Bycatch – The physiological response of unintentionally caught elasmobranchs

The worldwide fishing industry has long been a major contributor in providing massive quantities of food to the world’s population. As well as providing consumers with regular access to a key source of protein, the industry provides millions of jobs to people worldwide and is responsible for generating billions of dollars annually. Influenced by the consumer, the most in-demand marine fauna are therefore those most regularly harvested in the commercial fishing industry, including herring, cod, anchovy, tuna, flounder, mullet, squid, shrimp, salmon, crab and lobster. To catch large numbers of these species effectively, numerous methods are utilised by the industry, many of which can vary significantly in their function. Fishing methods differ depending on the target species, the conditions of the region being fished, and the availability of technology to the fishermen. Methods in current usage include nets, seine nets, trawls (e.g. bottom trawl), hooks and lines (e.g. long line and handline), lift nets, gillnets, entangling nets and traps (Ministry for Primary Industries, 2007) and all operate differently so as to most effectively capture their target species. Whilst commercial fishing has proved overwhelmingly successful in increasing seafood availability to humans and in providing significant economic gain, the industry often garners much controversy, notably due to the ecological and environmental impacts commercial fishing can cause.   While large scale environmental issues such as depletion of wild fish stocks and negative impacts on marine trophic levels are of great concern, the issue of bycatch is a subject met with much criticism from conservationists. In recent years, attention has been drawn most notably to elasmobranch bycatch, due to certain species (particularly shark species) becoming increasingly threatened as a result of the commercial fishing industry (Oceana, 2007).

What is Bycatch?

The term bycatch refers to the unintentional/incidental capture of non-target species during fishing operations. The term has been defined by the Organisation for Economic Co-operation and Development (1997) as ‘total fishing mortality, excluding that accounted directly by the retained catch of target species’. Bycatch arises due to many fishing methods and gear not being selective and subsequently results in the catching and discarding of millions of unintentionally caught fish. Bycatch can range from species of teleost, to turtles and cetaceans, to seabirds and elasmobranchs, and often results in the death of the bycatch species. Bycatch species are frequently discarded back into the ocean after capture, with a study conducted by Kelleher (2005) estimating that discards in the world’s commercial fishing industry to be 7.3 million tonnes annually. The most indiscriminate method of fishing are towed nets, which include trawl and seine nets (Bonfil, 2000). These methods of fishing gear account for the highest number and amount of non-target species caught incidentally, with bycatch rates from these gears reaching 60% of the target fish as in some temperate groundfish fisheries (Bonfil, 2000). Longlines are also a primary fishing method responsible for significant levels of bycatch, with typical levels in pelagic longline fisheries ranging from 20% of the total catch to about 4 times the target catch in some swordfish fisheries, and often 60% of the total catch in tuna longlines (Hazin et al, 1998).

The Elasmobranchs, a subclass of Chondrichthyes or cartilaginous fish that include the sharks and the rays and skates, are some of the most frequent bycatch found in commercial fishing gear. Tow netting and long line fishing have been shown in some cases to result in shark bycatch of 74.9% of the total catch for tow netting (Passerotti et al., 2010) and a 70% bycatch in long line fishing (Cahmi, 2009). The cumulative effects of stress and physical injury to elasmobranchs caught in fishing mechanisms has been shown to result in high mortality rate of the bycatch (Beerkircheretal, 2002). The mortality rate of elasmobranch bycatch is often species specific, due to the diversity of elasmobranch activity levels and life history. The most common elasmobranchs found in bycatch on pelagic long lines exhibit significantly high mortality rates, which include the dusky (Carcharhinus obscurus) with 48.7%, silky (Carcharhinus falciformis) with 66.3% and night sharks (Carcharhinus signatus) with 80.8%  (Beerkircheretal, 2002). The primary causes of high mortality rates in captured elasmobranchs is thought to be capture induced stress.

Bycatch: A thresher shark, silky shark and bat ray

Bycatch: The fate of a thresher shark, silky shark and bat ray

Capture Stress

Stress is defined as ‘a physiological state produced by an environmental factor that extends the normal adaptive responses of the animal, or disturbs the normal functioning to such an extent that the chances for survival are significantly reduced’ (Brett, 1958).  The stress response exhibited by elasmobranchs is associated with increased metabolic demands and costs, as energy is reallocated from metabolically demanding activities (e.g. growth, reproduction) to those most immediately essential for survival (e.g. respiration, cardiac functioning) (Barton and Iwama, 1991). Studies have shown that the magnitude of stress-response exhibited by teleosts is linked to swimming activity (aerobic vs anaerobic) and life history (sluggish benthic vs active pelagic), however given the diversity of elasmobranch activity levels and life history, a typical stress response encompassing the whole group is unlikely, thus the differential rates of mortality in elasmobranch bycatch species. As described in detail by Skomall et al (2007) in a review of the physiological responses of elasmobranchs to anthropogenic stressors, stress response in fish can be separated into ‘primary responses’ and subsequent ‘secondary responses’.

