescens, a non-indigenous species (NIS) in Sweden, and F. radicans, a recently
described species that so far has only been found inside the species poor Baltic Sea, are
the focus of this thesis.
Interactions with enemies (e.g. predators, herbivores, parasites) have been shown to
play a role in the success of NIS. The low consumption of Fucus evanescens by the
generalist gastropod Littorina littorea in Sweden was found to depend on high levels of
chemical defense in the introduced population, not the failure of the herbivore to
recognize F. evanescens as suitable food.
A survey of the relative abundance of F. radicans and F. vesiculosus and the most
common associated fauna along the Swedish Bothnian Sea coast showed that F.
radicans and F. vesiculosus are equally abundant throughout the range of F. radicans.
The most common associated fauna were found to be more abundant on F. radicans
compared to F. vesiculosus. In Sweden, where F. radicans had lower levels of defense
chemicals than F. vesiculosus, F. radicans was grazed more than F. vesiculosus in
bioassays. This could, together with other factors, influence the range of F. radicans.
Fucus radicans and F. vesiculosus are closely related, recently separated, and growing
sympatrically, therefore, possible reproductive barriers between F. radicans and F.
vesiculosus were studied. In Estonia F. radicans and F. vesiculosus reproduces at
different times of the year. No such clear reproductive barrier was found between the
two species in Sweden where they reproduce at the same time and fertilization success
and germling survival were the same for hybrids as for F. vesiculosus.
Since the high clonality of F. radicans means that the gentic diversity in F. radicans
populations is low I investigated how genetic diversity translates to phenotypic diversity
in nine traits. Phlorotannin levels, recovery after desiccation, and recovery after freezing
showed inherited variation, while the other six traits showed no variation related to
genetic diversity. Phenotypic variation in populations of F. radicans will be higher in
populations with higher genetic diversity and this might be beneficial to the community.
Keywords – Non-indigenous species; Enemy Release Hypothesis; Asexual
reproduction; Phlorotannins; Distribution
List of papers
This thesis is based on the following papers, which are referred to by
their roman numerals in the text:
I.
Forslund H, Eriksson O, Kautsky L (2012). Grazing and
geographic range of the Baltic seaweed Fucus radicans
(Phaeophyceae). Marine Biology Research 8:322-330.
II.
Forslund H, Wikström SA, Pavia H (2010). Higher resistance
to herbivory in introduced compared to native populations of
a seaweed. Oecologia 164:833-840.
III.
Forslund H, Kautsky L. Reproduction and reproductive
isolation in Fucus radicans (Phaeophyceae). Accepted for
publication in Marine Biology Research.
IV.
Johannesson K, Forslund H, Capetillo NÅ, Kautsky L,
Johansson D, Pereyra R, Råberg S (2012). Phenotypic
variation in sexually and asexually recruited individuals of the
Baltic Sea endemic macroalga Fucus radicans: in the field
and after growth in a common-garden. BMC Ecology 12.
In paper I I planned and performed the study and experiments as well as
wrote the paper and did the statistical analyses. For paper II I planned
and performed experiments and studies, wrote most of the paper and did
the statistical analyses. For paper III I planned and performed the
experiments and studies, wrote the text and performed statistical
analyses. For paper IV I planned and performed studies and
experiments.
Paper I and III is reprinted with permission from Taylor and Francis.
Paper II is reprinted with kind permission from Springer Science and
Business Media. Paper IV is reprinted with permission from BMC
Ecology.
Content
Foreword ........................................................................................................... 10
Introduction ....................................................................................................... 11
The Fucus species studied ............................................................................. 11
Objectives of the thesis ................................................................................. 13
The associated flora and fauna of seaweed beds ......................................... 13
Herbivory and herbivory defense in fucoid algae ......................................... 14
Non-indigenous species and marine introductions....................................... 15
Reproduction and reproductive isolation in Fucus species ........................... 17
Effects of genetic diversity on resilience and biodiversity in the Fucus
community..................................................................................................... 18
Study area ...................................................................................................... 19
The herbivores ............................................................................................... 21
Studies ............................................................................................................... 21
Surveys of relative abundance of F. radicans and F. vesiculosus and diversity
and abundance of the associated fauna ....................................................... 21
Herbivore defense and phlorotannins .......................................................... 22
Reproductive effort and reproductive isolation of F. radicans and F.
vesiculosus ..................................................................................................... 24
Genetic diversity and variation in traits in F. radicans .................................. 24
Results and discussion ....................................................................................... 25
Acknowledgements ........................................................................................... 30
References ......................................................................................................... 31
Svensk sammanfattning .................................................................................... 42
Tack! .................................................................................................................. 47
Appendix 1 ......................................................................................................... 49
Foreword
Under the surface of the ocean, where this thesis will take you, an alien
world meets us. More people have walked on the surface of the moon
than in the deepest trenches in the oceans. I hope and expect that we will
be endlessly awed by the mysteries that are uncovered as scientists
continue to learn more, but also that we will never learn everything there
is to know. My astronomy and astrophysics professor would spend hours
explaining a single theory for us, only to end the lecture by saying, “Or at
least this is what the scientists are saying right now. If you have a better
theory I’m willing to listen - what we know might change in a year
anyway.” I would step out from the university building into the night and
walk home, looking up at the stars and feeling awed by the thought of
both everything we do not know and everything we will never
understand. Studying biology only increased this sense of wonder but this
time the focus was much closer than the stars: my cells, the bacteria on
my skin, and the trees outside of my window - each no less amazing or
unknown than the cosmos.
Over the last decades we have learned that organisms in the ocean that
seem to be among the simplest forms of life, the algae, have intricate
systems that can measure the moon’s phases, sense light, send warning
messages and sense how much the water is moving. We have found that
a single genetic individual can be spread over a large area – it is as
though thousands of copies of you were living in an area so wide that it
would take more than a week to bike through.
This thesis focuses on a genus of seaweeds – the Fucus – that are present
along temperate shores on the northern hemisphere. Living under water,
they exist in an environment that is so foreign to us that it is hard to
imagine. They are so different from us that intuition and common sense
do not apply to them. They synthesize energy from the sun, they cannot
move, and while they might seem like a simple slimy presence along the
shores they have intricate systems to sense and react to their
environment.
10
Introduction
The Fucus species studied
Seaweeds of the genus Fucus (Phaeophyceae) are a group of large,
perennial brown seaweeds. They are found in temperate and arctic waters
on the northern hemisphere. On intertidal rocky shores they usually form
a belt with different fucoid species dominating at different shore levels.
Pelvetia canaliculata (L.) Decaisne & Thuret and Fucus spirals L. grows
in the splash zone, F. vesiculosus L., F. distichus L., F. ceranoides L. and
Ascophyllum nodosum L. form a zone at intermediate levels and F.
serratus L. and F. evanescens Agardh grow in the lower intertidal zone,
rarely exposed to the air (Chapman 1995; Munda 2004; Wahl et al.
2011). The zonation usually depends on both abiotic factors (exposure to
air, substrate, dessication) and biotic factors (competition, grazing)
(Lubchenco 1980; Kiirikki 1996b; Wahl et al. 2011).
Foundation species are species that provide structure, increases the
complexity of the habitat, provide shelter and protection from both
abiotic and biotic factors to an associated community (Dayton 1972; Roff
and Zacharias 2011). Since the Fucus community provides habitat and
shelter for many organisms (Colman 1940; Hagerman 1966; Kautsky et
al. 1992; Christie et al. 2009; Dijkstra et al. 2011) they can be considered
to be foundation species (e.g. Korpinen et al. 2010; Dijkstra et al. 2011).
Smaller epiphytic algae and sessile animals live directly on the Fucus
thallus. Small arthropods, isopods and gastropods live in and on the
Fucus thallus, finding shelter and food there (Colman 1940; Hagerman
1966; Kautsky et al. 1992; Christie et al. 2009). These small animals may
graze directly on the adult fucoid, juvenile fucoids, or the surface of the
fucoids (Lubchenco 1983; Chapman 1995; Malm et al. 1999). The
grazers are also provided with shelter against predators in the fucoid belt.
Small fish can not only find an important food source in the Fucus belt,
but also shelter from their predators (Hagerman 1966; Kautsky et al.
1992).
Fucus evanescens is native in the northern parts of the Atlantic and
Pacific Ocean and has been introduced to the southern Scandinavia and
the British Isles in the last century (Simmons 1898; Hylmö 1933; Powell
1957; Wikström et al. 2002). Fucus evanescens grows at the lower end of
the Fucus belt on rocky shores, but on Iceland where the tidal amplitude
11
is 4 m, they are exposed during low tide (Munda 2004). In Sweden F.
evanescens has a strong herbivore defense with higher levels of a defense
chemical, phlorotannins, and is less grazed than co-occurring Fucus
species. In contrast F. evanescens has lower levels of phlorotannins and
is grazed more than co-occurring Fucus species in Iceland (Wikström et
al. 2006).
Fucus vesiculosus is found in North Atlantic temperate coastal areas. It
has a large span of tolerance to environmental factors such as
temperature, exposure, and salinity (Lüning 1990; Bäck et al. 1992;
Chapman 1995; Nygård and Dring 2008). There are several different
morphs of F. vesiculosus, e.g. individuals growing at exposed sites have
few vesicles and individuals growing at calm sites have many vesicles
(Wærn 1952; Jordan and Vadas 1972). Different morphs have also been
noted in the Baltic Sea (Wærn 1952; Kalvas and Kautsky 1993). In the
northern parts of the Baltic Sea a smaller morph that was believed to be
salinity stressed were found (Wærn 1952; Ruuskanen and Bäck 1999).
With a combination of morphological and genetic studies Bergström et
al. (2005) managed to ascertain that this morph is in fact a separate
species, Fucus radicans Bergström & Kautsky. It was further found that
in Sweden, F. radicans is largely clonal, with one genetic clone
dominating large parts of the Swedish coast, even extending to Finland,
while in Estonia it is mainly sexually reproductive (Bergström et al.
