1 23

Phytochemistry ReviewsFundamentals and Perspectives ofNatural Products Research ISSN 1568-7767Volume 12Number 3 Phytochem Rev (2013) 12:517-529DOI 10.1007/s11101-012-9243-7

Biodiversity of benthic invertebrates andbioprospecting in Icelandic waters

Sesselja Omarsdottir, Eydis Einarsdottir,Helga M. Ögmundsdottir, JonaFreysdottir, Elin Soffia Olafsdottir,Tadeusz F. Molinski, et al.

1 23

Your article is protected by copyright and

all rights are held exclusively by Springer

Science+Business Media B.V.. This e-offprint

is for personal use only and shall not be self-

archived in electronic repositories. If you wish

to self-archive your article, please use the

accepted manuscript version for posting on

your own website. You may further deposit

the accepted manuscript version in any

repository, provided it is only made publicly

available 12 months after official publication

or later and provided acknowledgement is

given to the original source of publication

and a link is inserted to the published article

on Springer's website. The link must be

accompanied by the following text: "The final

publication is available at link.springer.com”.

Biodiversity of benthic invertebrates and bioprospectingin Icelandic waters

Sesselja Omarsdottir • Eydis Einarsdottir • Helga M. Ogmundsdottir •

Jona Freysdottir • Elin Soffia Olafsdottir • Tadeusz F. Molinski •

Jorundur Svavarsson

Received: 13 November 2011 / Accepted: 21 June 2012 / Published online: 4 July 2012

� Springer Science+Business Media B.V. 2012

Abstract Iceland is an island in the North Atlantic

Ocean, with an exclusive economic zone of 200

nautical miles that is largely unexplored with respect

to chemical constituents of the marine biota. Iceland is

a geothermally active area and hosts both hot and cold

adapted organisms on land and in the ocean around it.

In particular, the confluence of cold and warm water

masses and geothermal activity creates a unique

marine environment that has not been evaluated for

the potential of marine natural product diversity.

Marine organisms need to protect themselves from

other organisms trying to overgrow, and some need to

secure their place on the bottom of the ocean.

Unexplored and unique areas such as the hydrothermal

vent site at the sea floor in Eyjafjordur are of particular

interest. In 1992 a collaborative research programme

on collecting and identifying benthic invertebrates

around Iceland (BIOICE) was established, with par-

ticipation of Icelandic and foreign institutes, univer-

sities and taxonomists on benthic invertebrates from

all over the world. Since the programme started almost

2,000 species have been identified and of those 41

species are new to science. Our recent bioprospecting

project is directed towards the first systematic inves-

tigation of the marine natural product diversity of

benthic invertebrates occurring in Icelandic waters,

and their potential for drug-lead discovery in several

key therapeutic areas.

Keywords Marine biodiversity � Bioprospecting �Benthic invertebrates � Icelandic waters �Hydrothermal vent sites

S. Omarsdottir (&) � E. Einarsdottir � E. S. Olafsdottir

Faculty of Pharmaceutical Sciences, School of Health

Sciences, University of Iceland, 107 Reykjavik, Iceland

e-mail: sesselo@hi.is

H. M. Ogmundsdottir � J. Freysdottir

Faculty of Medicine, School of Health Sciences,

University of Iceland, Laeknagardur, Vatnsmyrarvegur

16, 101 Reykjavik, Iceland

J. Freysdottir

Centre for Rheumatology Research, Landspitali

University Hospital, 101 Reykjavik, Iceland

J. Freysdottir

Department of Immunology, Landspitali University

Hospital, 101 Reykjavik, Iceland

T. F. Molinski

Department of Chemistry and Biochemistry, University

of California San Diego, La Jolla, CA 92093, USA

T. F. Molinski

Skaggs School of Pharmacy and Pharmaceutical Sciences,

University of California San Diego, La Jolla, CA 92093,

USA

J. Svavarsson

Faculty of Life and Environmental Sciences, School of

Engineering and Natural Sciences, University of Iceland,

101 Reykjavik, Iceland

123

Phytochem Rev (2013) 12:517–529

DOI 10.1007/s11101-012-9243-7

Author's personal copy

Introduction

Cancer and chronic inflammatory and/or degenerative

diseases are major causes of morbidity and mortality

in Western countries; a rising trend that cannot be

explained solely by aging of Western societies.

Therefore it has become the primary objective of

health care policies in Western countries to find means

to prevent and/or treat these conditions (WHO 2011).

Natural products have been the source of most of the

active substances of Western medicine (Harvey 2008)

and many revolutionary drugs essential in today’s

medical care are of natural origin (Li and Vederas

2009).

