CHANGES IN DIVERSITY AMONG IN SPECIES DIVERSITY CHANGES OF IN THE SILL AREA GULLMARSFJORDEN SPECIES COMPOSITION AMONG EFFECTS ON CHANGES IN FUNCTIONS AND POSSIBLE CHANGES ECHINODERMS - ECOSYSTEM EXAMENSARBETE Abstract Increasing attention has been given marine benthic macrofauna due to its importance in marine ecosystems and for its value as bioindicator of environmental changes. One of the most abundant groups among benthic macrofauna are echinoderms which often hold keystone positions in the ecosystems and have proven to be good bioindicators. The aim of this study was to inventory echinoderms and analyze whether species diversity has change over time in Gullmarsfjorden, a fjord with limited water exchange and hence highly sensitive to environmental fluctuations. Also, what may have caused any changes and what potential effects can it have on ecosystems in the fjord, and which species may be valuable as bioindicators. The results show that species diversity of echinoderms has decreased significantly since the early 1900s and the main reduction have occurred among species living on/in soft or sandy bottoms. Many of the lost species are essential bioturbators and thus important to marine ecosystems. However, Echinocyamus pennatifidum, a which is a valuable bioturbator may have established in the fjord during the last century judging from this study. Species like Asterias rubens and miliaris, which are common in the fjord, have also proved to be valuable bioindicators for abiotic changes such as increased CO2-levels and pollution of heavy metals and PCB.

Sammanfattning Ökad uppmärksamhet har riktats mot marin bottenfauna de senaste åren till följd av dess betydelse inom marina ekosystem samt för deras värde som bioindikatorer av miljöförändringar. En av de mest förekommande djurgrupperna bland bottenlevande makrofauna är tagghudingar vilka ofta har nyckelpositioner i ekosystemen samt har visat sig vara bra bioindikatorer. Syftet med denna studie har varit att inventera tagghudingar samt analysera huruvida artmångfalden har förändrats över tiden i Gullmarsfjorden som är en fjord med begränsad vattenomsättning och således utgör en känslig miljö för eventuella förändringar. Syftet har också varit att se över vad som eventuellt kan ha orsakat dessa förändringar samt vilka effekter det kan ha på olika ekosystem i fjorden, men också vilka arter som kan vara värdefulla som bioindikatorer. Resultaten visar att artrikedomen bland tagghudingar har minskat avsevärt sedan början av 1900-talet och att den huvudsakliga minskningen har skett bland arter som lever på/i mjuka och sandiga bottnar. Bland de arter som förvunnit från Gullmarsfjorden är många betydelsefulla bioturbatorer och således viktiga inom de marina ekosystemen. Sjöborren Echinocyamus pennatifidum, som visats vara värdefull som bioturbator och därför gynnsam för bentiska ekosystem i fjorden, kan möjligen ha etablerat sig i fjorden under det senaste århundradet att döma från denna studie. Andra arter, som Asterias rubens och Psammechinus miliaris som också påträffats under studien har visat sig vara värdefulla bioindikatorer för abiotiska förändringar såsom syrebrist, ökade halter av CO2 samt föroreningar av tungmetaller och PCB.

Introduction Marine benthic macrofauna have over the years received increasing attention for its importance in marine ecosystems but also for its value as indicators of environmental changes so called bioindicators. In fact, recent European rules highlight the importance of using biological indicators to establish the ecological quality of European coasts and estuaries (Borja et. al. 2000; Shapouri 2012). Benthic macrofauna are considered optimal indicators of environmental change because they are relatively immobile and therefore cannot avoid fluctuations in water or sediment quality. In addition they have a long life-span and can thus indicate environmental changes with time (Kedra et. al. 2010; Nilsson & Rosenberg 1997; Borja et. al. 2000; Labrune et. al. 2007). Studies have revealed that benthic macrofauna respond rather quickly to anthropogenic and natural stress (Borja et. al. 2000). Moreover, macrofauna communities show high taxonomic diversity and represent all major feeding groups; filter- and suspension-feeders, feeders of sedimentary organic matter, predators and scavengers (Renaud et. al. 2011). Along with their abundance and diversity they can accordingly reflect conditions in several different areas and ecosystems (Langhamer 2010). In order to effectively use marine benthic macrofauna as bioindicators, it is important to have proper knowledge of the benthic ecosystems and their ecological processes to better identify potential changes. Several scientists have come to the conclusion that the composition of species may have a greater impact on ecological processes than the actual number of species (Cardinale et. al. 2000; Symstad et. al. 1998). More knowledge of species and their influence on ecological processes and relation to other species is therefore essential.