2005; Johannesson et al. 2011). The asexual reproduction is thought to be
achieved by adventitious branches becoming detached, forming rhizoids
and reattaching to a surface (Tatarenkov et al. 2005). Asexual
reproduction is uncommon in fucoids (Serrão et al. 1999; Johannesson et
al. 2011) and clonality has only been observed in the Baltic Sea
(Bergström et al. 2005; Tatarenkov et al. 2005).
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Objectives of the thesis
The main objective of my thesis was to study how different Fucus
species interacts with other organisms, e.g. herbivores and competitors,
and how these interactions affect the distribution of Fucus species. I also
wanted to study the reproduction and reproductive barriers between F.
radicans and F. vesiculosus and the link between genetic diversity and
phenotypic variation in F. radicans.
Specific objectives of the thesis were:
 To study the Non-Indigenous Species (NIS) F. evanescens in
Sweden and how interactions with a common grazer could
potentially affect the introduction to Sweden.
 To gain more knowledge about the recently described F. radicans
by studying the distribution, reproduction, associated flora and
fauna, and herbivore defense of F. radicans.
 To find and study reproductive barriers between F. radicans and
F. vesiculosus.
 To investigate how genetic diversity of F. radicans transfers to
phenotypic variation and to investigate how the clonality of F.
radicans could affect the heterogeneity of the Fucus community
in the Baltic Sea.
The associated flora and fauna of seaweed beds
A rich community of algae and animals usually lives in and on the larger
algae that structure the rocky temperate shores. These associated flora
and fauna species find substrate, shelter, and food in the seaweeds
(Hagerman 1966; Christie et al. 2009).
The epiphytic algae and animals that live on seaweeds can have a large
effect on them by shading and nutrition competition among other things
(reviewed in Wahl 1989). The mobile fauna can both benefit the
seaweeds by grazing epiphytic organisms (Råberg and Kautsky 2007)
and affect them negatively by direct grazing on the seaweeds (e.g.
Lubchenco 1983; Engkvist et al. 2000).
A single kelp individual can host more than 100 species and 90 000
individuals and fucoid belts can host hundreds of species with animal
densities of 100 000 individuals m-2 (Christie et al. 2009). Many factors,
such as genetic diversity, size, complexity, and species composition of
13
the host will affect the diversity and abundance of the associated
community (Hauser et al. 2006; Christie et al. 2009; Tomas et al. 2011).
A larger seaweed or patch of seaweeds will have room for more
individuals and probably be more heterogeneous. A more complex, more
branched, seaweed or a seaweed with different parts like kelp holdfast,
stipe, and blade gives better shelter and will constitute a more
heterogeneous habitat than a simple seaweed, and will be likely to host a
more abundant and diverse community (Hauser et al. 2006; Christie et al.
2009; Hansen et al. 2011). A more genetically diverse habitat is also
believed to correlate with a more heterogeneous habitat, which in turn is
believed to host a more diverse associated community (Johnson and
Agrawal 2005; Tomas et al. 2011).
Since the foundation species is an important factor in deciding the
diversity and abundance of the associated community (Dayton 1972) and
since F. radicans differs from F. vesiculosus in morphology and genetics
(Bergström et al. 2005; Tatarenkov et al. 2005) I wanted to investigare if
F. radicans has a different associated community compared to F.
vesiculosus.
Herbivory and herbivory defense in fucoid algae
Herbivores are animals that consume primary producers. Marine
herbivores, such as fish, isopods, gastropods, arthropods and other small
invertebrates are usually generalist in contrast to many terrestrial animals
that are highly specialized (Hay and Steinberg 1992). Herbivores can
either just graze on the surface of a seaweed (Norton et al. 1990), suck
the juices out of seaweeds (Hagerman 1966), or graze down whole stands
of seaweeds (Engkvist et al. 2000). Common grazers on fucoid algae are
gastropods, isopods, and amphipods (Hagerman 1966).
Since grazing can have such a large effect it could be expected that algae
would have some type of mechanism to cope with or defend against loss
of resources to herbivores. Some species are adapted to tolerate grazing
by compensatory growth and avoidance of the meristem being grazed
(Cerda et al. 2009). There could also be either structural defenses or
chemical defenses to deter grazing. Structural defense such as
calcifications are common in some seaweeds (Paul and Hay 1986), but
studies of fucoids suggest that they have no structural defense (Rohde et
al. 2004). Chemical defenses entail the production of a substance that
14
makes the algae an undesirable food source. The defense substance can
be either toxic or make the algae less nutritious (Hay 1996).
The fucoids contains phlorotannins (Ragan and Glombitza 1986), a group
of chemicals that has many functions such as protection from UV light
(Swanson and Druehl 2002), wound healing (Fulcher and McCully 1971;
Lüder and Clayton 2004), cell wall formation (Schoenwaelder and
Clayton 1999), polyspermy block (Scoenwaelder and Clayton 1998), and
adhesion (Vreeland et al. 1998). They also function as herbivore defense
(Geiselman and Conell 1981; Amsler and Fairhead 2006), but there are
contradicting results and suggestions that other factors, such as other
chemicals (Deal et al. 2003; Kubanek et al. 2004) and habitat value
(Jormalainen et al. 2001) will be more important for herbivore choice.
In this thesis herbivory defense and phlorotannin content in F. radicans,
F. vesiculosus and F. evanescens was studied to compare differences
between species (paper I), populations (paper II), and to investigate if
phenotypic variation in phlorotannin content was related to the genetic
diversity of F. radicans (paper IV).
Non-indigenous species and marine introductions
With the increasing mobility of humans and increasing transports of
good, including live organisms, the number of species that are introduced
into new habitats are increasing. The introduction of species are now
considered a large part of global change (Vitousek et al. 1996; Ricciardi
2007) and is changing communities by homogenizing them and by
causing extinctions and decline of species (Lodge 1993; Mack et al.
2000). Both the ecological and economic costs of non-indigenous species
(NIS) are high (Pimentel et al. 2005).
In marine communities accidental transport with ships is believed to be
the most common means of introductions. Ships could introduce species
either trough ballast water that can contain larvae, plankton, or
planktonic life stages of a number of organisms or through organisms
becoming attached to the hull or other equipment on the ships.
Aquaculture is another common cause of introductions and has lead both
to intentional and unintentional introductions. The aquaria trade, where
organisms sold for aquaria have been released and become established
are another common way of introduction of marine species (Shaffelke et
al. 2006; Williams and Smith 2007).
15
There are several theories about factors that either facilitate or prevent
introduction both in regards to the introduced organism and the recipient
community. The biotic resistance theory states that a more diverse
recipient community will be harder for an introduced species to establish
in (Maron and Vilà 2001). The enemy release hypothesis (ERH) states
that the introduced species will not have as many enemies (herbivores,
predators, parasites etc) in the recipient community since the enemies
there will be unable to recognize it as a host since they don’t share an
evolutionary history. This will give the introduced species a competitive
advantage over native competing species (Elton 1958; Keane and
Crawley 2002). The loss of enemies should allow the introduced species
to allocate more resources to growth, reproduction, and competition, an
idea that gave rise to the Evolution of Increased Competitive Ability
(EICA) hypothesis (Blossey and Nötzold 1995).
The ERH was developed studying plant herbivore systems that are
known for highly specialized enemies, while specialist enemies are very
rare in marine systems (Hay and Steinberg 1992). Even so the ERH states
that generalist enemies should also follow the general pattern suggested
and prefer native hosts over an introduced host (Keane and Crawley
2002). Many studies so far on invasions of seaweeds shows that they are
consumed less than native co-occuring seaweeds (Gianguzza et al. 2002;
Levin et al. 2002; Britton-Simmons 2004; Smith et al. 2004; Sumi and
Scheibling 2005). However, these studies have not studied resistance to
herbivory and thus cannot separate an exemplification of the ERH and
the NIS having a high level of resistance to herbivory.
Despite the low dispersal ability of Fucus species F. serratus has been
introduced to Iceland and to Eastern North America, probably from
southern Norway (Robinson 1903; Dale 1982; Coyer at al. 2006) and
Fucus evanescens has been introduced from the North Atlantic to
southern Sweden and the southern Baltic Sea (Simmons 1898; Hylmö
1933; Powell 1957; Wikström et al. 2002). Previous studies have shown
that common Swedish grazers, such as Idotea granulosa Rathke and
Littorina obtusata L., prefer other co-occurring Fucus species over F.
evanescens while in Iceland it is preferred over other co-occurring Fucus
species. These studies also showed that the phlorotannin levels of F.
evanescens in Sweden were higher than the other Swedish fucoids, and in
Iceland the levels were lower (Wikström et al. 2006). These results
16
cannot discern between F. evanescens being avoided by Swedish
herbivores because of the novelty as predicted by the ERH or because of
the higher levels of phlorotannins. To be able to separate these two
possible causes for the observed patterns of herbivory I made a study
where Swedish grazer were allowed to choose between F. evanescens
from Iceland and F. evanescens from Sweden (paper II). If herbivore
preference was determined by novelty the two populations would be
expected to be grazed in equal and low amounts. If on the other hand the
chemical defense was the cause for the observed patterns it could be
expected that the Swedish grazers would consume more of F. evanescens
from Iceland that has lower levels of phlorotannins.
Reproduction and reproductive isolation in Fucus species
Fucus species can be either dioecious with a thallus being either male or
female, or hermaphroditic with each thallus having receptacles that
contains both egg and sperm. Receptacles are formed at the apex of
braches and eggs and/or sperms forms in small vesicles, conceptacles, in
the receptacles. Eggs are formed in groups of up to eight eggs called
oogonia that are released from the receptacle before it breaks down into
individual eggs (Vernet and Harper 1980). The eggs vary in size between
48 x10-5 and 16x10-5 mm3 (Steen and Rueness 2004), are negatively
buoyant so that they sink when they are released, and photosynthetic
(McLachlan and Bidwell 1978). The sperm from in bundles of 64 called
antheridia (Vernet and Harper 1980). The sperm has one flagellum and
an orange eye-spot that allows them to swim away from the light,
towards the bottom where the eggs are (Manton and Clarke 1956).