Marine natural product chemistry is relatively new

compared with phytochemistry. The terrestrial biota

has been investigated for a long time, yet large areas of

the oceans are still unexplored. The oceans cover more

than 70 % of the Earth’s surface and the marine biota

have a very long evolutionary history and vast

biodiversity (Cragg and Newman 2005, 2012). The

interest in marine natural product chemistry and

pharmacology research has grown significantly for

the last decades along with improvements in technol-

ogy regarding collection, screening, identification and

structural elucidation of natural products (Newman

and Cragg 2004). To date, approximately 22,000

compounds have been described from marine organ-

isms (MarinLit 2011) and three drugs derived from

marine invertebrates, two anticancer drugs and one

analgesic drug, are already on the market (Fornier

2011; Glaser and Mayer 2009; Molinski et al. 2009).

Iceland’s biogeography

In Nature, continual competition between different life

forms for survival is manifested among sessile marine

organisms in adaptations for defense from predation,

resistance to overgrowth, and acquisition of space

for colonization at the bottom of the ocean. Some

organisms have accomplished this through evolution

and deployment of hard shells or sharp appendages to

fend of predators, or motility for escape. Other

organisms, without physical defense, produce sub-

stances that serve as chemical defenses (Pawlik 2011).

Fig. 1 The currents around

Iceland (Valdimarsson

2011)

518 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

This has resulted in a tremendous diversity of bioac-

tive compounds produced by a variety of marine

organisms, such as sponges (phylum: Porifera), cni-

darians and bryozoans.

Iceland has a unique geology and geographical

position in the midst of the North Atlantic Ocean. The

high latitude combined with geothermal activity create

unusual conditions in the waters surrounding Iceland

calling for adaptations in organisms, which could be

expected to create diverse chemical defenses. How-

ever, these extensive waters around Iceland are largely

unexplored with respect to chemical constituents of

pharmacological interest. Iceland is located in the

northern part of the North Atlantic Ocean, just south of

the Arctic Circle and is the largest part of the Mid

Atlantic Ridge that rises above sea level. It has an

exclusive economic zone (EEZ) of 200 nautical miles

(758,000 km2). Many bays and deep fjords of various

shapes and sizes indent the coastline, but the south

shore is characterized by sandy beaches (Ingolfsson

1996). The island has the Irminger Sea to the west, the

Iceland Sea to the north, the Norwegian Sea to the east,

and the Iceland Basin to the south (Fig. 1) (Hansen and

Osterhus 2000). Several extensive submarine ridges

divide these oceanic regions; the Reykjanes Ridge,

which is a part of the Mid Atlantic Ridge, Greenland-

Iceland Ridge to the northwest of Iceland, and the

Iceland-Faeroe Ridge to the east of Iceland (Malmberg

2004) (Fig. 2). The volcanic active Reykjanes Ridge

reaches about 300–400 nautical miles to the southwest

into the North Atlantic Ocean and separates depths of

2,000–3,000 m on each side (Malmberg 2004; Ulrich

1963). It is a natural boundary between different water

masses originated from the north and south (Malmberg

2004). The Reykjanes Ridge has numerous steep

seamounts, reaching some hundreds of meters above

the surrounding seafloor. The extensive Iceland-Fae-

roe Ridge is a part of the Greenland-Scotland Ridge

Fig. 2 The submarine ridges around Iceland

Phytochem Rev (2013) 12:517–529 519

123

Author's personal copy

separating the Nordic Seas and the North Atlantic

Ocean. This is the only large ridge of the Atlantic

Ocean crossing the ocean in easterly-westerly direc-

tion. It separates depths of more than 4,000 m on both

sides and it is a natural boundary between the relatively

warm Atlantic water south of the Iceland-Faeroe

Ridge, flowing northwards and the cold (\1 �C, often

–0.9 �C) and deep water masses of the Nordic Seas and

the Arctic Ocean (Hansen and Osterhus 2000). Con-

sequently, the oceanic waters around Iceland have

areas with temperatures ranging from –0.9 �C to

around 12 �C (Fig. 3). The continental shelf varies

from 20 to 100 km offshore and at the shelf break

the depth drops from a few hundred meters to

Fig. 3 The near-bottom

temperature (a) and salinity

(b) in Icelandic waters,

recorded in autumn 2010

(Marine Research Institute

2011)

520 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

1,000–1,500 m (Malmberg 2004; Malmberg and

Magnusson 1982). The maximum depth in the Icelan-

dic EEZ is around 3,300 m (Anonymous 2011).

Iceland is a geothermally active area hosting warm-

water adapted organisms of particular interest. The

main submarine hydrothermal vents in Icelandic

surrounding waters located on the Reykjanes Ridge

(250–350 m) (Ernst et al. 2000; German et al. 1994),

near the island of Kolbeinsey (Jan Mayen Ridge)

(100 m) (Fricke et al. 1989), and east of Grımsey

(400 m) (Hannington et al. 2001). Numerous sites of

hot springs that are connected to terrestrial based

geothermal system have been found at intertidal areas

around Iceland (Benjamınsson 1988; Marteinsson

et al. 2001). Marine invertebrates located at the

geothermal fields in intertidal areas need the warm

water for survival and they have probably been

genetically isolated for thousands of years (Ingolfsson

1996; Morritt and Ingolfsson 2000).

