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 Physiological Characteristics of Porphyra

 Physiological Characteristics of Porphyra

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346



RUI PEREIRA AND CHARLES YARISH



Some species of Porphyra occur in the intertidal (e.g., P. dioica, P. umbilicalis,

P. linearis) while others are found only in the low-intertidal (e.g., P. leucosticta, P. purpurea) or the subtidal regions (e.g. P. amplissima). Intertidal species are

naturally expected to survive salinity variations, but in reality not many studies

have looked into the effects of salinity in Porphyra. Stekoll et al. (1999) investigated

the effects of salinity on the growth of the conchocelis phase of P. abbottae, P. torta

and P. pseudolinearis. Those authors found that salinity between 20% and 40‰

had little effect on growth, but there was virtually no growth at salinity 10‰ and

below. Conitz et al. (2001), on the other hand, did not find significant effects of

salinity on growth of juvenile gametophytes of P. torta, from 30‰ to 7.5‰.

The effects of photon flux density (PFD) and photoperiod have been studied

for many species, especially due to their influence in the life cycle of virtually all

species. The gametophytes and sporophytes of Porphyra dioica, for instance, grow

in short-day, neutral-day and long-day photoperiods. However, formation of

conchosporangia and release of conchospores in the laboratory occurred only in

short days (Pereira et al., 2006).

In terms of nutrient removal, the works by Chopin et al. (1999), Carmona

et al. (2006) and Pereira et al. (2008), among others, showed that some species of

Porphyra perform well in that function. Chopin et al. (1999) showed that tissue

nitrogen (N) and phosphorus (P) of Porphyra increased in specimens grown near

salmon cages. Of the several species studied, these authors concluded that

Porphyra yezoensis and Porphyra purpurea respond to high nutrient loading in

coastal waters resulting from anthropogenic activities (salmon aquaculture and

intense scallop dragging).

Studies in the laboratory have also shown that Porphyra responds to high

concentrations of ammonium (NH4+), a common form of N in water enriched by

anthropogenic activities. Wu et al. (1984) studied the utilisation of NH4+ by

Porphyra yezoensis and obtained higher growth rates (11.6% day−1) and tissue nitrogen content (4.72% dry weight [dw]) with NH4+ concentration ranging from 5 to 10

ppm (approx. 350–700 µM). For the same species, Amano and Noda (1987)

reported that the optimal fertilising effect was obtained using 20 ppm NH4+ during

48 h. More recently, Carmona et al. (2006) assessed the bioremediation potential of

several native northeast American species of Porphyra and compared those with

well-known Asian species. In that study, growth and tissue N reached maximal

levels at inorganic N concentrations of 150–300 µM. Maximum growth rates

ranged from 10 to 25% day−1. Pereira et al. (2008) studying a North Atlantic species,

Porphyra dioica, also reported an interesting capacity to uptake equally well NO3−

or NH4+, in concentrations ranging from 25 to 300 µM, when only one of these N

forms is present. If both forms were present, the preference was for NH4+ even if

available at a much lower concentration than NO3−.

Still in terms of nutrient physiology, considerably fewer studies have focused on

aspects related to phosphorus (P) and carbon (C). Carmona et al. (2006) showed that

P biofiltering efficiency was higher when NH4+ was supplied in P. amplissima,

P. purpurea, P. umbilicalis and P. yezoensis, but not in P. katadai and P. haitanensis.



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These authors also determined that P uptake was not saturated up to 30 µM P in

P. umbilicalis and P. haitanensis, while uptake rate by P. purpurea was saturated at

15 mM P, regardless of the N source, and at even lower P concentrations in the

other species. Pereira et al. (2008) showed that, for P. dioica, P enrichment up to

400 µM P did not translate into higher P uptake. In fact, despite the increasing P

concentration, the total amount of P removed from the medium was the same.

Both studies confirm what was first pointed out by Hafting (1999) for P. yezoensis,

a lack of capacity to store P. Interestingly, Chopin et al. (2004) described the presence of polyphosphate granules in the cells of P. purpurea. Polyphosphate granules are a form of P storage in yeast, microalgae and some macroalgae Sommer

and Both, 1938; Lundberg et al., 1989; Chopin et al., 1997). Chopin et al. (2004),

however, also point out that these granules do not seem to have the same storage

function in P. purpurea.

