EXAMENS ECHINODERMS - ECOSYSTEM FUNCTIONS AND …hh.diva-portal.org/smash/get/diva2:651640/FULLTEXT01.pdfAbstract Increasing attention has been given marine benthic macrofauna due

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CHANGES IN SPECIES DIVERSITY AMONG ECHINODERMS IN THE SILL AREA OF GULLMARSFJORDEN

EFFECTS ON CHANGES IN SPECIES COMPOSITION AMONG ECHINODERMS - ECOSYSTEM FUNCTIONS AND POSSIBLE CHANGES

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 echinoderm species are essential

bioturbators and thus important to marine ecosystems. However, Echinocyamus

pennatifidum, a sea urchin which is a valuable bioturbator may have established in the fjord

during the last century judging from this study. Species like Asterias rubens and

Psammechinus 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 ecology, 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 seaweed 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 invertebrates 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 Marthasterias 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, Ophiocomina nigra, which was not found in the other inventories.

39

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16 14

0

5

10

15

20

25

30

35

40

45

1908 1930 2005 2012

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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.

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

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.

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 crustaceans, 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 algae 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

animals 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

Taxonomy 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 predation 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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Table 2. Compilation of species found at inventories by Théel (1908), Molander (1930), Gislén (1930), unpublished data

(2005) and present study.

Appendix 1.

1908 (Théel, 1908)

1930 (Molander, 1930;

Gislén, 1930)

2005 (unpublished data,

2005)

2012 (Present study)

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 Luidia 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 Ophiura albida 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

Antedon petasus X X X