One of the unique sites in Icelandic waters is the

hydrothermal vent site in the innermost part of

Eyjafjordur, a fjord in northern Iceland. These are

two clusters of smectite cones in shallow waters

(20–65 m depth) that were discovered in 1997

and 2004 and named Ystuvıkurstrytur and Ar-

narnesstrytur, respectively. Ystuvıkurstrytur are three

chimneys rising 33, 25, and 45 m from the 65 m deep

seafloor (Geptner et al., 2002; Marteinsson et al. 2001)

while Arnarnesstrytur is a larger hydrothermal area

located at 25–40 m depth and composed of a ridge of

cones of various sizes with highest one being 25 m

(Valtysson 2011). They are formed by precipitation

of SiO2-rich geothermal water (72–79 �C, pH 10)

flowing out of vent openings and Mg-rich seawater

(Geptner et al. 2002; Marteinsson et al. 2001) and it is

assumed that the formation of the cones began at the

end of the last Ice Age (Fig. 4a). On one hand these

cones resemble submarine hot springs with respect to

chemical composition and discharge of fluid, but on

the other hand, the structure of the chimneys resem-

bles more the deep-sea chimneys i.e. the black and

white smokers usually found at much greater depths

(2,000–6,000 m) (Geptner et al. 2002; Marteinsson

et al. 2001).

The macrofauna and flora living on these chimneys

has not yet been fully systematically mapped but

available information (pictures and videos) taken at

the hydrothermal vent site indicate a high diversity of

algae and benthic invertebrates occurring on and

sometimes covering the cones (Fig. 4b) (Valtysson

2011), with the exception of the top venting opening.

The origin and identification of the microbes isolated

from the geothermal fluid has been studied to a

certain extend. Fifty strains of thermophilic microbes

of terrestrial origin were isolated including a new

species (Marteinsson et al. 2001). The chimneys of

the Ystavıkurstrytur and Arnarnesstrytur vent sites are

unique ecosystems with a combination of ambient

cold seawater and out-flowing hot alkaline geother-

mal fluid, hosting warm-water adapted organisms of

particular interest for bioprospecting. These shallow

water vent sites host quite different organisms from

those in deep-waters and have the advantages of

being easily accessible by scuba diving in contrast to

the hydrothermal vent sites found in much deeper

waters.

Fig. 4 A picture of a smectite chimney in Eyjafjordur (a) and a

picture showing the diversity of benthic invertebrates living on

the chimneys (b) (photos: Erlendur Bogason)

Phytochem Rev (2013) 12:517–529 521

123

Author's personal copy

Biodiversity of benthic invertebrates in Icelandic

waters

Much of the basic knowledge of the benthic inverte-

brates in Icelandic waters stems from the remarkable

Ingolf Expedition in 1895 and 1896 (Wandel 1899).

During the Ingolf expedition numerous samples were

taken around Iceland, the Faeroe Islands and Greenland

during 2 months each of the respective 2 years. The

results were published later in the series The Danish

Ingolf Expedition, consisting of more than 5,500 printed

pages and numerous plates with illustrations.

The BIOICE project (Benthic Invertebrates of

Icelandic waters, 1991–2004) started with a pilot

cruise of the Norwegian RV Hakon Mosby in 1991 and

then formally in 1992. The BIOICE project was a

follow up of a similar project dealing with the benthic

animals around the Faeroe Islands, i.e. the BIOFAR

project (Norrevang et al. 1994). The objectives of the

BIOICE project were to map the distribution of

benthic invertebrates in Icelandic waters, and to

evaluate the species composition and biodiversity

within the Icelandic EEZ. The project had extensive

sampling effort in Icelandic waters. In all, 1050

samples at 579 stations were taken in 19 cruises with

the Icelandic RV Bjarni Sæmundsson, the Norwegian

RV Hakon Mosby and RV Magnus Heinason from the

Faeroe Islands, at depths between 18 and 3,018 m

(Fig. 5). The project relied much on international

cooperation, with nearly 200 participants from all over

the world. Within Iceland, the Ministry for the

Environment led the project, with participants from

the University of Iceland, Icelandic Institute of Natural

History and the Marine Research Institute.

A variety of sampling gear was used in the BIOICE

project, such as a modified Rothlisberg-Pearcy epi-

benthic sled (Brattegard and Fossa 1991; Rothlisberg

and Pearcy 1976), a Sneli sled (Sneli 1998), Agassiz

Fig. 5 A map of the 579 sampling stations of the BIOICE project

522 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

trawl, a Shipek sediment sampler and during two

cruises deep-sea photographs were also taken. The

samples were mostly preserved in 5 % neutralized

formalin or frozen, and later sorted at the Sandgerdi

Marine Centre, prior to dispatch abroad for identifi-

cation by specialists of the respective animal groups.

