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Marine Research Report
Bioluminescence – a source of marine energy?
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1
Bioluminescence – a source of
marine energy?
Dr. Jessica Craig
Prof. Imants G. Priede
February 2012
Oceanlab®, University of Aberdeen,
Main Street, Newburgh, Aberdeenshire,
U.K., AB41 6AA
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© Crown Copyright 2012
978-1-906410-32-2
Published by The Crown Estate on behalf of the Marine Estate.
This report is available on The Crown Estate website at: www.thecrownestate.co.uk
Dissemination Statement
This publication (excluding the logos) may be re-used free of charge in any format or medium. It
may only be re-used accurately and not in a misleading context. The material must be
acknowledged as Crown Estate copyright and use of it must give the title of the source publication.
Where third party copyright material has been identified, further use of that material requires
permission from the copyright holders concerned.
Disclaimer
The opinions expressed in this report are entirely those of the authors and do not necessarily reflect
the view of The Crown Estate, and The Crown Estate is not liable for the accuracy of the information
provided or responsible for any use of the content.
Suggested Citation
Craig J. and Priede, I.G. 2012.
‘Bioluminescence – a source of marine energy?’
The Crown Estate, 27 pages. ISBN: 978-1-906410-32-2.
i
Contents
Summary (i)
1. Introduction 1
2. Marine bioluminescence in the British Isles and adjacent seas 2
3. Energy extraction options 4
4. Bioluminescent energy calculations 7
5. Energy extraction proposals 9
5.1. Algae 9
5.2. Jellyfish 12
5.3. Bacteria 15
5.4. Leisure and tourism 16
6. Conclusions 17
References 19
Summary
This study investigates the potential for extraction of energy from bioluminescent marine organisms.
Bioluminescence species occurring around the British Isles and adjacent waters are listed. The report
considers a range of energy extraction options. The bioluminescent characteristics of various marine
animals, algae and bacteria are considered and the potential energy output calculated. Scenarios are
outlined in which energy harnessed from the production of bioluminescent light could be integrated
with existing and emerging commercial activities.
The most promising technology is the culture of planktonic algae (dinoflagellates) using methods
already developed for the production of algal biofuel. However, the energy available from
bioluminescence is less than 1% of that produced by the biofuel. We estimate that a plant extending
over 7 hectares would be necessary to sustain 1 kW of power generation exclusively from
bioluminescence.
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1. Introduction
Bioluminescence refers to light produced by living organisms. It is rare among terrestrial organisms
and virtually absent from freshwater environments. The majority of bioluminescent organisms live in
the marine environment, where they occur from the equator to the polar regions and from the coast
to the deep sea. A wide range of marine organisms are able to bioluminesce, including bacteria,
algae, fish, squid, crustaceans and jellyfish (Herring 1987; Haddock et al. 2010).
Bioluminescent light is produced by a chemical reaction. Although the chemistry is not the same for
all organisms, they do share the same base reaction. In this reaction, a luciferin (protein) reacts with
oxygen in the presence of a catalysing luciferase (enzyme). This produces an oxyluciferin which emits
a photon as it decays from a high energy state to a low energy state. Almost all the energy released
during the reaction is converted into light. In some cases, particularly among jellyfish, the oxygen,
luciferin and luciferase are combined in one molecule, a photoprotein, which emits lights when a
specific ion (such as Ca2+ or Mg2+) is added to the system (Shimomura 2006).
Although bioluminescence ranges in colour from ultra violet (wavelength, λ < 400 nm) to red (λ >
700 nm), most bioluminescence is blue or blue-green (ca. λ 450 – 500 nm), corresponding to the
wavelength of maximum optical transparency of seawater (Figure 1; Widder 2010). The intensity of
bioluminescent flashes largely depends on the emitting organism and ranges over several orders of
magnitude, from 108 to 1013 photons flash-1 (Figure 2; Priede at al. 2008).
In all organisms, except bacteria, light emission is controlled and only emitted in response to a
stimulus. Bioluminescent flashes generally range in duration from 10-1 to 101 seconds. In contrast,
bacteria only produce light when their population reaches a certain density threshold. When this
threshold is reached, bacteria produce a continuous glow. Light is produced by organisms for
defence, to find prey and for communication (Haddock et al. 2010).
Bioluminescence is most frequently used as a defence mechanism. This defence response can be
provoked by mechanical, electrical or chemical stimulation of the organism. The type and strength of
stimulation affects the intensity and duration of the resultant bioluminescent event. This possibly
provides a means of controlling bioluminescent light output and may facilitate its use as a resource.
To date the commercial application of bioluminescence has concentrated on a number of biomedical
and environmental assessment applications. The current major applications of bioluminescence
include using the firefly luminescence system as a method of measuring ATP (adenosine
triphosphate; used as a measure of biological activity); using photoproteins, such as aequorin from a
jellyfish, to detect intracellular Ca2+ (used to regulate various important biological processes), using
Cypridina luciferin within probes for measuring superoxide anions (an indicator of many pathological
conditions) and the use of bioluminescent bacteria to monitor pollution (Shimomura 2006; Girrotti
et al. 2008). There are also reports that during WWII, the Japanese collected large amounts of
bioluminescent ostracods (marine crustaceans), planning to use the material as a source of low
intensity light for use in the jungle, although it appears that none of the material was actually used
(Shimomura 2006).
The aim of this report is to investigate possibilities for harnessing bioluminescence for energy
production, as well as explore alternative avenues of profitable endeavour.
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Figure 1. Mean spectral maximum for bioluminescent animals living in shallow, deep
and benthic (seafloor) marine regions, wavelength in nm (adapted from Widder 2010).
Figure 2. Estimated quantum
emission (photons flash-1 into a
4π steridian sphere) for several
groups of marine bioluminescent
organisms: Copepoda;
Euphasiiacea (Euphaus.);
Amphipoda (Amph.);
Decapoda (De.); Scyphozoa
(Scypp.); Siphonophora (Siph.);
Pyrosoma (Py.); Dinoflagellata
(from Priede et al. 2008; Latz et
al. 2004a).
2. Marine bioluminescence in UK waters
Marine bioluminescence occurs among a wide range of different organisms. A list of the known
bioluminescent species around the British Isles and adjacent seas is shown in Table 1. Coastal species
and species that have been reported within the British coastal region are also indicated.