Eggs and sperm mature at different time of the year for different species
and even different populations (Berger et al. 2001; Steen and Rueness
2004). Gametes are synchronously released, cued by the moon and tidal
phase (Brawley 1992; Andersson et al. 1994). Gametes are released late
in the evening under calm conditions (Serrão et al. 1996b). Eggs releases
pheromones that attract sperm and the egg membrane has recognition
receptors that are species specific (Muller and Gassmann 1978) but
hybrids are still found (Coyer et al. 2002; Billard et al. 2005).
At lower salinities Fucus reproduction becomes problematic. The
polyspermy block of the eggs stops functioning with the results of several
sperm entering the egg, a condition that is lethal. The swimming of the
sperm also becomes very erratic, and this probably leads to them not
17
swimming away from the light (Serrão et al. 1996a; Serrão et al. 1999).
Thus sexual reproduction is most likely the life stage that limits the
spread to lower salinities, since Fucus thalli that comes from low salinity
areas can survive in salinities as low as 2 psu or even freshwater for
weeks (personal observation).
Fucus radicans, and to some extent Baltic Sea F. vesiculosus, also
reproduces asexually by adventitious branches that fall off forming
rhizoids and reattaching (Tatarenkov et al. 2005). It is possible that this
mechanism is not as sensitive as sexual reproduction to low salinities and
thus could be an advantage in the low salinities of the Baltic Sea.
Reproductive barriers are to be expected when two closely related
species live in sympatry as is the case of F. radicans and F. vesiculosus
in the Baltic Sea. Reproductive barriers are mechanisms that prevent
gene flow between two species or populations, preventing them from
interbreeding (Niklas 1997; Coyne and Orr 2004). Reproductive barriers
will provide information not only about the mechanisms that keeps
sympatric species isolated but also about mechanisms that could have
had a role in speciation (Coyne and Orr 2004).
Little was known about the reproduction of F. radicans, other than that it
is unique since the Swedish populations reproduces asexually to a large
extent which results in a high clonality. Thus the aim was to study the
reproductive effort, time of reproduction, and searching for possible
reproductive barriers between F. radicans and F. vesiculosus both in
Sweden and Estonia.
Effects of genetic diversity on resilience and biodiversity in the Fucus
community
Theoretically it is assumed that a community or ecosystem with high
diversity will be more resilient and adaptable since a system that has
many species will have species with different responses to disturbances,
and the likelihood of at least a few of these species surviving or adapting
to the disturbance would be higher compared to a system with just one or
two species (McNaughton 1977; Chapin 2000; Elmqvist et al. 2003).
There are studies that have shown that communities that have higher
species richness have a higher resilience (Steneck et al. 2002). There are
also studies that show that a more genetically diverse population can
withstand disturbance better (Hughes and Stachowicz 2004; Reusch et al.
18
2005; Gamfeldt and Källström 2007) and will host a more diverse
community (Booth and Grime 2003; Crutsinger et al. 2006). However,
there are also examples of very diverse systems that are still sensitive to
disturbance and have a low resilience (Bellwood et al. 2003).
Since F. radicans is clonal it has a low genetic diversity within the
population (Johannesson et al. 2011). In contrast F. vesiculosus has a
high genetic diversity although it is genetically differentiated at small
scales (Tatarenkov et al. 2007). For the low genetic variation of F.
radicans to affect the resilience and biodiversity of the Fucus community
it needs to be manifested in phenotypic traits. To investigate how the
genetic diversity in F. radicans affects the phenotypic variation we
measured the variation in nine phenotypic traits for three groups
consisting of clonal thalli and one group of genetically unique thalli.
Study area
The studies on F. radicans and F. vesiculosus (paper I, III, and IV) were
conducted within the Baltic Sea, i.e. the Bothnian Sea and northern Baltic
Proper. The Baltic Sea is atidal, but still has water level changes of up to
1 m that can last several days due to weather conditions. The salinity
varies from 15 psu at the entrance and 2 psu in the north (Bernes 2005).
In combination with the short history of the Baltic Sea under present
conditions (Voipio 1981; Björck 1995; Winsor et al. 2001) this probably
explains why the Baltic Sea is species poor with a combination of marine
and freshwater species (Remane and Schlieper 1971; Snoeijs 1999). Due
to the low salinity many species in the Baltic Sea functions at or close to
their physiological limits (e.g Westerbom et al. 2002; Bergström et al.
2003) and many populations are genetically differentiated from and have
a lower genetic diversity than populations outside the Baltic Sea
(Johannesson and André 2006).
For the study on F. evanescens (paper II) samples were collected from
the western parts of Iceland and the west coast of Sweden. Iceland is a
true marine area with tides of ~4 m and a salinity of 35 psu. On the
Swedish west coast the salinity varies and is usually within the range of
15 - 30 psu. The tides on the west coast are small, with an amplitude of
only ~0.2 m and they are often obscured by changes in water level due to
high or low pressures and strong winds. These fluctuations can last for
several days to weeks at a time.
19
The low salinity of the Swedish west coast decreases the species diversity
compared with areas with higher salinities. The species diversity is not
only lower in Sweden compared to Iceland the species composition in
Iceland and Sweden also differs in part due to different salinities and part
due to other factors that limits the range of species. There are differences
both in the grazer and seaweed community composition (Munda 2004;
Wikström 2006).
Figure 1. Collections of algae for paper II were made on Iceland (A)
and the Swedish west coast (B) and the bioassays were made at Tjärnö
Marine Laboratory (B). Experiments in paper I, III, and IV were
made at the Askö Laboratory (C). Algae for the study in paper IV
were collected in Finland (D). Fucus radicans range is marked in
grey.
20
The herbivores
In the studies of herbivore defense in paper I and IV, Idotea balthica
Pallas was used. In paper I I also used Gammarus spp. Idotea balthica is
an isopod that is common in the fucoid community (Salemaa 1979;
Wikström and Kautsky 2007). It is known to consume (Naylor 1955;
Ravanko 1969) and even prefer Fucus species over other species
(Jormalainen et al. 2001). Even though it is small it can occur in great
densities and are then known to be able to graze a large part of Fucus
thalli and can have a great negative effect to the point that it can severely
decimate a population (Engkvist et al. 2000).
Gammarus spp. generally prefers to consume filamentous algae and
microscopic algae that grow on the Fucus thalli (Ravanko 1969), but they
can also graze directly on the fucoids (Pavia et al. 1999; Kotta et al.
2006).
In paper II the gastropod Littorina littorea L. was used as herbivore.
Littorina littorea is a common herbivore on the west coast of Sweden
(Wikström et al. 2006), but it is not present on Iceland where F.
evanescens is native (Johannesson 1988). Gastropods can generally
consume most algae, but L. littorea has been shown to consume Fucus
species readily and it is generally sensitive to phlorotannins (e.g.
Geiselman and McConnell 1981; Lubchenco 1983; Wikström et al.
2006).
Studies
Surveys of relative abundance of F. radicans and F. vesiculosus and
diversity and abundance of the associated fauna
Surveys of the distribution pattern of F. radicans and F. vesiculosus
along the Swedish coast of the Bothnian Sea and their associated flora
and fauna were performed in August 2007 (paper I) and 2008 (Fig. 2). In
2008 a survey of Estonia was also made (Fig. 2).
I wanted to investigate if F. radicans became more common as the
salinity dropped in the northern parts of the Bothnian Sea and if this
change in cover were matched by a decrease in cover of F. vesiculosus.
21
The relative cover of F. radicans and F. vesiculosus were recorded at 16
sites along the Swedish coast (paper I).
I also wanted to investigate the associated flora and fauna. In the first
survey, in August – September 2007 (paper I) the abundance of the most
common grazers, Idotea spp., Gammarus spp., and Theodoxus fluviatilis
L., were collected by placing a mesh bag (mesh size < 1mm) over a
Fucus thallus. In the second, unpublished, study I collected F. radicans
and F. vesiculosus at six sites in Sweden and six sites in Estonia in
August 2008 (Fig 2). At each site six pairs of F. radicans and F.
vesiculosus were collected at 0.5 to 4 meters depth. The two thalli
making up a pair were growing within 1 m of each other to avoid
confounding differences in abiotic factors such as exposure, depth, and
bottom characteristics from affecting the taxon composition, richness and
density between the two Fucus species. A mesh bag (mesh size < 1mm)
was gently placed over the thallus being sampled and closed before
detaching the thallus and transporting it to the laboratory within two
days. Samples were frozen until they were sorted. Organisms larger than
1 mm were identified to the lowest possible taxonomic level. Animals
were counted and the Fucus thalli were dried and weighed.
Herbivore defense and phlorotannins
Since the most common herbivores, Idotea spp. and Gammarus spp.,
were found at higher abundances on F. radicans than F. vesiculosus
(paper I) bioassays were performed to investigate if this could be linked
to herbivory defense.
A comparison between F. evanescens from Iceland where it is native and
from Sweden where it is introduced were made to evaluate if a Swedish
grazer, L. littorea, prefers other Fucus species over F. evanescens
(Wikström et al. 2006) because of high levels of phlorotannins or the
novelty of it (paper II). To eliminate the effects of structure and
morphology on herbivore choice a bioassay where freeze dried and
pulverized algae were incorporated in agar and presented to L. littorea
were also made.
In paper IV I studied if grazing by Idotea spp. and phlorotannin content
differs depending on genotype, to investigate if genetic differences
manifests as differences in these traits.