In terms of C metabolism, there are seaweed species capable of using only

CO2 and others that can use CO2 or HCO3−. Bicarbonate utilisation has been suggested for P. leucosticta (Mercado et al., 1997), P. umbilicalis (Maberly, 1990) and,

although with a limited capacity, for P. linearis (Israel et al., 1999). For P. leucosticta and P. linearis, those authors detected the activity of intra- and extracellular

carbonic anhydrase (CA). In P. yezoensis, on the other hand, Gao et al. (1992)

found evidences for active HCO3− transport, in that CO2 uptake was extremely

slow compared with the photosynthesis, and that external CA was never found in

that species.

5. Porphyra in IMTA

According to the FAO (2009b), in 2006, 47% of the world’s fish food supply

was produced in aquaculture. This activity continues to grow more rapidly than

all other animal food-producing sectors and in 2006 accounted for 36% of the

world total aquatic animal production by weight. In turn, in 2007, aquatic plants

aquaculture represents nearly 23% of the world aquaculture production, based

principally in Asian countries. The seaweeds that are produced are for human

consumption or for extraction of hydrocolloids (agar, alginates or carrageenan).

There are two main biological techniques for treatment of animal aquaculture

waters: bacterial dissimilation into gases and plant assimilation into biomass.

Bacterial biofilters allow effective and significant aquaculture water recirculation

(van Rijn, 1996), but the technology is not simple and such systems usually accumulate nitrate and sludge that need to be disposed, and are expensive to operate.

Biofiltration by algae is assimilative (Krom et al., 1989) and they use excess nutrients (particularly C, N, and P) to produce new biomass that can easily be removed

from the water and that can have an economic value. In China, the annual production of over 7.4 Mt of seaweed (FAO, 2009a) may be responsible for removal

of more than 40,000 t of nitrogen (N) from coastal waters. It is clear that seaweed

production can help mitigate the potential environmental impacts of animal



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production and contribute to the development of an environmentally and

economically sustainable aquaculture.

The principle of Integrated Multi-trophic Aquaculture (IMTA) systems is to

build a simplified ecosystem where the resources provided, mainly feed and water,

will be used by two to three other extractive aquaculture organisms: molluscs and

seaweeds. This allows a system to virtually use much of the nutrients minimising

the production of wastes. The best examples of IMTA systems operating in

different parts of the world were described by Chopin et al. (2008).

Because of its morphological characteristics, high surface area to volume

ratio (SA/V), Porphyra is one of the most promising species to be used as biofilter

in IMTA. The thallus of Porphyra is a thin blade with one or two layers of cells,

all potentially involved in nutrient absorption. It can be argued that a thallus with

high surface area to volume ratio does not allow storage of nutrients in reserve

tissues like those of brown algae (e.g. Laminariales and Fucales). The advantage

of Porphyra is its rapid growth, over 25% day−1 (Pereira et al., 2006; Carmona

et al., 2006), which can allow repeated harvests and continuous removal of nutrients from the water. There are yet other factors supporting the use of Porphyra in

IMTA. When compared with most other seaweeds, besides its rapid growth rate,

Porphyra has high nutrient uptake rates, is capable of coping with high NH4+

concentrations and is able to store N in its tissue up to 6% dry weight (dw).

Furthermore, the biomass produced has several valuable applications.

The best growth rates and nutrient removal capacities are usually found in

species with high surface area to volume ratios as explained by the functionalform model (Hanisak et al., 1990; Littler and Littler, 1980). For that reason, a lot

of work has been done using thin blade-like species of Ulva (Chlorophyta).

Martínez-Aragón et al. (2002) compared phosphate removal, from sea bass cultivation effluents, by Ulva rotundata, Ulva intestinalis (formerly Enteromorpha

intestinalis) and Gracilaria gracilis. The maximum P uptake rate (2.86 mmol PO4−3

g−1 dw h−1) was found in U. rotundata. In a follow-up study with the same species

(Hernández et al., 2002), U. rotundata also showed the highest NH4+ uptake rate,

89.0 mmol g−1 dw h−1. Chung et al. (2002) recorded an uptake rate of 114.6 mmol

NH4+ g−1 dw h−1 for U. pertusa. Fujita (1985) obtained, for U. lactuca, uptake rates

between 2 × 103 and 3.6 × 103 mg N g−1 dw h−1. The same author obtained, for

U. intestinalis, a maximal uptake of 14 × 103 mg N g−1 dw h−1. Mata et al. (2006)

reported what is likely to be the highest N uptake rate for a seaweed in integrated

aquaculture environment. In that work, the authors report a total ammonia nitrogen

(TAN) uptake rate of 90 µmol l−1 h−1 at a TAN flux of about 500 µmol l−1 h−1 and

with 5 g fresh weight (fw) l−1 stocking density. This is the equivalent to approximately

4.5 mg N day−1 g−1 fw of the alga.