Table 1 New species to science described from the BIOICE project

Group Species Reference

Protozoa: Foraminifera Pyrgo labrum (Gudmundsson 1998)

Pyrgo pyxis (Gudmundsson 1998)

Nodosaria haliensis (Eiland and Gudmundsson 2004)

Cnidaria: Hydrozoa Eudendrium islandicum (Schuchert 2000)

Cladocarpus paraformosus (Schuchert 2000)

Mollusca: Gastropoda Protulira thorvaldsoni (Waren 1996)

Coccopigya lata (Waren 1996)

Alvania angularis (Waren 1996)

Alvania incognita (Waren 1996)

Brookesena turrita (Waren 1996)

Onoba improcera (Waren 1996)

Mikro globulus (Waren 1996)

Bryozoa Daisyella bathyalis (Rosso 2002)

Amphiblestrum frigidum (Rosso 2002)

Annelida: Polychaeta Bathyvermilia islandica (Sanfilippo 2001)

Chaetozone jubata (Chambers and Woodham 2003)

Myrioglobula islandica (Parapar 2003)

Myrioglobula malmgreni (Parapar 2003)

Terebellides bigeniculatus

Amphicteis wesenbergae

Ophelina basicirra

Ophelina bowitzi

(Parapar et al. 2011a, b)

(Parapar et al. 2011a)

(Parapar et al. 2011b)

(Parapar et al. 2011b)

Arthropoda: Crustacea:

Malacostraca: Amphipoda

Andaniexis lupus (Berge and Vader 1997)

Andaniexis eilae (Berge and Vader 1997)

Phippsiella bioice (Berge and Vader 1997)

Ampelisca islandica (BellanSantini and Dauvin 1997)

Stegocephalina biofar (Berge and Vader 1997)

Stegocephalina idea (Berge and Vader 1997)

Stegocephaloides barnardi (Berge and Vader 1997)

Megamphorus raptor (Myers 1998)

Laothoes pallaschi (Coleman 1999)

Metandania wimi (Berge, 2001)

Mysidacea Pseudomma maasaki (Meland and Brattegard 2007)

Pseudomma islandicum (Meland and Brattegard 2007)

Isopoda Haliophasma mjoelniri (Negoescu and Svavarsson 1997)

Quantanthura tyri (Negoescu and Svavarsson 1997)

Astacilla boreaphilis (Stransky and Svavarsson 2006)

Tanaidacea Paragathotanais vikingus (Bird 2010)

Echinodermata Amphioplus hexabrachiatus (Stohr 2003)

Ophioscolex tripapillatus (Stohr and Segonzac 2005)

Chordata Myxine jespersenae (Moller et al. 2005)

Phytochem Rev (2013) 12:517–529 523

123

Author's personal copy

Fig. 6 A map showing the collections sites, collection depths and number of benthic invertebrate specimens collected in Icelandic

waters in the recent bioprospecting project

Table 2 The number and taxonomy of the benthic invertebrate specimens collected in the bioprospecting project

Phylum Subphylum Class Subclass Order Common names No. of specimens

Porifera Sponges 384

Bryozoa Moss animals 7

Echinodermata Asterozoa Ophiuroidea Brittle star 3

Asterozoa Asteroidea Starfish 21

Echinozoa Holothuroidea Sea cucumber 4

Echinozoa Echionidea Sea urchin 8

Cnidaria Scyphozoa Jellyfish 1

Anthozoa Octocorallia Alcyonacea Soft corals 2

Anthozoa Hexacorallia Actiniaria Sea anemone 18

Anthozoa Hexacorallia Scleractinia Stony corals 3

Mollusca Gastropoda Snails & slugs 21

Bivalvia Bivalves 5

Arthropoda Crustacea Crabs, shrimps, etc. 19

Annelida Polychaeta Worms 8

524 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

The BIOICE project augmented considerably the

knowledge of the benthic invertebrates in Icelandic

waters. In all, 41 new species have now been described

(Table 1) and over 1,000 species not known previously

in these waters were reported. The project highlighted

the effects of the large Greenland-Iceland-Faeroe Ridge

on the distribution of the benthic animals in these waters,

where most species are either found north or south of the

Ridge (Brix and Svavarsson 2010; Stransky and Sva-

varsson 2006). The project has also provided valuable

information of potentially important groups for evalu-

ation of marine natural product diversity, such as

mass occurrences of the sponges (phylum: Porifera)

(Klitgaard and Tendal 2004). The project also allowed

evaluation of diversity patterns of benthic organisms

(Svavarsson 1997), showing that the deepest part (below

around 2,000 m) of the Nordic Seas (the Greenland,

Iceland and Norwegian Seas) is rather species poor,

while the shallower waters are fairly diverse with a

species-diversity maximum at 320–1,100 m. The diver-

sity of this group of organisms south of the Greenland-

Iceland-Faroe Ridge was very high.