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Table 1. Bioluminescent marine organisms reported in the British Isles and adjacent seas (inclusion area indicated in light blue on the inserted map). *Coastal species or species that have been reported in coastal areas. (Tett 1971; Herring 1976; Buskey & Swift 1985; Herring 1985; Herring 1987; Widder et al. 1989; Tett 1992; Haddock & Case 1999; Poupin et al. 1999; Haddock et al. 2010; MSBIAS (www.marinespecies.org); MarLIN (www.marlin.ac.uk))
Classification Species Bacteria Vibrio fischeri Vibrio harveyi Vibrio logei Dinoflagellata (Algae) Alexandrium tamarense Ceratium furca Ceratium fusus Ceratium horridum Ceratium tripus Gonyaulax catenata* Gonyaulax polygramma Gonyaulax scrippsae Gonyaulax spinifera Lingulodinium polyedrum Noctiluca scintillans Peridinium divergens* Peridinium ovatum* Peridinium steinii* Polykrikos schwartzii* Prorocentrum micans Protoperidinium bipes Protoperidinium brevipes Protoperidinium cerasus Protoperidinium claudicans Protoperidinium conicoides Protoperidinium conicum Protoperidinium crassipes Protoperidinium curtipes Protoperidinium depressum Protoperidinium divergens Protoperidinium excentricum Protoperidinium leonis Protoperidinium minutum Protoperidinium nudum Protoperidinium oceanicum Protoperidinium ovatum Protoperidinium pallidum Protoperidinium pellucidum Protoperidinium pentagonum Protoperidinium punctulatum Protoperidinium pyriforme Protoperidinium saltans Protoperidinium steinii Protoperidinium subinerme Amphipoda Cyphocaris anonyx Cyphocaris richardi Scina borealis Scina crassicornis
Copepoda Centraugaptilus horridus Euaugaptilus magnus Heterorhabdus norvegicus Heterorhabdus papilliger Heterorhabdus spinifrons Lucicutia flavicornis Lucicutia grandis Metridia longa Metridia lucens* Oncaea conifera Pleuromamma abdominalis Pleuromamma borealis Pleuromamma gracilis Pleuromamma robusta Pleuromamma xiphias Decapoda Acanthephyra pelagica Acanthephyra purpurea Pasiphaea tarda Sergestes arcticus Sergia robustus (robusta) Systellaspis debilis Euphausiidae Meganyctiphanes norvegica* Nyctiphanes couchii Stylocheiron longicorne Stylocheiron maximum Thysanoessa inermis Thysanoessa longicaudata Thysanoessa raschii* Ostracoda Conchoecia spinirostris Ophioroid Amphipholis squamata* Amphiura filiformis* Polychaeteae Tomopteris helgolandica Tomopteris septentrionalis Chaetognath Sagitta elegans Sagitta tasmanica Appendicularian Oikopleura dioica* Thaliacian Cyclosalpa bakeri Pyrosoma atlanticum Hydroida (Medusae) Aequorea forskalea* Aequorea macrodactyla Aequorea vitrina Campanularia sp.* Clytia hemisphaerica* Eutonina indicans Halicreas minimum Halopsis ocellata Lizzia sp.* Obelia sp.* Octophialucium funerarium Tima bairdi* Leptomedusae (Medusae) Cosmetira pilosella* Mitrocomella polydiademata*
Trachylina (Medusae) Aegina citrea Aeginura grimaldii Solmissus incise Coronatae (Medusae) Atolla parva Atolla vanhoeffeni Atolla wyvillei Nausithoe atlantica Nausithoe globifera Paraphyllina ransoni Periphylla periphylla Semaeostomeae (Medusae) Chrysaora hysoscella Pelagia noctiluca* Ctenophora Beroe cucumis* Bolinopsis infundibulum* Siphonophora Abylopsis tetragona Chuniphyes multidentata Diphyes dispar Hippopodius hippopus Nanomia cara Praya dubia Rosacea plicata Vogtia glabra Vogtia serrata Bivalvia Pholas dactylus * Cephalopoda Bathyteuthis abyssicola Brachioteuthis bowmani Brachioteuthis picta Brachioteuthis riisei Galiteuthis armata Gonatus steenstrupi Heteroteuthis dispar * Histioteuthis bonnellii Histioteuthis reversa Loligo vulgaris* Mastigoteuthis schmidti Octopoteuthis sicula Ommastrephes bartramii Ommastrephes pteropus Onychoteuthis banksii Sepiola affinis Sepiola atlantica* Sepiola rondeletii* Spirula spirula * Teuthowenia megalops Elasmobranchii Etmopterus princeps Etmopterus spinax Osteichthyes Argyropelecus hemigymnus Argyropelecus olfersii Epigonus telescopes Himantolocphus groenlandicus Malacocephalus laevis* Maurolicus muelleri Nezumia aequalis Sternoptyx diaphana Xenodermichthys copei
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3. Energy extraction options
There are a number of options available to exploit the energy resources of marine organisms. The
most common and direct use of marine energy reserves is as nutrition for both humans and animals
(Fig 3A). However, in terms of a source of extractable energy, the simplest option is to directly
combust the organisms to produce heat energy (Fig. 3B: Crude fuel). All organisms are primarily
composed of water, carbohydrates, proteins and lipids. The latter three of these substances have
calorific values of 17.2 kJ g-1, 23.7 kJ g-1 and 36.1 kJ g-1, respectively (Lucas 1993). Table 2 shows the
intrinsic calorific content of range of marine organisms. The calorific content of the ash free dry
weight of these organisms ranges over an order of magnitude, from 5.50 x 103 kJ kg-1 for marine
bacteria to 3.05 x 104 kJ kg-1 for the copepod Metridia longa.
Figure 3. Schematic of energy extraction options from the biomass of marine
species, including bioluminescent organims. A: Direct nutrition, B: Crude fuel,
C: Refined fuel, D: Bioluminescent light source, E: Bioluminescent energy source.
The combustion process produces heat energy which can then, if required, be converted into
electrical energy. However, a number of energy costs are involved in this process, in particular, the
evaporation of the water content from the organism (see Box 1). In addition to this, the efficiency of
the heat to electrical energy conversion is limited by the theoretical Carnot Limit1. In reality this
theoretical efficiency value is never reached, although recent studies claim that up to 90% of the
Carnot Limit may be achievable with technological advancements (web.mit.edu; Wu et al. 2009).
Thus the final net energy output will be a fraction of the intrinsic energy content.
1 A theoretical value which sets an absolute limit on the efficiency with which heat energy can be turned into
useful work.
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An alternative method to exploit the energy reserves of marine species is the targeted extraction of
high energy and/or high value products, such as oil (Fig. 3C). The extraction of oil from algae for
biofuel has been in consideration for a number of years and extensive research is being conducted
into its viability as a commercial enterprise. This option is discussed in more detail in section 5.1.
A further option for energy exploitation of marine species is to use the light produced by
bioluminescent species. In this case, the light may either be used directly as a source of illumination
(Fig. 3D), or converted into electricity (Fig. 3E). To assess the potential energy production from
bioluminescent light, the flash characteristics of different species are considered in section 4.
Table 2. Calorific, water and lipid (oil) content of a range of marine groups and species. These values have
been reported in the literature, but it should be noted that the biochemical composition of species varies
with the age and sex of the organisms as well as the environment in which they grow (Raymont et al. 1971;
Finlay & Uhlig 1981; Croxall & Prince 1982; Larson 1986; Ikeda & Skjoldal 1989; Simon & Azam 1989; Davies
1993; Ikeda & Hirakawa 1998; Mansour et al. 1999; Kim et al. 2010; Nurnadia et al. 2011). *Mean value
calculated from a range of reported values.
Group Species
Calorific content (kJ kg
-1 of ash free dry weight)
Water content (% wet weight)
Lipid (oil) content
(% dry weight)
Marine bacteria 5.50x103
46 - 82 (% volume)
Dinoflagellates 2.29x104 12.6 *
Noctiluca spp. 6.60x103
Medusae 1.89x104 95 - 97 3.4 *
Ctenophores 1.68x104 95 - 97
Beroe cucumis 1.92x104 96
Bolinopsis infundibulum 1.47x104 0.5 *
Polychaetes 2.36x104 *
Tomopteris helgolandica 2.89x104 * 22
Copepods 2.31x104 64 - 82 20.1
Metridia longa 3.05x104 * 77
Euphausiids 2.33x104 68 - 82 15.5
Thanoassa spp. 2.27x104 68 - 82 14.7
Meganyctiphanes norvegica 2.78x104 * 75 - 80 17.7 *
Amphipods 1.97x104 * 78 - 83 9.5
Chaetognaths 2.27x104 * 89 6.5
Fish 2.42x104 60 - 82
Squid 2.34x104 74 - 84 19.4
Appendicularia 95 - 97 6.5 *
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Box 1. Some of the issues that surround bio-energy can be understood by considering the case of a draught horse. The standard value for 1 horsepower is 750 W (Watts) based on the original estimate of the continuous working capacity of a brewery horse by James Watt in 1782. The direct energy content of the carcase of a mammal is approximately 7000 kJ kg-1 live weight. Assuming the horse weighs 750 kg this represents a chemical energy store of 5,250,000 kJ which could theoretically be released if the carcase was combusted in a furnace. If we compare this with keeping the horse alive and working it at 750 W, it would take 81 days, working 24h per day to realise the same amount of energy. Working a horse continuously for 24 h a day is of course not feasible and also 750 W is a rather optimistic energy output for a horse. The horse would also have to be fed at the equivalent of over 750 W to maintain it, assuming 30% efficiency ca. 220 MJ day-1. In the case of bioluminescence, having grown some algae (or other bioluminescent organism) we can chose to either extract the stored chemical energy by combustion or keep the algae alive and repeatedly extract energy by stimulating bioluminescence. The algae would need a supply of nutrients to sustain this in the same way as the horse has to be fed. However, data in the literature giving the chemical energy content of various animals, crops and foods (which is useful for dietary consumption estimates) ignores the practical problem of removing the water content before combustion takes place. The latent heat of evaporation of water is: 2260 kJ kg-1. To this must be added the energy required to heat the water to boiling point (100°C) from room temperature (20°C) = 4.18 × 80 = 334 kJ kg-1 So total cost of water removal is 2260 + 334 = 2594 kJ kg-1. For the horse carcase, assuming 70 % water content (525 kg water) this would be an energy loss of 1,362,060 kJ reducing the combustion energy available to 3,887,940 kJ In most marine biomass the water content is somewhat higher e.g. using the same figures but with 85% water content. The energy content of the carcase decreases to: 2,625,000 kJ The cost of water removal increased to: 1,653,930 kJ The net energy available is then 971,070 kJ This indicates that for most wet marine biomass direct combustion is not likely to be profitable owing to the high cost of drying. For traditional biomass, e.g. wood and peat, the water content is much lower and the drying is done for “free” by standing the material for a year or more, essentially dried by solar energy which is not accounted for. Oil can be extracted without drying by disrupting cells, mechanically, chemically or by heat and allowing oil to float to the surface.
