Comparison of the metabolism of Acartia clausi and A. tonsa: influence of temperature and salinity

In the Marseilles region (French Mediterranean coast), A. clausi is one of the most abundant copepod species of the Gulf of Fos while A. tonsa constitutes the almost exclusive copepod species of the Berre lagoon, a neighbouring semi-closed brackish area communicating with the gulf. As different ecophysiological capabilities to stand the various temperature, salinity and food conditions could explain why these two species do not coexist in the same environment, comparative experiments were performed on metabolism and feeding. The respiration and ammonia excretion of the two species were measured in different combinations of temperature (10, 15 and 20 degrees C) and salinity (15, 25 and 35 per thousand). For each temperature, at the salinity of 35 per thousand, respiration rates were less in A. clausi than in A. tonsa, the contrary being observed at the lowest salinity. At any temperature ammonia excretion was greater at the intermediate salinity in A. tonsa and least in A. clausi. In Acartia tonsa, Q(10) of respiration and excretion were minimum at the lowest salinity, while in A. clausi they were unaffected by salinity variation. The O:N atomic ratio (from respiration and ammonia excretion rates) was significantly more elevated in A. clausi (mean 21.2; range 13.6-28.7) than in A. tonsa (mean 11.3; range 4.2-25) suggesting a more proteinic oriented metabolism in the later. Feeding experiments where Dunaliella tertiolecta30 per thousand) or lagoon (<16 per thousand) salinity. The relationships between ingestion and food concentration in the two species were not significantly different. These different results are compared to other ecophysiological information concerning these Acartia species (survival tolerances, osmotic regulation, feeding behaviour) and are discussed in relation with the characteristics of their niches in the studied region.     

Copepods induce paralytic shellfish toxin production in marine dinoflagellates

Among the thousands of unicellular phytoplankton species described in the sea, some frequently occurring and bloom-forming marine dinoflagellates are known to produce the potent neurotoxins causing paralytic shellfish poisoning. The natural function of these toxins is not clear, although they have been hypothesized to act as a chemical defence towards grazers. Here, we show that waterborne cues from the copepod Acartia tonsa induce paralytic shellfish toxin (PST) production in the harmful algal bloom-forming dinoflagellate Alexandrium minutum. Induced A. minutum contained up to 2.5 times more toxins than controls and was more resistant to further copepod grazing. Ingestion of non-toxic alternative prey was not affected by the presence of induced A. minutum. The ability of A. minutum to sense and respond to the presence of grazers by increased PST production and increased resistance to grazing may facilitate the formation of harmful algal blooms in the sea.     

Acartia tonsa (Сopepoda) in the Black and Caspian Seas: Review of its success and some lessons

The variety of aquatic nonindigenous animals in marine habitats worldwide includes more than 16 planktonic Copepoda species. Acartia tonsa is a very successful one, distributed in many seas. Its invasion into European seas was analyzed before (Brylinski,1981), but from that time A.tonsa extended its range in European aquatic habitats. The author describes the history of the A.tonsa invasion into the Ponto-Caspian basin as well as some misleading earlier publications. Morphologic differences between A.clausi and A.tonsa, the neglect of which led to the wrong identification, were examined. The data on A.tonsa and total copepod dynamics in the Sevastopol Bay during the period of 1976~1996 and the same data on the Caspian Sea since 1981 were analyzed. The average size of A.tonsa in new habitats decreased, and its relative density in the Black and Caspian Seas gradually increased.     

Telotroch formation, survival, and attachment in the epibiotic peritrich Zoothamnium intermedium (Ciliophora, Oligohymenophorea)

Abstract. Aspects of the life cycle of the peritrich ciliate Zoothamnium intermedium , an epibiont on calanoid copepods in the Chesapeake Bay, were investigated using host and epibiont cultures. Experiments were designed to characterize the formation, survival, and attachment of free-swimming stages (telotrochs) and to assess whether telotrochs preferentially attach to primary ( Acartia tonsa and Eurytemora affinis ) or alternate hosts from the zooplankton community (the rotifer Brachionus plicatilis , barnacle nauplii, polychaete larvae, and a harpacticoid copepod). The results showed that telotroch formation started 2 h after the death of the host, with >90% of the zooids leaving the host carapace within 7 h. Formation of telotrochs was triggered only by the death of the host, failing to occur when the host was injured or unable to swim. Telotrochs failed to attach to non-living substrates and survived for only 14 h in the absence of host organisms, suggesting that members of Z. intermedium are obligate epibionts. Attachment success decreased with telotroch age, indicating that colonization success in nature may strongly depend on the ability to find a suitable host in a short period of time. Individuals exhibited no preferences in colonizing juvenile or adult stages of A. tonsa or E. affinis . While telotrochs were able to colonize barnacle nauplii and the harpacticoid copepod in the absence of individuals of A. tonsa or E. affinis , they did not attach to the rotifers or polychaete larvae. Telotrochs preferentially colonized individuals of A. tonsa when in the presence of other non-calanoid host species.     