22
In all bioassays one branch from one thallus were used in the control
treatment and another from the same thallus in the grazing treatment. The
branches were weighed before and after the experiments were grazers
were allowed the choice between species (paper I) or populations
(paper II). In the experiment in paper IV with genetic individuals there
was no-choice experiments performed. Phlorotannin content was
measured (see the respective papers for methods) in all the bioassays.
Figure 2. Sites in the 2008 survey of F. radicans and F. vesiculosus.
23
Reproductive effort and reproductive isolation of F. radicans and F.
vesiculosus
Fucus radicans is clonal (Bergström et al. 2005) and the adventitious
branches of F. radicans produces rhizoids and reattach more than those
of F. vesiculosus (Tatarenkov et al. 2005). The difference in levels of
clonality and rate of successful asexual reproduction could be caused
either by factors that affects the reproduction or by a difference in
reproductive allocation between F. radicans and F. vesiculosus.
Therefore reproductive effort of F. radicans and F. vesiculosus in
Sweden and Estonia was studied in paper III. Reproductive effort was
measured as eggs released per receptacle, receptacles per dry weight
algae and adventitious branches per wet weight algae.
Fucus radicans and F. vesiculosus are closely related and recently
diverged (Pereyra et al. 2009). Since they also live in sympatry
throughout the range of F. radicans it could be expected that some
hybrids would be found, and although there are intermediate forms (pers
obs.) no individuals that are identified as genetic hybrids have been
found (pers comm. with Kerstin Johannesson and Ricardo Pereyra).
Since no hybrids has been found and genetic studies shows that F.
radicans and F. vesiculosus are reproductively isolated (Pereyra et al.
2009) reproductive barriers should be in place and I made a few studies
to try and find out which if any they were.
First I measured the time of reproduction by observing at what time the
receptacles were mature and the period of egg release. Second, I made
artificial crosses between Swedish F. radicans and F. vesiculosus and
measured the fertilization success and survival after two weeks.
Genetic diversity and variation in traits in F. radicans
In paper IV the genetic diversity and how this affects the phenotypic
variation in nine traits were studied to investigate if the low genetic
diversity of F. radicans could be expected to affect the heterogeneity of
the Baltic Sea Fucus community. Three clones with ten replicate thalli
and one group of ten unique genetic individuals were studied and the
variation in traits was compared between the clones and the group of
unique individuals.
24
The traits studied were recovery after freezing, recovery after
desiccation, photochemical yield under ambient conditions, phlorotannin
content, grazing, growth rate, thallus width, distance between
dichotomies, and water content after desiccation. For details on the
methods used to measure these see paper IV.
Results and discussion
The results from the studies in paper I, III, and IV indicates not only the
previously known morphological, genetic, and reproductive differences
between F. radicans and F. vesiculosus (Bergström et al. 2005) but also
differences in the associated community, in herbivore defense, and
reproductive allocation and timing. Further, I found differences in
reproduction and chemical composition between the two studied
populations of F. radicans i.e. between the Swedish Bothnian Sea and
Estonia.
Salinity (Khfaji and Norton 1979), grazing (Lubchenco 1982; Worm and
Chapman 1998), and competition (Lubchenco 1980; Chapman 1990) all
have the potential to affect the distribution of seaweeds. Since F.
radicans is only found in low salinities I investigated if there was a
gradient in the abundance of F. radicans in response to salinity and if this
gradient could be mirrored in reverse for the potential competitor F.
vesiculosus. My survey in paper I showed that there were no such
gradient, but that the two species were equally and randomly distributed
along the Swedish Bothnian Sea coast. Since we know of no abiotic
factor that limit the range of F. radicans this raises the question of why
F. radicans is not found further south. A possible explanation for the
distribution of F. radicans could be that, as I show in paper I, a common
grazer, I. baltica, is both more abundant on F. radicans and consumes
more of F. radicans compared to F. vesiculosus, possibly because F.
radicans has lower levels of phlorotannins. Another reason could be that
F. vesiculosus is a stronger competitor, but there have been no studies
that compare the competitive abilities of F. radicans and F. vesiculosus
directly. The growth rate was found to be the same for F. radicans and F.
vesiculosus in a common garden experiment (paper I). However since F.
vesiculosus thalli are significantly larger there could be shading (Choi
2005) and whiplash effects (Kiirikki 1996a) as well as competition for
space (Lubchenco 1980). Since F. radicans is a newly evolved species
25
(Pereyra et al. 2009) another explanation for the current range of F.
radicans could be that it is still spreading further south. Since fucoid
algae usually don’t spread far or fast (Arrontes 1993; Serrão et al. 1997)
this process could take a long time.
The most common grazers, I. baltica and Gammarus spp., in the Baltic
Sea were more common on F. radicans compared to F. vesiculosus in
Sweden and F. radicans were also grazed more than F. vesiculosus in
Sweden (paper I). However, since F. radicans and F. vesiculosus in
Sweden hosts the same amounts of taxa, but F. radicans is smaller (Fig.
3 and paper I Fig. 3), this means that a specified biomass of F. radicans
will contain more species than the same biomass of F. vesiculosus.
Combined with the results in paper I that also suggest that a specified
biomass of F. radicans will contain a higher abundance of animals
compared to the same biomass of F. vesiculosus this suggests that it
would be interesting to measure the average biomass of F. radicans and
F. vesiculosus for a specified area. This would indicate if the abundance
and diversity of the associated community could be expected to depend
on the relative abundance of F. radicans and F. vesiculosus. This was the
first study of the associated community of F. radicans in Estonia and I
found that there was no difference between F. radicans and F.
vesiculosus in abundance and taxon richness. However both F. radicans
and F. vesiculosus were host to species that were not found on the other
Fucus species (Table 1). The data needs further analysis to understand
more details about what species makes these differences. However, these
preliminary results indicate that the identity of the host species is
important both in Sweden and Estonia and that a site where both F.
radicans and F. vesiculosus grows will likely host a more diverse and
abundant associated community than a site with only one of the two
Fucus species.
26
Figure 3. Preliminary data from the second survey showed that A) there
was no difference in number of taxa per thallus, B) that in Sweden more
animals were found on Fucus vesiculosus than on F. radicans but that
there were no difference in animal abundance in Estonia, and C) that
Swedish F. vesiculosus were heavier than F. radicans but that there were
no difference in dry weight between the two species in Estonia. Error
bars shows a 95% confidence interval.
27
Since biodiversity at different levels (ecosystem, community, population)
have been shown to be beneficial for the resilience and function of
communities (Hughes and Stachowicz 2004; Hooper et al. 2005;
Stachowicz et al. 2007; Hughes et al. 2008) this finding has an important
implication for the management of the Baltic Sea. It is important to
separate the two Fucus species in inventories and since we don’t know
what factors that determines if F. radicans or/and F. vesiculosus are
present at a site and what induces and makes the vegetative reproduction
of F. radicans possible, further studies are needed.
In the studies of phlorotannin as herbivore defense (paper I and II) I
found that the grazers consumed more of the algae that had the lowest
levels of phlorotannins. The Swedish F. radicans were grazed
significantly more by I. baltica and Gammarus spp. and had significantly
lower levels of phlorotannins compared to Swedish F. vesiculosus
(paper I). This further confirms previous studies that show the effect
phlorotannin has as herbivore defense (Geiselman and McConnell 1981;
Amsler and Fairhead 2006; Wikström et al. 2006).
The Icelandic F. evanescens was grazed significantly more by L. littorea,
both as live tissue and incorporated in agar, than the Swedish F.
evanescens that had significantly higher levels of phlorotannins (paper
II). This shows that it is the herbivory defense measured as phlorotannin
levels in this study, not novelty of the species to the area that influences
the consumption by L. littorea in this system. These results show that
assuming that a NIS (Non-Indigenous Species) will have the same
characteristics when it is introduced as where it is native is not always
correct, and it has been pointed out that studies of NIS will benefit from
studying the NIS both in the native and recipient community (Hierro et
al. 2005) or other Fucus species.
In Estonia F. radicans reproduces in August and September, while F.
vesiculosus reproduces in May and June (paper III). The release of eggs
is usually synchronous, but a few eggs can be released later than the
peak, thus there could be a small overlap in reproduction. However, this
difference in time would function as a reproductive barrier that can
explain how two so closely related species that grows in sympatry could
form and remain isolated. In Sweden F. vesiculosus in the southern part
of the Baltic Sea reproduce at two times (Berger et al. 2001) and it is
28
possible that the difference in time of reproductive period could be
beneficial in avoiding competition with filamentous algae (Berger et al
2001; Berger et al. 2004; Kraufvelin et al. 2007).
In Sweden there was no difference between F. radicans and F.
vesiculosus in time of reproduction at the scale studied here. However,
recent studies indicates that difference in reproductive timing at the
scales of hours could function as reproductive barriers (Monteiro et al.
2012) and studies at finer scales are necessary to rule out reproductive
barriers at the scales of hours. Hybridizing F. radicans and F. vesiculosus
in the laboratory showed that the fertilization success and survival during
the first two weeks after fertilization for hybrids were the same as that for
F. vesiculosus zygotes and germlings. This means that no reproductive
barriers between F. radicans and F. vesiculosus were found in Sweden.
The long term survival and reproductive abilities of the hybrids needs to
be investigated to be able to understand if the reason the hybrids in paper
III did not survive is because of them being hybrids or because the
environmental conditions in the laboratory were unfavorable.
Swedish F. radicans produces significantly more adventitious branches
than Estonian F. radicans and both Swedish and Estonian F. vesiculosus
and significantly fewer receptacles than Estonian F. radicans and F.
vesiculosus (paper III). These differences in reproductive allocation
indicate that Swedish F. radicans has an asexual reproductive mode,
further confirming that F. radicans reproduces mainly asexually
(Bergström et al. 2005; Tatarenkov et al. 2005).