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4. Bioluminescent energy calculations
The intensity, duration and spectral characteristics of bioluminescent emissions have been measured
for relatively few species. However, table 3 shows the average bioluminescent light characteristics of
several species, covering a range of different animal groups and dinoflagellates (algae).
Bioluminescent bacteria are not listed in table 3 as they generate a continuous glow, not discrete
flashes of light (see Section 5.3 for more details on bacterial bioluminescence).
The energy of a single flash, from the organisms listed, varies from 10-12 to 10-9 kJ flash-1. Based on
these values, a calculation has also been made to show the number of individual flashes that would
be required to create 1 kW of light, which ranges in magnitude from 108 to 1011.
Bioluminescent flashes may be stimulated multiple times in a single organism. Stimulation may be
provided by mechanical, electrical or chemical means. It is important to note, however, that after an
initial bioluminescent flash, subsequent flashes can be of lower intensity, as the bioluminescent
potential of the organism becomes exhausted. The full bioluminescent potential is restored given a
sufficient period of time. This recovery time will vary between species and on the initial state of
exhaustion. In the case of dinoflagellates, for example, studies have shown that recovery can occur
in 0.5 – 6 hours (Widder & Case 1981).
To convert bioluminescent light into electrical energy, photovoltaic cells would be required. Thus the
final energy output from the conversion of light to electricity would be dependent on the efficiency
of the photovoltaic cell. The efficiency of photovoltaic cells used for the conversion of solar light to
electrical energy tend to be in the region of 10 – 15 % at a light intensity of 1 sun, although recent
advances in the use of different materials report efficiencies up to 42 % (Green et al. 2011). Such
high efficiencies are reported for high light intensities, > 1 sun. The average sunlight intensity in the
U.K. is about 100 W m-2 (Mackay 2008); several orders of magnitude brighter than bioluminescent
light. At lower light intensities the power efficiency of silicon and organic photovoltaic cells are less
efficient (Reich et al. 2009, Steim et al. 2011). However, demand for photovoltaic cells for indoor use
has lead to the development of techniques to improve their efficiency at lower light levels (Steim et
al. 2011).
Photovoltaic cells designed to convert sunlight into electrical energy are designed to be able to
absorb light from a wide spectral window to respond to the broadest possible span of the solar
spectrum. This is achieved using a stack of photovoltaic cells each with peak sensitivity in different
regions of the solar spectrum (Forrest 2005). Most bioluminescent light emission is blue or blue
green (ca. λ 450 - 500 nm) and of narrow bandwidth (λ 26 – 100 nm) (Widder et al. 1983), so
photovoltaic cells sensitive to the blue bandwidth (e.g. Zhang et al. 2010) would be most suitable for
the conversion of bioluminescent light into electrical energy.
In the future, there may be possibilities of producing a higher bioluminescent light yield through
genetic modification of organisms. Non-bioluminescent bacteria can be genetically engineered to
bioluminesce (Sagi et al. 2003; Girotti et al. 2008) and a successful attempt was made to increase the
light output from an extracted luciferase (Fujii et al. 2007). However, no studies to date can be found
demonstrating an enhanced light yield from a live multicellular animal. Thus this approach would
require extensive research and development.
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Table 3. Light and energy output estimates for bioluminescent emissions from a range of marine species.
(Nicol 1958; Clark et al. 1962; Swift et al. 1977; Lapota & Losee 1984; Latz et al. 1990; Bowlby et al. 1990;
Bowlby & Case 1991; Latz et al. 2004a; Priede et al. 2008)
Classification Species Quantum emission
(photons flash−1
)
Peak wavelength
(nm) (*assumed)
Average duration
(s)
Energy of single flash (J flash
−1)
Flashes required for
1 kW
Copepoda
Gaussia princeps 1.80x1011
480* 8.7 7.45x10-8
1.17x1011
Pleuromamma xiphias
1.80x1010
480* 0.4 7.45x10-9
5.07x1010
Metridia lucens 3.44x1012
480 6.7 1.42x10-6
4.70x109
Euphausiiacea
Meganictyphanes norvegica
7.55x1010
480 13 3.12x10-8
4.16x1011
Euphausia eximia 1.00x1010
480*
4.14x10-9
Nyctiphanes simplex
1.00x1011
480*
4.14x10-8
Amphipoda
Cyphocaris faurei 5.70x1010
480*
2.36x10-8
Scina crassicornis 3.10x1010
480*
1.28x10-8
Decapoda Acanthephyra pelagica
2.73x1012
490 3.5 1.11x10-6
3.16x109
Scyphozoa
Periphylla periphylla
3.50x1010
465 2.4 1.50x10-8
1.61x1011
Atolla wyvillei 1.20x1011
470 2 5.07x10-8
3.94x1010
Siphonophora
Vogtia glabra 1.40x1011
470 4 5.92x10-8
6.76x1010
Vogtia spinosa 3.20x1011
470 6.5 1.35x10-7
4.81x1010
Pyrosoma Pyrosoma atlanticum
2.30x1013
493 59 9.27x10-6
6.37x109
Dinoflagellata
Ceratium fusus 1.10x109 474 0.2 4.61x10
-10 5.18x10
11
Ceratocorys horrida
9.20x109 474 0.2 3.86x10
-9 4.77x10
10
Lingulodinium polyedrum
1.90x108 474 0.1 7.96x10
-11 1.57x10
12
Pyrocystis fusiformis
6.90x1011
472 0.2 2.90x10-7
7.23x108
In terms of the conversion of bioluminescent light into electricity, the current limited efficiency of
photovoltaic cells, combined with the low light intensity of the bioluminescent emissions (relative to
solar light), may render this option uneconomic as a stand-alone technology. However, it may be
feasible to integrate the harvesting of light with another energy extraction process. In this report we
consider the integration of bioluminescent energy extraction with various existing and emerging
commercial activities.
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5. Energy extraction proposals
5.1 Algae
In recent years there has been a lot of interest in the use of algae to produce biofuel. There are
several benefits that are offered by this biofuel production option compared to other methods
which extract oil from land crops. One of the principal advantages is the short growth cycle of algae
which increases the potential productivity by several orders of magnitude per unit area compared to
terrestrial plant options. In addition to this, algae can be produced on non-arable land so does not
compete with food production (Turner et al. 2011). However, challenges do remain before algal
biodiesel can become a viable option. One of the main challenges to making this process viable is the
high energy input required to dry the algae to extract the oil. The drying process requires large
amounts of fossil fuel derived energy, currently rendering algal biofuel uneconomic and
unsustainable (Sander & Murphy 2010). However, further research and development is currently
underway. In the U.K., the Carbon Trust Challenge has invested in the development of a sustainable,
cost-effective biofuel from algae (www.carbontrust.co.uk). Within the E.U., the European Industrial
Bioenergy Initiative (EIBI) supports demonstration and flagship projects for the production of
bioenergy that is not yet commercially available (www.biofuelstp.eu).
There are two ways that the economic viability of algal biofuel production can be augmented: either
by extracting additional high value co-products from the cultured algae; or by increasing the energy
output of the process. Various high value co-products are currently being considered, including
animal and fish feed, food and food additives, chemical feedstocks, health and beauty products, as
well as pharmaceuticals (Dyer-Smith & Allen 2011). In addition to these revenue generating
products, processes that increase the energetic yield during the production of algae will also
improve the net energy balance of algal biofuel production. Harvesting bioluminescent light from
algae during the incubation period has the potential to serve as an additional source of energy
output. The combination of these energy extraction options is illustrated by figure 4, in which
bioluminescent light is stimulated within the biomass during incubation, prior to the extraction of
oil.