Stress Hormones

When species of elasmobranchs are caught as bycatch, the main physiological stressors impacting their survival arise initially from compromised oxygen availability. In situations where elasmobranchs are caught in fishing gear and cannot effectively ventilate their gills, they can be subjected to both hypoxia and exhaustive exercise, which will result in the onset of the primary neuroendocrine response. The primary neuroendocrine response initiates the rapid increase of stress hormones, catecholamines and corticosteroids, in the form of adrenaline and noradrenaline in the fish (Skomal et al, 2007). These molecules trigger general physiological changes that prepare the body for physical activity (Fitzgerald, 2011). For example, levels of catecholamines in blue and shortfin mako sharks have been shown to increase by 1600 fold in response to capture in longline fishing gear (Hight et al, 2007).  With the onset of the primary neuroendocrine response, such elevated levels of catecholamines in the blood instigates a secondary stress response, where the narrowing of the fishes blood vessels (vasoconstriction) can occur. This leads to metabolic acidosis and anoxia and potentially to irreversible tissue, organ and cell damage (Hight et al, 2007).  Elevated levels of catecholamines in the blood of the elasmobranch can also be responsible for causing hyperglycaemia and also hyperlactatemia as secondary stress responses in the fish, which too can result in metabolic acidosis.  This development of hyperglycaemia in response to capture-stress in elasmobranchs has been studied extensively (Mazeaud et al, 1977) (Barton and Iwama, 1991) (Hoffmayer et al, 2001), with these elevated glucose levels often used to quantify the secondary stress response.

Acid-base unbalance

A secondary stress response also exhibited by elasmobranchs is a decline in blood pH as result of capture-stress.  This decline is fuelled by a combination of respiratory and metabolic acidosis and eventually results in acidemia. Acidosis refers to disorders that lower cell/tisue pH to < 7.35 whereas acidemia refers to an arterial pH < 7.35 (Walter, 2008). Metabolic acidosis is caused by an increase in hydrogen ion production in the body when reacting to hypoxic conditions or as result of intense exercise (when struggling to escape) via the onset of anaerobic glycolysis. This process causes a significant depletion of glycogen and an associated accumulation of lactic acid in the fishes body, specifically L-lactate (Skomal et al, 2007). Blood lactate levels thus become significantly elevated when the fish is exposed to conditions of compromised oxygen availability due to this anaerobic respiration. This subsequent accumulation of hydrogen ions in the white muscle of the fish gradually cause leakage of hydrogen ions into the blood and their increasing abundance causes a rapid reduction in both muscle and blood pH (Skomal et al, 2007) Metabolic acidosis is often accompanied by respiratory acidosis which further reduces the elasmobranchs blood pH levels. Respiratory acidosis is caused by decreased ventilation which results in elevated carbon dioxide concentrations in the body and thus a decline in blood pH. Carbon dioxide accumulates rapidly in the gills of the elasmobranch if restricted oxygen availability occurs (e.g in nets where gills can’t ventilate sufficiently) which increases the partial pressure of arterial carbon dioxide (PaCO2). This increased level of PaCO2 in the blood as a result of the elasmobranchs inability to ventilate results in the decrease of the bicarbonate (HCO3−)/PaCO2 ratio. Bicarbonate is a vital component in the pH buffering system of the body due to its alkalinity, whereby it assists in maintaining acid-base homeostasis. Thus, the resulting decrease in the (HCO3−)/PaCO2 ratio leads to a decrease in blood pH. The cumulative physiological effects of both metabolic and respiratory acidosis results in acidemia, which can cause neurological and cardiovascular complications in the fish (Hobler et al, 1973).