In the last study (paper IV) I compared the phenotypic variation in nine
traits for three groups of F. radicans clones and one group of unique F.
radicans individuals to see if a population that has low genetic diversity
will have low phenotypic variation. Variation in phlorotannin content,
recovery after desiccation, and recovery after freezing was found to
depend on genetic variation while the other traits were independent of
genetic variation. However, phenotypic variation within the clones was
only 68% of the variation within the group of unique individuals.
Phenotypic variation could be assumed to confer benefits to the
population, and if the species is a habitat for other species, for the
associated community as well (Hughes and Stachowicz 2004). The
results indicate that the genetic diversity of F. radicans will be
29
manifested as phenotypic variation and that sites where one or a few
clones dominate will have a more homogenous Fucus population than
those with higher genetic diversity.
In this thesis I found that F. evanescens has different chemical
compositions in the studied regions and that F. radicans has different
chemical compositions, reproductive periods, and reproductive modes in
the studied regions. These results further confirms that we cannot assume
that one species has the same characteristic over larger regions, and these
possible variations has to be taken into account when making
assumptions about the ecology and ecophysiology of one species and its
interactions over larger regions.
Acknowledgements
Thanks to Lena Kautsky and Ove Eriksson for comments on the thesis. I also
want to thank Jonne Kotta for help with the survey in Estonia. Thanks to Meg
Peresich for proof reading parts of the thesis.
30
References
Amsler CD, Fairhead VA (2006). Defensive and sensory chemical
ecology of brown algae. Advances in Botanical Research 43:1-91.
Andersson S, Kautsky L, Kalvas A (1994). Circadian and lunar gamete
release in Fucus vesiculosus in the atidal Baltic Sea. Marine
Ecology-Progress Series 110:195-201.
Arrontes J (1993). Nature of the distributional boundary of Fucus
serratus on the north shore of Spain. Marine Ecology Progress
Series 93:183-193.
Bellwood DR, Hoey AS, Choat JH (2003). Limited functional
redundancy in high diversity systems: resilience and ecosystem
function on coral reefs. Ecology Letters 6:281-285.
Berger R, Malm T, Kautsky L (2001). Two reproductive strategies in
Baltic Fucus vesiculosus (Phaeophyceae). European Journal of
Phycology 36:265-273.
Berger R, Bergström L, Graneli E, Kautsky L (2004). How does
eutrophication affect different life stages of Fucus vesiculosus in
the Baltic Sea? a conceptual model. Hydrobiologia 514:243-248.
Bergström L, Bruno E, Eklund B, Kautsky L (2003). Reproductive
strategies of Ceramium tenuicorne near its inner limit in the
brackish Baltic Sea. Botanica Marina 46:125-131.
Bergström L, Tatarenkov A, Johannesson K, Jönsson RB, 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.
Bernes C (2005). Change Beneath the Surface - An In-Depth Look at
Sweden’s Marine Environment. Värnamo, Monitor 19,
Naturvårdsverket.
Billard E, Serrão EA, Pearson GA, Engel CR, Destombe C, Valero M
(2005). Analysis of sexual phenotype and prezygotic fertility in
natural populations of Fucus spiralis, F. vesiculosus (Fucaceae,
Phaeophyceae) and their putative hybrids. European Journal of
Phycology 40:397-407.
Blossey B, Nötzold R (1995). Evolution of increased competitive ability
in invasive nonindigenous plants - a hypothesis. Journal of Ecology
83:887-889.
Björck S (1995). A review of the history of the Baltic Sea, 13.0-8.0 ka
BP. Quaternary International 27:19-40.
31
Booth RE, Grime JP (2003). Effects of genetic impoverishment on plant
community diversity. Journal of Ecology 91:721-730.
Brawley SH (1992). Fertilization in natural populations of the dioecious
brown alga Fucus ceranoides and the importance of the
polyspermy block. Marine Biology 113:145-157.
Britton-Simmons KH (2004). Direct and indirect effects of the
introduced alga Sargassum muticum on benthic, subtidal
communities of Washington State, USA. Marine Ecology-Progress
Series 277:61-78.
Bäck S, Collins JC, Russel G (1992). Comparative ecophysiology of
Baltic and Atlantic Fucus vesiculosus. Marine Ecology Progress
Series 84:71-82.
Cerda O, Karsten U, Rothäusler E, Tala F, Thiel M (2009).
Compensatory growth of the kelp Macrocystis integrifolia
(Phaeophyceae, Laminariales) against grazing of Peramphithoe
femorata (Amphipoda, Ampithoidae) in northern-central Chile.
Journal of Experimental Marine Biology and Ecology 377:61-67.
Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds
HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz
S (2000). Consequences of changing biodiversity. Nature 405:234242.
Chapman ARO (1990). Competitive interactions between Fucus spiralis
L and Fucus vesiculosus L (Fucales, Phaeophyta). Hydrobiologia
204:205-209.
Chapman ARO (1995). Functional ecology of fucoid algae - 23 years of
progress. Phycologia 34:1-32.
Christie H, Norderhaug KM, Fredriksen S (2009). Macrophytes as
habitat for fauna. Marine Ecology-Progress Series 396:221-233.
Choi HG, Norton TA (2005). Competitive interactions between two
fucoid algae with different growth forms, Fucus serratus and
Himanthalia elongata. Marine Biology 146:283-291.
Colman J (1940). On the faunas inhabiting intertidal seaweeds. Journal of
the Marine Biological Association of the United Kingdom 24:129183.
Coyer JA, Peters AF, Hoarau G, Stam WT, Olsen JL (2002).
Hybridization of the marine seaweeds, Fucus serratus and Fucus
evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old
zone of secondary contact. Proceedings of the Royal Society of
London 269:1829-1834.
32
Coyer JA, Hoarau G, Skage M, Stam WT, Olsen JL (2006). Origin of
Fucus serratus (Heterokontophyta; Fucaceae) populations in
Iceland and the Faroes: a microsatellite-based assessment.
European Journal of Phycology 41:235-246.
Coyne JA, Orr HA (2004). Speciation, Sinauer Associates, Inc.
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders
NJ (2006). Plant genotypic diversity predicts community structure
and governs an ecosystem process. Science 313:966-968.
Dale M (1982). Phytosociological structure of seaweed communities and
the invasion of Fucus serratus in Nova Scotia. Canadian Journal of
Botany 60:2652-2658.
Dayton PK 1972. Towards an understanding of community resilience and
the potential effects of enrichments to the benthos at McMurdo
Sound, Antarctica. In: Parker BC ed. Conservations problems in
Antarctica. Lawrence, Kansas, Allen Press, Inc.
Deal MS, Hay ME, Wilson D, Fenical W (2003). Galactolipids rather
than phlorotannins as herbivore deterrents in the brown seaweed
Fucus vesiculosus. Oecologia 136:107-114.
Dijkstra JA, Boudreau J, Dionne M (2011). Species-specific mediation of
temperature and community interactions by multiple foundation
species. Oikos 121:646-654.
Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B,
Norberg J (2003). Response diversity, ecosystem change, and
resilience. Frontiers in Ecology and the Environment 1:488-494.
Elton C (1958). The ecology of invasions by animals and plants. London,
Methuen.
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.
Fulcher RG, McCully ME (1971). Histological studies on the genus
Fucus. V. An autoradiographic and electron microscopic study of
the early stages of regeneration. Canadian Journal of Botany
49:161-165.
Gamfeldt L, Källstrom B (2007). Increasing intraspecific diversity
increases predictability in population survival in the face of
perturbations. Oikos 116:700-705.
Geiselman JA, McConnell OJ (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.
33
Gianguzza P, Airoldi L, Chemello R, Todd CD, Riggio S (2002).
Feeding preferences of Oxynoe olivacea (Opisthobranchia :
Sacoglossa) among three Caulerpa species. Journal of Molluscan
Studies 68:289-290.
Hagerman L (1966). The macro- and microfauna associated with Fucus
serratus L., with some ecological remarks. Ophelia 3:1-43.
Hansen J, Wikström S, Axemar H, Kautsky L (2011). Distribution
differences and active habitat choices of invertebrates between
macrophytes of different morphological complexity. Aquatic
Ecology 45:11-22.
Hauser A, Attrill MJ, Cotton PA (2006). Effects of habitat complexity on
the diversity and abundance of macrofauna colonising artificial
kelp holdfasts. Marine Ecology Progress Series 325:93-100.
Hay ME, Steinberg PD (1992). The chemical ecology of plant-herbivore
interactions in marine versus terrestrial communities. In: Rosenthal
GA, Berenbaum MR ed. Herbivores: Their Interactions with
Secondary Plant Metabolites, Volume 2, Second Edition:
Ecological and Evolutionary Processes (Herbivores). San Diego,
California, Academic press. 372-413.
Hay ME (1996). Marine chemical ecology: What's known and what's
next? Journal of Experimental Marine Biology and Ecology
200:103-134.
Hierro JL, Maron JL, Callaway RM (2005). A biogeographical approach
to plant invasions: the importance of studying exotics in their
introduced and native range. Journal of Ecology 93:5-15.
Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S,
Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H,
Symstad AJ, Vandermeer J, Wardle DA (2005). Effects of
biodiversity on ecosystem functioning: A consensus of current
knowledge. Ecological Monographs 75:3-35.
Hughes AR, Stachowicz JJ (2004). Genetic diversity enhances the
resistance of a seagrass ecosystem to disturbance. Proceedings of
the National Academy of Sciences of the United States of America
101:8998-9002.
Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M
(2008). Ecological consequences of genetic diversity. Ecology
Letters 11:609-623.
Hylmö DE (1933). Algenimmigration nach der schwedischen Westküste.
Botaniska Notiser 1933:377-390.
34
Johannesson K (1988). The paradox of Rockall: why is a brooding
gastropod (Littorina saxatilis) more widespread than one having a
planktonic larval dispersal stage (L. littorea)? Marine Biology
99:507-513.
Johannesson K, André C (2006). Life on the margin: genetic isolation
and diversity loss in a peripheral marine ecosystem, the Baltic Sea.