Figure 4. Schematic of option for extraction of bioluminescent light and refined
fuel from the biomass of marine algae.
The only class of algae that includes bioluminescent species is Dinophyceae; the dinoflagellates.
Although there are over 3000 strains of algae that are being considered for their suitability for
10
biofuel production, the most appropriates classes are the green algae and the diatoms (Sheehan et
al. 1998). These algal groups have been considered most appropriate for the quantity and type of
lipids they produce. However, the quality and quantity of lipid content can be enhanced through
genetic improvement and modification (Lundquist et al. 2010; Radakovits et al. 2010; Singh et al.
2011). Although the authors of the present report find no evidence for current investigations into
the production of a suitable bioluminescent dinoflagellate species or a strain genetically engineered
to bioluminesce, this remains a possible avenue for future research.
Dinoflagellates require mechanical stimulation above a certain threshold to produce
bioluminescence (Latz et al. 1994; Latz et al. 2004a,b; Cussatlegras & Le Gal 2005). The threshold
varies between species, but in general, an accelerating flow with shear force (≥ 0.6 N m-2) is required
to maximise the bioluminescent output (Blaser et al. 2002; Cussatlegras & Le Gal 2005). Within an
algal production plant the mechanical stimulation could be generated by a purpose built system.
However, mechanical stirring is a necessary component of the algal cultivation process and
potentially it would be possible to integrate the process of stirring and stimulation into one unit.
Two of the systems in consideration for the cultivation of photosynthetic algae are raceway ponds
(open systems) and photobioreactors (PBRs; closed systems) (Chisti 2007). In PBRs the algae is
contained within transparent structures enabling greater control over the environmental conditions
and reducing the risk of contamination. During the algal biofuel production process turbulence is
created in both the open and closed systems which could be used as a site of bioluminescence
stimulation. In the open system, a unit is required to mix and circulate the algal broth. In the closed
system, turbulence is required at two points in the process; within the growth chambers to prevent
sedimentation and also at the degassing zone to extract the build up of oxygen within the algal
broth. Where turbulence is created, a bioluminescent species would be stimulated to produce
bioluminescence.
Photosynthetic algae2 require a day and night light regime for optimum growth. Daylight is known to
inhibit the production of bioluminescent emissions in photosynthetic dinoflagellates (Hamman et al.
1981; Buskey et al. 1992). As a result of this photoinhibition of bioluminescent emissions during the
light cycle, bioluminescent light could only be harvested during the dark cycle. Using production
values that have been previously estimated for the algal biofuel process, it is possible to estimate
the potential bioluminescent light output from a hypothetical production plant. Table 4 shows the
estimated energetic output from a range of dinoflagellate species. The energetic output per unit
weight is species dependent, ranging from 6.37 x 10-4 to 2.32 kJ kg-1. Assuming an algal production
plant can produce an algal biomass of 22 g m-2 day-1 (following the estimate of Lundquist et al.
(2010)) the potential energetic output from the stimulation of bioluminescent flashes depends on
the number of times a day each cell is stimulated. Although bioluminescence may be stimulated
repeatedly in a single organism, the bioluminescent potential of the organism becomes exhausted
often resulting in subsequent flashes of lower intensity. The full recovery time varies between
species, but can be assumed to be 0.5 – 6 hours in dinoflagellates (Widder & Case 1981). Thus, if
each cell were stimulated twice a day the energetic output would range from 2.80 x 10-5 kJ m-2 day-1
for the species Lingulodinium polyedrum to 1.02 x 10-1 kJ m-2 day-1 for the species Pyrocystis
fusiformis. Increasing the rate of stimulation of each cell to from 2 to 24 times a day would increase
2 Photosynthetic algae convert sunlight into chemical energy, including oil.
11
the potential energetic output of each species by just over an order of magnitude (Table 4),
assuming full recovery of bioluminescent potential between flashes.
Table 4. Estimated energetic output per unit weight (kJ kg-1
) and the daily energetic output per unit area assuming a theoretical algal production scenario (kJ m
-2 day
-1) for a range of dinoflagellate species.
Dinoflagellate species
Energy output
a
(kJ kg-1
)
Energy output a,b,c
(kJ m-2
day-1
)
assuming stimulation of each cell twice per day
Energy output a,b,d
(kJ m-2
day-1
)
assuming stimulation of each cell 24 times per day
Ceratium fusus 3.69x10-3
1.62x10-4
1.95x10-3
Ceratocorys horrida 3.08x10-2
1.36x10-3
1.63x10-2
Lingulodinium polyedrum
6.37x10-4
2.80x10-5
3.36x10-4
Pyrocystis fusiformis 2.32 1.02x10-1
1.23
a
Assuming a wet weight of 1.6x10-7
g per dinoflagellate cell b Assuming a total biomass productivity of 22g m
-2 day
-1 (Lundquist et al. 2010).
c Assuming a 6 h recovery period of bioluminescent potential for each dinoflagellate cell, with light harvested
during a 12 h dark period of the growth cycle. d Assuming a 0.5 h recovery period of bioluminescent potential for each dinoflagellate cell, with light harvested
during a 12 h dark period of the growth cycle.
Converting the bioluminescent light produced during the algal production process into electrical
energy would increase the net energy balance of the algal biofuel production process. As an
indication of the significance of the bioluminescent energy contribution, the energetic output from
the dinoflagellate bioluminescence can be compared to the energetic output from the oil content of
the algae. Lundquist et al. (2010) estimate that the daily oil production from this algal production
plant would be 5.5 x 10-3 l m-2 day-1 (equivalent to 20000 l hectare-1 year-1). The energy content of oil
is 33 MJ l-1, giving a daily energy output of 180 kJ m-2 day-1. This calculation does not take into
account any of the energetic costs of processing or drying the algae it simply provides the potential
energy output of the oil content. Therefore the potential energy output from the bioluminescence of
the dinoflagellate Pyrocystis fusiformis (1.23 kJ m-2 day-1) represents about 1% of the energy
potential of its oil content. If this output from bioluminescence can be achieved, it would require an
area of 70244 m2 or over 7 hectares to generate 1kW of power.
The light and temperature regimes in the U.K. are not considered optimum for the production of
photosynthetically derived algal biofuel. The Carbon Trust Challenge aimed to undertake the
production of algal biofuel in equatorial regions where temperatures are higher and light regimes
are stable throughout the year. Thus, the production of algae in pond raceways and PBRs may not be
suitable to the U.K. climate.
However, alternative systems have also been researched and developed which use different
production techniques or create alternative fuels to oil (Mascarelli 2009; Savage 2011). One
technique which has been developed in the U.S. by the company Solazyme uses heterotrophic3 algae
which grow in the dark by consuming sugars (Mascarelli 2009; solazyme.com). In 2010, Solazyme
3 An organism that cannot synthesize its own food and is dependent on complex organic substances for
nutrition.
12
supplied the U.S. Navy with 80,000 l of algal derived diesel and jetfuel using this technique. Other
alternatives include the harvesting of ethanol, which is excreted by some types of algae, as
developed by the U.S. company Algenol Biofuels (www.algenol.com). Other companies that are
involved in the production of algal biofuel include Petrosun, Green Star, SGI, Solix Biofuels, Sapphire
Energy, BioFuel Systems SL, Petro Algae, and HR Biopetroleum. The possibility exists that
bioluminescent light harvesting could be applied to any of these techniques.
5.2 Jellyfish
Bioluminescence in common among jellyfish4 and around the British Isles and adjacent waters there
are at least 37 known bioluminescent species of medusae, nine bioluminescent species of
siphonophore and two bioluminescent species of ctenophore (Table 2). In this section, the possibility
of combining the extraction of bioluminescent energy from jellyfish with other commercial
applications is explored.
