Jodie L. Rummer

Physiological Effects of Swim Bladder Overexpansion and Catastrophic Decompression on Red Snapper

Abstract The commercial and recreational harvests of red snapper Lutjanus campechanus in the Gulf of Mexico have declined over the past five decades, prompting strict regulations. Release mortality associated with catastrophic decompression (CD) is a possible cause for the continuing decline, although to date no physiological data exist to support this assumption. Using a flow-through high-pressure chamber, subadult red snapper were acclimated to 101.2, 405.3, 608.0, and 1,215.9 kPa, simulating depths typical of their distribution (as deep as 200 m), and then decompressed at a rate of 10.1 kPa/s. Lateral and dorsal X-ray imaging in combination with necropsy showed that swim bladders expanded in a predictable manner. Ventral expansion into the caudal body cavity space occurred at lower pressures, whereas expansion into the cranial portion of the body cavity occurred at the highest pressure. Expansion patterns resulted in over 70 different overexpansion injuries, the most severe being to vital organs. Our r...

Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen

SUMMARY Erythropoietin (EPO) is a glycoprotein hormone that regulates the proliferation and differentiation of erythroid progenitor cells in mammals. Although EPO has been identified in fish, the specific function and effects of hypoxia have not been investigated previously. In this study, we have demonstrated a relationship between increases in renal EPO levels and decreases in spleen EPO levels and spleen-somatic index (SSI), with increases in haemoglobin (Hb) concentration in the blood during hypoxia exposure in rainbow trout. Splenic contraction and the subsequent red blood cell release accounts for the initial increase in Hb concentration in the blood, whereas EPO action probably accounts for the later increases in hemoglobin concentration in the blood. Our data indicate that fish and mammalian erythropoietic systems are similar in response to hypoxia, in that erythropoiesis in fish is influenced by EPO.

Finding the best estimates of metabolic rates in a coral reef fish

SUMMARY Metabolic rates of aquatic organisms are estimated from measurements of oxygen consumption rates () through swimming and resting respirometry. These distinct approaches are increasingly used in ecophysiology and conservation physiology studies; however, few studies have tested whether they yield comparable results. We examined whether two fundamental measures, standard metabolic rate (SMR) and maximum metabolic rate (MMR), vary based on the method employed. Ten bridled monocle bream (Scolopsis bilineata) were exercised using (1) a critical swimming speed (Ucrit) protocol, (2) a 15 min exhaustive chase protocol and (3) a 3 min exhaustive chase protocol followed by brief (1 min) air exposure. Protocol 1 was performed in a swimming respirometer whereas protocols 2 and 3 were followed by resting respirometry. SMR estimates in swimming respirometry were similar to those in resting respirometry when a three-parameter exponential or power function was used to extrapolate the swimming speed– relationship to zero swimming speed. In contrast, MMR using the Ucrit protocol was 36% higher than MMR derived from the 15 min chase protocol and 23% higher than MMR using the 3 min chase/1 min air exposure protocol. For strong steady (endurance) swimmers, such as S. bilineata, swimming respirometry can produce more accurate MMR estimates than exhaustive chase protocols because oxygen consumption is measured during exertion. However, when swimming respirometry is impractical, exhaustive chase protocols should be supplemented with brief air exposure to improve measurement accuracy. Caution is warranted when comparing MMR estimates obtained with different respirometry methods unless they are cross-validated on a species-specific basis.

Root Effect Hemoglobin May Have Evolved to Enhance General Tissue Oxygen Delivery

Holding Your Breath Hemoglobin and myoglobin are widely responsible for oxygen transport and storage (see the Perspective by Rezende). The ability of diving mammals to obtain enough oxygen to support extended dives and foraging is largely dependent on muscle myoglobin (Mb) content. Mirceta et al. (p. 1303) found that in mammalian lineages with an aquatic or semiaquatic lifestyle, Mb net charge increases, which may represent an adaptation to inhibit self-association of Mb at high intracellular concentrations. Epistasis results from nonadditive genetic interactions and can affect phenotypic evolution. Natarajan et al. (p. 1324) found that epistatic interactions were able to explain the increased hemoglobin oxygen-binding affinity observed in deer mice populations at high altitude. In mammals, the offloading of oxygen from hemoglobin is facilitated by a reduction in the bloods pH, driven by metabolically produced CO2. However, in fish, a reduction in blood pH reduces oxygen carrying capacity of hemoglobin. Rummer et al. (p. 1327) implanted fiber optic oxygen sensors within the muscles of rainbow trout and found that elevated CO2 levels in the water led to acidosis and elevated oxygen tensions. The evolutionary origin of the unloading of oxygen at low pH is traced back to teleosts. [Also see Perspective by Rezende] The Root effect is a pH-dependent reduction in hemoglobin-O2 carrying capacity. Specific to ray-finned fishes, the Root effect has been ascribed specialized roles in retinal oxygenation and swimbladder inflation. We report that when rainbow trout are exposed to elevated water carbon dioxide (CO2), red muscle partial pressure of oxygen (PO2) increases by 65%—evidence that Root hemoglobins enhance general tissue O2 delivery during acidotic stress. Inhibiting carbonic anhydrase (CA) in the plasma abolished this effect. We argue that CA activity in muscle capillaries short-circuits red blood cell (RBC) pH regulation. This acidifies RBCs, unloads O2 from hemoglobin, and elevates tissue PO2, which could double O2 delivery with no change in perfusion. This previously undescribed mechanism to enhance O2 delivery during stress may represent the incipient function of Root hemoglobins in fishes.