The extensive background information of BIOICE

and the large coverage of the sampling have led to

further studies in the area. Recently, the first samples

of the IceAGE (Icelandic Animals, Genetics and

Ecology) project were taken during a month long

expedition in September 2011 on the German RV

Meteor (Brix S 2011 A report from the IceAge

expedition, unpublished). The objectives of the Ic-

eAGE project are partly to evaluate changes in the

species distributions in Icelandic waters due to

changes in the temperature, which has increased

slightly the last 10–15 year (Astthorsson et al. 2007).

Furthermore, the objectives were to use the current

data and earlier BIOICE data to model distributions of

Fig. 7 Expression of

surface markers on DCs.

Expression of a CD86 and

b HLA-DR on DCs matured

with or without crude extract

and fractions of Isodyctia

palmata (0.1–100 lg/ml) or

the positive control, vitamin

D3 (4 9 10-8M). The

results are shown as the

mean of four

experiments ? standard

error of mean and expressed

as percentage positive cells,

with the exception of the

results for the crude extract

(n = 1). *Different from

DCs matured without

fractions, p \ 0.05. mDC

mature DCs, VD3 vitamin

D3, Extract crude extract,

fraction A hexan fraction,

fraction BC chloroform

fractions, fraction D butanol

fraction, fraction E water

fraction

Phytochem Rev (2013) 12:517–529 525

123

Author's personal copy

benthic organisms. Last and not least the aim was to

sample specimens for analysis of the molecular

genetics of the deep-water organisms, in order to

augment information on their systematic and phylog-

eny. Additionally, several samples collected in the

IceAGE expedition, were frozen for further bioactivity

and chemical studies.

Bioprospecting benthic invertebrates

A recent research project has been initiated that aims

to investigate the potential of Icelandic marine

invertebrates as a source of new bioactive compounds.

Extracts of organisms that show interesting bioactivities

are subjected to bioassay-guided isolation in order to

identify the active constituents. The aim is to find

bioactive compounds that could prove to be of value as

potential drug leads and subsequently be used for further

pharmacological research and development. To date,

504 benthic invertebrate specimens have been collected

by scuba diving at the hydrothermal vent sites and by sea

excursions at the following locations at depths from 25

to 400 m (Fig. 6). The collected specimens were sorted

and the number of specimens in each phylum and class is

listed in Table 2. The majority of the specimens are of

Fig. 8 Secretion of cytokines by DCs. Secretion of a IL10 and

b IL-12p40 by DCs matured with or without crude extract and

fractions of Isodyctia palmata (0.1–100 lg/ml) or the positive

control vitamin D3 (4 9 10-8M). The results are shown as the

mean of four experiments ? standard error of mean, with the

exception of the results for the crude extract (n = 1). To correct

for difference in baseline cytokine secretion between different

DC donors the results are expressed as secretion index (SI),

which is calculated by dividing the concentration of cytokines

secreted by DCs matured with extract or fractions by the

concentration of cytokines secretion by DCs matured without

extract/fractions. *Different from DCs matured without frac-

tions, p \ 0.05. mDC mature DCs, VD3 vitamin D3, Extract

crude extract, fraction A hexan fraction, fraction BC chloroform

fractions, fraction D butanol fraction, fraction E water fraction

526 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

the phylum Porifera. Well-grounded estimation of the

number of collected species is about 250, although

taxonomical identification of all specimens is not

completed. All collected marine invertebrates are kept

at -20 �C. Lyophilized and homogenized invertebrates

are extracted 2–3 times with CH2Cl2:CH3OH (1:1) and

dried in vacuo. Stock solutions of 25 mg/ml (DMSO)

were prepared and stored at (-20 �C). Two hundred and

thirty extracts (at 33 lg/ml) have been screened for in

vitro cytotoxic effects on SkBr-3 breast cancer cells, Pc-

3 prostate cancer cells and HCT-116 colon cancer cells

and 25 extracts of sponges and bryozoans were shown to

decrease the viability by more than 50 % compared with

untreated cells by colorimetric assay. The active extracts

(IC50 * 10–15 lg/ml) were further fractionated by

modified Kupchan solvent partition and the cytotoxic

effects of the fractions measured using the same method.

Isolation of active compounds from three sponge (two

Halichondria sp. and one Haliclona sp.) is in progress.

