Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia

Deigweiher, Katrin; Koschnick, Nils; Pörtner, Hans‐Otto; Lucassen, Magnus

doi:10.1152/ajpregu.90403.2008

Cited by 96 publications

(110 citation statements)

References 48 publications

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“…Additionally, damselfish larvae reared at elevated pCO 2 (550 to 1030 ppm) exhibited up to an 18% increase in length-at-age, which the authors suggested could be accomplished either through in creased energy intake or decreased energy expenditure (Munday et al 2009). In a captive rearing environment, prey are consistently provided at higher quantities than what is expected in nature; thus, larvae in the present study may have been able to increase their energy intake to compensate, or overcompensate, for an in crease in the metabolic cost of acid -base balance under acidified conditions (Deigweiher et al 2008. This has been demonstrated with mussels in both laboratory and natural marine environments, where food availability predominantly influences growth compared to increased pCO 2 ).…”

Section: Swimming Activitymentioning

confidence: 49%

Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus

Bignami¹,

Sponaugle²,

Cowen³

2014

Aquat. Biol.

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Negative impacts of CO 2 -induced ocean acidification on marine organisms have proven to be variable both among and within taxa. For fishes, inconsistency confounds our ability to draw conclusions that apply across taxonomic groups and highlights the limitations of a nascent field with a narrow scope of study species. Here, we present data from a series of 3 experiments on the larvae of mahi-mahi Coryphaena hippurus, a large pelagic tropical fish species of high economic value. Mahi-mahi larvae were raised for up to 21 d under either ambient seawater conditions (350 to 490 µatm pCO 2 ) or projected scenarios of ocean acidification (770 to 2170 µatm pCO 2 ). Evaluation of hatch rate, larval size, development, swimming activity, swimming ability (U crit ), and otolith (ear stone) formation produced few significant effects. However, larvae unexpectedly exhibited significantly larger size-at-age and faster developmental rate during 1 out of 3 experiments, possibly driven by metabolic compensation to elevated pCO 2 via a corresponding decrease in routine swimming velocity. Furthermore, larvae had significantly larger otoliths at 2170 µatm pCO 2 , and a similar but non-significant trend also occurred at 1200 µatm pCO 2 , suggesting potential implications for hearing sensitivity. The lack of effect on most variables measured in this study provides an optimistic indication that this large tropical species, which inhabits the offshore pelagic environment, may not be overly susceptible to ocean acidification. However, the presence of some treatment effects on growth, swimming activity, and otolith formation suggests the presence of subtle, but possibly widespread, effects of acidification on larval mahi-mahi, the cumulative consequences of which are still unknown.KEY WORDS: Ocean acidification · Larval fish · Otolith · Mahi-mahi · CO 2 · U crit · Behavior OPEN PEN ACCESS CCESSAquat Biol 21: 249-260, 2014 250 cope with increased environmental partial pressure of carbon dioxide ( pCO 2 ). Embryonic and larval fishes are not equip ped with the same physiological mechanisms as juveniles and adults, but are capable of some internal pH regulation (Brauner 2008). Nonetheless, existing literature indicates that early life stages of fishes are more susceptible to elevated pCO 2 relative to adults (reviewed by Pörtner et al. 2005). As the primary period of dispersal for many marine fishes, the larval stage is critical to population replenishment and connectivity (Cowen & Sponaugle 2009); therefore, our understanding of the broader population-and ecosystem-level impacts of ocean acidification requires consid eration of this life stage.The impact of ocean acidification on larval fishes is highly variable among studies and taxa. The range of effects include reduced growth and survival (Baumann et al. 2011), skeletal deformation (Pimentel et al. 2014a), altered neurological function (Nilsson et al. 2012), and disrupted behavior (Munday et al. 2010, Ferrari et al. 2012, Hamilton et al. 2014. Some species have experienced m...

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Section: Swimming Activitymentioning

confidence: 49%

Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus

Bignami¹,

Sponaugle²,

Cowen³

2014

Aquat. Biol.