Aerobic scope predicts dominance during early life in a tropical damselfish

1. A range of physiological traits are linked with aggression and dominance within social hierarchies, but the role of individual aerobic capacity in facilitating aggression has seldom been studied. Further, links previously observed between an individuals metabolic rate and aggression level may be context dependent and modulated by factors such as social stress and competitor familiarity. 2. We examined these issues in juvenile Ambon damselfish, Pomacentrus amboinensis, which display intraspecific competition for territories during settlement on coral reefs. 3. Individuals were measured for routine metabolic rate, aerobic scope (AS) and anaerobic capacity using intermittent-flow respirometry before dyadic dominance contests. Post-contest, fish were measured for metabolic rate in isolation and while interacting with their previous competitor or a stranger in adjacent transparent respirometers. 4. In arena contests, AS was correlated with aggression and dominance, while routine metabolic rate and anaerobic capacity were not related to dominance. Post-contest, subordinates showed a rise in metabolic rate and decrease in available AS, presumably due to social stress. Dominants increased metabolic rate in the presence of a previous competitor, possibly due to the stresses of hierarchy maintenance. 5. Metabolic rate during aggressive interactions did not approach that measured during exhaustive exercise, suggesting individuals do not fully utilise their AS during aggression. A greater AS may, however, allow faster post-contest recovery. 6. These results demonstrate a link between AS and dominance during intraspecific competition for territory. Selection on AS could therefore follow, either indirectly through correlations with other traits influencing resource-holding potential, or directly if AS carries benefits important for territory acquisition or holding, such as an enhanced capacity to cope with socially induced stress.

Climate change and the performance of larval coral reef fishes: the interaction between temperature and food availability

We tested the impacts of temperature and variable food availability on the development and metabolic rate of the larvae of a coral reef damselfish, Amphiprion percula. Our results suggest that larval fishes will be severely impacted, both independently and synergistically, by climate-change related elevated temperatures and reductions in food supply.

Species-specific effects of near-future CO2 on the respiratory performance of two tropical prey fish and their predator

Ocean surface CO2 levels are increasing in line with rising atmospheric CO2 and could exceed 900μatm by year 2100, with extremes above 2000μatm in some coastal habitats. The imminent increase in ocean pCO2 is predicted to have negative consequences for marine fishes, including reduced aerobic performance, but variability among species could be expected. Understanding interspecific responses to ocean acidification is important for predicting the consequences of ocean acidification on communities and ecosystems. In the present study, the effects of exposure to near-future seawater CO2 (860μatm) on resting (M˙ O2rest) and maximum (M˙O2max) oxygen consumption rates were determined for three tropical coral reef fish species interlinked through predator-prey relationships: juvenile Pomacentrus moluccensis and Pomacentrus amboinensis, and one of their predators: adult Pseudochromis fuscus. Contrary to predictions, one of the prey species, P. amboinensis, displayed a 28-39% increase in M˙O2max after both an acute and four-day exposure to near-future CO2 seawater, while maintaining M˙O2rest. By contrast, the same treatment had no significant effects on M˙O2rest or M˙O2max of the other two species. However, acute exposure of P. amboinensis to 1400 and 2400μatm CO2 resulted in M˙O2max returning to control values. Overall, the findings suggest that: (1) the metabolic costs of living in a near-future CO2 seawater environment were insignificant for the species examined at rest; (2) the M˙O2max response of tropical reef species to near-future CO2 seawater can be dependent on the severity of external hypercapnia; and (3) near-future ocean pCO2 may not be detrimental to aerobic scope of all fish species and it may even augment aerobic scope of some species. The present results also highlight that close phylogenetic relatedness and living in the same environment, does not necessarily imply similar physiological responses to near-future CO2.

Elevated CO2 enhances aerobic scope of a coral reef fish

The oceans are absorbing excess atmospheric CO2, and this is causing ocean acidification. Surprisingly, one coral reef damselfish exhibits enhanced aerobic performance after living at projected future ocean CO2 levels for 17 days. Identifying both the winners and losers under climate change scenarios is vital to conserving marine biodiversity.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Exposure of clownfish larvae to suspended sediment levels found on the Great Barrier Reef: impacts on gill structure and microbiome

Worldwide, increasing coastal development has played a major role in shaping coral reef species assemblages, but the mechanisms underpinning distribution patterns remain poorly understood. Recent research demonstrated delayed development in larval fishes exposed to suspended sediment, highlighting the need to further understand the interaction between suspended sediment as a stressor and energetically costly activities such as growth and development that are essential to support biological fitness. We examined the gill morphology and the gill microbiome in clownfish larvae (Amphiprion percula) exposed to suspended sediment concentrations (using Australian bentonite) commonly found on the inshore Great Barrier Reef. The gills of larvae exposed to 45 mg L−1 of suspended sediment had excessive mucous discharge and growth of protective cell layers, resulting in a 56% thicker gill epithelium compared to fish from the control group. Further, we found a shift from ‘healthy’ to pathogenic bacterial communities on the gills, which could increase the disease susceptibility of larvae. The impact of suspended sediments on larval gills may represent an underlying mechanism behind the distribution patterns of fish assemblages. Our findings underscore the necessity for future coastal development to consider adverse effects of suspended sediments on fish recruitment, and consequently fish populations and ecosystem health.