Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis

Anthropogenic CO₂ emissions are acidifying the world’s oceans. A growing body of evidence demonstrates that ocean acidification can impact survival, growth, development and physiology of marine invertebrates. Here, we tested the impact of long-term (up to 16 months) and trans-life-cycle (adult, embryo/larvae and juvenile) exposure to elevated pCO₂ (1,200 μatm, compared to control 400 μatm) on the green sea urchin Strongylocentrotus droebachiensis. Female fecundity was decreased 4.5-fold when acclimated to elevated pCO₂ for 4 months during reproductive conditioning, while no difference was observed in females acclimated for 16 months. Moreover, adult pre-exposure for 4 months to elevated pCO₂ had a direct negative impact on subsequent larval settlement success. Five to nine times fewer offspring reached the juvenile stage in cultures using gametes collected from adults previously acclimated to high pCO₂ for 4 months. However, no difference in larval survival was observed when adults were pre-exposed for 16 months to elevated pCO₂. pCO₂ had no direct negative impact on juvenile survival except when both larvae and juveniles were raised in elevated pCO₂. These negative effects on settlement success and juvenile survival can be attributed to carry-over effects from adults to larvae and from larvae to juveniles. Our results support the contention that adult sea urchins can acclimate to moderately elevated pCO₂ in a matter of a few months and that carry-over effects can exacerbate the negative impact of ocean acidification on larvae and juveniles.     

Effects of ocean acidification on the early developmental stages of the horned turban,Turbo cornutus

To estimate the impact of CO₂-driven ocean acidification on the early life stages of gastropods, the effects of increased partial pressure of seawater carbon dioxide (pCO₂) (800–2,000 μatm) on the early developmental stages and larval shell length of the commercially important gastropod, the horned turban snail, Turbo cornutus were investigated. Increase in experimental seawater pCO₂ had an increasingly negative impact on the early developmental rate; the proportion of embryos or larvae displaying retarded development increased at higher pCO₂. The proportion of embryos that developed to the 4-cell stage at 2 h after fertilization decreased linearly with increasing pCO₂. At ~1,000 μatm pCO₂, retarded development was observed in ~50 % of larvae. No embryos developed to the 4-cell stage at 2,000 μatm pCO₂ within 2 h of fertilization. A similar trend continued until 24–26 h after fertilization; the proportion of larvae attaining veliger stage by 24–26 h also decreased with increasing pCO₂. The shell length of T. cornutus veligers decreased gradually as seawater pCO₂ increased, but markedly decreased in seawater under nearly unsaturated and unsaturated conditions (≤1.04) of the aragonite saturation state (Ω _aragonite). The results indicate that increased pCO₂ seawater has a progressive and acute effect on embryonic and larval T. cornutus, and imply that the extended early developmental period and/or the downsized larval shell produced by ocean acidification will have a negative impact on survival, settlement and recruitment well into the future.     

Predicted impact of ocean acidification on a marine invertebrate: elevated CO<Subscript>2</Subscript> alters response to thermal stress in sea urchin larvae

Ocean acidification (OA) and the biological consequences of altered seawater chemistry have emerged as a significant environmental threat to healthy marine ecosystems. Because a more acidic ocean interferes with fixation of calcium carbonate to form shells or calcified skeletons, future ocean chemistry may significantly alter the physiology of calcifying marine organisms. These alterations may manifest themselves directly in the calcification process, or have synergistic effects with other environmental factors such as elevated temperatures. New tools permit us to explore subtle changes in gene expression patterns in response to environmental conditions. We raised sea urchins (Strongylocentrotus franciscanus) under conditions simulating future atmospheric CO₂ levels of 540 and 970 ppm. When larvae raised under elevated CO₂ conditions were subjected to 1-h acute temperature stress, their ability to mount a physiological response (as measured by expression of the molecular chaperone hsp70) was reduced relative to those raised under ambient CO₂ conditions. These results represent the first use of gene expression assays to study the effects of OA on sea urchin development. They highlight the importance of looking at multiple environmental factors simultaneously as this approach may reveal previously unsuspected biological impacts of atmospheric changes.     