Benthic macrofauna play an important part in estuarine and coastal ecosystems, where they are an essential factor of the system dynamics, this include making up a large component of the food web and connecting primary producers to top consumers (Yu et. al. 2012; Harley et. al. 2006; Meire et. al. 2005). Despite the importance of estuarine ecosystems to marine diversity and , the high rate of human activities associated to estuaries and along coasts is leading to changes in these natural marine habitats (Yu et. al. 2012; Meire et. al. 2005; Hylland et. al. 1996). Knowing their importance, coastal marine environments are a focus of concern regarding the possible impacts of anthropogenic climate change (Harley et. al. 2006).

Gullmarsfjorden Gullmarsfjorden, or Gullmarn, is a fjord located on the Swedish West coast in Bohuslän. It is the only sill fjord in Sweden (Bergqvist 1975; Lawett 2009; Enebjörk & Fränne 2006; Karlsson 1982; Enebjörk et. al. 2006). A sill fjord is a fjord with a shallower part at the mouth created by the barrier-forming process acting at the foot of the glacier which formed the fjord in the first place (Dobson & Frid 2009). The sill has a mean depth of approximately 40-50 meters (Hjerpe et. al. 2004; Bergqvist 1975; Enebjörk & Fränne 2006; Hagberg & Tunberg 2000), which are considerable shallower then the fjord basin where the greatest depth is measured at 118.5 meters (Enebjörk & Fränne 2006; Hagberg & Tunberg 2000; Bekkby & Rosenberg 2006). This sill prevents continuous exchange of water between the fjord basin and the deep waters of Skagerrak (Bergqvist 1975) and normally water exchanges occur only about once a year (Enebjörk & Fränne 2006; Rosenberg et. al. 2002; Enebjörk et. al. 2006). The complexities of the water exchange that exist between the fjord basin and Skagerrak due to the sill have generated hydrological conditions, such as low temperature and high salinity, that would otherwise be seen in depths of 200-300 meters in the sea (Hjerpe et. al. 2004; Bergqvist 1975; Enebjörk & Fränne 2006). The consequence of this is that Gullmarsfjorden possesses a very rich and partly unique marine wildlife along with species that is otherwise only found on great depths or in arctic waters (Hjerpe et. al. 2004; Lawett 2011). However, the limited water exchange makes the fjord basin highly sensitive to hypoxia and pollution as well as eutrophication, which makes ecosystems in Gullmarsfjorden very vulnerable (Hjerpe et. al. 2004; Enebjörk & Fränne 2006; Enebjörk et. al. 2006).

The richness of the fjord regarding marine species have made it well known by marine scientists long since, and it is regarded as one of the best researched marine areas (Bergqvist 1975) and adjacent to Gullmarsfjorden are three marine research stations, Kristineberg Marine Research Station, Klubban Biological Station and Bornö Station (Enebjörk & Fränne 2006). On March 31, 1983 Gullmarsfjorden was declared a conservation area by the County Administrative Board of Gothenburg and Bohuslän, and in 2001 the fjord also received Natura 2000 status (Jonsson 2011), and became the first protected marine area in Sweden (Norling & Sköld 2002). In 1990 all trawling was banned in the fjord with the purpose of using the area as reference area for marine biological research together with the desire to protect reproduction and nursery area for many valuable fish species (Lindegarth et. al. 2000). But, on July 1, 1999 trawling was allowed again in some parts of the fjord, though highly restricted (Jonsson 2011).

Echinoderms Among benthic macrofauna one of the most abundant groups in the marine environment are echinoderms, and they hold a key position both in terms of biomass and ecological relevance (Barbaglio et. al. 2012; Coteur et. al. 2003). The echinoderms are a large group of approximately 7000 known species (Solomon et. al. 2008; Uthicke et. al. 2009; Dupont et. al. 2010) which are divided into five classes: Asteroidea (sea stars), Ophiuroidea (brittle stars), Echinoidea (sea urchins and sand dollars), Crinoidea (sea lilies and feather stars) and Holothuroidea (sea cucumbers) (Dorit et. al. 1991; Castor & Huber 1997; Solomon et. al. 2008; Dupont et. al. 2010; Uthicke et. al. 2009). In 1986 a sixth class of echinoderms was discovered named Concentricycloidea (sea daisies) in which only three species are known (Campbell et. al. 2008; Barnes et. al. 2001). Unique to echinoderms and common to all six classes is that they are exclusively marine (Dorit et. al. 1991; Solomon et. al. 2008; Dupont et. al. 2010; Uthicke et. al. 2009) and occurs in abundance in all oceans at all depths (Solomon et. al. 2008; Dupont et. al. 2010; Uthicke et. al. 2009).