DMSP-consuming bacteria associated with the calanoid copepod Acartia tonsa (Dana)

DMSP-consuming bacteria (DCB) were recovered from the body and fecal pellets of the copepod Acartia tonsa (Dana). The most probable number of DCB associated with starved A. tonsa was 9.2x10(2) cells copepod(-1). The abundance of DCB recovered from the copepod body increased to 1.6-2.8x10(4) after the copepod fed on DMSP-containing alga. DCB abundance associated with fecal pellets averaged 1.2x10(4) cells pellet(-1). In enrichment cultures, the DCB grew with a doubling time of 1.1-2.9 days, and consumed DMSP at a rate of 4.5-7.5 fmol cell(-1) day(-1). The apparent DMSP-to-DMS conversion efficiency was 25-41% for DCB from copepod body, and 99% for DCB from fecal pellets. Our study demonstrated that copepods and their fecal pellets may harbour dense populations of DCB, and that the copepod-bacteria coupling represents a novel mechanism for DMSP consumption in the water column.     

High-speed video analysis of the escape responses of the copepod Acartia tonsa to shadows

The copepod Acartia tonsa exhibits a vigorous escape jump in response to rapid decreases in light intensity, such as those produced by the shadow of an object passing above it. In the laboratory, decreases in light intensity were produced using a fiber optic lamp and an electronic shutter to abruptly either nearly eliminate visible light or reduce light intensity to a constant proportion of its original intensity. The escape responses of A. tonsa to these rapid decreases in visible light were recorded on high-speed video using infrared illumination. The speed, acceleration, and direction of movement of the escape response were quantified from videotape by using automated motion analysis techniques. A. tonsa typically responds to decreases in light intensity with an escape jump comprising an initial reorientation followed by multiple power strokes of the swimming legs. These escape jumps can result in maximum speeds of over 800 mm s(-1) and maximum accelerations of over 200 m s(-2). In A. tonsa, photically stimulated escape responses differ from hydrodynamically stimulated responses mainly in the longer latencies of photically stimulated responses and in the increased number of power strokes, even when the stimulus is near threshold; these factors result in longer escape jumps covering greater distances. The latency of responses of A. tonsa to this photic stimulus ranged from a minimum of about 30 ms to a maximum of more than 150 ms, compared to about 4 ms for hydrodynamically stimulated escape jumps. Average response latency decreased with increasing light intensity or increasing proportion of light eliminated. Little change was observed in the vigor of the escape response to rapid decreases in visible light over a wide range of adaptation intensities.     

Relationship between specific dynamic action and protein deposition in calanoid copepods

The link between specific dynamic action (SDA) and protein deposition was investigated in copepodites stage V of two calanoid copepod species, the neritic Acartia tonsa and the oceanic Calanus finmarchicus. This was done by measuring respiration before, during, and after a specific feeding period and measuring the incorporation of carbon into proteins. These were also measured on individuals incubated with cycloheximide, an antibiotic that inhibits protein synthesis. The cycloheximide treatment significantly diminished the magnitude of SDA in both A. tonsa and C. finmarchicus, and inhibited carbon incorporation into protein in both species. This provides evidence that the rate at which protein deposition takes place greatly affects the magnitude of SDA. The specific respiration rates of both starving and feeding copepods were generally higher in A. tonsa than in C. finmarchicus. This influenced SDA, the magnitude of SDA normalised to an 8 h feeding period being threefold higher in A. tonsa (78.7+/-25.7 nlO(2) μgC(-1)) than in C. finmarchicus (27.5+/-11.6 nlO(2) μgC(-1)). This difference may arise due to differences in energy allocation in the organisms of the copepodite V stage of the two species. In this stage C. finmarchicus deposits large quantities of storage lipids, predominately wax esters, whereas A. tonsa deposits proteins during somatic growth.     