The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2

Given the threats of greenhouse gas emissions and a changing climate to marine ecosystems, there is an urgent need to better understand the response of not only adult corals, which are particularly sensitive to environmental changes, but also their larvae, whose mechanisms of acclimation to both temperature increases and ocean acidification are not well understood. Brooded larvae from the reef coral Pocillopora damicornis collected from Nanwan Bay, Southern Taiwan, were exposed to ambient or elevated temperature (25 or 29 °C) and pCO₂ (415 or 635 μatm) in a factorial experiment for 9 days, and a variety of physiological and molecular parameters were measured. Respiration and rubisco protein expression decreased in larvae exposed to elevated temperature, while those incubated at high pCO₂ were larger in size. Collectively, these findings highlight the complex metabolic and molecular responses of this life history stage and the need to integrate our understanding across multiple levels of biological organization. Our results also suggest that for this pocilloporid larval life stage, the impacts of elevated temperature are likely a greater threat under near-future predictions for climate change than ocean acidification.     

Metal contamination increases the sensitivity of larvae but not gametes to ocean acidification in the polychaete Pomatoceros lamarckii (Quatrefages)

Ocean acidification is not happening in isolation but against a background of chronic low-level pollution for most coastal marine environments. The reproductive and larval stages of marine invertebrates can be highly sensitive to the impacts of both environmental pollutants and ocean acidification, but very little is currently known regarding the potential impacts of combined contaminant and high CO₂ exposures on the health of marine organisms. Ocean acidification research to date has focused heavily on the responses of calcifying marine invertebrate larvae and algae, and as such the polychaetes as a group, despite their ecological importance, remain understudied. Here, we investigate the effects of elevated seawater CO₂ (pH range 8.1–7.4, plus an extreme pH of 7.2 in the sperm motility experiments), in combination with the environmental pollutant copper (0.002 μM), on the early life history stages of the intertidal polychaete Pomatoceros lamarckii from two populations. P. lamarckii sperm appear to be robust to elevated seawater CO₂. Whilst all three of the sperm motility end points measured showed a response to elevated CO₂, these responses were small and not linear. The percentage of motile sperm and sperm curvilinear velocity were significantly reduced in the lower pH treatments of 7.4 and 7.2, whereas sperm straight-line velocity (VSL) was mostly unaffected except for an increased VSL at pH 8.0. Fertilisation success was investigated using two populations from the South West (UK), one from Torquay and one from Plymouth Sound. Fertilisation success was slightly but significantly reduced at the 7.6 and 7.4 pH treatments for both populations (a 9.0 % reduction in fertilisation success from pH 8.1 to 7.4 for Torquay), but with a greater effect observed in the population from Plymouth Sound (a 13.33 % reduction in fertilisation success). No additional impact of 0.002 μM copper exposure on fertilisation success was found. Larval survival was found to be much more sensitive to elevated CO₂ than sperm function or fertilisation, and a significant interaction with copper exposure was observed. These results demonstrate the potential for polychaete larvae to be affected by predicted ocean acidification conditions and that chronic coastal pollutants, such as copper, have the potential to alter larval susceptibility to ocean acidification conditions.     

海洋酸化对鱼类感觉和行为影响的研究进展

海洋酸化是指大气增多的二氧化碳(CO2)溶解于海水而导致海水p H值降低的过程。海洋酸化将改变海水碳酸盐平衡体系,使依赖于原化学环境的多种海洋生物乃至生态系统面临巨大威胁。海洋酸化对钙质生物影响的研究最早引起大家关注,而海洋鱼类具有较完善的酸碱调节机制,大家普遍认为酸化对其影响不大。但在过去的5年中,不少实验证明海洋酸化会影响海洋鱼类仔稚鱼的感觉和行为,减弱其野外的生存能力及增加被捕食率,很可能将威胁自然种群补给量和影响全球的渔业资源量。本文从嗅觉、听觉、视觉及高级意识和相关行为角度,综述近几年海洋酸化对鱼类感觉和行为影响的研究进展,介绍了鱼类神经行为生物学的研究,为全面了解和预测海洋酸化的生态、经济和社会效应提供科学依据。     

Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution

Experimental ocean acidification leads to a shift in resource allocation and to an increased [HCO₃ ^?] within the perivisceral coelomic fluid (PCF) in the Baltic green sea urchin Strongylocentrotus droebachiensis. We investigated putative mechanisms of this pH compensation reaction by evaluating epithelial barrier function and the magnitude of skeleton (stereom) dissolution. In addition, we measured ossicle growth and skeletal stability. Ussing chamber measurements revealed that the intestine formed a barrier for HCO₃ ^? and was selective for cation diffusion. In contrast, the peritoneal epithelium was leaky and only formed a barrier for macromolecules. The ossicles of 6 week high CO₂-acclimatised sea urchins revealed minor carbonate dissolution, reduced growth but unchanged stability. On the other hand, spines dissolved more severely and were more fragile following acclimatisation to high CO₂. Our results indicate that epithelia lining the PCF space contribute to its acid–base regulation. The intestine prevents HCO₃ ^? diffusion and thus buffer leakage. In contrast, the leaky peritoneal epithelium allows buffer generation via carbonate dissolution from the surrounding skeletal ossicles. Long-term extracellular acid–base balance must be mediated by active processes, as sea urchins can maintain relatively high extracellular [HCO₃ ^?]. The intestinal epithelia are good candidate tissues for this active net import of HCO₃ ^? into the PCF. Spines appear to be more vulnerable to ocean acidification which might significantly impact resistance to predation pressure and thus influence fitness of this keystone species.     

Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei

Effects of acclimation to projected near-future ocean acidification (OA) conditions on physiology, reproduction and development were investigated in the tropical sea urchin Echinometra mathaei. Following 6 weeks in control or one of the three elevated pCO₂ (pH_NIST 7.5–8.1; pCO₂ ~485–1,770 μatm) conditions, adult urchins exhibited a slight decline of growth in low pH treatments and moderately reduced respiration at intermediate levels. At 7 weeks, gametes from adults were used to produce larvae that were reared in their respective parental treatments. To assess whether larvae from acclimated parents are more resilient to elevated pCO₂ than those not acclimated, larvae from control animals were also reared in the elevated pCO₂ treatments. There was no difference in female ‘spawnability’ and oocyte size between treatments, but male spawning ability was reduced in increased pCO₂ conditions. In elevated pCO₂ treatments, the percentage of normal larvae and larval size decreased in the progeny of control- and elevated pCO₂-acclimated parents, and arm asymmetry increased. Thus, acclimation of the parents did not make the progeny more resilient or sensitive to OA effects. Negative effects of increased pCO₂ on reproduction and development may impact on recruitment and population maintenance of this species.     

Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species

Ocean acidification, as a result of increased atmospheric CO₂, is predicted to lower the pH of seawater to between pH 7.6 and 7.8 over the next 100 years. The greatest changes are expected in polar waters. Our research aimed to examine how echinoid larvae are affected by lower pH, and if effects are more pronounced in polar species. We examined the effects of lowered pH on larvae from tropical (Tripneustes gratilla), temperate (Pseudechinus huttoni, Evechinus chloroticus), and a polar species (Sterechinus neumayeri) in a series of laboratory experiments. Larvae were reared in a range of lower pH seawater (pH 6.0, 6.5, 7.0, 7.5, 7.7, 7.8 and ambient), adjusted by bubbling CO₂ gas. The effect of pH on somatic and skeletal growth, calcification index, development and survival were quantified, while SEM examination of the larval skeleton provided information on the effects of seawater pH on the fine-scale skeletal morphology. Lowering pH resulted in a decrease in survival in all species, but only below pH 7.0. The size of larvae were reduced at lowered pH, but the external morphology (shape) was unaffected. Calcification of the larval skeleton was significantly reduced (13.8–36.9% lower) under lowered pH, with the exception of the Antarctic species, which showed no significant difference. SEM examination revealed a degradation of the larval skeletons of Pseudechinus and Evechinus when grown in reduced pH. Sterechinus and Tripneustes showed no apparent difference in the skeletal fine structure under lowered pH. The study confirms the need to look beyond mortality as a single endpoint when considering the effects of ocean acidification that may occur through the 21st century, and instead, look for a suite of more subtle changes, which may indirectly affect the functioning of larval stages.     