The results of N uptake by Porphyra, although lower than those reported for

A. armata, are very interesting and promising. In laboratory conditions, Pereira

et al. (2006) obtained an N uptake rate of 1.5 mg N day−1 g fw of P. dioica. Also

in the laboratory, Carmona et al. (2006) obtained a maximum removal of 1.75 mg

N day−1 g−1 fw of P. purpurea and P. haitanensis. In both cases, tissue N recorded



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was over 6% dw. As mentioned earlier, Porphyra has other characteristics that

constitute important advantages when choosing a biofilter. Particularly relevant,

in terms of the potential role of Porphyra in ecosystem sustainability, is the ability

of some species to uptake N equally well in the form of NH4+ or NO3− as shown

by Pereira et al. (2006) and Carmona et al. (2006).

The results obtained so far show that Porphyra has an important role in the

nutrient balance in the ecosystems. If we consider a 10:1 dw:fw ratio and average

values of 5.5% N, 0.7% P and 38% C in tissue dw, we realise that the aquaculture

of Porphyra removes, annually, a significant amount of these nutrients from water.

In fact, considering FAO last production figures (FAO, 2009a), approximately

1.51 Mt of Porphyra were produced in 2007. This may equal to a removal of

9,063 t of N, 1,057 t of P and 57,404 t of C, every year.

These results are not just theoretical but supported by field studies of production of Porphyra and its nutrient removal capacity (e.g. Chopin et al., 1999; He

et al., 2008). In the most recent paper, He et al. (2008) showed the bioremediation

capability and efficiency of large-scale Porphyra cultivation in the removal of inorganic nitrogen and phosphorus from open sea area. The study took place in

2002–2004, in a 300 ha nori farm along the Lusi coast, Qidong County, Jiangsu

Province, China. Nutrient concentrations were significantly reduced by the seaweed cultivation. Compared with a control area, Porphyra farming resulted in the

reduction of NH4–N, NO2–N, NO3–N and PO4–P by 50–94%, 42–91%, 21–38%

and 42–67%, respectively. Nitrogen and phosphorus contents in dry Porphyra

thalli harvested from the Lusi coast averaged 6.3% and 1.0%, respectively. The

authors concluded that the annual biomass production of P. yezoensis (about 800

kg dw ha−1 from a 300 ha cultivation) equaled to an average of 14,708 kg of tissue

N and 2,373 kg of tissue P harvested. These results indicate clearly that Porphyra

can efficiently remove excess nutrient from nearshore eutrophic coastal areas.

The nutrient uptake capacity of Porphyra can also be useful in inland IMTA

systems, providing biofiltration for intensive fish aquacultures. The effluents from

these systems can reach high concentrations of both NH4–N and NO3–N.

Porphyra is capable of coping with high concentrations N in either form whether

for uptake or growth.

The main constraint in the case of land-based tank cultivation is the area of

cultivation needed to significantly reduce the nutrient loads of the effluents.

For instance, for an effluent with 143 µM N and 10 µM P at a flux of 190 l min−1,

Carmona et al. (2006) calculates that 282 m2 of Porphyra amplissima cultivation

are needed to remove 90% of the N. Pereira et al. (2006), for Porphyra dioica,

calculated that 179 m2 of culture area would be needed to remove 50% of the N.

This is considering that approximately 600 g of N are released per day by ton of

fish (data from a 50 fish pond, 36 m3 each, turbot and sea bass farm, as described

by Matos et al., 2006). Those authors refer, however, that in an IMTA system, the

performance of P. dioica is likely to improve. Under those tank cultivation conditions, the algae would have more nutrients and CO2 available, owing to the constant

water flux. This would also allow to experiment with higher stocking densities,



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RUI PEREIRA AND CHARLES YARISH



0

100

200

300

400

500

600



600



Biomass needed (kg)



500



400



300



200



100



0



15 -1 )

y

da

t (%



20



2



3

4

N content

(% dw



)



5



25

30

ra

th

ow

r

G



Figure 2. Three-dimensional simulation model of the biomass of Porphyra dioica needed to achieve

an 80% reduction in a N load (during 12 h light day) of 600 g N day−1 (195 l min−1 × 150 µM-N).



possibly increasing nutrient removal. Ultimately, the best nutrient removal

performance would be the result of the conditions that could yield the optimal

combination of growth and tissue N content, for a given stocking density (Fig. 2).