Feeding rates and productivity of the copepod Acartia bifilosa in a highly turbid estuary; the Gironde (SW France)

Acartia spp. are the dominant copepod species in the Gironde estuary, seaward of the turbidity maximum area. Acartia bifilosa develop a large population in spring and early summer whereas Acartia tonsa appear in late summer. High values and high variability of chlorophyll a/suspended particulate matter ratio are found seaward of the turbidity maximum area. Feeding rates of A. bifilosa were measured by fluorometry. Phytoplankton ingestion was found to be highly variable, between 8 to 80% of copepod carbon body weight. Except for adult females, copepods were heavier in summer than in winter. PB ratios, estimated by the instantaneous growth rate method, varied from 0.03 d^–1 to 0.14 d^–1. The gut contents and P/B ratios of Acartia bifilosa were related to chl a/SPM ratio. From those data, and a few obtained for A. tonsa, it is concluded that only in summer months phytoplankton ingestion is enough to maintain secondary production.     

Copepod grazing on a phytoplankton community containing the toxic dinoflagellate Dinophysis acuminata

Copepod grazing on the toxic dinofiagellate Dinophysis acuminatafrom the west coast of France (La Rochelle) was studied witha concentrated (40–70 µm) phytoplankton assemblagedominated by Leptocylindrus danicus, D.acuminata, Ceratium fususand Ceratium furca. Copepod nauplii were also present. Threeto five copepods/copepodites (Acartia clausi, Isias clavipesand Centropages typicus) were incubated together with the phytoplankton.Dinophysis acuminata was grazed upon by all copepod species.However, to some extent, I.clavipes and C.typicus avoided itas food. Dinophysis acuminata cells represented for them only5–10% of total ingested carbon during the first 24 h,and almost all individuals survived and thrived well. In contrast,A.clausi did not avoid D.acuminata. which represented 30% ofingested carbon in 1 day. Acartia clausi then had a lower survivalthan the two other copepod species. However, the survival ofA.clausi was high in control incubations, where a plankton communitywithout D.acuminata was used as food. It is concluded that theokadaic acid of D acuminata is potentially toxic to some grazers,and/or might function as an allelopathic grazer repellent.     

Sublethal effects of cupric ion activity on the phototaxis of three calanoid copepods

Using wavelengths near maximal photosensitivity, phototactic responses of two estuarine calanoid copepods (Acartia tonsa, Acartia hudsonica) and one nearshore, neritic copepod (Temora longicornis) were measured after 24 h exposures to sublethal concentrations of free cupric ions. A nitrilotriacetate-trace metal ion buffer system was used to control the free cupric ion activity (pCu = negative log of the free cupric ion activity), which determines organismic response. All three species exhibited positive phototaxis at pCu 13.0 reported for unpolluted surface sea waters and estuarine waters. As cupric ion activity increased, percent positive phototactic response decreased, indicating a strong sublethal effect of free cupric ions on photobehavior. Changes in photobehavior occurred at cupric ion activities that have been reported for many estuaries and coastal waters near urban and industrialized areas. Temora longicornis was much less phototactically sensitive than the two estuarine species. It also exhibited phototactic sign switching as pCu changed.     

Zooplankton community composition and copepod grazing on the West Florida Shelf in relation to blooms of Karenia brevis

Blooms of the toxin producing dinoflagellate Karenia brevis occur routinely on the West Florida Shelf of the Gulf of Mexico. Nutrient supplies are thought to play a large role in the formation and maintenance of these blooms. The role of top-down control has been less well studied, but grazing, or the lack thereof, on these toxic species may also enhance the formation of large biomass blooms in this region. Zooplankton community structure and copepod species composition were analyzed from samples collected on the West Florida Shelf (WFS) during a NOAA funded ECOHAB regional Karenia Nutrient Dynamics project during October 2007–2010. In 2008 there was no statistical difference in the abundance of zooplankton at bloom and non-bloom stations, however in 2009 there was a statistically significant difference (p < 0.05) between the abundance of zooplankton at stations with Karenia present. To investigate copepod ingestion rates in relation to K. brevis, shipboard and laboratory experiments of the single label method of ¹⁴C labeled phytoplankton culture, and time course ingestion experiments with isolated copepods were performed. Calculated ingestion rates suggest that the copepod species Centropages velificatus, and Acartia tonsa ingested K. brevis, however rates were variable among collection sites and K. brevis strains. Parvocalanus crassirostris did not ingest K. brevis in any of the experiments.     