Jellyfish play a natural and important part of marine ecosystems. However, there is concern that
jellyfish numbers may be increasing worldwide and that jellyfish blooms are becoming more
frequent, although confirmation of such trends is hindered by the absence of baseline data (Mills
2001; Pauly 2009; Richardson et al. 2009; Purcell 2012; www.bbc.co.uk/news). A number of
anthropogenic factors are believed to contribute to increased jellyfish numbers. Overfishing reduces
the numbers of competitors and predators of jellyfish, allowing their population to increase (Parsons
& Lalli 2002; Richardson et al. 2009). Eutrophication (increased concentrations of nutrients from
fertiliser runoff and sewage) encourages the development of algal blooms which can create
favourable conditions for the proliferation of jellyfish (Purcell 2001). Additionally, warming of the sea
surface as a result of climate change may also increase jellyfish numbers (Parsons & Lalli 2002;
Purcell et al. 2007; Gibbons & Richardson 2008; Lynam et al. 2010). An EU funded project called The
EcoJel Project (www.jellyfish.ie) was established in 2007 to assess the opportunities and detrimental
effects of jellyfish in the Irish Sea.
One of the major issues of increasing numbers of jellyfish is their predation of vulnerable life stages
of fish (fish eggs and larvae) (Hay 1990; Paurcell & Arai 2001; Lynam et al. 2005). It is hypothesized
that increasing jellyfish populations have the potential to displace fish communities (Purcell 2007;
Richardson et al. 2009). This would shift the ecosystem to a more gelatinous one, having a
detrimental effect on fish stocks. There is also evidence that jellyfish blooms cause high mortality of
farmed fish (Bämsted et al. 1998; Doyle et al. 2008; Ferguson et al. 2010; Baxter et al. 2011) and
have been responsible for blocking the cooling systems of nuclear reactors (www.bbc.co.uk/news).
Within UK waters there is some evidence to suggest that jellyfish numbers are increasing in the
North Sea (Attrill et al. 2007) and the Irish Sea (Lynam et al. 2011). If jellyfish numbers and blooms
are increasing in UK waters it would be pertinent to take advantage of this resource as part of any
management approach.
4 Free swimming gelatinous animals that include medusae, siphonophores and ctenophores.
13
Jellyfish could be fished or cultured to exploit their bioluminescent properties. The harvest of
jellyfish could also be combined with other commercial uses of jellyfish (Fig. 5). Table 4 provides an
estimate of the energy and power output of a range of jellyfish species per unit weight. Although the
energy produced per flash is of the same order of magnitude (10-8 J; Table 3) for each of the species
listed in Table 5, the energetic output per unit weight varies over two orders of magnitude, from
10-10 to 10-8 kJ kg-1, as a result of differences in the average weight of individual jellyfish.
Figure 5. Schematic of option for extraction of bioluminescent light and
various valuable products from jellyfish.
Table 5. Energy output per unit weight for a range of jellyfish (Lancraft et al. 1991; Lucas 2009; Lebrato & Jones 2009)
Jellyfish species Average wet weight (g) Energy output a
(kJ kg-1
) Power output a (kW kg
-1)
Periphylla periphylla 6 2.72x10-9
1.13x10-9
Atolla wyvillei 64 7.98x10-10
3.99x10-10
Vogtia glabra 1 5.61x10-8
1.40x10-8
a Assuming stimulation of each individual once
Jellyfish are currently used for food, clinical and industrial applications. In Asia, semi-dried jellyfish
represents a multi-million dollar seafood business (Hsieh et al. 2001; Omori & Nakano 2001; You et
al. 2007). Edible jellyfish are supplied by both aquaculture techniques (You et al. 2007) and jellyfish
fisheries (Omori & Nakano 2001; Nishikawa et al 2008). In some areas of China, jellyfish (Rhopilema
esculentum) aquaculture has now replaced traditional fish and shrimp aquaculture (You et al. 2007).
Most of the world’s jellyfish fisheries are based in Asia, where demand has been growing since the
1970s (Kingsford et al. 2000; Omori & Nakano 2001). In response to this demand, jellyfish fisheries
are expanding worldwide. The US has started harvesting the Cannonball jellyfish (Stomolophus
meleagris) for export to the food markets of Asia where there is high demand. Cannonball jellyfish
are very abundant in coastal US waters and are often problematic for net based fisheries. The
jellyfish can crush the target species or even damage nets as a result of their weight and bulk.
Harvesting these jellyfish provides economic and ecological benefits (Hsieh et al. 2001). In addition
14
to those of the U.S., jellyfish exports are reported from Australia, India (Hsieh et al. 2001) Namibia
and the U.K.5 (You et al. 2007).
Omori & Nakano (2001) list the most important edible jellyfish species (Table 6). None of the listed
species are bioluminescent. However, one of them, the Dustbin-lid jellyfish (also known as the Barrel
jellyfish; Rhizostoma pulmo; synonym R. octopus), is present on the western and southern coasts of
Britain (Sabatini 2004) and is considered a bloom forming species (Lilley et al. 2009). Although this
particular species is not of interest from the perspective of bioluminescence applications, it may
have potential for future commercial exploitation in British waters as an export to the Asian food
market.
Table 6. Identified species of edible jellyfish (Omori & Nakano 2001)
Cephea cephea (Forskål, 1775) Catostylus mosaicus (Quoy & Gaimard, 1824) Crambione mastigophora Maas 1903 Crambionella orsisi (Vanhöffen, 1888) Lobonema smithii Mayer, 1910 Lobonemoides gracilis Light, 1914 Rhizostoma pulmo (Macri, 1778) Rhopilema esculentum Kishinouye, 1891 Rhopilema hispidum (Vanhöffen, 1888) Neopilema nomurai Kishinouye, 1922 Stomolophus meleagris L. Agassiz, 1862
Jellyfish are also exploited for their medicinal values. Although there is little scientific evidence for
the purported effectiveness of jellyfish in weight loss, softening skin, treating burns, arthritis,
fatigue, hypertension, back pain and ulcers; it remains popular in the Asian medicinal market.
However, there have been some recent reports in the scientific literature showing preliminary
positive effects of jellyfish collagen extracts on arthritis (Hsieh et al. 2001; Ohta et al. 2009), fatigue
(Ding et al. 2011) and hypertension (Morinaga et al. 2010). In the West, collagen extracts for
pharmaceutical and nutritional applications are generally obtained from pig, bovine and poultry
sources, although consideration has been given to the benefits of collagen extraction from jellyfish
(Nagai et al. 2000; Addad et al. 2011; Gomez-Guillen 2011).
Pelagia noctiluca is a bioluminescent jellyfish species that has been found to be widespread in Irish
and UK waters (Russell 1970; Doyle et al. 2008; Bastian et al. 2011). It is not an edible species but
there has been some investigation into the extraction of its collagen. However, the concentration of
collagen in the body tissues of P. noctiluca is low compared to the Dustbin-lid jellyfish (R. Pulmo)
(Addad et al. 2011) and it may be unlikely to provide an efficient collagen source.
The photoproteins of several jellyfish species have been used for pharmaceutical applications. These
photoproteins are triggered to luminesce by the addition of the calcium (Ca2+). This property has
5 N.B. The authors of this present report find no further evidence of U.K. exports of jellyfish to the Asian food
market other than the reference in You et al. (2007).
15
been harnessed as a technique to measure intracellular calcium for a wide range of medical research
applications. More than 25 bioluminescent species are known to use Ca2+ regulated photoproteins,
although to date only seven photoproteins have been isolated and characterised (Vysotski et al.
2006). Thus there is scope for the discovery of photoproteins that perform better than those
currently employed. However, once selected for pharmaceutical use, the photoproteins are cloned
and synthetically produced, rather than extracted from the original species (Markova et al. 2002;
Vysotski et al. 2006; Inouye 2008). Consequently, there is likely to be little scope for commercial
exploitation of jellyfish for extraction of their photoproteins.
5.3 Bacteria
Bioluminescent bacteria are currently used for monitoring environmental pollutants (reviewed in
Girotti et al. 2008). However, there are investigations into potential future uses of bioluminescent
bacteria.