Echinoderms have several important functions in ecosystems including acting as bioturbators and ecosystem engineers as well as being an important part of the food chain both as prey and predators (Dupont et. al. 2010). Many echinoderm species also hold keystone positions (Uthicke et. al. 2009; Dupont et. al. 2010), meaning that they have impacts on other species or processes in ecosystems beyond that what might be expected based on their abundance (Dalerum et. al. 2008). Due to their importance within ecosystems, their value as bioindicators have over the years received increased attention among scientists as well. Studies have shown that some echinoderms have proved to be valuable indicators of contaminations in the environment since they accumulate for instance heavy metals and PCB (Mah & Blake 2012; Coteur et. al. 2003). Scientists have also examined the impact of ocean acidification on echinoderms and potential following effects within ecosystems (Dupont et. al. 2010), and what effects upcoming ocean warming due to the climate change may have on echinoderm fertilization (Byrne et. al. 2010).

Unfortunately, echinoderms on the Swedish west coast have shown a negative trend in diversity over the past few years (Svensson & Karlsson 2010). Seven species of echinoderms have been added to the 2010 Red list which now comprises a total of 32 echinoderm species since 2005, and two of them, Amphiura securigera and Echinocardium pennatifidum, are recently discovered in Swedish waters (Karlsson et. al. 2010). Reasons for this reduction in some species are uncertain, although it is believed that trawling, eutrophication which generates sedimentation and hypoxia, and pollution, may be responsible factors (Norling & Sköld 2002; Karlsson et. al. 2010). In addition, insufficient knowledge of the situation of individual species among echinoderms has resulted in many species being assigned to the category Data Deficient (DD) of the Red List (Karlsson et. al. 2010). Thus, thorough inventories are highly important to assess the situation of species, along with repeated sampling to reflect how populations may change over time (Kedra et. al. 2010; Svensson & Karlsson 2010).

Aim of the study The purpose of this project is to analyze whether species diversity among echinoderms in Gullmarsfjorden has changed over time and how the situation is today. An enhanced knowledge of the species as well as the ecosystem provides a better position to determine possible future changes in the marine environment and how to take action against them. It also helps us understand the changes that have already taken place and what it could possibly be due to. The aim is therefore to try to determine the reasons for any changes in species diversity, but mainly what potential effects it may have on the ecosystem. The results of this study will hopefully provide valuable data for further investigations on echinoderm diversity associated with environmental changes and the value of echinoderms as bioindicators. Materials and methods

Study site and sampling The study was conducted in the outer sill area of Gullmarsfjorden between Lysekil and Grundsund and its associated archipelago. This area houses two deep trenches, Gåsörännan between Gåsö and Skaftlandet and Flatholmsrännan between Flatholmen and Stångenäset, through which water exchanges between the the fjord and the deeper parts of Skagerrak (Bergqvist 1975).This archipelago area houses diverse depths with a maximum of about 50 meters (Enebjörk & Fränne 2006; Bekkby & Rosenberg 2006), along with various bottom types (hard, shell-gravel, and soft bottoms) which provide numerous habitats and ecosystems (Hjerpe et. al. 2004).

Four sites where selected for sampling (figure 1), all with different bottom types in order to maximize inventoried ecosystems for echinoderms. Site 1 and 2 are located at the mouth of the fjord between Lysekil and Fiskebäckskil. Site 1 have a depth of approximately 15 meters and bottom (mainly Laminaria spp.) while site 2 have a depth of 12 meters and soft-shell bottom. Site 3 and 4 are located further south, in Gåsörännan outside Skaftölandet and Grundsund, with hard-shell bottom at a depth of approximately 40 meters and clay bottom at a depth of 37 meters respectively.

At each site one bottom scrape was made in order to collect epifaunal using a 1 meter wide trawl with 20 mm masks. All echinoderms were collected and placed in aquariums with running water received from 38 meters depth and then identified to the lowest possible taxonomic level using Hayward & Ryland (2011) and Moen & Svensen (2009). Sampling took place on August 22, 2012.