Algal toxins alter copepod feeding behavior

Using digital holographic cinematography, we quantify and compare the feeding behavior of free-swimming copepods, Acartia tonsa, on nutritional prey (Storeatula major) to that occurring during exposure to toxic and non-toxic strains of Karenia brevis and Karlodinium veneficum. These two harmful algal species produce polyketide toxins with different modes of action and potency. We distinguish between two different beating modes of the copepod's feeding appendages-a "sampling beating" that has short durations (<100 ms) and involves little fluid entrainment and a longer duration "grazing beating" that persists up to 1200 ms and generates feeding currents. The durations of both beating modes have log-normal distributions. Without prey, A. tonsa only samples the environment at low frequency. Upon introduction of non-toxic food, it increases its sampling time moderately and the grazing period substantially. On mono algal diets for either of the toxic dinoflagellates, sampling time fraction is high but the grazing is very limited. A. tonsa demonstrates aversion to both toxic algal species. In mixtures of S. major and the neurotoxin producing K. brevis, sampling and grazing diminish rapidly, presumably due to neurological effects of consuming brevetoxins while trying to feed on S. major. In contrast, on mixtures of cytotoxin producing K. veneficum, both behavioral modes persist, indicating that intake of karlotoxins does not immediately inhibit the copepod's grazing behavior. These findings add critical insight into how these algal toxins may influence the copepod's feeding behavior, and suggest how some harmful algal species may alter top-down control exerted by grazers like copepods.     

Nutritive Value and Selection of Food Particles by Copepods During a Spring Bloom of Phaeocystis sp. in the English Channel, as Determined by Pigment and Fatty Acid Analyses

In this study phytoplankton pigments and fatty acids were usedas biomarkers to study trophic relationships between phytoplanktonand zooplankton. These markers permit the characterization ofboth suspended matter and copepods, allowing examination ofthe transfers from food to zooplankton. A drogue study was carriedout to follow a water mass in the coastal waters off the easternEnglish Channel over a 3-day period, with samples collectedevery 3 h. The study focused on the dominant calanoid copepodspecies: Temora longicornis, Acartia clausi and Pseudocalanuselongatus. Our study was performed during the spring phytoplanktonbloom when solitary cells of Phaeocystis sp. formed 90% of thetotal phytoplankton. Fatty acid analyses provided an indicationof the low nutritive value of these algal cells; in contrastto other algal species which had higher nutritional value (e.g.colony-forming diatoms, Cryptophytes and dinoflagellates). Ourresults suggest that all species selectively grazed on Phaeocystissp. and non-selectively on diatoms. Dinoflagellates were avoidedby all species. Temora longicornis selectively grazed on Cryptophytes,which may be related to the nutritional value of this algae.The fatty acid composition of the three copepod species indicatedan ‘herbivorous’ diet for P.elongatus and an omnivorousone for A. clausi and T. longicornis, which is less opportunist.     

Comparative carbon-specific ingestion rates of phytoplankton by Acartia tonsa,Centropages velificatus and Eucalanus pileatus grazing on natural phytoplankton assemblages in the plume of the Mississippi River (northern Gulf of Mexico continental shelf)

During four cruises in continental shelf waters of the northern Gulf of Mexico in the winters of 1981–83, we performed quantitative studies on the grazing of the copepods Acartia tonsa, Centropages velificatus, and Eucalanus pileatus, on phytoplankton using natural particulate assemblages as food. Stations were in, or adjacent to the plume of the Mississippi River, thereby providing wide spectra of phytoplankton and suspended riverine particulate concentrations. Phytoplankton cell volume was converted to carbon, and this, coupled with carbon content measurements of these three copepod species, allowed comparisons of daily ingestion effort even though the copepods were of different sizes. Data were expressed in the same units (% of copepod body carbon ingested copepod ^–1 d^–1) for each species. Over similar ranges of phytoplankton carbon concentrations (0.21–92.06 gCl^–1), Acartia tonsa had higher carbon-specific ingestion rates (x = 22.31%, range = 0.08–152.37%) than C. velificatus (x = 2.8%, range = 0.00–31.09 %) or E. pileatus (x = 1.27%, range = 0.10–2.80%). Carbon-specific ingestion rates increased with increasing phytoplankton carbon concentration for A. tonsa (R² = 0.81) and there was no evidence of saturated feeding on the carbon concentrations offered. A similar, but weaker trend was evident for E. pileatus (R² = 0.71), but not C. velificatus (R² = 0.49). Over a wide range of suspended particulate concentrations (10.6–95.2 mg l^–1), there was no systematic effect of particulates on carbon-specific ingestion rate for any of the three copepod species. However, A. tonsa appeared more adept at grazing in highly turbid water than C. velificatus or E. pileatus.     

Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa

The recent discovery of cryptic species in marine holoplankton, organisms that 'drift' in oceanic currents throughout their life cycle, contrasts with their potential for long-distance passive dispersal and presumably high gene flow. These observations suggest that holoplankton species are adapting to surprisingly small-scale oceanographic features and imply either limited dispersal or strong selection gradients. Acartia tonsa is a widespread and numerically dominant estuarine copepod containing deep mitochondrial lineages within and among populations along the northwestern Atlantic coast. In this study, we intensively investigated A. tonsa populations in Chesapeake Bay with the goals of testing species status for the deep lineages and testing for their association with environmental features over space and time. Phylogenetic analyses of DNA sequences from mitochondrial cytochrome c oxidase I (mtCOI) and the nuclear ribosomal internal transcribed spacer (nITS) resolved two concordant monophyletic clades. Deep divergence between the two clades (13.7% uncorrected sequence divergence for mtCOI and 32.2% for nITS) and genealogical concordance within sympatric populations strongly suggest that the two clades represent reproductively isolated cryptic species. Based on restriction fragment length polymorphisms of mtCOI, representatives from the two clades were found consistently associated with contrasting salinity regimes (oligohaline vs. meso-polyhaline) with an overlap between 2 and 12 PSU in samples from 1995 to 2005. Finding these patterns in one of the best-known estuarine copepods reinforces the conclusion that marine biodiversity is underestimated, not only in terms of species numbers, but also with respect to niche partitioning and the potential importance of ecological divergence in marine holoplankton.     

Ingestion of the dinoflagellate, Pfiesteria piscicida, by the calanoid copepod, Acartia tonsa

The dinoflagellate, Pfiesteria piscicida, can form harmful algal blooms in estuarine environments. The dominant copepod species usually found in these waters is Acartia tonsa. We tested the ability of A. tonsa to graze the non-toxic zoospore stage of P. piscicida and thus serve as a potential biological control of blooms of this algal species. A. tonsa grazed the non-toxic zoospore stages of both a non-inducible P. piscicida strain (FDEPMDR23) and a potentially toxic strain (Tox-B101156) at approximately equal rates. Ingestion of P. piscicida increased with cell concentration and exhibited a saturated feeding response. Both the maximum number of cells ingested (I_max) and the slope of the ingestion curve (α) of A. tonsa feeding on P. piscicida were comparable to these ingestion parameters for A. tonsa fed similar-sized phytoplankton and protozoan species. When these laboratory ingestion rates were combined with abundance estimates of A. tonsa from the Pocomoke Estuary and Chesapeake Bay, we found that significant grazing control of the non-toxic zoospore stage of P. piscicida by A. tonsa would only occur at high copepod abundances (>10 copepods L⁻¹). We conclude that under most in situ conditions the potential biological control of blooms of P. piscicida is exerted by microzooplankton grazers. However, in the less saline portions of estuaries where maximum concentrations of copepods often occur with low abundances of microzooplankton, copepod grazing coefficients can be similar to the growth rates of P. piscicida.     

Discrimination between Acartia (Copepoda: Calanoida) species using their diffraction pattern in a position, rotation invariant digital correlation

Digital images of Acartia discaudata, A. clausi, A. margalefiand A. tonsa were processed to obtain their diffraction pattern.To discriminate between species and sex all diffraction patternswere correlated with a spatial filter, invariant to positionand rotation, for each Acartia male and female. This filterwas made up using a combination of different images of eachspecies and sex. Considering the great similarity between thecopepod species used in this work and between the male and femaleof each species the results obtained are very good. It is concludedthat the method used to discriminate between species of thiscongeneric group can be very useful for the development of anautomated system for the identification of copepods.     