Bioluminescent bacteria produce a continuous glow once a certain cell density is reached. As no
other stimulus is required to produce the light, one possible application of bacterial bioluminescence
is as a source of illumination (Fig. 6). The electronics company Philips is currently exploring the
possibility for bioluminescent home lighting in an experimental project called the Microbial Home
System. Part of this project includes a ‘Bio-light’ design (www.design.philips.com), consisting of glass
cells containing live bacterial cultures that emit soft green bioluminescent light in the home (Figure
7). Bioluminescent bacteria glow continuously without the need for any kind of external stimulation
(electrical, mechanical, chemical or photic) making it suitable to such an application. The intensity of
light production is dependent on the species as well as the bacterial cell density. In optimum
conditions the light output of several bioluminescent bacteria species are indicated in Table 7. At a
cell density of 250 x 106 cells ml-1, the brightest bacterial strain of those listed in Table 6, Vibrio
harveyi, would produce 2.03 x 10-7 Watts l-1. This is equivalent to a daily energy output of
1.75 x 10-5 kJ l-1 day-1.
Figure 6. Schematic of option for use of bioluminescent bacteria as a light source.
Although the intensity of light emitted by the Philips prototype is currently deemed insufficient to
act as a primary source of illumination in the home, other applications for bioluminescent bacterial
light have been suggested. These options include night-time road markings (e.g. bioluminescent
plants that indicate where the edge of the road is), warning strips on flights of stairs, kerbsides etc,
informational markings in low-light settings (eg. theatres, cinemas, nightclubs), and new genres of
atmospheric interior lighting with, for example, possible therapeutic and mood-enhancing effects.
16
Figure 7. Prototype of the bioluminescent bacterial lighting design from Philip’s Bio-light
project.
Table 7. Estimated power output from several species of bioluminescent marine bacteria (Bourgois et al. 2001).
Bacteria species
Light output
a
(Photons s-1
cell
-1)
Peak wavelength
(nm)
Power per cell
(W cell-1
)
Cells required for
1 kW
Power per litre
b
(W l-1
)
Daily energetic
output (kJ l
-1 day
-1)
Vibrio harveyi 2 490 8.11x10-19
1.23x1021
2.03x10-7
1.75x10-5
Vibrio fischeri 0.6 490 2.43x10-19
4.11x1021
6.08x10-8
5.25x10-6
Photobacterium phosphoreum
0.5 490 4.93x10-19
4.93x1021
5.07x10-8
4.38x10-6
a Assuming steady state conditions with adequate oxygen supply
b Assuming a cell density of 250 x 10
6 cells ml
-1, indicated as an optimum density for bioluminescent output
(Bourgois et al. 2001).
5.4 Leisure and tourism
As a final note, it is worth mentioning the high degree of public interest in bioluminescent creatures.
Various bioluminescent fantasy forms have featured in the blockbuster films ‘Avatar’ and ‘Monsters’
as well as various video games. In the U.S., the American Museum of Natural History in New York has
announced a new exhibition to run throughout 2012 entitled ‘Creatures of light: Nature’s
bioluminescence’ (www.amnh.org). In addition to this, areas such as Bioluminescent Bay in Puerto
Rico attract huge numbers of tourists to kayak through the glowing waters, rich in bioluminescent
dinoflagellates (www.tripadvisor.co.uk).
In the U.K. there are reports of naturally occurring dinoflagellate bioluminescence in coastal waters
in the Moray Firth (personal obs., B. Ruck, Director of Moray First Marine Ltd) and occasionally in
various locations on the west coast of Britain (Staples 1966; Tett 1992). Although the occurrence of
natural bioluminescence in British waters may not be frequent enough to drive a tourist industry,
there may be scope for development of artificial installations. At present there are two U.K. based
aquaria where bioluminescent flashlight fish are displayed (The Deep in Hull and Bristol Blue Reef).
However, there may be potential for expanding the role of bioluminescence within the British leisure
and tourism industry. Future projects could include educational facilities such as exhibitions, or
possibly more entertainment focussed enterprises such as bioluminescent pools.
17
6 Conclusions
This report explores possibilities for the use of bioluminescence as an energy resource. The energy
released per single bioluminescent flash is species dependent and varies over several orders of
magnitude from 10-11 to 10-6 J flash-1 for marine animals and algae (Table 2). Bacteria emit a
continuous glow when the population density exceeds a certain threshold, with power output in the
region of 10-19 W cell-1 (Table 7).
The bioluminescent light generated by marine organisms could be converted into electrical energy.
Photovoltaic cells are used to convert solar light into electrical energy with efficiencies generally in
the region of 10 - 15%. Photovoltaic cells are less efficient at lower light intensities, so the
conversion of bioluminescent light into electrical energy would likely fall below 10 %.
The low light output of bioluminescent species relative to solar light may render the conversion of
bioluminescent light into electrical energy uneconomic as a stand-alone option. However,
alternative scenarios have been considered in this report including the integration of photic energy
extraction with other commercial activities. The potential energy output has been considered for the
bioluminescent emissions of algae (dinoflagellates), jellyfish and bacteria.
Of the dinoflagellate species investigated, Pyrocystis fusiformis generates bioluminescence of
greatest light intensity, producing 2.32 kJ kg-1 if each cell is stimulated to flash once (Table 4).
Bioluminescent flashes may be stimulated multiple times in a single cell, although time is required
for a cell to recover its full bioluminescent potential. The bioluminescent flashes of dinoflagellates
are short in duration, typically 100 – 200 ms (Table 3).
The energetic output per unit weight of the jellyfish species investigated ranged from 7.98 x 10-10 to
5.61 x 10-8 kJ kg-1 (Table 5). The bioluminescent flashes of jellyfish are usually several seconds in
duration (Table 3).
The energetic output per unit weight for dinoflagellates is 4 to 10 orders of magnitude greater than
for jellyfish species (Table 4 & 5). Although the energy per individual flash is generally higher for
jellyfish species than for dinoflagellate species (Fig. 2; Table 2), dinoflagellates are substantially
smaller (ca. 5 x 10-5 m diameter) than jellyfish species (> 10-2 m diameter). This results in a greater
energetic output per unit weight for dinoflagellates than for larger organisms (jellyfish, fish,
crustaceans etc.). The size of the organism is important to consider in terms of the extraction of
bioluminescent energy, as stimulation (mechanical, electrical or chemical) of larger organisms will
require greater use of energy and resources than the stimulation of smaller organisms.
Integrating the harvest of bioluminescent light with algal biofuel production may be possible.
However, at present the algal strains under consideration for use in this process do not include
bioluminescent dinoflagellates. If a bioluminescent strain were to be selected, the potential annual
energy output would largely depend on the quantum light emission of the species, the minimum
recovery time required between consecutive flashes and the total dark period during which flashes
could be elicited. Using values from the dinoflagellate Pyrocystis fusiformis, the daily potential
bioluminescent energy output from a hypothetical algal biofuel production plant would be
1.23 kJ m-2 day-1 (assuming an algal production of 22g m-2 day-1 ; Lundquist et al. 2010). This
energetic output represents about 1% of the energetic content of the potential oil harvest derived
18
from the same quantity of algae. Using optimistic assumptions, a plant extending over more than 7
hectares would be necessary to sustain an output of 1kW from algal generated bioluminescence.
The possibility of integrating the harvest of bioluminescent light from jellyfish with other commercial
activities was also explored. The commercial activities considered were the harvesting of jellyfish for
export to the Asian food market, extracting jellyfish collagen and the extraction of photoproteins.
However, at present no known species of bioluminescent jellyfish that occurs in British waters is
considered edible or suitable for the extraction of collagen, and photoproteins are manufactured
synthetically. In addition to this, the energetic output per unit weight of jellyfish is several orders of
magnitude lower than that of smaller species, such as dinoflagellates.
There are currently investigations into the possibility of utilising the light generated by
bioluminescent bacteria as a direct source of illumination. At present the light intensity of these
systems are low, but bacterial bioluminescence may have potential to serve as a form of low
intensity warning or information lighting.
In addition to options to extract the energy from bioluminescent emissions, these may also be scope
to extend the use of bioluminescence in the British tourism and leisure industry.
19
References
Addad S, Exposito J-Y, Faye Cm, Ricard-Blum S, Lethias C (2011) Isolation, characterization and
biological evaluation of jellyfish collagen for use in biomedical applications. Marine Drugs
9:967-983
Attrill MJ, Wright J, Edwards M (2007) Climate-related increases in jellyfish frequency suggest a more
gelatinous future for the North Sea. Limnology and Oceanography 52:480-485
Bamstedt U, Fossa JH, Martinussen MB, Fossagen A (1998) Mass occurrence of the physonect
siphonophore Apolemia uvaria (Lesueur) in Norwegian waters. Sarsia 83:79-85
Bastian T, Stokes D, Kelleher JE, Hays GC, Davenport J, Doyle TK (2011) Fisheries bycatch data
provide insights into the distribution of the mauve stinger (Pelagia noctiluca) around Ireland.
