The present study investigated quantitatively the significance of HNLC (high-nutrient low-chlorophyll) regions and its grazing control with the improved iron fertilization for climate change. The limitation of iron (Fe) for phytoplankton growth in HNLC regions was confirmed by sulfur compounds (S) such as volcanic ash and hydrogen sulfide (H 2S) in batch cultures, whose chemical sediment of Fe 3S 4 showed 4.06 wt%. The technologies developed for iron fertilization since 1993 till now were not practical to provide sufficient amounts of bioavailable iron due to sedimentary iron sulfides induced by undersea volcanic sulfur compounds. The proposed technology for iron fertilization was improved to enhance the bioavailable iron to phytoplankton by keeping minimal sulfur compounds in HNLC regions. The low productivity of phytoplankton by grazing control in HNLC regions was 6% diatoms whose 52% was grazed by copepods and 42% by krill on the basis of data analysis in 2000 EisenEx Experiment at boundary of Antarctic and African tectonic plates. All of the previous iron fertilization experiments were conducted at volcanic sulfur compounds enriched HNLC regions. The present study revealed that the enhanced phytoplankton productivity in batch culture without sedimentary iron sulfides can be possible only if sulfur compounds are minimal, as is in Shag Rocks (53 °S, 42 °W) of South Georgia in Scotia Sea in the Southern Ocean.
The hypothesis of iron fertilization was speculated by English biologist Joseph Hart in 1934, raised by John Gribbin in 1988, and renewed by American oceanographer John Martin four months later. As reviewed by Dugdale and Wilkerson [
In order to differentiate the global ocean into four oceanic regions in terms of accumulation rates of iron (Fe) and sulfur (S), the accumulation rate of Fe in the ocean, ( d F e d t ), is given by :
d F e d t = ( F ˙ e ) i n − ( F ˙ e ) o u t + ( F ˙ e ) g e n − ( F ˙ e ) c o n − ( F ˙ e ) r x n
where:
( F ˙ e ) i n = the input rate of Fe (nmol∙m−2∙d−1) from desert dust, volcanic ash, rivers, and bottom sediments,
( F ˙ e ) o u t = the output rate of Fe during Fe Cycle is negligible due to short term (hours) biological iron uptake,
( F ˙ e ) g e n = the generation rate of Fe from vertical mixing, upwelling and biogenic recycling of cellular iron within the ocean [
( F ˙ e ) c o n = the consumption rate of Fe by phytoplankton assimilation,
( F ˙ e ) r x n = the removal term for dissolved Fe by scavenging on the sinking particulate matter and chemical reaction rate of Fe with volcanic S compounds as sedimentary FeS and FeS2.
Oceans are subdivided into four regions based on the amounts of nutrient and chlorophyll; HNLC (high-nutrient, low-chlorophyll), HNHC (high-nutrient, high-chlorophyll), LNLC (low-nutrient, low-chlorophyll), and LNHC (low-nutrient, high-chlorophyll), as shown in
It is assumed that d F e d t ≫ 0 for HC (high-chlorophyll) regions (as is in HNHC and LNHC) if Fe supplied largely from deserts and upwelling. When d F e d t < 0 and the accumulation rate of volcanic S compounds, d S d t ≫ 0 for LC (low-chlorophyll) regions (as is in HNLC and LNLC) are satisfied if Fe is rarely replenished from deserts and subsurface water upwelling while volcanic S compounds are abundant. We present a review of the four oceanic regions listed above is presented here. 1) The southern Omani coast was studied to evaluate HNLC characteristics during the late Southwest Monsoon (Aug.-Sep.) [
Region | Oceanic Location (Relative Accumulation Rates of Fe and S) | Major Nutrient Sources | |
---|---|---|---|