Molecular Ecology 15:2013-2029.
Johannesson K, Johansson D, Larsson K, Cecilia H, Perus J, Forslund H,
Kautsky L, Pereyra R (2011). Frequent clonality in fucoids (Fucus
radicans and F. vesiculosus; Fucales, Phaeophyceae) in the Baltic
Sea. Journal of Phycology 47: 990-998.
Johnson MTJ, Agrawal AA (2005). Plant genotype and environment
interact to shape a diverse arthropod community on evening
primrose (Oenothera biennis). Ecology 86:874-885.
Jordan AJ, Vadas RL (1972). Influence of environmental parameters on
intraspecific variation in Fucus vesiculosus. Marine Biology
14:248-252.
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.
Kalvas A, Kautsky L (1993). Geographical variation in Fucus
vesiculosus morphology in the Baltic and North Seas. European
Journal of Phycology 28:85-91.
Kautsky H, Kautsky L, Kautsky N, Lindblad C (1992). Studies on the
Fucus vesiculosus community in the Baltic Sea. Acta
Phytogeographica Suecica 78:33-48.
Keane RM, Crawley MJ (2002). Exotic plant invasions and the enemy
release hypothesis. Trends in Ecology & Evolution 17:164-170.
Khfaji AK, Norton TA (1979). The effects of salinity on the distribution
of Fucus ceranoides. Estuarine and Coastal Marine Science 8:433439.
Kiirikki M (1996a). Experimental evidence that Fucus vesiculosus
(Phaeophyta) controls filamentous algae by means of the whiplash
effect. European Journal of Phycology 31:61-66.
Kiirikki M (1996b). Mechanisms affecting macroalgal zonation in the
northern Baltic Sea. European Journal of Phycology 31:225-232.
Korpinen S, Jormalainen V, Pettay E (2010). Nutrient availability
modifies species abundance and community structure of Fucus
associated littoral benthic fauna. Marine Environmental Research
70:283-292.
35
Kotta J, Orav-Kotta H, Paalme T, Kotta I, Kukk H (2006). Seasonal
changes in situ grazing of the mesoherbivores Idotea baltica and
Gammarus oceanicus on the brown algae Fucus vesiculosus and
Pylaiella littoralis in the central Gulf of Finland, Baltic Sea.
Hydrobiologia 554:117-125.
Kraufvelin P, Ruuskanen AT, Nappu N, Kiirikki M (2007). Winter
colonisation and succession of filamentous macroalgae on artificial
substrates and possible relationships to Fucus vesiculosus
settlement in early summer. Estuarine Coastal and Shelf Science
72:665-674.
Kubanek J, Lester SE, Fenical W, Hay ME (2004). Ambiguous role of
phlorotannins as chemical defenses in the brown alga Fucus
vesiculosus. Marine Ecology Progress Series 277:79-93.
Levin PS, Coyer JA, Petrik R, Good TP (2002). Community-wide effects
of nonindigenous species on temperate rocky reefs. Ecology
83:3182-3193.
Lodge DM (1993). Biological invasions - lessons for ecology. Trends in
Ecology & Evolution 8:133-137.
Lubchenco J (1980). Algal zonation in the New England rocky intertidal
community: An experimental analysis. Ecology 61:333-344.
Lubchenco J (1982). Effects of grazers and algal competitiors on fucoid
colonization in tide pools. Journal of Phycology 18:544-550.
Lubchenco J (1983). Littornia and Fucus: Effects of herbivores,
substratum heterogeneity, and plant escapes during succession.
Ecology 64:1116-1123.
Lüder UH, Clayton MN (2004). Induction of phlorotannins in the brown
macroalga Ecklonia radiata (Laminariales, Phaeophyta) in
response to simulated herbivory-the first microscopic study. Planta
218:928-937.
Lüning K. (1990). Seaweeds – their environment, biogeography and
ecophysiology. John Whiley & Sons, Inc, USA.
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA
(2000). Biotic invasions: Causes, epidemiology, global
consequences, and control. Ecological Applications 10:689-710.
Manton I, Clarke B (1956). Observations with the electron microscope
on the internal structure of the spermatozoid of Fucus. Journal of
Experimental Botany 7:416-432.
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.
36
Maron JL, Vila M (2001). When do herbivores affect plant invasion?
Evidence for the natural enemies and biotic resistance hypotheses.
Oikos 95:361-373.
McLachlan J, Bidwell RGS (1978). Photosynthesis of eggs, sperm,
zygotes, and embryos of Fucus serratus. Canadian Journal of
Botany 56:371-373.
McNaughton SJ (1977). Diversity and stability of ecological
communities: A comment on the role of empiricism in ecology.
The American Naturalist 111:515-525.
Monteiro CA, Serrao EA, Pearson GA (2012). Prezygotic barriers to
hybridization in marine broadcast spawners: Reproductive timing
and mating system variation. PLoS ONE 7.
Muller DG, Gassmann G (1978). Identification of sex attractant in
marine brown alga Fucus vesiculosus. Naturwissenschaften
65:389-390.s
Munda IM (2004). The structure and distribution of Fucacean
associations in the Icelandic coastal area. Acta Botanica Islandica
14:103-159.
Naylor E (1955). The diet and feeding mechanism of Idotea. Journal of
the Marine Biological Association of the United Kingdom 34:347355.
Niklas KJ (1997). The evolutionary biology of plants. Chicago and
London, The University of Chicago press.
Norton TA, Hawkins SJ, Manley NL, Williams GA, Watson DC (1990).
Scraping a living: a review of littorinid grazing. Hydrobiologia
193:117-138.
Nygård CA, Dring MJ (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.
Paul VJ, Hay ME (1986). Seaweed susceptibility to herbivory: chemical
and morphological correlates. Marine Ecology Progress Series
33:255-264.
Pavia H, Carr H, Aberg P (1999). Habitat and feeding preferences of
crustacean mesoherbivores inhabiting the brown seaweed
Ascophyllum nodosum (L.) Le Jol. and its epiphytic macroalgae.
Journal of Experimental Marine Biology and Ecology 236:15-32.
Pereyra R, Bergström L, Kautsky L, Johannesson K (2009). Rapid
speciation in a newly opened postglacial marine environment, the
Baltic Sea. BMC Evolutionary Biology 9:70.
37
Pimentel D, Zuniga R, Morrison D (2005). Update on the environmental
and economic costs associated with alien-invasive species in the
United States. Ecological Economics 52: 273-288.
Powell HT (1957). Studied in the genus Fucus L. II Distribution and
ecology of forms of Fucus distichus L. emend Powell in Britain
and Ireland. Journal of the Marine Biological Association of the
United Kingdom 36:663-693.
Råberg S, Kautsky L (2007). Consumer affect prey biomass and diversity
trough resource partitioning. Ecology 88:2468-2473.
Ragan MA, Glombitza K (1986). Phlorotannins, brown algal
Polyphenols. In: Round FE, Chapman DJ ed. Progress in
Phycological Research. Bristol, Biopress. Pp. 129-241.
Ravanko O (1969). Benthic algae as food for some evertebrates in the
inner part of the Baltic. Limnologica 7:203-205.
Remane A, Schlieper C (1971). Biology of brackish water. Die
Binnengewässer vol XXV. Stuttgart, Wiley.
Reusch TBH, Ehlers A, Hammerli A, Worm B (2005). Ecosystem
recovery after climatic extremes enhanced by genotypic diversity.
Proceedings of the National Academy of Sciences of the United
States of America 102:2826-2831.
Ricciardi A (2007). Are modern biological invasions an unprecedented
form of global change? Conservation Biology 21:329-336.
Robinson CB (1903). The distribution of Fucus serratus in America.
Torreya 3:132-134.
Roff J, Zacharias M (2011). Marine conservation ecology. Earthscan,
UK.
Rohde S, Molis M, Wahl M (2004). Regulation of anti-herbivore defence
by Fucus vesiculosus in response to various cues. Journal of
Ecology 92:1011-1018.
Ruuskanen A, Bäck S (1999). Morphological variation of northern Baltic
Sea Fucus vesiculosus L. Ophelia 50:43-59.
Salemaa H (1979). Ecology of Idotea spp (Isopoda) in the northern
Baltic. Ophelia 18:133-150.
Schaffelke B, Smith J, Hewitt C (2006). Introduced macroalgae – a
growing concern. Journal of Applied Phycology 18:529-541.
Schoenwaelder MEA, Clayton MN (1998). The secretion of phenolic
compounds following fertilization in Acrocarpia paniculata
(Fucales, Phaeophyta). Phycologia 37:40-46.
38
Schoenwaelder MEA, Clayton MN (1999). The presence of phenolic
compounds in isolated cell walls of brown algae. Phycologia
38:161-166.
Serrão EA, Kautsky L, Brawley SH (1996a). 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.
Serrão EA, Pearson G, Kautsky L, Brawley SH (1996b). Successful
external fertilization in turbulent environments. Proceedings of the
National Academy of Sciences of the United States of America
93:5286-5290.
Serrão EA, Kautsky L, Lifvergren T, Brawley SH (1997). Gamete
dispersal and pre-recruitment mortality in Baltic Fucus vesiculosus.
Phycologia 36(supplement).
Serrão EA, Brawley SH, Hedman J, Kautsky L, Samuelson G (1999).
Reproductive success of Fucus vesiculosus (Phaeophyceae) in the
Baltic Sea. Journal of Phycology 35:254-269.
Serrão EA, Alice LA, Brawley SH (1999). Evolution of the Fucaceae
(Phaeophyceae) inferred from nrDNA-ITS. Journal of Phycology
35:382-394.
Simmons HG. (1898). Algologiska notiser II. Eininge Algenfunde bei
Drøbak. Botaniska Notiser 117-123.
