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Oxygen requirements in the airbreathing fish Pangasianodon hypophthalmus and Channa striata

Sjannie Lefevre

Summary

The two air-breathing species Pangasianodon hypophthalmus (pangasius) and Channa striata (channa) are important production fish for export and local consumption. Both were classified as obligate air-breathers, i.e. air-breathing is necessary for their survival. However, pangasius seemed to have very well-developed gills, indistinguishable from active water breathing fish, which indicated from the outset that aquatic respiration is likely to be important. As for channa, several older studies have found survival to be dependent on both aquatic and aerial oxygen uptake, but in this case the reduction in two of the gill arches made their classification as obligate more likely. 

The main objective of the project was to investigate the dependence on both aerial and aquatic oxygen uptake, in order to evaluate a potential benefit of introducing aeration into the current farming practices of these economically important species. The major part of the experiments concerned measurements of oxygen consumption, because oxygen consumption is intimately related to hypoxia, energetics, and thereby growth. To obtain reliable and reproducible estimates of oxygen uptakes in air-breathing fish, it is necessary that oxygen uptake from both air and water can be quantified over extended periods. This required the development of a bimodal intermittent-closed respirometry system; using the principles of intermittent-closed respirometry developed for water breathers, in both the air- and the water-phases. The bimodal intermittent-closed principle was also applied to a swimming respirometer, thus expanding measurements from resting animals to active animals. 

In pangasius we measured oxygen consumption in resting fish during normoxia and hypoxia and in swimming fish during normoxia with and without access to air, to assess the importance of air-breathing, and also to investigate whether air-breathing increases cost of transport. In addition to the laboratory experiments, we performed measurements in the field of swimming depth and oxygen levels experienced by individually tagged fish, to relate laboratory data to the field. The outcome of the investigations clearly showed that pangasius is highly facultative in its air-breathing dependency. Due to the well-developed gills it can completely cover both its swimming and resting metabolism during normoxia without air-breathing (Manuscripts III and V). Furthermore, air-breathing during swimming increases the cost of transport, indicating that there is a significant energetic cost of surfacing (Manuscript VIII). In hypoxia it will shift to air-breathing, but some individuals would rely more on water-breathing if they were disturbed (Manuscript III). This indicates that the capacity for aquatic breathing is also important in hypoxic situations, where air-breathing is not advantageous, i.e. when a predation threat is perceived. Measurements from the field confirmed a high surfacing frequency, due to severe hypoxia in the ponds (Manuscript IV). It is likely that aeration of the water would decrease the airbreathing activity, making both more time and more energy available for feeding and growth, but more behavioural studies are needed to confirm this hypothesis. Several growth studies performed by the Vietnamese collaborators during the project seem to PhD Thesis Sjannie Lefevre  indicate enhanced growth in normoxic water, but due to high variability within the data, interpretations are difficult. Growth studies using recirculation systems would be a next step in the process. 

In channa, we used bimodal intermittent-closed respirometry to investigate the effect of hypoxia on oxygen consumption and dependence on air-breathing during digestion (Manuscript VII), which is indirectly linked to growth. While this species is more dependent on air-breathing than pangasius, in line with its small gills, it is also surprisingly dependant on water-breathing. Digestion was prolonged in severe hypoxia, as the metabolic elevation induced by digestion was 30% longer in hypoxia than in normoxia. This is strong evidence that channa may, somewhat surprisingly, also benefit from aeration of the culture ponds. This new knowledge puts the traditional classification of air-breathing species as obligate or facultative into perspective. Clearly, dependence on air-breathing is continuous rather than categorical, and it is important that species in aquaculture are described in relation to situations that are relevant to growth and thereby aquaculture, rather than in relation to their ability to survive with or without air-breathing, as this has little relevance to aquaculture. 

In addition to the experiment concerning the direct effects of hypoxia, we also investigated the effects of nitrite (Manuscripts V and VI), which is a functional form of hypoxia. As nitrite is taken up over the gills and induces formation of methaemoglobin and nitrosylhaemoglobin, which cannot bind oxygen, it potentially limits aerobic scope. Furthermore, nitrite severly affects ion-regulation, because it replaces the chloride uptake in the gills. To evaluate the effects of nitrite in both pangasius and channa, we measured lethal tolerance level (LC50), as well as effects on ion balance and haemoglobin levels. In pangasius we also measured the effect of nitrite on partitioning, and swimming performance, to investigate if the nitrite induced reductions in oxygen carrying capacity would affect aerobic scope. We found that both air-breathers were very tolerant to nitrite in comparison to the previously studied water-breathers, with C. striata being twice as tolerant as P. hypophthalmus. Ion balance was not affected in P. hypophthalmus, but was highly disturbed in C. striata, indicating interesting basic differences in the coping mechanism against nitrite in these two species. The lethal nitrite levels and the levels needed to induce physiological changes were compared to levels measured in the field, and it can be concluded that in the present aquaculture systems of these species, the concentrations of nitrite never exceed levels that have any significant effect on respiratory physiology. The results gained from this PhD project are surprising, given that both pangasius and channa have always been classified as obligate air-breathers, i.e. species that cannot survive without access to air, leading to the assumption that aquatic oxygen is not important and hence would not affect growth. In contrast, the data obtained throughout this PhD project point to the importance of aquatic aeration for growth in air-breathers, which was previously not thought to be cost effective. The results have therefore opened new avenues for the improvement of culture practices and trials are now underway in Vietnam to study the effects of aeration on growth in situ. PhD Thesis Sjannie Lefevre