Desert (Fe) | Volcano (Number) (S) | ||
HNLC | 1) Southern Ocean 2) Equatorial Pacific 3) Subarctic Pacific ( d F e d t < 0 , d S d t ≫ 0 ) ( | d F e d t | ≪ | d S d t | ) | 1) Austalian/Patagonian/ Kalahari/Antarctic Polar 2) Gobi/Atacama 3) Gobi | 1) Erebus (Antarctica) (19)/ Huaynaputina (Peru) (29)/ Hudson (Chile) (137) 2) Huaynaputina (Peru) (29)/ Hudson (Chile) (137)/ Cotopaxi (Ecuador)(43) Galapagos Islands (Ecuador) (12) 3) Aleutian (40)/ Augustine (USA) (15)/ Kamchatka (Russia)(29) |
LNLC | 1) Ryu Kyu/Izu-Bonin Arc 2) Hawaii 3) western North Pacific Subtropical Gyre/Guam 4) Iceland ( d F e d t < 0 , d S d t > 0 ) ( | d F e d t | < | d S d t | ) | 1) Gobi 2) (Gobi) 3) (Gobi) 4) Highlands of volcanic desert | 1) Japan (108) 2) Hawaii (15) 3) Anatahan (USA) 4) Iceland (130) |
HNHC | Benguela upwelling system ( d F e d t ≫ 0 , d S d t < 0 ) ( | d F e d t | ≫ | d S d t | ) | Kalahari, Namib | None active but extinct; Angola(0), Namibia (1), South Africa (4) |
LNHC | 1) Pacific coast of Mexico 2) Northeast Pacific 3) Northwest Pacific 4) Northeastern Canada 5) Peruvian coast 6) New Zealand 7) Southern Africa 8) The Antarctic ( d F e d t ≫ 0 , d S d t > 0 ) ( | d F e d t | > | d S d t | ) | 1) Chihuahuan, Sonoran, Mojave 2) Gobi, Great Basin 3) Gobi 4) Arctic, Sahara 5) Patagonian, Atacama 6) Great Victoria, Great Sandy, Gibson, Simpson 7) Kalahari, Namib 8) Antarctic, Great Victoria, Great Sandy, Gibson, Simpson, Patagonian, Atacama, Kalahari, Namib | 1) Barcena, Socorro and 9 others 2) Augustine (15), Kasatochi, Redoubt (13) Pavlof (40), Cleveland (19) 3) Hokkaido (17), Honshu (46), 4) Greenland, Iceland, Newfoundland Seamounts, Fogo Seamounts 5) Peru (29) and Chile (137) 6) White Island, Kermadec Islands 7) Madagascar (5), Mozambique (1), Tanzania (22), South Africa (4) 8) Erebus (19) |
the most productive fishery areas in the world with sand storms from Kalahari and Namib deserts in winter without any active volcanoes (
There are four more regions associated with major fisheries and coastal upwelling Currents-; 1) Canary Current with Sahara desert but no volcanoes; 2) California Current with deserts of Mojave, Colorado and Great Basin but no active volcanoes; 3) Humboldt Current with desert of Atacama but no volcanic fallout due to Chilean volcanic ashes blown to the south and Argentina; and 4) Somali Current with desert of Danakil-Kaisut but no fallout of volcanic ashes since Southwest Monsoon during summer moves three active volcanic ashes from northeastward along with the coastal waters. These five coastal upwelling regions meet the criteria of d F e d t ≫ 0 , d S d t < 0 , and | d F e d t | ≫ | d S d t | for HNHC regions. 4) Indonesia has 127 active volcanoes but no desert. However, western Australian dusts from Great Victoria, Great Sandy, Gibson, Tanami, and Little Sandy deliver Fe-enriched dusts (7 - 18 wt% Fe compared to the common 3.5 - 6.0 wt%) to Indonesian marine waters. Java Sea is surrounded by active volcanoes while the South Java Current flows eastward along the coast during the Northwest Monsoons. Nitrate (0.5 - 1.5 μM), phosphate (0.05 - 0.4 μM), silicate (4 - 14 μM), and chlorophyll-a (0.3 - 1.0 μg・l−1) were monitored in Java Sea [
Iron in volcanic ashes have been reported in a number of complex forms that include Fe2O3, Fe3O4, FeCl2, FeCl3, FeF2, FeF3, FeS, FeS2, FeSO4 and Fe2(SO4)3 [
Volcanic ash samples from 5 other volcanic eruptions, as morphologically examined in
The relationship between S content and the elapsed time was modeled by the first order decay [
Volcano | Eruption (year) | Fe (mg/kg) | CA S (mg/kg) | Fe/S | CA/CAOb | lnCA/CAO | Timec (yr) |