In addition, 77 of the extracts have been screened for

immunomodulating activity in a human dendritic cell

model (Freysdottir et al. 2011). In this model, immature

monocyte-derived dendritic cells (DCs) are stimulated

with pro-inflammatory cytokines and lipopolysaccha-

rides to become mature DCs in the absence or presence

of extracts from the marine invertebrates. The effect of

the extracts on the stimulation of the dendritic cells is

determined by measuring the expression of surface

molecules participating in stimulation of naıve T cells

(HLA-DR and CD86) and the secretion of the pro-

inflammatory cytokines IL-6 and IL-12p40 and the anti-

inflammatory cytokine IL-10, all important in directing

the differentiation of naıve T cells towards Th17, Th1 or

Treg phenotypes, respectively. The maturation of DCs

in the presence of seven crude extracts (one bryozoan,

three porifera, two mollusca and one echinodermata) at

50–100 lg/ml obtained from marine invertebrates

resulted in lower proportion of DCs expressing CD86

and HLA-DR, reduction of the mean expression of these

molecules and lower secretion of the cytokines IL-

12p40 and IL-10 in comparison with DCs matured

without extracts. This pattern of response indicates

reduced inflammatory capacity of the DCs, as well as

reduced ability to stimulate naıve T cells. Bioassay-

guided isolation is in progress and further screening of

fractions of Isodyctia palmata sponge extract revealed

the highest activity for the nonpolar fractions, where the

secretion of IL-12p40 was almost completely sup-

pressed (Figs. 7, 8). Interestingly, the active extracts and

fractions were not cytotoxic. These results indicate the

presence of immunomodulating compound or com-

pounds in this sponge with drastic impact on the

activation of dendritic cells, which might suppress T cell

maturation towards the Th1 and/or Th17 phenotypes

with possible application in the treatment of autoim-

mune diseases.

Conclusion

Iceland has a unique geology and geographic location

on the Mid Atlantic Ridge providing unusual growing

conditions and diverse environmental settings for the

benthic invertebrates. Adaptation of the organisms to

this unusual and diverse environment might have

developed rich biodiversity and encourage the

search for pharmacologically interesting compounds.

Increased knowledge on marine biota around Iceland

has resulted from research projects such as the

BIOICE program. The total number of species of

benthic invertebrates in Icelandic waters may exceed

6,000 species. Extensive knowledge of distribution

and occurrences of these species is indeed very

important for further focused exploration of diversity

of bioactive compound in these waters. The mapping

of marine biodiversity of Icelandic waters and collab-

oration with other research groups on collection and

identification of the marine invertebrates is crucial for

the present bioprospecting project. The aim of that

project is to discover pharmacologically interesting

natural products from benthic invertebrates living in

Icelandic waters. Although the project is still in its

initial phase, preliminary results already include a

positive hit-list of extracts and fractions with activity

against cancer cells and on dendritic cells in vitro and

bioassay-guided isolation is in progress. In terms of

drug development it will be of great interest to

discover if the marine environment around Iceland

has influenced the evolution of unique and pharmaco-

logically active compounds by benthic invertebrates

occurring there.

Acknowledgments We thank Erlendur Bogason for scuba

diving, collection of samples and for taken pictures. Marine

Research Institute, the research vessel Meteor and several

fishermen are gratefully acknowledged for helping with

collection of benthic invertebrates. We also like to thank

Hedinn Valdimarsson at Marine Research Institute for useful

information and figures used in this paper. Rosa Olafsdottir,

Phytochem Rev (2013) 12:517–529 527

123

Author's personal copy

Institute of Earth Sciences is also acknowledged for preparing

figures used in this paper. We thank Dr. Hans Tore Rapp,

University of Bergen for identifying the sponges. Dr. Doralyn

Dalisay is acknowledged for performing a part or the cytotoxicity

tests. The Icelandic Research Fund, The University of Iceland

Research Fund and The Eimskip Fund of the University of

Iceland are acknowledged for financial support.

References

Anonymous (2011) Icelandic fisheries, information centre of the

Icelandic ministry of fisheries and agriculture. http://

www.fisheries.is/ecosystem. Cited 30 Oct 2011

Astthorsson OS, Gislason A, Jonsson S (2007) Climate vari-

ability and the Icelandic marine ecosystem. Deep Sea Res

Part II Top Stud Oceanogr 54:2456–2477

BellanSantini D, Dauvin JC (1997) Ampeliscidae (Amphipoda)

from Iceland with a description of a new species (Contri-

bution to the BIOICE research programme). J Nat Hist

31:1157–1173

Benjamınsson J (1988) Jardhiti ı sjo og flædarmali vid Island.

Natturufrædingurinn 58:153–169

Berge J (2001) Description of two new species of Stegocepha-

lidae (Crustacea, Amphipoda): Metandania wimi and

Stegocephalina trymi. Sarsia 86:213–220

Berge J, Vader W (1997) Stegocephalid (Crustacea, Amphi-

poda) species collected in the BIOFAR and BIOICE pro-

grammes. Sarsia 82:347–370

Bird GJ (2010) Tanaidacea (Crustacea, Peracarida) of the North-

east Atlantic: the Agathotanaidae of the AFEN, BIOFAR

and BIOICE projects, with a description of a new species of

Paragathotanais Lang. Zootaxa 2730:1–22

Brattegard T, Fossa JH (1991) Replicability of an epibenthic

sampler. J Mar Biol Assoc UK 71:153–166

Brix S (2011) A report from the IceAge expedition. http://

www.ifm.zmaw.de/fileadmin/files/leitstelle/meteor/M85/

M85-3-SCR.pdf

Brix S, Svavarsson J (2010) Distribution and diversity of des-

mosomatid and nannoniscid isopods (Crustacea) on the

Greenland-Iceland-Faeroe Ridge. Polar Biol 33:515–530

Chambers SJ, Woodham A (2003) A new species of Chaetozone

(Polychaeta : Cirratulidae) from deep water in the northeast

Atlantic, with comments on the diversity of the genus in

cold northern waters. Hydrobiologia 496:41–48

Coleman CO (1999) On Laothoes (Crustacea, Amphipoda;