ICES Journal of Marine Science 68:436-443
Baxter EJ, Sturt MM, Ruane NM, Doyle TK, McAllen R, Harman L, Rodger HD (2011) Gill damage to
atlantic salmon (Salmo salar) caused by the common jellyfish (Aurelia aurita) under
experimental challenge. PLoS ONE 6:e18529
Blaser S, Kurisu F, Satoh H, Mino T (2002) Hydromechanical stimulation of bioluminescent plankton.
Luminescence 17:370-380
Bowlby MR, Case JF (1991) Flash kinetics and spatial patterns of bioluminescence in the copepod
Gaussia princeps Marine Biology 110:329-336
Bowlby MR, Widder EA, Case JF (1990) Patterns of stimulated bioluminescence in two pyrosomes
(Tunicata: Pyrosomatidae). Biological Bulletin 179:340-350
Buskey EJ, Strom S, Coulter C (1992) Bioluminescence of heterotrophic dinoflagellates from Texas
coastal waters. Journal of Experimental Marine Biology and Ecology 159:37-49
Buskey EJ, Swift E (1985) Behavioral responses of oceanic zooplankton to stimulated
bioluminescence. Biological Bulletin 168:263-275
Chisti Y (2007) Biodiesel from microalgae. Biotechnology Advances 25:294-306
Clarke GL, Conover RJ, David CN, Nicol JAC (1962) Comparative studies of luminescence in copepods
and other pelagic marine animals. Journal of the Marine Biological Association of the United
Kingdom 42:541-564
Croxall JP, Prince PA (1982) Calorific content of squid (Mollusca: Cephalopodia). British Antarctic
Survey Bulletin 55:27-31
Cussatlegras AS, Le Gal P (2005) Dinoflagellate bioluminescence in response to mechanical stimuli in
water flows. Nonlinear Processes in Geophysics 12:337-343
20
Davis ND (1993) Caloric content of oceanic zooplankton and fishes for studies of salmonid food
habits and their ecologically related species (NPAFC Doe.) FRI-UW-93 12, Fisheries Research
Institute, University of Washington, Seattle
Ding J-F, Li Y-Y, Xu J-J, Su X-R, Gao X, Yue F-P (2011) Study on effect of jellyfish collagen hydrolysate
on anti-fatigue and anti-oxidation. Food Hydrocolloids 25:1350-1353
Doyle TK, De Haas H, Cotton D, Dorschel B, Cummins V, Houghton JDR, Davenport J, Hays GC (2008)
Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters.
Journal of Plankton Research 30:963-968
Dyer-Smith C, Allen S (2011) Biofuels from algae. Postnote 384, Houses of Parliament, London
Farber-Lorda J, Gaudy R, Mayzaud P (2009) Elemental composition, biochemical composition and
caloric value of Antarctic krill.: Implications in energetics and carbon balances. Journal of
Marine Systems 78:518-524
Ferguson HW, Christian MJD, Hay S, Nicolson J, Sutherland D, Crumlish M (2010) Jellyfish as vectors
of bacterial disease for farmed salmon (Salmo Salar). Journal of Veterinary Diagnostic
Investigation 22:376-382
Finlay BJ, Uhlig G (1981) Calorific and carbon values of marine and freshwater Protozoa. Helgoland
Marine Research 34:401-412
Gibbons MJ, Richardson AJ (2009) Patterns of jellyfish abundance in the North Atlantic.
Hydrobiologia 206:51-65
Girotti S, Ferri EN, Fumo MG, Maiolini E (2008) Monitoring of environmental pollutants by
bioluminescent bacteria. Analytica Chimica Acta 608:2-29
Gomez-Guillen MC, Gimenez B, Lopez-Caballero ME, Montero MP (2011) Functional and bioactive
properties of collagen and gelatin from alternative sources: A review. Food Hydrocolloids
25:1813-1827
Haddock SHD, Case JF (1999) Bioluminescence spectra of shallow and deep-sea gelatinous
zooplankton: ctenophores, medusae and siphonophores. Marine Biology 133:571
Haddock SHD, Moline MA, Case JF (2010) Bioluminescence in the sea. Annual Review of Marine
Science 2:443-493
Hamman JP, Biggley WH, Seliger HH (1981) Photoinhibition of stimulable bioluminescence in marine
dinoflagellates. Photochemistry and Photobiology 33:909-914
Hay SJ, Hislop JRG, Shanks AM (1990) North Sea Scyphomedusae; summer distribution, estimated
biomass and significance particularly for 0-group Gadoid fish. Netherlands Journal of Sea
Research 25:113-130
21
Herring PJ (1976) Bioluminescence in decapod Crustacea. Journal of the Marine Biological
Association of the United Kingdom 56:1029-1047
Herring PJ (1985) Bioluminescence in the Crustacea. Journal of Crustacean Biology 5:557-573
Herring PJ (1987) Systematic distribution of bioluminescence in living organisms. Journal of
Bioluminescence and Chemiluminescence 1:147
Hsieh Y-HP, Leong F-M, Rudloe J (2001) Jellyfish as food. Hydrobiologia 351
Ikeda T, Hirakawa K (1998) Metabolism and body composition of zooplankton in the cold
mesopelagic zone of the southern Japan Sea. Plankton Biology and Ecology 45:31-44
Ikeda T, Skjoldal HR (1989) Metabolism and elemental composition of zooplankton from the Barents
Sea during early Arctic summer. Marine Biology 100:173-183
Inouye S (2008) Cloning, expression, purification and characterization of an isotype of clytin, a
calcium-binding photoprotein from the luminous Hydromedusa Clytia gregarium. The
Journal of Biochemistry 143:711-717
Kim HS, Yamaguchi A, Ikeda T (2010) Metabolism and elemental composition of the euphausiids
Euphausia pacifica and Thysanoessa inspinata during the phytoplankton bloom season in the
Oyashio region, western subarctic Pacific Ocean. Deep-Sea Research Part II - Topical Studies
in Oceanography 57:1733-1741
Kingsford MJ, Pitt KA, BM G (2000) Management of jellyfish fisheries, with special reference to the
order Rhizostomeae. . Oceanography and Marine Biology: An Annual Review 143:711-717
Lancraft TM, Hopkins TL, Torres JJ, Donnelly J (1991) Oceanic micronektonic macrozooplanktonic
community structure and feeding in ice covered Antarctic waters during the winter (Ameriez
1988). Polar Biol 11:157-167
Lapota D, Losee JR (1984) Observations of bioluminescence in marine plankton from the Sea of
Cortez. Journal of Experimental Marine Biology and Ecology 77:209-239
Larson RJ (1986) Water content, organic content, and carbon and nitrogen composition of medusae
from the northeast Pacific. Journal of Experimental Marine Biology and Ecology 99:107-120
Latz MI, Bowlby MR, Case JF (1990) Recovery and stimulation of copepod bioluminescence. Journal
of Experimental Marine Biology and Ecology 136:1-22
Latz MI, Case JF, Gran RL (1994) Excitation of bioluminescence by laminar fluid shear associated with
simple couette flow. Limnology and Oceanography 39:1424-1439
Latz MI, Nauen JC, Rohr J (2004a) Bioluminescence response of four species of dinoflagellates to fully
developed pipe flow. Journal of Plankton Research 26:1529-1546
22
Latz MI, Juhl AR, Ahmed AM, Elghobashi SE, Rohr J (2004b) Hydrodynamic stimulation of
dinoflagellate bioluminescence: a computational and experimental study. Journal of
Experimental Biology 207:1941-1951
Lebrato M, Jones DOB (2009) Mass deposition event of Pyrosoma atlanticum carcasses off Ivory
Coast (West Africa). Limnology and Oceanography 54:1197-1209
Lilley MKS, Houghton JDR, Hays GC (2009) Distribution, extent of inter-annual variability and diet of
the bloom-forming jellyfish Rhizostoma in European waters. Journal of the Marine Biological
Association of the United Kingdom 89:39-48
Lucas A (1993) Bioénergétique des animaux aquatiques, Vol. Masson, Paris
Lucas CH (2009) Biochemical composition of the mesopelagic coronate jellyfish Periphylla periphylla
from the Gulf of Mexico. Journal of the Marine Biological Association of the United Kingdom
89:77-81
Lundquist TJ, Woertz C, Quinn NWT, Benemann JR (2010) A realistic technology and engineering
assessment of algae biofuel production, Energy Biosciences Institute
Lynam CP, Lilley MKS, Bastian T, Doyle TK, Beggs SE, Hays GC (2011) Have jellyfish in the Irish Sea
benefited from climate change and overfishing? Global Change Biology 17:767-782
MacKay DJC (2009) Sustainable energy — without the hot air, UIT Cambridge
Mansour MP, Volkman JK, Jackson AE, Blackburn SI (1999) The fatty acid and sterol composition of
five marine dinoflagellates. Journal of Phycology 35:710-720
Markova SV, Vysotski ES, Blinks JR, Burakova LP, Wang BC, Lee J (2002) Obelin from the
bioluminescent marine Hydroid Obelia geniculata: cloning, expression, and comparison of
some properties with those of other Ca2+-regulated photoproteins. Biochemistry 41:2227-
2236
Mascarelli AL (2009) Algae: fuel of the future? Environmental Science & Technology 43:7160-7161
Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean
conditions? Hydrobiologia 451:55-68
Morinaga Y, Iwai K, Tomita H, Takaya Y, Naraoka T, Matsue H (2010) Chemical nature of a new
antihypertensive peptide derived from jellyfish. Food Science and Technology Research
16:333-340
Nagai T, Worawattanamateekul W, Suzuki N, Nakamura T, Ito T, Fujiki K, Nakao M, Yano T (2000)
Isolation and characterization of collagen from rhizostomous jellyfish (Rhopilema asamushi).