---|---|---|---|---|---|---|---|
Mount Ontake, Japan | 2014 | 33,312 | 29,531 | 1.13 | 1 | 0 | 0 |
Kasatochi, Alaska | 2008 | 157,942 | 14,572 | 10.8 | 0.493 | −0.70 | 6 |
Lombok, Indonesia | 1994 | 60,961 | 701 | 87.0 | 0.0240 | −3.74 | 20 |
Mount Pinatubo, Philippines | 1991 | 73,857 | 385 | 191.8 | 0.0130 | −4.33 | 23 |
Mount St. Helens, Washington | 1980 | 23,235 | 955 | 24.3 | 0.0323 | −3.43 | 34 |
Volcanic stone | |||||||
Mount Baekdua | 969 | 24,368 | 191 | 127.6 | - | - | - |
Soil | |||||||
Tongyoung, Korea | - | 26,014 | 1350 | 19.3 | - | - | - |
Note: aVolcanic stone not ash; bCAO was taken from Ontake; and cTime elapsed since 2014 of Ontake eruption. Concentrations of sulfur and iron were measured using an inductively coupled plasma (ICP) (Optima 5300DV, Perkin Elmer).
Mount St. Helens, Mount Pinatubo, Lombok, and Kasatochi, had the same initial sulfur concentration of the fresh Ontake volcanic ash. Based on the present data set in
The effects of Fe and volcanic ash upon the growth of phytoplankton were experimentally examined under aerobic culture of Chlorella vulgaris with various JM media; with its own Fe, mixture of 75% clay and 25% volcanic ash, fresh 100% volcanic ash, without its own Fe. The growth curves for 4 similarity experiments of 4 ecosystems (
S compounds (S, SO2, SO3, H2S, H2SO4, sulfates) induce bio-available Fe2+(aq) toward rapid black iron sulfide (FeS) ( Δ G r ∘ = − 1207.719 kJ ⋅ mol − 1 between FeOOH and H2S) and slow pyrite (FeS2) sedimentations ( Δ G r ∘ = − 30.7648 between FeS and H2S, and -30 kJ∙mol−1 between FeS and S˚) [
Iron sulfate heptahydrate (FeSO4・7H2O) has been used in the iron fertilization experiments as main source of iron due to its high solubility in water. Each 25 gram was dissolved in two bottles with 1 liter distilled water; one was bubbled with H2S gas (50 ppm, 2 LPM, 30 minutes) while another was kept as blank.
(Model Dmax2500/PC) for the presence of iron sulfides in form of Greigite-Fe3S4 among sulfur and iron oxide, as shown in
The effect of S compounds upon the growth of phytoplankton was experimentally examined. H2S generated by the decomposed white of egg was prepared to see its removal of Fe in JM medium with EDTA-Fe as sedimentary iron sulfide (FeS).
present JM culture media, cell density in 104 cells/ml was measured (
Characteristics of HNLC regions were well described by high surface nitrate, low DO, high SO2 dispersion and Fe-limited profiles in
SO2 concentration in air over the Sierra Negra Volcano in Galapagos Islands during an eruption in October 2005 showed that SO2 plume (
The previous 14 iron enrichment experiments on mesoscale size since IronEx I of 1993 till Haida Gwaii of 2012 (
SINK (HNLC) | CARRIER | SOURCE | ||||
---|---|---|---|---|---|---|
S | Fe | |||||
Current | Wind | Volcano (Number) | Tectonic Plate | Desert | ||
Southern Ocean | Antarctic Circumpolar, East Wind Drift | Westerly, Polar Jet Stream | Erebus (Antarctica) (19), | Antarctic/ Pacific/Scotia/ African/Australian | Surrounded | Australian/ Patagonian/ Kalahari/ Antarctic Polar |
Huaynaputina (Peru) (29), | ||||||
Hudson (Chile) (137) | ||||||
Equatorial Pacific | Peru (Humboldt), South Equatorial | Equatorial | Galapagos Islands (12), | Pacific/Cocos/ Nazca/South American | Surrounded | Gobi/Atacama |
Huaynaputina (Peru) (29), | ||||||
Hudson (Chile) (137), | ||||||
Cotopaxi (Ecuador) (43) | ||||||
Subarctic Pacific | Alaska, Kamchatka, Kuroshio, Subarctic, North Pacific | Aleutian Low | Aleutian (40), Augustine (15), Kasatochi, Redoubt (USA) (13), Kamchatka (Russia) (29) | Pacific/Okhotsk/ North American | Blocked | Gobi |