Eusiridae) from the North Atlantic Ocean, with description

of a new species. J Nat Hist 33:799–811

Cragg GM, Newman DJ (2005) Biodiversity: a continuing

source of novel drug leads. Pure Appl Chem 77:7–24

Cragg GM, Newman DJ (2012) Natural products a sources of

new drugs over the 30 years from 1981 to 2010. J Nat Prod

75:311–335

Eiland M, Gudmundsson G (2004) Taxonomy of some recent

Nodosariinae (Foraminifera) from the North Atlantic, with

notes on wall lamination. Micropaleontology 50:195–210

Ernst GGJ, Cave RR, German CR, Palmer MR, Sparks RSJ

(2000) Vertical and lateral splitting of a hydrothermal

plume at Steinaholl, Reykjanes Ridge, Iceland. Earth Pla-

net Sci Lett 179:529–537

Fornier MN (2011) Approved agents for metastatic breast can-

cer. Semin Oncol 38(Suppl 2):S3–S10

Freysdottir J, Sigurpalsson MB, Omarsdottir S, Olafsdottir ES,

Vikingsson A, Hardardottir I (2011) Ethanol extract from

birch bark (Betula pubescens) suppresses human den-

dritic cell mediated Th1 responses and directs it towards

a Th17 regulatory response in vitro. Immunol Lett 136:

90–96

Fricke H, Giere O, Stetter K, Alfredsson GA, Kristjansson JK,

Stoffers P, Svavarsson J (1989) Hydrothermal vent com-

munities at the shallow subpolar Mid-Atlantic Ridge. Mar

Biol 102:425–429

Geptner A, Kristmannsdottir H, Kristjansson J, Marteinsson V

(2002) Biogenic saponite from an active submarine hot

spring, Iceland. Clay Clay Miner 50:174–185

German CR, Briem J, Chin C, Danielsen M, Holland S, James R,

Jonsdottir A, Ludford E, Moser C, Palmer MR, Olafsson J,

Rudnicki MD (1994) Hydrothermal activity on the Reyk-

janes Ridge: the Steinaholl vent-field at 63�060N. Earth

Planet Sci Lett 121:647–654

Glaser KB, Mayer AM (2009) A renaissance in marine phar-

macology: from preclinical curiosity to clinical reality.

Biochem Pharmacol 78:440–448

Gudmundsson G (1998) Distributional limits of Pyrgo species at

the biogeographic boundaries of the Arctic and the North-

Atlantic Boreal regions. J Foraminifer Res 28:240–256

Hannington M, Herzig P, Stoffers P, Scholten J, Botz R, Garbe-

Schonberg D, Jonasson IR, Roest W, Party SS (2001) First

observations of high-temperature submarine hydrothermal

vents and massive anhydrite deposits off the north coast of

Iceland. Mar Geol 177:199–220

Hansen B, Osterhus S (2000) North Atlantic-Nordic seas

exchanges. Prog Oceanogr 45:109–208

Harvey AL (2008) Natural products in drug discovery. Drug

Discov Today 13:894–901

Ingolfsson A (1996) The distribution of intertidal macrofauna

on the coasts of Iceland in relation to temperature. Sarsia

81:29–44

Klitgaard AB, Tendal OS (2004) Distribution and species

composition of mass occurrences of large-sized sponges in

the northeast Atlantic. Prog Oceanogr 61:57–98

Li JW, Vederas JC (2009) Drug discovery and natural products:

end of an era or an endless frontier? Science 325:161–165

Malmberg SA (2004) The Iceland basin-topography and

oceanographic features, vol 109. Marine Research Insti-

tute, Reykjavik, pp 1–13

Malmberg SA, Magnusson G (1982) Sea surface temperature

and salinity in south Icelandic waters in the period

1868–1965, vol 6. Marine Research Institute, Reykjavik,

pp 1–31

Marine Research Institute (2011) Marine research institute of

Iceland. http://www.hafro.is. Cited 30 Oct 2011

MarinLit Database (2011) Department of Chemistry, University

of Canterbury, New Zealand. http://www.chem.canterbury.

ac.nz/marinlit/marinlit.shtml. Cited 30 Oct 2011

Marteinsson VT, Kristjansson JK, Kristmannsdottir H, Dahlk-

vist M, Saemundsson K, Hannington M, Petursdottir SK,

Geptner A, Stoffers P (2001) Discovery and description of

giant submarine smectite cones on the seafloor in Eyjaf-

jordur, northern Iceland, and a novel thermal microbial

habitat. Appl Environ Microb 67:827–833

528 Phytochem Rev (2013) 12:517–529

123

Author's personal copy

Meland K, Brattegard T (2007) New Mysida (Crustacea) in the

genera Amblyops and Pseudomma from the Iceland Basin.