Elevated CO2 alters larval proteome and its phosphorylation status in the commercial oyster, Crassostrea hongkongensis

Ocean acidification (OA) is beginning to have noticeable negative impact on calcification rate, shell structure and physiological energy budgeting of several marine organisms; these alter the growth of many economically important shellfish including oysters. Early life stages of oysters may be particularly vulnerable to OA-driven low pH conditions because their shell is made up of the highly soluble form of calcium carbonate (CaCO₃) mineral, aragonite. Our long-term CO₂ perturbation experiment showed that larval shell growth rate of the oyster species Crassostrea hongkongensis was significantly reduced at pH < 7.9 compared to the control (8.2). To gain new insights into the underlying mechanisms of low-pH-induced delays in larval growth, we have examined the effect of pH on the protein expression pattern, including protein phosphorylation status at the pediveliger larval stage. Using two-dimensional electrophoresis and mass spectrometry, we demonstrated that the larval proteome was significantly altered by the two low pH treatments (7.9 and 7.6) compared to the control pH (8.2). Generally, the number of expressed proteins and their phosphorylation level decreased with low pH. Proteins involved in larval energy metabolism and calcification appeared to be down-regulated in response to low pH, whereas cell motility and production of cytoskeletal proteins were increased. This study on larval growth coupled with proteome change is the first step toward the search for novel Protein Expression Signatures indicative of low pH, which may help in understanding the mechanisms involved in low pH tolerance.     

Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis

The impact of elevated CO₂ and temperature on photosynthesis and calcification in the symbiont-bearing benthic foraminifer Marginopora vertebralis was studied. Individual specimens of M. vertebralis were collected from Heron Island on the southern Great Barrier Reef (Australia). They were maintained for 5 weeks at different temperatures (28, 32 °C) and pCO₂ (400, 1,000 µatm) levels spanning a range of current and future climate-change scenarios. The photosynthetic capacity of M. vertebralis was measured with O₂ microsensors and a pulse-amplitude-modulated chlorophyll (Chl) fluorometer, in combination with estimates of Chl a and Chl c ₂ concentrations and calcification rates. After 5 weeks, control specimens remained unaltered for all parameters. Chlorophyll a concentrations significantly decreased in the specimens at 1,000 µatm CO₂ for both temperatures, while no change in Chl c ₂ concentration was observed. Photoinhibition was observed under elevated CO₂ and temperature, with a 70–80 % decrease in the maximum quantum yield of PSII. There was no net O₂ production at elevated temperatures in both CO₂ treatments as compared to the control temperature, supporting that temperature has more impact on photosynthesis and O₂ flux than changes in ambient CO₂. Photosynthetic pigment loss and a decrease in photochemical efficiency are thus likely to occur with increased temperature. The elevated CO₂ and high temperature treatment also lead to a reduction in calcification rate (from +0.1 to >?0.1 % day^?1). Thus, both calcification and photosynthesis of the major sediment-producing foraminifer M. vertebralis appears highly vulnerable to elevated temperature and ocean acidification scenarios predicted in climate-change models.     

Decreased pH does not alter metamorphosis but compromises juvenile calcification of the tube worm Hydroides elegans

Using CO₂ perturbation experiments, we examined the pre- and post-settlement growth responses of a dominant biofouling tubeworm (Hydroides elegans) to a range of pH. In three different experiments, embryos were reared to, or past, metamorphosis in seawater equilibrated to CO₂ values of about 480 (control), 980, 1,480, and 2,300 μatm resulting in pH values of around 8.1 (control), 7.9, 7.7, and 7.5, respectively. These three decreased pH conditions did not affect either embryo or larval development, but both larval calcification at the time of metamorphosis and early juvenile growth were adversely affected. During the 24-h settlement assay experiment, half of the metamorphosed larvae were unable to calcify tubes at pH 7.9 while almost no tubes were calcified at pH 7.7. Decreased ability to calcify at decreased pH may indicate that these calcifying tubeworms may be one of the highly threatened species in the future ocean.     

Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release

To evaluate the effects of temperature and pCO₂ on coral larvae, brooded larvae of Pocillopora damicornis from Nanwan Bay, Taiwan (21°56.179′N, 120°44.85′E), were exposed to ambient (419–470 μatm) and high (604–742 μatm) pCO₂ at ~25 and ~29 °C in two experiments conducted in March 2010 and March 2012. Larvae were sampled from four consecutive lunar days (LD) synchronized with spawning following the new moon, incubated in treatments for 24 h, and measured for respiration, maximum photochemical efficiency of PSII (F _v/F _m), and mortality. The most striking outcome was a strong effect of time (i.e., LD) on larvae performance: respiration was affected by an LD × temperature interaction in 2010 and 2012, as well as an LD × pCO₂ × temperature interaction in 2012; F _v/F _m was affected by LD in 2010 (but not 2012); and mortality was affected by an LD × pCO₂ interaction in 2010, and an LD × temperature interaction in 2012. There were no main effects of pCO₂ in 2010, but in 2012, high pCO₂ depressed metabolic rate and reduced mortality. Therefore, differences in larval performance depended on day of release and resulted in varying susceptibility to future predicted environmental conditions. These results underscore the importance of considering larval brood variation across days when designing experiments. Subtle differences in experimental outcomes between years suggest that transgenerational plasticity in combination with unique histories of exposure to physical conditions can modulate the response of brooded coral larvae to climate change and ocean acidification.     

Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH

We examined the response of the tropical sand dollar Arachnoides placenta to reduced seawater pH in experiments spanning ca. 50 % of the planktonic larval duration. A. placenta inhabits intertidal sandy beaches where we observed a minimum in situ pH range 0.06 pH units (pH 8.10–8.16). The responses of gametes and larvae to seawater pH were tested in vitro in ambient (pH 8.14, pCO₂ = 525.7 μatm, total alkalinity = 2,651 μmol kg soln^?1) and three reduced pH seawater treatments (7.8–7.0). Percentage fertilisation decreased significantly with decreasing pH across a range of sperm/egg ratios (4:1 up to 4,000:1). A. placenta reached the advanced pluteus stage in 4 days, and during this time, we saw no difference in survival rate of larvae between the ambient (67 %) and pH 7.79 (72 %) treatments. Four-day survival was, however, reduced to 44 and 11 % in the pH 7.65 and 7.12 treatments, respectively. Larval development and morphometrics varied among pH treatments. Embryos reared in pH 7.12 exhibited arrested development. Larvae reared at pH 7.65 showed delayed development and greater mortality compared with those reared at pH 7.79 and 8.14. When larval morphometrics are compared among larvae of the same size, differences in larval width and total arm length between pH treatments disappear. These results suggest that variation in larval size among the three highest pH treatments at a given time are likely the result of slower development and apparent shrinkage of surviving larvae and not direct changes in larval shape. There were no differences in the percentage inorganic content (a proxy for calcification) in larvae reared in either an ambient or a pH 7.7 treatment. The responses of fertilisation and development to decreased pH/increased pCO₂ in A. placenta are within the range of those reported for other intertidal and subtidal echinoid species from colder latitudes.     

Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata

Marine organisms inhabiting environments where pCO₂/pH varies naturally are suggested to be relatively resilient to future ocean acidification. To test this hypothesis, the effect of elevated pCO₂ was investigated in the articulated coralline red alga Corallina elongata from an intertidal rock pool on the north coast of Brittany (France), where pCO₂ naturally varied daily between 70 and 1000 μatm. Metabolism was measured on algae in the laboratory after they had been grown for 3 weeks at pCO₂ concentrations of 380, 550, 750 and 1000 μatm. Net and gross primary production, respiration and calcification rates were assessed by measurements of oxygen and total alkalinity fluxes using incubation chambers in the light and dark. Calcite mol % Mg/Ca (mMg/Ca) was analysed in the tips, branches and basal parts of the fronds, as well as in new skeletal structures produced by the algae in the different pCO₂ treatments. Respiration, gross primary production and calcification in light and dark were not significantly affected by increased pCO₂. Algae grown under elevated pCO₂ (550, 750 and 1000 μatm) formed fewer new structures and produced calcite with a lower mMg/Ca ratio relative to those grown under 380 μatm. This study supports the assumption that C. elongata from a tidal pool, where pCO₂ fluctuates over diel and seasonal cycles, is relatively robust to elevated pCO₂ compared to other recently investigated coralline algae.     