Figure 1. Gullmarsfjorden on the Swedish west-coast, with marked positions (1-4) of the sampling sites .(1-4). Historical data and statistical analyze Results from previous inventories made by Théel (1908), Molander (1930), Gislén (1930), and unpublished data sampled by students at Halmstad University (2005) were summarized to provide comparable data of echinoderms species diversity over the last hundred years. All echinoderm species from each inventory are presented in appendix 1. As Molander (1930) and Gislén (1930) conducted their inventories more or less during the same period and were published the same year, their results have been combined into one species list. This compilation has been used to discuss encountered species and changes in species composition.

Every identified species from each inventory were assigned to one of three general categories of bottom type; hard, shell-gravel and soft bottom, depending on which type they usually occur. These three categories were used as variables in a discriminant analysis to compare the different species communities and to see how the different inventories differ from each other regarding the species composition. This analysis was made using SPSS Statistics 20.

Results In the present study (2012) a total of 14 species were identified across all sites; 4 asteroids, 6 ophiuroids and 4 echinoids (table 1). Highest diversity was observed in site 2 with eight species found followed by site 3 with seven species. Site 1 showed the lowest diversity with four species found and in site 4 five species was found. A small number of echinoids in site 1 and 3 along with one asteroid in site 2 could not be accurately identified and was not included in the statistical analysis. Ophiothrix fragilis was the species that were found at most sites (site 2, 3 and 4). Site 3 showed four species that was only found at this site, three ophiuroids and one echinoid. Two species, Asterias rubens and Psammechinus miliaris, was only found in site 1, whereas glacialis was only found in site 2 and Brissopsis lyrifera was only found in site 4. Of the three classes found, only echinoids occurred at all four sites, and no species of crinoidea, holothuroidea or concentricycloidea were found in any of the four sites. No species were found at all four sites.

Table 1. Depth, bottom type and sampled species at each site. Statistical analysis and assessment of historical data A comparison of the previous inventories and the present one show how the number of species in Gullmarsfjorden has developed, which can be seen in figure 2. 1908s inventory has the highest number of species identified, and the present study shows the lowest number of identified species. A reduction in the number of species can be seen between each inventory conducted. Between 1908 and 1930 there has been a decrease of 43.6%, between 1930 and 2005 a decrease of 27.3%, and between 2005 and the present inventory, a decrease of 12.5% have occurred. Thus, between 1908 and the present inventory the number of species have decreased with 64.1%. In addition to reduced number of species between the different inventories there is also a difference in the class distribution between the inventories, and the number of found classes has decreased from five to three (figure 3). Four specific species, three in 1930 (Ophiura ophiura, Ophiocten affinis, Ophiura robusta) of which one (O. ophiura) also was found in 2005, and one (Echinocardium pennatifidum) in the present study, was not documented in 1908s inventory. None of these three species found in 1930 and 2005 was found in the present study. The inventory of 1908 and the present one had one species in common, , which was not found in the other inventories.

45 39 40 35 30 25 22 20 16 14 15 10

5 Numberofspecies found 0 1908 1930 2005 2012 Year of the inventory Figure 2. The number of species found at each inventory

Figure 3. Percentage distribution of echinoderm classes at each inventory. The discriminant analysis showed that 91.7% of the variables were correctly classified (figure 4). Samples from all years are clearly separated with species compositions that differ from each other, except 1908 and 2012 which are grouped together which mean that they have a more similar species composition compared to the other two inventories. 2005 have a species composition that differs from 1908 and 2012, and from 1930. 1930s inventory has in turn a species composition that differs even more from 1908 and 2012 compared to 2005.

Figure 4. A discriminant plot that shows how the species composition differs between the different inventories. The plot shows the years of the inventory along with three symbols for each year representing the three analyzed variables; hard bottom, shell-gravel bottom, and soft bottom. 1908 and 2012 are grouped together which means that they have a more similar species composition compared to 1930 and 2005. 1930 and 2005 are clearly separated and thus have a species composition that differs both from each other and from 1908 and 2012.

diagram showing the grouping of the inventories as a result of the discriminant analysis. Each inventory shows three circles which represent the three analyzed variables; hard bottom, shell-gravel bottom and soft bottom. Discussion A clear reduction of echinoderms species can be seen over the last hundred years based on the analyzed inventories in this study. The number of species found in each inventory differs with a clear decrease in species diversity between the different years, and with almost 65 % less species in the present inventory compared to Théels (1908). It is a reasonable assumption that the high number of species documented in Théels inventory is a result of several years of studies conducted over numerous sites, compared to the other three inventories which was conducted over a few single years and on much fewer sites. This is important to keep in mind during the comparisons of the different inventories, but despite the difference in number of sampling sites and time of collection the later inventories still gives us an indication of how the situation of echinoderm diversity looked at the time of the inventory. In addition, the two inventories from 2005 (unpublished data) along with the present inventory are spot inventories, whereas the other two are general inventories.