Zootaxa 1628:43–58

Molinski TF, Dalisay DS, Lievens SL, Saludes JP (2009) Drug

development from marine natural products. Nat Rev Drug

Discov 8:69–85

Moller PR, Feld TK, Poulsen IH, Thomsen PF, Thormar JG

(2005) Myxine jespersenae, a new species of hagfish

(Myxiniformes: Myxinidae) from the North Atlantic

Ocean. Copeia 2:374–385

Morritt D, Ingolfsson A (2000) Upper thermal tolerances of the

beachflea Orchestia gammarellus (Pallas) (Crustacea:

Amphipoda: Talitridae) associated with hot springs in

Iceland. J Exp Mar Bio Ecol 255:215–227

Myers AA (1998) New and little known Corophioidea (Am-

phipoda: Gammaridea) from Faroese and Icelandic waters.

J Mar Biol Assoc UK 78:211–222

Negoescu I, Svavarsson J (1997) Anthurideans (Crustacea,

Isopoda) from the North Atlantic and the Arctic Ocean.

Sarsia 82:159–202

Newman DJ, Cragg GM (2004) Marine natural products and

related compounds in clinical and advanced preclinical

trials. J Nat Prod 67:1216–1238

Norrevang A, Brattegard T, Josefson AB, Sneli JA, Tendal OS

(1994) List of Biofar stations. Sarsia 79:165–180

Parapar J (2003) Oweniidae (Annelida, Polychaeta) from Ice-

landic waters, collected by the BIOICE project, with a

description of Myrioglobula islandica n. sp. Sarsia 88:

274–290

Parapar J, Helgason GV, Jirkov I, Moreira J (2011a) Taxonomy

and distribution of the genus Amphicteis (Polychaeta:

Ampharetidae) collected by the BIOICE project in Ice-

landic waters. J Nat Hist 45:1477–1499

Parapar J, Moreira J, Helgason GV (2011b) Distribution and

diversity of the Opheliidae (Annelida, Polychaeta) on the

continental shelf and slope of Iceland, with a review of the

genus Ophelina in northeast Atlantic waters and descrip-

tion of two new species. Org Divers Evol 11:83–105

Pawlik JB (2011) The chemical ecology of sponges on Carib-

bean reefs: Natural products shape natural systems. Bio-

science 61:888–898

Rosso A (2002) A new anascan cheilostome bryozoan from

Icelandic deep waters and its uniserial colony growth pat-

tern. Sarsia 87:35–45

Rothlisberg PC, Pearcy WG (1976) Epibenthic sampler used to

study ontogeny of vertical migration of Pandalus jordani

(Decapoda, Caridea). Fish B NOAA 74:994–997

Sanfilippo R (2001) Bathyvermilia islandica (Polychaeta,

Serpulidae): a new deep-water species from south of Ice-

land. Sarsia 86:177–182

Schuchert P (2000) Hydrozoa (Cnidaria) of Iceland collected by

the BIOICE programme. Sarsia 85:411–438

Sneli JA (1998) A simple benthic sledge for shallow and deep-

sea sampling. Sarsia 83:69–72

Stohr S (2003) A new fissiparus amphiurid brittlestar (Echino-

dermata: Ophiuroidea) from southwest of Iceland. Sarsia

88:373–378

Stohr S, Segonzac M (2005) Deep-sea ophiuroids (Echinoder-

mata) from reducing and non-reducing environments in the

North Atlantic Ocean. J Mar Biol Assoc UK 85:383–402

Stransky B, Svavarsson J (2006) Astacilla boreaphilis sp nov

(Crustacea: Isopoda: Valvifera) from shallow and deep

North Atlantic waters. Zootaxa 1259:1–23

Svavarsson J (1997) Diversity of isopods (Crustacea): new data

from the Arctic and Atlantic Oceans. Biodivers Conserv

6:1571–1579

Ulrich J (1963) Der Formenschats des Meeresbodens. Geogr

Rundschau 15:136–148

Valdimarsson H (2011) Marine research institute, Reykjavik.

www.hafro.is. Cited 30 Oct 2011

Valtysson H (2011) Vistey-Biodiversity in arctic waters, Aku-

reyri. http://www.vistey.is. Cited 30 Oct 2011

Wandel CF (1899) Report of the voyage. Bianco Luno (F.

Dreyer), Copenhagen

Waren A (1996) New and little known Mollusca from Iceland

and Scandinavia. Sarsia 81:197–245

WHO (2011) World Health Organization http://www.who.

int/en/. Cited 30 Oct 2011

Phytochem Rev (2013) 12:517–529 529

123

Author's personal copy