Smith JE, Hunter CL, Conklin EJ, Most R, Sauvage T, Squair C, Smith
CM (2004). Ecology of the invasive red alga Gracilaria salicornia
(Rhodophyta) on O'ahu, Hawai'i. Pacific Science 58:325-343.
Snoeijs P (1999). Marine and brackis waters. Acta Phytogeographica
Suecica 84:187-212.
Stachowicz JJ, Bruno JF, Duffy JE (2007). Understanding the effects of
marine biodiversity on communities and ecosystems. Annual
Review of Ecology Evolution and Systematics 38:739-766.
Steen H, Rueness J (2004). Comparison of survival and growth in
germlings of six fucoid species (Fucales, Phaeophyceae) at two
different temperature and nutrient levels. Sarsia 89:175-183.
Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes
JA, Tegner MJ (2002). Kelp forest ecosystems: biodiversity,
stability, resilience and future. Environmental Conservation
29:436-459.
Sumi CBT, Scheibling RE (2005). Role of grazing by sea urchins
Strongylocentrotus droebachiensis in regulating the invasive alga
39
Codium fragile ssp tomentosoides in Nova Scotia. Marine Ecology
Progress Series 292:203-212.
Swanson AK, Druehl LD (2002). Induction, exudation and the UV
protective role of kelp phlorotannins. Aquatic Botany 73:241-253.
Tatarenkov A, Bergström L, Jönsson RB, Serrão EA, Kautsky L,
Johannesson K (2005). Intriguing asexual life in marginal
populations of the brown seaweed Fucus vesiculosus. Molecular
Ecology 14:647-651.
Tatarenkov A, Jönsson RB, Kautsky L, Johannesson K (2007). Genetic
structure in populations of Fucus vesiculosus (Phaeophyceae) over
spatial scales from 10 m to 800 km. Journal of Phycology 43:675685.
Tomas F, Abbott JM, Steinberg C, Balk M, Williams SL, Stachowicz JJ
(2011). Plant genotype and nitrogen loading influence seagrass
productivity, biochemistry, and plant-herbivore interactions.
Ecology 92:1807-1817.
Vernet P, Harper JL (1980). The costs of sex in seaweeds. Biological
Journal of the Linnean Society 13:129-138.
Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996).
Biological invasions as global environmental change. American
Scientist 84:468-478.
Voipio A (1981). The Baltic Sea. Amsterdam, Elsevier.
Vreeland V, Waite JH, Epstein L (1998). Polyphenols and oxidases in
substratum adhesion by marine algae and mussels. Journal of
Phycology 34:1-8.
Wærn M (1952). Rocky-shore algae in the Öregrund archipelago. Acta
Phytogeographica Suecica 30:1-298.
Wahl M (1989). Marine epibiosis 1. Fouling and antifouling - some basic
aspects. Marine Ecology Progress Series 58:175-189.
Wahl M, Jormalainen V, Eriksson BK, Coyer JA, Molis M, Schubert H,
Dethier M, Karez R, Kruse I, Lenz M, Pearson G, Rohde S,
Wikström SA, Olsen JL (2011). Stress ecology in Fucus: Abiotic,
biotic and genetic interactions. In Lesser M ed: Advances in marine
biology, Oxford, Academic Press. 37-106.
Westerbom M, Kilpi M, Mustonen O (2002). Blue mussels, Mytilus
edulis at the edge of the range: population structure, growth and
biomass along a salinity gradient in the north-eastern Baltic Sea.
Marine Biology 140:991-999.
40
Wikström SA, 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.
Wikström SA, Steinarsdottir MB, Kautsky L, Pavia H (2006). Increased
chemical resistance explains low herbivore colonization of
introduced seaweed. Oecologia 148:593-601.
Wikström SA, 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.
Williams SL, Smith JE (2007). A global review of the distribution,
taxonomy, and impacts of introduced seaweeds. Annual Review of
Ecology, Evolution, and Systematics 38:327-359.
Winsor P, Rodhe J, Omstedt A (2001). Baltic Sea ocean climate: an
analysis of 100 yr of hydrographic data with focus on the
freshwater budget. Climate Research 18:5-15.
Worm B, Chapman ARO (1998). Relative effects of elevated grazing
pressure and competition from a red algal turf on two postsettlement stages of Fucus evanescens C. Ag. Journal of
Experimental Marine Biology and Ecology 220:247-268.
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Svensk sammanfattning
Tångarter är vanligt förekommande på norra halvklotet och utgör en
viktig del av ekosystemen längs kusterna eftersom den ger skydd och
utgör substrat och föda för många andra växter och djur. På svenska
västkusten finns ett flertal tångarter naturligt och en introducerad art,
ishavstång (Fucus evanescens). I Östersjön finns betydligt färre arter och
norr om Öland trodde man länge att blåstång (Fucus vesiculosus) var den
enda arten som kunde växa men man har nyligen hittat ytterligare en art
där – smaltång (Fucus radicans).
Främmande arter blir allt vanligare när transporter mellan områden och
avsiktliga introduceringar av organismer bland annat för odling ökar.
Främmande arter anses vara ett stort miljöproblem eftersom de innebär
att artsammansättningen i världen blir mer likartad och ibland
utkonkurreras de inhemska helt av de främmande arterna. Ett flertal
teorier diskuterar hur interaktionen mellan arter i systemet som den
främmande arten har introducerats till och den främmande arten påverkar
hur framgångsrik introduktionen är. Om systemet som den främmande
arten introducerats till är artrikt skulle man kunna tänka sig att det är
svårare för den främmande arten att etablera sig eftersom det kommer
finnas fler arter att konkurrera med och fler arter som kan påverka den
främmande arten negativt genom bete, parasitism och andra fiender.
Eftersom den främmande arten oftast saknar en gemensam evolutionär
historia med fiender i systemet som den introducerats till skulle man,
enligt ”Enemy Release” hypotesen (ERH), också kunna förvänta sig att
fienderna inte skulle veta att den främmande arten är ett lämpligt byte.
Det skulle innebära att den främmande arten får en fördel gentemot dess
konkurrenter och kan lägga mer resurser på tillväxt och förökning och på
så sätt få lättare att etablera sig.
För att testa om ERH kan vara en förklaring till att ishavstång har kunnat
etablera sig på den svenska västkusten och där inte konsumeras i någon
större utsträckning undersökte jag om de inhemska betarna konsumerade
mer ishavstång från Island, där den är inhemsk eller mer ishavstång från
Sverige. Om ERH gäller för ishavstång borde betarna äta lika mycket av
både den svenska och den isländska tången. Om de konsumerar olika
mycket av tången från de två länderna tyder det på att någon annan
mekanism styr betarnas preferens. I försöken konsumerade de svenska
betarna betydligt mer av ishavstång från Island än från Sverige.
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Ishavstång från Island innehöll betydligt lägre halter av florotanniner, en
kemikalie som har visat sig fungera som ett försvar mot betare.
Resultaten från studien visar att ERH inte kan förklara de mönster som
har observerats i Sverige, betarnas beteende beror antagligen inte på att
ishavstången är introducerad till Sverige utan på att den har högre halter
av försvarsämnen än konkurrenterna.
Det har länge varit känt att det finns många olika former av blåstång som
är en mycket variabel art. Vanligen anses förklaringen till dess olika
utseendena bero på miljöfaktorer som till exempel att blåstång inte har
några blåsor på exponerade lokaler men många blåsor på väldigt
skyddade lokaler. Ett annat exempel är en liten smalbladig form av
blåstång som påträffas i Bottenhavet. Att den var så liten ansågs bero på
den låga salthalten. Salthaltsstress är ett välkänt fenomen där marina arter
blir mindre i områden med lägre salthalt eftersom mycket energi går åt
till att reglera salthalten och det osmotiska trycket i cellerna vilket lämnar
mindre energi till tillväxt. Ett välkänt exempel på detta är blåmusslor som
är betydligt mindre i Östersjön än på västkusten. Men eftersom den lilla
varianten av blåstång växte bredvid den vanliga insåg man att det inte
kunde röra sig om två formvarianter med olika grad av salthaltstress. Om
den ena varianten var salthaltsstressad så borde den andra också vara det.
Med hjälp av noggranna morfologiska och genetiska studier kunde det
avgöras att den mindre morfen är en egen art, smaltång och de genetiska
studierna visade att smaltång till stor del är klonal.
Att smaltång nyligen upptäcktes innebär att det är mycket som man inte
vet om den och man vet inte heller om skillnaderna jämfört med blåstång
är så stora att de har någon effekt på de organismer som lever i
tångbältet. Men Östersjön är ett artfattigt hav som påverkas mycket av
människan genom en hög belastning av näringsämnen och gifter i
avrinningsområdet som är stort i förhållande till Östersjöns yta. Att det
finns två arter av tång i Bottenhavet och delar av norra egentliga
Östersjön skulle kunna vara viktigt för tångbältet och hela det ekosystem
som baseras på tången. Ett system med fler arter borde teoretiskt vara
mer heterogent och resilient, och många studier visar att så också är fallet
men det finns också studier som visar att diversa system är känsliga. Mitt
syfte med studierna av smaltång som presenteras i avhandlingen har varit
att ta reda på mer om smaltång och att jämföra den med blåstång för att
undersöka hur tångbältets organismer interagerar med den för att utröna
vilken betydelse smaltång har för Östersjön.