What can clearly be seen through the different inventories is that the difference in species composition over the years has been due to the loss of species and not so much the addition of new species. The four species that have been found in the later inventories but are not listed in Théels inventory (1908), all belongs to soft benthic communities, indicating that this habitat have suffered great changes in Gullmarsfjorden. The discriminant plot shows the grouping of the inventories based on the species found and on what type of bottom they were located. The plot indicates that the 1930s inventory and the 2005s inventory differs a lot, both from each other and from the other two with regards to species composition, whereas the 1908s inventory and the present inventory do not separate meaning that they have a similar species composition. The reason why has most likely to do with the fact that a number of species found in all four inventories have been located on other types of bottoms in the 1930s inventory and the 2005s inventory compared to the other inventories. The 1930s inventory also differs from the other inventories by the presence of the two species Ophiocten affinis and Ophiura robusta which are not found in the other three inventories. These two species are classified as Near Threatened in the Red List (Karlsson et. al. 2010) and could possibly be just temporary visitors since they don’t occur in the later inventories. Both the 1930s inventory and the 2005s inventory have one species in common, Ophiura ophiura, which are not found in the other two inventories. The present inventory is grouped close together with the 1908s inventory, probably because almost every species found were common to the 1908s study and they show many similarities in regards to the bottom type on which the species was found. In terms of species composition, one species (Echinocardium pennatifidum) were recovered only in the present study and one species (Ophiocomina nigra) was found in only the present inventory and the one from 1908. The reason for the absence of this species in the inventories from 1930 and 2005 is unclear and one may wonder whether this species actually disappeared from Gullmarsfjorden and then returned, or if it decreased severely in abundance, or simply was missed in the other inventories.

Among the 14 identified species of echinoderms found in the present inventory, only three classes (Asteroidea, Ophiuroidea and Echinoidea) of the six representing echinoderms where encountered for. No species of Crinoidea or Holothurioidea was found in contrast to previous inventories. Greatest decrease between the years has occurred among the holothurioids which have reduced from ten to two species between 1908 and 1930, and are totally absent in the later inventories. The distribution of echinoderm classes shown in figure 3 shows that the percentage distribution of echinoderm classes has changed between the inventories and the question is why. As the majority of species among holothurioids as well as among echinoids and ophiuroids occurs on soft or sandy bottoms the question is whether echinoids and ophiuroids have outcompeted holothurioids and hence are responsible for its reduction, or if the loss of holothurioids caused by other factors simple have left room for echinoids and ophiuroids to increase.

The reasons for the decline in species diversity amongst echinoderms are for the most parts unclear due to lack of research on the specific species. However, primary reasons for changes in the composition of macrobenthos are often an indicative of changes in environmental conditions (Labrune et. al. 2007). These changes are considered to be of anthropogenic and/or natural origin (Labrune et. al. 2007), and some of the most studied factors are the effects of trawling and eutrophication. Physical disturbance due to commercial trawling is considered one of the largest anthropogenic impacts on marine ecosystems threatening diversity and production in marine benthic habitats (Lindegarth et. al. 2000; Olsgard et. al. 2008; de Juan et. al. 2007; Hinz et. al. 2009; Shephard et. al. 2010). Studies have shown that trawling have had negative impact on benthic habitats in Gullmarsfjorden (Jonsson 2011), and trawling may thus very well be one explanation to the decreasing species diversity among echinoderms noted over the last hundred years in the fjord. It may also be a contributing factor to the clear separation and different species composition seen in the discriminant plot between the studied inventories. Although trawling is highly restricted in Gullmarsfjorden since 1999 (Jonsson 2011), previous trawling intensity may have been extensive enough to cause decreased species diversity among echinoderms and perhaps the restricted trawling activity is still extensive enough to negatively influence echinoderms directly or indirectly. It has been well documented that disturbance such as trawling often shift community structures from larger invertebrates such as , molluscs and echinoderms to smaller and more opportunistic polychaetes (Shephard et. al. 2010). The consequence of this may be that trophic levels in ecosystems change as a result of the loss of crustaceans, molluscs and echinoderms which are considered larger benthic predators and thus have a high impact on organisms in lower trophic levels (Jennings et. al. 2001). The loss of these invertebrates affects organisms in higher trophic levels as well, as they are a valuable food source for even larger predators, such as fishes. Another consequence may be that removal of benthic organisms that contribute to habitat complexity and structure, may lead to degradation of the habitat so it is no longer suitable for associated species (Kaiser et. al. 2000).