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“…Similar observation of a bi-phasic acclimation reaction of acid-base transporters to environmental hypercapnia were observed in teleosts, including Atlantic cod (Gadus morhua) 50 and eelpout (Zoarces viviparus). 122 However during prolonged acclimation to hypercapnic conditions, expression levels of acid-base relevant transporters returned back to control levels potentially shifting to an energetically favorable reorganization of physiological features to cope with moderate hypercapnic conditions over longer exposure times. Furthermore, this reorganization of physiological features, including a metabolic shift upon chronic exposure to hypercapnic conditions is essential in order to reduce extra-free radical stress and keep cellular metabolic and redox state in balance.…”

Section: Role Of Ion Regulatory Epithelia During Acclimation To Envirmentioning

confidence: 99%

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Hwang

Tseng

2015

Tissue Barriers

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Cephalopods have evolved complex sensory systems and an active lifestyle to compete with fish for similar resources in the marine environment. Their highly active lifestyle and their extensive protein metabolism has led to substantial acid-base regulatory abilities enabling these organisms to cope with CO 2 induced acid-base disturbances. In convergence to teleost, cephalopods possess an ontogeny-dependent shift in ion-regulatory epithelia with epidermal ionocytes being the major site of embryonic acid-base regulation and ammonia excretion, while gill epithelia take these functions in adults. Although the basic morphology and excretory function of gill epithelia in cephalopods were outlined almost half a century ago, modern immunohistological and molecular techniques are bringing new insights to the mechanistic basis of acidbase regulation and excretion of nitrogenous waste products (e.g. NH 3 /NH 4 C ) across ion regulatory epithelia of cephalopods. Using cephalopods as an invertebrate model, recent findings reveal partly conserved mechanisms but also novel aspects of acid-base regulation and nitrogen excretion in these exclusively marine animals. Comparative studies using a range of marine invertebrates will create a novel and exciting research direction addressing the evolution of pH regulatory and excretory systems.

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“…This observation suggests that prolonged RBC shrinkage may have compromised membrane integrity resulting in atypically fragile cells, a phenomenon that has also been observed in lungfish (Koldkjaer et al, 2002). Regardless, it does appear that an NHE isoform may be operating on the sablefish RBC membrane to maintain pH and cell volume homeostasis, likely a 'housekeeping' NHE1 (Claiborne et al, 1999;Deigweiher et al, 2008); however, further studies are required to address this.…”

Section: Cell Volume Regulationmentioning

confidence: 99%

Use it or lose it? Sablefish,Anoplopoma fimbria, a species representing a fifth teleostean group where the βNHE associated with the red blood cell adrenergic stress response has been secondarily lost

Rummer

Roshan-Moniri

Balfry

et al. 2010

Journal of Experimental Biology

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SUMMARYLike most teleosts, sablefish (Anoplopoma fimbria Pallas 1814) blood exhibits a moderate Root effect (~35% maximal desaturation), where a reduction in blood pH dramatically reduces O 2 carrying capacity, a mechanism important for oxygenating the eye and filling the swim bladder (SB) in teleosts. Although sablefish lack a SB, we observed a well-defined choroid rete at the eye. The adrenergically mediated cell swelling typically associated with a functional red blood cell (RBC) b-adrenergic Na + /H + exchanger (bNHE), which would normally protect RBC pH, and thus O 2 transport, during a generalized acidosis, was not observed in sablefish blood. Neither isoproterenol (a b-agonist) nor 8-bromo cAMP could elicit this response. Furthermore, RBC osmotic shrinkage, known to stimulate NHEs in general and bNHE in other teleosts such as trout and flounder, resulted in no significant regulatory volume increase (RVI), further supporting the absence of a functional RBC bNHE. The onset of the Root effect occurs at a much lower RBC pH (6.83-6.92) than in other teleosts, and thus RBC bNHE may not be required to protect O 2 transport during a generalized acidosis in vivo. Phylogenetically, sablefish may represent a fifth group of teleosts exhibiting a secondary reduction or loss of bNHE activity. However, sablefish have not lost the choroid rete at the eye (unlike in the other four groups), which may still function with the Root effect to oxygenate the retina, but the low pH onset of the Root effect may ensure haemoglobin (Hb)-O 2 binding is not compromised at the respiratory surface during a general acidosis in the absence of RBC bNHE. The sablefish may represent an anomaly within the framework of Root effect evolution, in that they possess a moderate Root effect and a choroid rete at the eye, but lack the RBC bNHE and the SB system.

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Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia

Abstract: Deigweiher K, Koschnick N, Pö rtner H, Lucassen M. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia.

Cited by 96 publications

References 48 publications

Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus

Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Use it or lose it? Sablefish,Anoplopoma fimbria, a species representing a fifth teleostean group where the βNHE associated with the red blood cell adrenergic stress response has been secondarily lost

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