Polar Jet Stream |
global distribution of oceanic dissolved oxygen (DO) (
Most of SO2 (CA) from yearly continuous volcanic eruptions at Mt. Erebus of the Antarctic are quickly dissipated at the deep ocean of the Southern Ocean due to its enormous amount of oceanic volumetric flow rate (1.3 × 108 m3∙sec−1, QA) of water causing much higher mass flow rate ( m ˙ A = C A ⋅ Q A ) of SO2 dissolution and subsequently locking volcanic sulfur compounds, as observed in the oxygen minimum zones (~1100 m) of the abundant H2S pool (~150 μM) [
Although the aeolian dust over continents carry abundant iron (Fe) (3.5 - 6.0 wt% or 7.0 - 18.0 wt% clay in Tasmania of Australia) to HNLC regions, most of them are sedimented out from the upper surface waters as insoluble iron sulfides (FeS/FeS2) with reaction of sulfur compounds (S, SO2, SO3, H2S, H2SO4, sulfates) in the ocean, available from volcanic eruptions either in submarine or in air, while only negligible amounts of iron (1 × 10−8 %) {=(4 × 10−6 ppm/3.5 × 104 ppm) × 100)} are available in HNLC regions, assuming 4 × 10−6 ppm Fe (0.07 nmol L−1) [
Although 14 iron fertilization experiments during the last 24 years have been conducted [
The sulfate concentration increased horizontally towards the volcanic source [
Experiment | Date | Location | Tectonic Plate | Volcano (Number) |
---|---|---|---|---|
IronEx I | (Month/Year) | 5˚S, 90˚W | Pacific/Nazca | Galapagos Islands (12) |
IronEx II | June 1995 | 4˚S, 107˚W | Pacific/Nazca | near Seamount A at East Pacific Rise |
SOIREE | February 1999 | 61˚S, 140˚E | Antarctic/Australian | Erebus (19) |
EisenEx | November 2000 | 48˚S, 21˚E | Antarctic/African | Erebus (19)/near Marion at African Plate |
SEEDS I | July 2001 | 48.5˚N, 164.5˚E | Pacific/Okhotsk | Kamchatka Peninsula (29) |
SOFEX-N | January 2002 | 55˚S, 172˚W | Pacific/Antarctic | Erebus (19) |
SOFEX-S | March 2002 | 66˚S, 172˚W | Pacific/Antarctic | Erebus (19) |
SERIES | July 2002 | 51˚N, 144.5˚W | Pacific/North American | Augustine (15) |
EIFEX | February 2004 | 50˚S, 2˚E | Antarctic/ South American | Erebus (19)/near Bouvet at African Plate |
SAGE | March 2004 | 46.5˚S, 172.5˚E | Pacific/Australian | Erebus (19)/near Chatham Islands with volcanic ash from Taupo Volcanic Zone |
FeeP | July 2008 | 27.6˚N, 22.4˚W | African/Eurasian | near El Hierro of Canary Islands |
SEEDS II | July 2004 | 48˚N, 166˚E | Pacific/Okhotsk | Kamchatka Peninsula (29) |
LOHAFEX | March 2009 | 48˚S , 16˚E | Antarctic/African | Erebus (19)/near Marion/Bouvet at African Plate |
Haida Gwaii | July 2012 | 52.7˚N, 139.3˚W | Pacific/North American | Bowie Seamount |
Fourteen previous iron enrichment experiments from IronEx I in 1993 to Haida Gwaii in 2012 have been conducted by dumping a few hundred tons of Fe in form of FeSO4. The previous iron fertilizations (
The substitution of ferredoxin by flavodoxin, the use of plastocyanin instead of cytochrome bƒ and a variant stoichiometry of photosynthetic complexes are notable adaptive strategies to facilitate diatom growth in low-iron condition [
Diatoms are important primary producers (>40%) in the ocean with a high sinking velocity of 0.96 m∙d−1 for large centric diatoms [
d X d d t = ( X ˙ d ) i n − ( X ˙ d ) o u t + μ d − ( U c + U k )
where ( X ˙ d ) i n = diatoms input rate,
( X ˙ d ) o u t = diatoms output rate,
X d = concentration of diatoms in patch at time t of days since the first rion fertilization,
μ d = growth rate of diatoms,
u c = diatoms loss rate by copepods,
u k = diatoms loss rate by krill.