Eutrophication is also considered a major contributing factor to reduced species diversity. Gullmarsfjorden annually receive large quantities of nutrients from farmlands within the drainage area of the fjord (Enebjörk & Fränne 2006), and being an area sensitive to pollution, hypoxia and eutrophication it comes with consequences. Increased nutrition generates increased primary production resulting in decreasing light supply with depth (Enebjörk & Fränne 2006), and may lead to overgrowth of shallow bays (Norling & Sköld 2002). It also causes filamentous to increase rapidly and outcompete the natural seaweed belt (Lawett 2011), which for many echinoderms and other organisms make out primary components in the food-web (Moen & Svensen 2009). Many echinoids have keystone functioning as grazes on macroalgae and thus keeping the structure of species communities (Iken et. al. 2010). Alternation in primary production and species composition amongst algae may have a negative impact on these grazing species and as a consequence make ecosystems change from being top-down controlled to down-up controlled, thus changing the whole communities. Clear reductions in depth distribution of macro vegetation have also been seen in Gullmarsfjorden since the late 1990s, indicating an effect of eutrophication on the flora in the fjord (Enebjörk & Fränne 2006). With increased primary production, along with trawling and dredging, comes an increased sedimentation as well (Lawett 2011; Karlsson 2013c; Hansson 2010b; Hansson 2010c), which can generate habitat modifications. Species that naturally occur in firmer sediments as well as hard bottoms can thus be adversely affected by increased sedimentation (Enebjörk & Fränne 2006). This is considered to be the main reason for the reduction of species such as Porania pulvillus (Karlsson 2013c), Ocnus lacteus (Hansson 2010b), Hippasteria phrygiana (Hansson 2010a), and Echinocyamus pusillus (Hansson 2010c). The first three of these echinoderms species appear to have disappeared from Gullmarsfjorden according to the analyzed inventories in this study, raising the question if Gullmarsfjorden suffer from increased sedimentation. E. pusillus on the other hand, have been recovered in all four inventories and show no signs of disappearing from the fjord, which may indicate that this species perhaps have a higher tolerance against sedimentation, or that it has a slightly different habitat which has not been as exposed yet. Additionally, increased sedimentation often generates oxygen depletion on bottoms (Norling & Sköld 2002; Nilsson 2000; Bernes 2005) which can have severe consequences for benthic fauna in a fjord with reduced water exchange. For example, Amphiura filiformis have shown to have negative growth response to hypoxia due to increase load of organic matter (Nilsson 1999). However, according to the four inventories, A. filiformis show no signs of decreasing, but whether the species is suffering from negative growth response or not even if it occures in the fjord cannot be determined from this study. The various consequences due to eutrophication are thus supposed to be an additional great contributor to decreased species diversity within Gullmarsfjorden (Karlsson 2013a; Hansson 2010a; Karlsson 2013c; Hansson 2010b; Hansson 2010c). Just like trawling, eutrophication may accordingly very well be a contributing factor the clear separation seen in the discriminant plot.

In addition to trawling and eutrophication it is also possible that the increased activity of recreational boats may have had a contributory effect to the changes in species diversity seen among echinoderms. Recreational boats anchoring have been shown to negatively affect the bottoms by damaging the bottom vegetation, and through friction destroy habitats (Åslund et. al. 2010). Furthermore, the increased levels of recreational boats have also led to increased amounts of organic waste discharged into coastal areas, which in turn contributes to the eutrophication (Johansson 2009).