It is clear that Porphyra can play an important role in the sustainable development of intensive aquaculture. Species of Porphyra have high ammonia uptake

rates, high ammonia uptake efficiencies, high yields and high protein contents

(N content). Detailed economic studies are now needed to confirm the feasibility

of such systems.

In conclusion, we think Porphyra is a very promising marine organism for

biotechnological exploitation, one of the best seaweed for application in sustainable aquaculture (IMTA) and an interesting organism to be used as a model in

biological studies.

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Biodata of Gamze Turan and Amir Neori, authors of “Intensive Seaweed Aquaculture:

A Potent Solution Against Global Warming”

Dr. Gamze Turan is a faculty member at Ege University, Fisheries Faculty, Aquaculture

Department, Izmir, Turkey. She obtained her Ph.D. from Ege University Institute

of Natural and Applied Sciences in 2007 in Aquaculture and continued her research

on seaweeds, their cultivation, and usage. Dr. Turan’s scientific interests cover the

areas of seaweed cultivation, and their usage as phycocolloids, human food, animal

feed, fish feed, fertilizers and soil conditioners, biomass for fuel, cosmetics, integtated

multitrophic aquaculture (IMTA), wastewater treatment, etc. She has published

over 20 peer-reviewed publications.

E-mail: gamze.turan@ege.edu.tr

Dr. Amir Neori is a senior scientist at the Israel Oceanographic & Limnological

Research, Ltd. The National Center for Mariculture, Eilat, Israel. He obtained

his Ph.D. from the University of California San Diego – Scripps Institution of

Oceanography in 1986 in Marine Biology and continued his research in sustainable

mariculture and algae in his present capacity. Dr. Neori’s scientific interests are

in the area of environmentally-friendly aquaculture, algal aquaculture, reduction in

aquaculture environmental impact, integrated multitrophic aquaculture (IMTA), and

biofuel from algae. He has published over 70 peer-reviewed publications.

E-mail: neori@ocean.org.il; aneori@gmail.com



Gamze Turan



Amir Neori



357

A. Israel et al. (eds.), Seaweeds and their Role in Globally Changing Environments,

Cellular Origin, Life in Extreme Habitats and Astrobiology 15, 357–372

DOI 10.1007/978-90-481-8569-6_20, © Springer Science+Business Media B.V. 2010



INTENSIVE SEA WEED AQUACULTURE: A POTENT SOLUTION

AGAINST GLOBAL WARMING



GAMZE TURAN1 AND AMIR NEORI2

Fisheries Faculty, Aquaculture Department, Ege University,

Bornova, Izmir, 35100, Turkey.

2

Israel Oceanographic & Limnological Research Ltd, National Center

for Mariculture, P.O. Box 1212, Eilat, 88112, Israel



1



1. Introduction

On the basis of current understanding of the relationship between climate change

and energy policy, development of an effective and multistructured renewable energy

sector is crucial, as acknowledged in the United Nations Framework Convention on

Climate Change (UNFCCC) and the fourteenth Conference of the Parties (COP14), held in December 2008 in Ponzan, Poland. The worldwide energy demand is

increasing rapidly as many industries and populations are rapidly expanding. Since

fossil fuels are finite resources and their combustion leads to a further increase of

greenhouse gases, such as CO2, SO2, and NOx, their continued use is not sustainable.

Today, renewable energy sources supply 14% of the total global energy demand.

Some expect that in 2040, 50% of the world energy supply will come from renewable

sources (Demirbas, 2008). Additional efforts and further research and development

on biofuels, toward environmentally and economically sustainable processes, are

essential for the full exploitation of this given market opportunity.

The substitution of conventional fuels by biofuels can reduce pollution and

support sustainability. First-generation biofuels, such as biodiesel and bioethanol

derived from biomass, have their environmental benefits related to carbon-neutral

energy. However, increasing biofuel production from land crops strains the global

food supply. Owing to these limitations, second-generation (bio) fuels – from

biomasses that generate carbon neutral energy without competing with food production – have been developed. These can be produced from the residual nonfood

parts of current crops, as well as novel energy crops, such as seaweeds.

The culture of seaweeds has unique characteristics, which make it different

and in many ways attractive in comparison with other biofuel sources. Seaweeds,

also known as “marine macroalgae,” “aquatic plants,” or “sea vegetables,” are

autotrophic organisms that produce biomass using sunlight and extracting from

the water-dissolved inorganic nutrients, including carbon. Several seaweed species

359



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