Sublethal stress: Impact of solar UV radiation on protein synthesis in the copepod Acartia tonsa

Aquatic organisms respond to environmental challenges such as thermal stress with the rapid induction of highly conserved polypeptides known as stress proteins or heat shock proteins (Hsps). Solar ultraviolet radiation (UVR, 280-400 nm) is an important environmental stressor in marine ecosystems. Here, we present results of experiments conducted with the marine copepod Acartia tonsa to follow the de novo protein synthesis and measure the level of constitutive and inducible isoforms of the Hsp70 gene family of stress proteins after UV exposure. Animals were collected from Tampa Bay, Florida (USA), and exposed to solar radiation (full spectrum), UV-A (320-400 nm) and PAR (400-700 nm), or PAR only, for periods of 0.5-4 h. Controls were kept in the dark. Protein synthesis was robust under all treatments when the copepods were exposed to low solar radiation intensities. Conversely, high solar radiation intensities (both UV-B and UV-A) caused an overall suppression in the protein synthesis of the copepods with no detectable induction of stress-inducible isoforms of Hsps. Immunochemical assays (western blotting) showed that UVR increased levels (3.5-4-fold increase compared to the dark control) of the constitutively expressed 70 kDa heat-shock (Hsc70) protein in A. tonsa, without indication of inducible isoform upregulation.     

Ocean acidification-induced food quality deterioration constrains trophic transfer

Our present understanding of ocean acidification (OA) impacts on marine organisms caused by rapidly rising atmospheric carbon dioxide (CO(2)) concentration is almost entirely limited to single species responses. OA consequences for food web interactions are, however, still unknown. Indirect OA effects can be expected for consumers by changing the nutritional quality of their prey. We used a laboratory experiment to test potential OA effects on algal fatty acid (FA) composition and resulting copepod growth. We show that elevated CO(2) significantly changed the FA concentration and composition of the diatom Thalassiosira pseudonana, which constrained growth and reproduction of the copepod Acartia tonsa. A significant decline in both total FAs (28.1 to 17.4 fg cell(-1)) and the ratio of long-chain polyunsaturated to saturated fatty acids (PUFA:SFA) of food algae cultured under elevated (750 μatm) compared to present day (380 μatm) pCO(2) was directly translated to copepods. The proportion of total essential FAs declined almost tenfold in copepods and the contribution of saturated fatty acids (SFAs) tripled at high CO(2). This rapid and reversible CO(2)-dependent shift in FA concentration and composition caused a decrease in both copepod somatic growth and egg production from 34 to 5 eggs female(-1) day(-1). Because the diatom-copepod link supports some of the most productive ecosystems in the world, our study demonstrates that OA can have far-reaching consequences for ocean food webs by changing the nutritional quality of essential macromolecules in primary producers that cascade up the food web.     

Life in the extreme environment at a hydrothermal vent: haemoglobin in a deep-sea copepod.

This is the first study, to my knowledge, quantifying the respiratory pigment haemoglobin discovered in a deep-sea copepod. Haemoglobin in copepods has previously been documented in only one other species from the deep water of an Italian lake. Specimens of the siphonostomatoid Scotoecetes introrsus Humes were collected during submersible dives at 2500 m depth near a hydrothermal vent at the East Pacific Rise (9 degrees N). The haemoglobin content in the copepods' haemolymph was 4.3 +/- 0.6 micrograms per individual female (n = 6) and 1.8 +/- 0.1 micrograms per individual male (n = 6). Weight-specific concentrations of haemoglobin were identical for females and males (0.25 +/- 0.04 and 0.26 +/- 0.02 microgram per microgram dry weight, respectively). These haemoglobin concentrations are higher than those found in other small crustaceans. Activity of the electron transport system indicated that the respiration rates in S. introrsus (13.7 +/- 7.7 microliters O2 per milligram dry weight per hour) were similar to those in the shallow-water copepod Acartia tonsa (9.1 +/- 1.3 microliters O2 per milligram dry weight per hour). It was concluded that the possession of highly concentrated haemoglobin allows S. introrsus to colonize a geologically young, thermally active site such as the vicinity of a hydrothermal vent, despite the prevailing oxygen depletion.