Caroline Methling:
Cardio-respiratory Physiology of the European Eel (Anguilla anguilla) in Extreme Environments

Date: 15-01-2013    Supervisor: John Fleng Steffensen




The main objective of this PhD thesis was to study the cardio-respiratory capabilities of the European eel (Anguilla anguilla) under extreme conditions. Three environmental conditions were studied i.e. temperature, dissolved oxygen and carbon dioxide, while a fourth condition was physiological and focused on the impressive spawning migration of A. anguilla.

Ambient temperature influences the rate of most biological functions including metabolic processes, which in turn determines the overall metabolic capacity. In Paper I it is demonstrated that A. anguilla has a wide thermal optimum as absolute aerobic scope (MSABS) was constant between 10°C and 30°C, and eels were able to maintain a high oxygen uptake, even at the highest temperature studied (30°C). Still, the scope for other activities was considerably reduced as aerobic metabolism could only be increased about 3 fold at the highest temperature. Resting and maximum oxygen consumption (MO2) and thus MSABS were significantly suppressed at 0°C in accordance with the observed torpidity of eels at low temperatures. The ability to regulate MO2 during hypoxia was assessed by determination of the critical O2 partial pressure (PCRIT) at 0, 10, 20 and 30°C and PCRIT was found to be positively correlated with temperature. Excess post-hypoxic oxygen consumption (EPHOC) was quantified after 2 hours of severe hypoxia exposure and also increased with temperature. The duration of EPHOC was about 3 times shorter at 0°C, than at 10, 20 and 30°C. The fraction of MSABS utilized for recovery was elevated at the temperature extremes, indicating that hypoxia narrows the thermal tolerance of A. anguilla.

In Paper II it is demonstrated that temperature also influenced the contractile properties of ventricular muscle in vitro, in that the time-course of contraction, and thus maximum attainable heart rate in vivo, greatly depended on ambient temperature. The relative ventricular mass was increased after long term acclimation to 0°C and 10°C compared to individuals acclimated to 20°C, indicative of a compensatory mechanism for the limitation in heart rate at low temperature in A. anguilla. The force of contraction and myocardial power production increased after an acute decrease in ambient temperature from 20°C to 10°C (mimicking the vertical movements performed during the spawning migration). This may serve to offset the depressant effect on heart rate and thus ensure adequate cardiac performance when diving to cooler depths. Furthermore, the individual contribution of three different sarcolemmal Ca2+ channels (L-type, NCX and SOCE) to the generation of force also depended on ambient temperature.

Elevations in CO2 partial pressure (hypercapnia) is a common phenomenon in aquaculture facilities of A. anguilla. In Paper III it is demonstrated, that when exposed to a constant high level of hypercapnia (60mmHg), eels took a longer time (22%) to digest a meal size of fixed proportions (0.5% body weight) compared to eels held under normocapnic conditions, while eels exposed to oscillating CO2 partial pressures (20-60mmHg) had a reduced post-prandial ammonia excretion. This suggests that depending on the specific conditions, hypercapnia may limit the appetite and feed intake as it takes longer time to process a meal, and/or that a smaller amount of the dietary energy and nitrogen content will be allocated to growth due to a reduced absorption /assimilation efficiency. Regardless, these results demonstrate that hypercapnia adversely affects the postprandial processes in A. anguilla.

Pop-up satellite archival tags (PSATs) have recently been applied in attempts to follow the oceanic spawning migration of A. anguilla. Due to the size of these tags, it is likely that their hydraulic drag constitutes an additional cost during swimming, which may have implications for successful migration. In Paper IV, migration stage eels were subjected to swimming trials at increasing speeds of 0.3 - 0.9 body lengths s-1, first without and subsequently with, a scaled down PSAT dummy attached, while rates of oxygen consumption (MO2) were measured. The tag increased MO2 during swimming and elevated the minimum cost of transport (COTmin) by 26%. Standard (SMR) and active metabolic rate (AMR) as well as aerobic metabolic scope remained unaffected, which suggests that the observed effects were caused by increased drag. Swimming with a tag decreased the critical swimming speed (Ucrit) and also altered swimming kinematics as verified by significant changes to tail beat frequency (f), body wave speed (v) and Strouhal number (St). The results demonstrate that energy expenditure, swimming performance and efficiency all are significantly affected in migrating eels fitted with external tags.