The majority of echinoderm species that seem to have disappeared from Gullmarsfjorden over the years normally occur on/in soft or sandy bottoms. This comes as no surprise as bottom trawling mainly occur on soft substrates (Bradshaw et. al. 2012) and remove all in its way, but also because of the increased sedimentation and hypoxia due to eutrophication (Lawett 2011; Karlsson 2013c; Norling & Sköld 2002; Nilsson 2000; Bernes 2005) which makes soft bottoms inhospitable for the benthic fauna. Many of the soft bottom echinoderms, i.e. irregular sea urchins, holothurioids and burrowing ophiuroids, are known to be very important bioturbators (Gilbert et. al. 2007; Barberá et. al. 2011; Hollertz & Duchene 2001), and therefore play an important part in oxygenation of the bottoms, as well as recycling of organic matter and keeping the structure of benthic communities (Gutiérrez et. al. 2000; Hollertz & Duchene 2001). Hence, reduction of several infaunal echinoderms can have multiple impacts on benthic communities as well as on several abiotic factors. However, a potential establishment of a new echinoid found in the present inventory Echinocardium pennatifidum, is a positive turn with regard to bioturbation as studies have shown that this species is one of the most effective bioturbator (Gilbert et. al. 2007; Lohrer et. al. 2004; Uthicke et. al. 2009) and thus can be a valuable addition to the benthic fauna and hold a keystone position in Gullmarsfjorden. Echinocardium pennatifidum has not been found in earlier inventories in Gullmarsfjorden (Théel 1908; Molander 1930; Gislén 1930; unpublished data 2005) and is considered a relatively new species among echinoids in Swedish waters (Karlsson et. al. 2010). The species have been reported in Swedish waters from a dozen sites in Skagerrak and Kattegatt by Jägerskiöld during the 1920-30s (Karlsson 2013a). However, when these sites were revisited by the Swedish Initiative during 2006-2009, the species was only recovered from one of them (Karlsson 2013a). In this inventory the specimens of Echinocardium pennatifidum was recovered from two sites in the present inventory, one with soft-shell bottom (site 2) and the other with clay bottom (site 4), while the species normally is seen on fine gravel-shell bottoms (Karlsson 2013a) indicating that the presence of the species on site 4 was merely a coincidence. Today the species is classified as Vulnerable in the Red List (Karlsson et. al. 2010), but the fact that the species was recovered on more than one site gives hope of a potential establishment and further monitoring of the species development in the fjord is therefore essential.

Echinoderms are important when it comes to bioturbation which is an essential process in making the soft sediment inhabitable for other species. Amongst echinoids the genus Echinocardium have been found to dominate bioturbation processes (Barberá et. al. 2011) which make the absence of the two Echinocardium species, Echinocardium flavescens and Echinocardium chordatum, in the present study from the outer sill area of the fjord somewhat worrying. Further examinations to determine whether these species have completely disappeared from the fjord and particularly what may be causing their reduction is highly recommended. Fortunately the echinoid Brissopsis lyrifera, which have proved to be an important bioturbator as well because of its size and common occurrence (Hollertz & Duchene 2001) show no signs of disappearing from the sill area of the fjord. Additionally, B. lyrifera has proved to highly influence the meiofauna in the sediment by causing disturbance, both by non-selective on meiofauna and alternation of the physical and chemical environment of the sediment due to its bioturbation (Austen & Widdicombe 1998; Hollertz & Duchene 2001). This results in lower sediment stability which affect the meiofauna community (Austen & Widdicombe 1998).

Among asteroids the species Asterias rubens has received great attention from scientists for its value as a bioindicator for heavy metals and PCB (Temara et. al. 1998; Coteur et. al. 2003). Studies have shown that uptake of Pb, Cd and PCB by the body compartments of A. rubens are directly related to the concentrations of these substances in the surrounding seawater (Temara et. al. 1998; Coteur et. al. 2003). Also, the species have proved to work well as a short-term bioindicator for metal contamination as their pyloric caeca shows a relatively rapid uptake and loss of metals and thus reacts quickly to environmental contaminations (Temara et. al. 1998). It also works well as a long-term bioindicator due to the fact that their body wall and endoskeleton accumulates metals rather quickly while showing long retention times (Boisson et. al. 2002; Temara et. al. 1998). A. rubens shows a stable presence in the fjord based on the analyzed inventories and can thus serve as a valuable tool in further analyzes of toxins and heavy metals found in Gullmarsfjorden.

Because of the increasing atmospheric CO2 levels, the world´s oceans are becoming warmer and slowly more acidic. An increasing scientific interest has risen about the potential impacts ocean acidification may have on echinoderms and its potential as bioindicator. As yet, little is known about how echinoderms will be affected by ocean acidification, but it is likely that they will be affected in varied ways including acid-base regulation, growth, reproduction, feeding and ultimately mortality (Miles et. al. 2007). The level of sensitivity to acidification and increased CO2-levels also appears to fluctuate among different species. For example, studies have shown that Psammechinus miliaris is a poor regulator of acid-base balance in response to short term environmental hypoxia and hypercarbia (abnormally high levels of