Oxidative Stress

Compromised oxygen availability often experienced by elasmobranchs captured as bycatch, is also followed by a delayed period of oxidative stress and the formation of potentially damaging free radicals, especially when released back into the ocean after capture (Gillian et al, 2012). This lack of oxygen availability can result in irreversible physiological damage from lipid peroxidation (the oxidative degradation of lipid membranes) and also the release of cell death signals from dysfunctional mitochondria that can no longer supply adenosine triphosphate (ATP) (Gillian et al, 2012). Oxidative stress is caused by an imbalance between the systemic manifestation of reactive oxygen species and the fish’s ability to readily detoxify the reactive oxygen species (ROS) or to repair the resulting damage. Following re-oxygenation of the organism after being subjected to prolonged hypoxia (i.e being released back in to the ocean/being able to ventilate gills again), the mitochondrial electron transport chain resumes normoxic levels of ATP generation. This results in the increase of the formation of highly reactive free radical species. High levels of ROS in the body of the fish can cause both reversible and irreversible damage to macromolecules including proteins, nucleic acids and the lipid membranes of cells and organelles (lipid peroxidation). Other damaging events include protein unfolding on a cellular level and irreversible organ failure on an organismal level as ATP and the associated adenylate energy charge fall (Gillian et al, 2012).

Plasma Osmolality

An additional stress response exhibited by elasmobranchs (and teleosts) during capture events is an increase in osmolality, which is a measurement of the body’s electrolyte-water balance. Shark species have been shown to exhibit an increase in plasma osmolality when subjected to periods of acute stress, with dusky sharks having showed an increase in concentration of Mg2+, K+, and Ca2+ by 6% under stressful conditions (Cliff and Thurman, 1984). The proposed explanation behind this increase in plasma osmolality is that in the bodies of elasmobranchs under stress, water shifts out of the vascular compartment in response to raised intracellular lactate or increased sodium influx into the blood (Piiper et al. 1972). This increase in lactate in the body results from the anaerobic glycolysis exhibited by the fish when experiencing hypoxia or exhaustive exercise as discussed previously.  Lactate increase during anaerobic metabolism causes a disturbance in cellular function which can compromise the integrity of cell membranes (Cliff and Thurman 1984) which can result in the leakage of electrolytes from the muscle cells (Piiper et al. 1972). Mako sharks (Isurus oxyrinchus) have also shown to exhibited increased levels of K+, Ca2+, Cl-, Na+ and high osmolalities after capture (Wells et al. 1986), as has the spiny dogfish (Squalus acanthias), where Ca2+, Cl-, Na, K+ and Mg2+ levels were all elevated in response to capture (Mandelman et al. 2007). In some cases, such elevated electrolyte levels can be damaging to the fish. Hyperkalemia is a condition resulting from elevated levels of electrolyte potassium in the blood. Concentrations of K+ above 7mM/l compromise the electrochemical gradients necessary for the function of excitable tissues such as cardiac and skeletal muscle, inducing bradycardia (slow resting heart rate), decreased cardiac output, and anaerobic metabolism in normally aerobic muscle cells (Lai et al. 1990)

Concluding thoughts

It is evident from this review that stress associated with unintentional elasmobranch capture can result in high mortality levels or at the least significant physiological damage in these fish. The increase in levels of reactive oxygen species associated with re-oxygenation after post-capture release can cause significant physiological damage to the organisms. Analysis of changes in blood chemistry and levels of catecholamines, lactate, blood pH, electrolyte levels and glucose production provide an indication of stress and are useful in quantifying the stress responses of these fish as a result of capture. The importance of stress-related research in sharks and other elasmobranchs is of significant importance at this time in history due to the increasing growth of the commercial fishing industry and the predicted increase in elasmobranch bycatch. At this time, the capture-induced stress responses of elasmobranchs are of a lower priority for research and conservation than teleost species. This is due to the historically low economic value of elasmobranchs in comparison to teleosts (Alfonso et al, 2011). Understanding the stress response of elasmobranchs could provide information that may aid in the development of commercial fishing gear that limits the stress inducing factors that negatively impact the physiology of these fish. Additional research into the stress response of elasmobranchs is essential, for example expanding the research to include other species of sharks and rays and also expanding the stressors tested. There has been significant development of fishing gear in recent years that are more selective in their methods of fish capture, which have been shown to limit the amount of bycatch. However these types of gear have not yet been implemented worldwide. This is due to the often high price of production of these nets and lines, resulting in higher costs for fishermen. For fishermen in less economically developed areas,  a lower income may prevent the purchase of these more selective fishing methods, and so consequently use older, more primitive fishing gear that are prone to high numbers of bycatch. Large predatory fish biomass, including that of sharks and other elasmobranchs, has been reduced by 90% since the industrial revolution (Myers and Worm, 2003), and the conservation of these fish is essential in preventing these species from disappearing from our oceans altogether. Increase in research into capture stress and the reasons behind unintentional capture of not just elasmobranchs but all marine fauna frequently found in bycatch could be used to modify existing fish gear, as well as promoting further development of more selective and less stress inducing fishing methods in the future.

Photo © Brian Skerry

Photo © Brian Skerry

– JK

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