Food Chemistry 70:205-208
Nicol JAC (1958) Observations on luminescence in Noctiluca. Journal of the Marine Biological
Association of the United Kingdom 37:535-549
23
Nishikawa J, Thu NT, Ha TM, Thu PT (2008) Jellyfish fisheries in northern Vietnam. Plankton &
Benthos Research 3:227-234
Nurnadia AA, Azrina A, Amin I (2011) Proximate composition and energetic value of selected marine
fish and shellfish from the West coast of Peninsular Malaysia. International Food Research
Journal 18:137-148
Ohta N, Sato M, Ushida K, Kokubo M, Baba T, Taniguchi K, Urai M, Kihira K, Mochida J (2009) Jellyfish
mucin may have potential disease-modifying effects on osteoarthritis. Bmc Biotechnology
9:11
Omori M, Nakano E (2001) Jellyfish fisheries in southeast Asia. Hydrobiologia 451:19-26
Parsons TR, Lalli CM (2002) Jellyfish population explosions: revisiting a hypothesis of possible causes.
Lamer 40:111-121
Pauly D, Graham W, Libralato S, Morissette L, Deng Palomares M (2009) Jellyfish in ecosystems,
online databases, and ecosystem models. Hydrobiologia 616:67-85
Pauly D, Graham W, Libralato S, Morissette L, Deng Palomares M (2009) Jellyfish in ecosystems,
online databases, and ecosystem models. Hydrobiologia 616:67-85
Poupin J, Cussatlegras A-S, Geistdoerfer P (1999) Plancton marin bioluminescent, Laboratoire
d’Océanographie de l’École Navale, Brest
Priede IG, Jamieson A, Heger A, Craig J, Zuur AF (2008) The potential influence of bioluminescence
from marine animals on a deep-sea underwater neutrino telescope array in the
Mediterranean Sea. Deep-Sea Research Part I: Oceanographic Research Papers 55:1474-
1483
Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and
environmental perturbations. Annual Review of Marine Science 4:209-235
Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review.
Hydrobiologia 451:27-44
Purcell JE, Uye S, Lo W (2007) Anthropogenic causes of jellyfish blooms and their direct
consequences for humans: a review. Marine Ecology Progress Series 350:153-174
Radakovits R, Jinkerson RE, Darzins A, Posewitz MC (2010) Genetic engineering of algae for
enhanced biofuel production. Eukaryotic Cell 9:486-501
Raymont JEG, Srinivasagam RT, Raymont JKB (1971) Biochemical studies on marine zooplankton VIII.
Further investigations on Meganyctiphanes norvegica (M. Sars). Deep Sea Research and
Oceanographic Abstracts 18:1167-1178
24
Reich N, van Sark WV, Alsema E, Kan S, Silvester S, van der Heide ASH, Lof RW, Schropp REI (2005)
Weak light performance and spectral response of different solar cell types, Utrecht
University
Richardson AJ, Bakun A, Hays GC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and
management responses to a more gelatinous future. Trends in ecology & evolution (Personal
edition) 24:312-322
Russell FS (1970) The Medusae of the British Isles. Vol.II - Pelagic Scyphozoa, with a supplement the
first volume of Hydromedusae, Vol. Cambridge University Press, Cambridge
Sabatini M (2004) Rhizostoma pulmo. Dustbin-lid jellyfish. Marine Life Information Network: Biology
and Sensitivity Key Information. Marine Biological Association of the United Kingdom,
Plymouth
Savage N (2011) Algae: The scum solution. Nature 474:S15-S16
Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. Department of Energy’s
Aquatic Species Program - Biodiesel from algae, National Renewable Energy Laboratory
Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific Publishing
Co. Pte. Ltd., Singapore
Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria.
Marine Ecology Progress Series 51:201-213
Singh A, Nigam PS, Murphy JD (2011) Renewable fuels from algae: An answer to debatable land
based fuels. Bioresource Technology 102:10-16
Staples RF (1966) The distribution and characteristics of surface bioluminescence in the oceans (TR -
184), U.S. Naval Oceanographic Office, Washington
Steim R, Ameri T, Schilinsky P, Waldauf C, Dennler G, Scharber M, Brabec CJ (2011) Organic
photovoltaics for low light applications. Solar Energy Materials and Solar Cells 95:3256-3261
Sugahara T, Ueno M, Goto Y, Akiyama K, Yamauchi S, Shiraishi R, Doi M (2009) Immunostimulation
effect of the jellyfish collagen. In: Animal Cell Technology: Basic and Applied Aspects, Vol 15.
Springer, Dordrecht, p 293-299
Swift E, Biggley WH, Napora TA (1977) The bioluminescence emission spectra of Pyrosoma
atlanticum, P. spinosum (Tunicata), Euphausia tenera (Crustacea) and Gonostoma sp.
(Pisces). Journal of the Marine Biological Association of the United Kingdom 57:817-823
Tett P (1992) The ecology of plankton in Scottish coastal waters. Proceedings of the Royal Society of
Edinburgh Section B Biological Sciences 100:27-54
Tett PB (1971) The relation between dinoflagellates and the bioluminescence of sea water. Journal
of the Marine Biological Association of the United Kingdom 51:183-206
25
Vysotski E, Markova S, Frank L (2006) Calcium-regulated photoproteins of marine coelenterates.
Molecular Biology 40:355-367
Widder EA (2010) Bioluminescence in the ocean: Origins of biological, chemical, and ecological
diversity. Science 328:704-708
Widder EA, Bernstein SA, Bracher DF, Case JF, Reisenbichler KR, Torres JJ, Robison BH (1989)
Bioluminescence in the Monterey Submarine Canyon: image analysis of video recordings
from a midwater submersible. Marine Biology 100:541-551
Widder EA, Case JF (1981) Two flash forms in the bioluminescent dinoflagellate, Pyrocystis
fusiformis. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and
Behavioral Physiology 143:43-52
Wu DM, Hagelstein PL, Chen P, Sinha KP, Meulenberg A (2009) Quantum-coupled single-electron
thermal to electric conversion scheme. Journal of Applied Physics 106:094315-094315-
094315
You K, Ma C, Gao H, Li F, Zhang M, Qiu Y, Wang B (2007) Research on the jellyfish (Rhopilema
esculentum Kishinouye) and associated aquaculture techniques in China: current status.
Aquaculture International 15:479-488
26
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