CO2 in the blood), and shows a low tolerance to pH below 7.0 (Miles et. al. 2007). Arm regeneration is affected by decreased pH during higher temperatures in Amphiura filiformis (Wood et. al. 2010), and some species of ophiuroids have also showed changes in oxygen uptake with reduced pH (Wood et. al. 2011). Wood et. al. (2010) also proved that Ophiura ophiura is able to survive increased temperatures and lower pH in the seawater but to a cost of reduced fitness and regeneration, which may indirectly reduce survival through poorer body condition and slower recovery from arm damage. For P. miliaris however, there is luckily no indication of species reduction in Gullmarsfjorden according to the four inventories analyzed in this study. The fact that O. ophiura is absent in the present inventory may perhaps indirectly have to do with abiotic changes causing reduced fitness and regeneration making it sensitive to other disturbances such as trawling and predation. Another species highly sensitive to acidification is the ophiuroid Ophiothrix fragilis which in a study by Dupont et. al. (2010) showed 100% mortality among larval at only a 0.2 unit decrease of pH. Being a very common and highly abundant species in many coastal communities O. fragilis may serve as a very good bioindicator of pH fluctuation. So far, no indications of reduction of this species can be detected by the analyzed inventories. As P. miliaris and O. fragilis show no indication of species reduction according to the inventories analyzed, abiotic changes such as acidification, hypoxia and hypercarbia, which may have occurred in Gullmarsfjorden over the last hundred years, are so far not severe enough to make these two species disappear. However, even if abiotic changes are not severe enough to eliminate species it may still have an impact, and therefore it is highly important to conduct further investigations on species abundance in addition to species occurrence.

Conclusions A change in species composition among echinoderms and a clear reduction in the number of species can be seen in Gullmarsfjorden over the last century, which may be natural as well as anthropogenicly caused. Based on echinoderm species composition and its development over the years which can be deduced from the four analyzed inventories, it seems that echinoderms in Gullmarsfjorden have suffered from problems with trawling and eutrophication, and primarily increased sedimentation. Concrete effects due to changes in abiotic factors, such as ocean acidification and hypercarbia due to increased levels of CO2 in the atmosphere, is more uncertain and cannot be positively determined from this study. Echinoderm species belonging to soft bottom communities have suffered the largest reduction in species diversity indicating that soft bottom environments in Gullmarsfjorden have been negatively affected over the last hundred years. How this will affect the benthic community in general in short-term as well as long-term is uncertain, and more research is needed to determine the degree of influence different species have on the ecosystems. Some of the species recovered in the present inventory, as well as some found in the previous inventories, have proved to hold keystone positions as bioturbators and some have shown to be valuable bioindicators for pollutants and abiotic changes. Therefore, it is important to keep monitoring the situation of echinoderms in Gullmarsfjorden to follow its development in the future, and also to investigate more species potential of holding keystone positions, or acting as bioindicator which will help in the observation of marine environmental changes.

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Appendix 1. Table 2 . Compilation of species found at inventories by Théel (1908), Molander (1930), Gislén (1930), unpublished data (2005) and present study. 1908 1930 2005 2012 (Théel, 1908) (Molander, 1930; (unpublished data, (Present study) Gislén, 1930) 2005) Asteroidea Marthasterias glacialis X X X X Asterias rubens X X X X Astropecten irregularis X X X Henricia spp. X X X X Crossaster papposus X X Psilaster andromeda X sarsii X Hippasteria phrygiana X Porania pulvillus X Lepasterias muelleri X X Stichastrella rosea X Solaster endeca X Echinoidea Echinocardium pennatifidum X Echinocyamus pusillus X X X X Brissopsis lyrifera X X X X Psammechinus miliaris X X X X Echinocardium chordatum X X X Echinus acutus X X Echinus esculentus X X X Strongylocentrotus droebachiensis X X Spatangus purpureus X Echinocardium flavescens X Holothurioidea Ocnus lacteus X X Leptopentacta elongata X X Leptosynapta inhaerens X Leptosynapta bergensis X Labidoplax buskii X Paracucumaria hyndmani X Thyone fusus X Psolus phantapus X Mesothuria intestinalis X Parastichopus tremulus X Ophiuroidea Ophiothrix fragilis X X X X X X X X Amphiura chiajei X X X X Amphiura filiformis X X X X Ophiopholis aculeata X X X Ophiocomina migra X X Ophiura ophiura X X Ophiocten affinis X Ophiura robusta X Ophiura sarsii X Crinoidea petasus X X X