If diatoms input rate was close to diatoms output rate in a controlled patch volume,
( X ˙ d ) i n ≈ ( X ˙ d ) o u t
∴ d X d d t = μ d − ( U c + U k )
According to the definition [
μ d = 1 X d d X d d t = d ln X d d t
If assuming that copepods and krill were grown by their grazing diatoms, diatoms loss rates by copepods and krill could be similarly defined as,
U c = d ln X c d t
U k = d ln X k d t
∴ d X d d t = d ln X d d t − ( d ln X c d t + d ln X k d t )
Thus,
d X d = d ln X d − ( d ln X c + d ln X k )
By integration,
∴ X d = k + ln ( X d X c ⋅ X k )
where k = X d o + ( ln X c o ⋅ X k o X d o ) .
X d = concentration of diatoms in patch at time t of days since the first iron fertilization,
X c = concentration of copepods in patch at time t of days since the first iron fertilization,
X k = concentration of krill in patch at time t of days since the first iron fertilization,
k = initial constant,
X d o = initial concentration of diatoms in patch,
X c o = initial concentration of copepods in patch,
X k o = initial concentration of krill in patch.
There could be 3 special cases at steady state such that the apparent diatoms growth rate was greater, equal and less than grazing loss rates by both of copepods and krill. For simplicity, let's took the second case that the apparent diatoms growth rate was equal to grazing loss rates by copepods and krill as below.
μ d = U c + U k
d ln X d d t = d ln X c d t + d ln X k d t
∴ d ln X d = d ln ( X c ⋅ X k )
Since there was the inverse relationship between copepods and krill abundances [
X c = c 1 X k
where c 1 = inversely proportional constant between copepods and krill.
∴ d ln X d = d ln c 1
By integration,
ln ( X d X d o ) = c 2
where c 2 = integration constant
∴ X d = X d o ⋅ e C 2
If we wanted to sequester the atmospheric CO2 by the efficient growth rate of diatoms with iron enrichment, we had to keep the concentrations of diatoms after the iron fertilization (Xd) to be greater than concentrations of diatoms before the iron fertilization (Xdo) with the constraint as,
∴ X d > X d o ⋅ e C 2
If the grazing rate U was slightly modified from previous definition as,
U = F (nV)
where F = clearance rate (ml∙ind−1∙h−1),
n = number of grazers (ind),
V = experimental volume (ml) = S∙H,
S = experimental surface area (m2),
H = upper 150 m of the water column [
From
( n V ) = { ( n ) S } ( 1 H ) = 238485 ind ⋅ m − 2 150 m = 1590 ind ⋅ m − 3
From
Therefore, the grazing rate by copepods, U c , was given by,
U c = F ( n V ) = ( 20.3 ml ⋅ ind − 1 ⋅ h − 1 ) ( 1590 ind ⋅ m − 3 ) ( 1 m 3 10 6 ml )
∴ U c = 0.0323 h − 1
From Experiment 2 with dominant diatom Pseudonitzschia of
C C 0 = e − U k t
where C = free concentration of Biogenic Silica [BSi] (μmol∙l−1).
C0 = initial concentration of Biogenic Silica [BSi] (μmol∙l−1).
1.7 5.7 = e − U k 1 (96)
∴ U k 1 = 0.0126 h − 1
for Euphausia superba,
1.9 6.5 = e − U k 2 (90)
∴ U k 2 = 0.0137 h − 1
for Calanus propinquus.