Ocean acidification and temperature rise: effects on calcification during early development of the cuttlefish Sepia officinalis

This study investigated the effects of seawater pH (i.e., 8.10, 7.85 and 7.60) and temperature (16 and 19 °C) on (a) the abiotic conditions in the fluid surrounding the embryo (viz. the perivitelline fluid), (b) growth, development and (c) cuttlebone calcification of embryonic and juvenile stages of the cephalopod Sepia officinalis. Egg swelling increased in response to acidification or warming, leading to an increase in egg surface while the interactive effects suggested a limited plasticity of the swelling modulation. Embryos experienced elevated pCO₂ conditions in the perivitelline fluid (>3-fold higher pCO₂ than that of ambient seawater), rendering the medium under-saturated even under ambient conditions. The growth of both embryos and juveniles was unaffected by pH, whereas ⁴⁵Ca incorporation in cuttlebone increased significantly with decreasing pH at both temperatures. This phenomenon of hypercalcification is limited to only a number of animals but does not guarantee functional performance and calls for better mechanistic understanding of calcification processes.     

Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification

The accumulation of carbon dioxide in the atmosphere will lower the pH in ocean waters, a process termed ocean acidification (OA). Despite its potentially detrimental effects on calcifying organisms, experimental studies on the possible impacts on fish remain scarce. While adults will most likely remain relatively unaffected by changes in seawater pH, early life-history stages are potentially more sensitive, due to the lack of gills with specialized ion-regulatory mechanisms. We tested the effects of OA on growth and development of embryos and larvae of eastern Baltic cod, the commercially most important fish stock in the Baltic Sea. Cod were reared from newly fertilized eggs to early non-feeding larvae in 5 different experiments looking at a range of response variables to OA, as well as the combined effect of CO₂ and temperature. No effect on hatching, survival, development, and otolith size was found at any stage in the development of Baltic cod. Field data show that in the Bornholm Basin, the main spawning site of eastern Baltic cod, in situ levels of pCO₂ are already at levels of 1,100 μatm with a pH of 7.2, mainly due to high eutrophication supporting microbial activity and permanent stratification with little water exchange. Our data show that the eggs and early larval stages of Baltic cod seem to be robust to even high levels of OA (3,200 μatm), indicating an adaptational response to CO₂.     

Effect of increasing sea water pCO2 on the northern Atlantic krill species Nyctiphanes couchii

Surprisingly little is known about potential effects of ocean acidification on krill of the Northern Hemisphere as ecologically very important food web component. Sub-adult individuals of the northern Atlantic krill species Nyctiphanes couchii (caught at Austevoll near Bergen, Norway, in January 2013) were exposed in the laboratory to four different levels of pCO₂ (430, 800, 1,100, and 1,700 µatm) for 5 weeks in order to assess potential changes in a set of biological response variables. Survival decreased and the frequency of moulting-related deaths increased with increasing pCO₂. Survival was considerably reduced at relatively high pCO₂ of 1,700 µatm and tended to be negatively affected at 1,100 µatm pCO₂. However, the experimental results show no significant effects of pCO₂ on inter-moult period and growth at pCO₂ levels below 1,100 µatm. No differences in length measurements of the carapace and uropod were observed across pCO₂ levels, indicating no effect of changing carbonate chemistry on the morphology of those calciferous parts of the exoskeleton. The results suggest that sub-adult N. couchii may not suffer dramatically from predicted near-future changes in pCO₂. However, potential detrimental effects on the moulting process and associated higher mortality at 1,100 µatm pCO₂ cannot be excluded. Further experiments are needed in order to investigate whether early life stages of N. couchii show a different sensitivity to elevated sea water pCO₂ and whether those results are transferable to other krill species of the Northern Hemisphere.