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Vid två inventeringar samlade jag in data om vilka organismer som lever
i och på smaltång och blåstång. Vid den första inventeringen gjordes en
beräkning av densiteten av de tre viktigaste betande arterna samt en
uppskattning av den relativa täckningsgraden av smaltång och blåstång
på 16 lokaler längs Sveriges kust från Väddö i söder till Umeå i norr. Om
smaltång är mer anpassad till en låg salthalt, som man skulle kunna tänka
sig eftersom den hittills bara hittats i låga salthalter, skulle man kunna
förvänta sig att den blev vanligare ju mer salthalten minskade i och med
att man kom längre norrut samtidigt som blåstång skulle bli mindre
vanlig eftersom den är anpassad för högre salthalter. I den andra
inventeringen gjordes en insamling av alla arter som hittades i en
tångruska genom att en finmaskig påse träddes över en tångplanta innan
den skars loss från bottnen och tången med alla medföljande organismer
frös ner för senare artbestämning. Denna inventering gjordes på sex
lokaler i Sverige och sex lokaler i Estland. Smaltång och blåstång var lika
vanliga inom smaltångens utbredningsområde förutom på de tre
nordligaste lokalerna, där vi inte fann någon blåstång och där man
tidigare bara funnit enstaka exemplar av blåstång. Med tanke på att vi
hittade lokaler med nästan bara blåstång och smaltång längre söderut är
det inte otänkbart att det bara är av slumpmässiga skäl, men det kan
också vara så att de nordligaste lokalerna (som ligger tätt och bara ca fem
mil norr om nästa lokal) utgör en gräns som inte blåstång klarar att växa
norr om. Längre norrut blir det för låg salthalt för att någon tång över
huvud taget ska kunna växa. Smaltång hyser fler djur per viktenhet
jämfört med blåstång, vilket är ett resultat som jag fick vid båda
inventeringarna i Sverige, men inte i Estland där densiteten djur var lika
stor på smaltång och blåstång. Resultaten visar även att smaltång i
Sverige har lägre halter florotanniner än blåstång och att tånggråsuggor
(Idotea balthica) föredrar att äta av smaltång om de får valet mellan
smaltång och blåstång.
För att två nära besläktade arter som lever i samma område, som
smaltång och blåstång gör, ska förhindras från att hybridisera med
varandra och så småningom bli en art krävs att det finns barriärer som
förhindrar ett genutbyte. Dessa barriärer kan vara olika former av
processer som förhindrar att de två arterna kan föröka sig med varandra
eller som gör att avkomman antingen inte är livsduglig eller steril.
Genom att notera när de toppar där ägg och spermier finns, receptaklerna,
mognade hos smaltång och blåstång från Sverige och Estland kunde jag
44
konstatera att i Estland förökar sig blåstång under maj – juni och
smaltång under augusti – september. Det innebär att det i Estland finns en
stark reproduktiv barriär som förklarar att de två arterna kan vara
separata trots att de växer i helt blandade bestånd. I Sverige finns ingen
sådan skillnad i tid för reproduktion och när jag korsade smaltång och
blåstång på konstgjord väg var befruktningsgraden och överlevnaden de
två första veckorna lika hög för hybrider som för blåstång. Det innebär
att jag inte hittade någon reproduktiv barriär i Sverige. Ytterligare studier
där man följer avkomman under en längre tid och studerar
reproduktionen i naturlig miljö krävs för att förstå vilka reproduktiva
barriärer som kan förklara att man inte har hittat hybrider av smaltång
och blåstång i Sverige.
I mina studier kunde jag se att smaltång producerar mer adventivgrenar,
som är de delar som ger vegetativ förökning, än svensk och estnisk
blåstång och estnisk smaltång. Den svenska smaltången har också färre
receptakler än vad blåstång och estnisk smaltång har. Dessa resultat
stämmer väl överens med tidigare genetiska och experimentella studier
som visar att smaltång i hög grad förökar sig vegetativt och bildar kloner.
En studie av hur genetisk diversitet påverkar fenotypisk variation, det vill
säga om genetisk diversitet påverkar hur mycket olika egenskaper som
storlek och tålighet varierar är intressant eftersom teorier om att en ökad
diversitet leder till högre resiliens i ett system. Eftersom smaltång är
klonal i hög utsträckning fanns möjligheten att titta på hur mycket
individer med samma genetiska identitet varierar och om denna
variationen är större eller mindre än variationen hos en grupp som består
av genetiskt unika individer.
Genom att studera variationen av nio egenskaper hos tre grupper
bestående av ett flertal plantor av samma klon och en grupp med
genetiskt unika individer, kunde jag konstatera att variationen var större i
gruppen av unika individer för återhämtning efter uttorkning, för
återhämtning efter frysning och för florotanninhalter. För övriga sex
mätta egenskaper fanns det ingen skillnad mellan de olika grupperna i
variation. Detta tyder på att den fenotypiska variationen ökar när den
genetiska variationen i en smaltångspopulation ökar, men påverkan är
egenskapsspecifik.
45
Studierna som jag har sammanfattat i avhandlingen visar att det finns
skillnader i egenskaper mellan blåstång och smaltång och att dessa
skillnader verkar påverka andra organismer i tångsamhället. Det är därför
viktigt att man i kommande inventering av Östersjöns särskiljer de två
arterna och att myndigheter strävar efter att förvalta Östersjön på ett sätt
som främjar både smaltång och blåstång samt den genetiska variationen
inom arterna. Eftersom vi inte vet vad som främjar smaltång och blåstång
eller den vegetativa förökningen behövs ytterligare studier. Studierna
visar också att det finns stora skillnader inom arter mellan områden och
att det är viktigt att inte dra generella slutsatser om en arts egenskaper
utifrån studier i ett område.
Tack Kerstin Juneberg för kommentarer på den svenska sammanfattningen!
46
Tack!
Först av allt vill jag tacka Lena Kautsky och Ove Eriksson som har
handlett mig under min doktorandtid. Lenas entusiasm och kärlek till
alger och speciellt tång är inspirerande och smittsamt. Ove har lärt mig
mycket om forskarvärlden och att skriva kort och koncist.
Sofia Wikström som handledde mig under mitt ex-jobb vilket ju ledde till
att jag började doktorera på Botan har lärt mig många värdefulla saker –
den viktigaste är nog att ”om man inte bryr sig om hur det ser ut klara
man det mesta” som en kommentar när vi låg ner på de glashala
klipporna vid hällkaret på Ursholmen och försökte åla oss in i
våtdräkterna till turisternas nöje.
Sonja Råberg, Henrik Pavia och Jonne Kotta har alla samarbetat med mig
och hjälpt mig att komma hit. Kerstin Johannesson, Ricardo Pereyra,
Daniel Johansson och alla andra på Tjärnö vill jag tacka för diskussioner
kring genetik och ett givande samarbete kring genetiken hos tången.
Ellen Schagerström har kommit som en frisk fläkt mot slutet av min
doktorandtid – och varit ett utmärkt levande referensverk via chatt.
Jessica Oremus och Annika Lindström har varit ovärderliga assistenter
utan vars hjälp mycket av det praktiska arbetet med avhandlingen hade
varit omöjligt. Sara, Anders, Cissi och Nastassja har också varit till stor
hjälp under fältarbetet.
Suss, Mattias, Eva, Calle, Eddie och Clara. Ni har hjälpt mig så mycket
och dessutom gjort Askövistelsen mycket trevligare. Jag har ju haft mitt
andra hem på Askö vissa somrar och att få lite sällskap och omtanke
förutom hjälp med det praktiska har gjort att det har känts hemtrevligt.
Tove, min rumskollega som disputerar dagen efter mig, vi har haft
mycket kul och det har varit skönt att dela rum med någon som varit i
samma fas. Lycka till! Alla andra doktorander på Botan vill jag tacka
bland annat för alla roliga diskussioner om allt mellan himmel och jord –
jag kommer sakna er. Till ni andra som också jobbar på Botan, från
professorer, TA-personal till före detta kursare – tack för hjälp, stöttning
och kamratskap.
Pappa är nog den person som gjort att jag blivit naturvetare – vi forskade
ju tillsammans redan innan jag börjat skolan! Tack för att du smittat mig
47
med din nyfikenhet och alltid har varit villig och intresserad av att hjälpa
mig med studierna eller annat.
Mamma du är inspirerande, uppmuntrande och har alltid stöttat mig i allt
jag har hittat på även när jag har förvånat dig eller velat göra saker som
du inte är intresserad av. Tack också för att du tog med mig på vår
Kanada resa – det var då jag bestämde mig för att studera biologi.
Hela min bonusfamilj – Göran, Christina, Gabbi, Theo, Wille, Alice,
Britt, Folke och Björn – jag ser er verkligen som en bonus som alla tillför
något viktigt till familjen.
Harald, Lotten och Brums Mums med kompani – ni kommer ju knappast
läsa det här men det är kanske just det jag uppskattar – ni visar att det
finns ett viktigt och kul liv utanför den akademiska världen som kräver
min fulla uppmärksamhet ibland.
Tomas – jag ser fram emot framtiden med dig – puss!
48
Appendix 1
F. radicans
Anisoptera spp. larvae
Asellus aquaticus
Balanus improvisus
Ceramium tenuicorne
Chiromnimus
Chironomidae
Chorda filum
Cladophora glomerata
Cyanophthalma obscura
Dichtyosiphon foeniculosus
Ectocarpales
Elachista fucicola
Electra crustalenta
Enteromorpha spp.
Fishfry
Furcellaria lumbricalis
Gammarus oceanicus
Gammarus salinus
Gammarus zaddachi
Gammarus tigrinus
Hydrobia spp
Idotea balthica
Idotea viridis
Jaera albifrons
Leptocheiros pilosus
Leptocheirus spp.
Lymnea stagnalis
Mya arenaria
Mytilus edulis
Nereis diversicolor
Palaemon adspersus
Parvicardium spp.
Pisicola geometra
Polysiphonia fibrillosa
Polysiphonia fucoides
Polysiphonia stricta
Praunus flexuosus
Praunus inermis
Prostoma obscurum
Prostomatella obscurum
Pungitius pungitius
Radix balthica
Rivularia
Skivsnäcka (Anisus contortus?)
Theodoxus fluviatilis
Trichoptera spp.
Ulva intestinalis
Total Number of taxa
x
x
x
Sweden
F. vesiculosus
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
29
F. radicans
x
Estonia
F. vesiculosus
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
35
x
x
x
33
x
x
x
32
49