Since diatoms were mainly (70%) ingested by Euphausia superba and Calanus propinquus, as shown in “BSi ingested %” of
∴ U k = U k 1 + U k 2 = 0.0263 h − 1
Since U c and U k were determined, the apparent diatoms growth rate was given by,
μ d = U c + U k = 0.0323 h − 1 + 0.0263 h − 1 = 0.0586 h − 1
From
It was summarized as;
1) The apparent growth rate of diatoms (0.0037 h−1) and the sum (0.0586 h−1) of grazing loss rates by copepods (0.0323 h−1) (52%) and krill (0.0263 h−1) (42%) gave the overall diatoms growth rate of 0.0623 h−1 (=0.0037 + 0.0586) equivalent to 1.5 d−1, which was comparable to 1.79 d−1 between day 4 and 7 of the centric diatom of Chaetocerus debilis in the western Subarctic Pacific [
2) The doubling rate of diatoms after grazed by copepods and krill was 0.13 d−1 from dividing (0.0037 h−1) (24 h/d) by ln2, which was comparable to 0.18 - 0.67 d−1 of chlorophyll in the Antarctic [
3) For the efficient sequestration of atmospheric CO2, it was necessary to increase the amount of diatom due to the relatively small apparent growth rate of residual diatom (0.0037 h−1, 6%). To overcome such extreme grazing controls (94%) by copepods and krill, the duration and area of the iron enrichment experiment should be extended to more than 3 months (Dec.-Feb.) when chlorophyll-a reached its peak concentration (≥0.75 mg∙m−3) with a large area of phytoplankton blooms (~145,000 km2), as observed in the South Georgia [
The present study examined empirically the Fe limitations induced by sulfur compounds of volcanic ash and hydrogen sulfide to improve the iron fertilization for the efficient phytoplankton productivity and estimated analytically the grazing control by copepods and krill over diatoms in HNLC regions. The limitation of Fe for phytoplankton growth in HNLC regions was confirmed by sulfur compounds such as volcanic ash and hydrogen sulfide (H2S) in batch cultures. Distribution of XRD pattern for the sedimentary materials induced by the chemical reaction between dissolved FeSO4∙7H2O and H2S gas bubbling in distilled water, showed that the chemical sediment of Fe3S4 constituted 4.06 wt% of total sedimentary materials among sulfur, iron oxide and Fe3S4. The low productivity of 6% diatoms was caused by grazing control in HNLC regions with 52% by copepods and 42% by krill on the basis of data analysis in 2000 EisenEx Experiment. Oceans were classified by four characteristic regions (HNLC, LNLC, HNHC and LNHC) based on the relative magnitude of the accumulation rates of Fe from deserts and S compounds from volcanoes. All of the previous iron fertilization experiments were conducted at volcanic sulfur compounds enriched HNLC regions. The present study revealed that the enhanced phytoplankton productivity in batch culture without sedimentary iron sulfides can be possible only if sulfur compounds are minimal, as is in Shag Rocks (53˚S, 42˚W) of South Georgia in Scotia Sea in the Southern Ocean.
The authors express sincere gratitude to Hiroyuki Yokoi, ICST, Tokyo, Japan, Kristi L. Wallace of Alaska Volcano Observatory, United States Geological Survey, H. C. Ryu of COSMAX, Prof. J. Y. Hwang of the Department of Earth and Environmental Sciences of Pusan National University, and Dr. H. C. Choi, South Korea, for providing samples of Ontake volcanic ash, Kasatochi volcanic ash, Lombok volcanic ash, Pinatubo volcanic ash, Baekdu volcanic stone and Tongyoung clay, St. Helens volcanic ash, respectively. Data from the Ph.D. thesis in 2000 EisenEx Experiment were kindly permitted by Lecturer Dr. Sabine Schultes of Department of Biology at II Ludwig-Maximilians-University of Munich, Germany for the present study. This work was funded by companies of ICST and G-LAND, and the University of Suwon.
The authors declare no conflicts of interest regarding the publication of this paper.
Kim, T.-J., Hong, G.H., Kim, D.G. and Baskaran, M. (2019) Iron Fertilization with Enhanced Phytoplankton Productivity under Minimal Sulfur Compounds and Grazing Control Analysis in HNLC Region. American Journal of Climate Change, 8, 14-39. https://doi.org/10.4236/ajcc.2019.81002