Stress-related physiological changes and post-release survival of elephant fish (Callorhinchus milii) after longlining, gillnetting, angling and handling in a controlled setting
Introduction
Stress from capture in fishing gear, restriction of respiration (i.e. asphyxiation), exhaustive exercise and handling cause disruptions to fish physiology and biochemistry (Skomal and Mandelman, 2012). These acute stressful events elicit an immediate neuroendocrine response, known as primary response, which in turn induces a suite of secondary effects including the rapid mobilization and utilization of energy (Cooke et al., 2002; Skomal and Bernal, 2010). The secondary responses may progress to a more chronic stress event that can have sublethal tertiary effects on the individuals’ feeding, growth, immune system and reproduction, thereby potentially resulting in consequences at the population level (Cooke et al., 2002; Skomal and Bernal, 2010). The time for recovery from secondary responses is species-specific and highly dependent on the degree of stress (see Skomal and Bernal, 2010). In elasmobranchs (i.e. sharks and rays), the physiological response to acute and chronic stress and the ability to cope with stress appear to vary considerably (see Skomal and Mandelman, 2012). These interspecific variations and the diverse methodologies (and stressors) applied in studies to date make interspecific comparisons difficult.
Studies investigating the responses to capture stress in elasmobranchs have significantly increased and the majority have focused on secondary responses such as changes in blood metabolites (e.g. lactate and glucose), electrolytes (e.g. potassium and sodium), acid-base balance, osmotic balance, immunological function and movement (e.g. Brill et al., 2008; Butcher et al., 2015; Cliff and Thurman, 1984; Frick et al., 2009, Frick et al., 2010a, Frick et al., 2010b, Frick et al., 2012; Gallagher et al., 2014; Heard et al., 2014; Hoffmayer and Parsons, 2001; Mandelman and Farrington, 2007; Manire et al., 2001; Skomal, 2006; Van Rijn, 2009; Van Rijn and Reina, 2010). The present study examines the physiological secondary responses to stress after capture in fishing gear and handling using repeated blood sampling in a holocephalan species. Only physiological secondary stress indicators, such as lactate, glucose, potassium, osmolality and haematocrit, will be measured due to the difficulty associated with measuring the primary stress indicators in elasmobranch species identified as stress hormones (Pankhurst, 2011).
Elephant fish (Callorhinchus milii, Holocephali, Chondrichthyes) are caught by recreational and commercial fishers using hook-and-line, gillnet, longline, seine and trawl in southern Australia and New Zealand (Braccini et al., 2009; Francis, 1998; Walker et al., 2005). These fishers release annually large numbers of elephant fish in response to bag limits, quotas or as bycatch, but its discard rates are not well documented (Georgeson et al., 2014). The total commercial catch on the continental shelf in southern Australia in 2013/14 was 133 t whole mass (Georgeson et al., 2014) and it is believed that more than half of the catch was discarded (58%) (SharkRAG, 2014). The recreational catch of elephant fish from southern Australia is unknown, but an estimated total catch in 2008 by hook-and-line from Western Port, Victoria was 45 t whole mass and a discard rate of around 20% (Braccini et al., 2009). This recreational catch is comprised mostly of mature individuals which migrate seasonally into Western Port bay to lay eggs (Bell, 2012; Braccini et al., 2009). Immediate and delayed mortality of discarded mature elephant fish can significantly reduce recruitment and consequently affect the sustainability of the stock (Braccini et al., 2009).
Severe physiological stress caused by capture in fishing gear followed by handling can lead to immediate and delayed mortality of discarded fish (Dapp et al., 2016; Ellis et al., 2017; Wedemeyer et al., 1990; Wood et al., 1983). Delayed mortality is one of the most significant issues affecting marine fisheries management as stock size can be overestimated and fishing mortality can be underestimated (Davis, 2002). To our knowledge, the relationship between physiological stress caused by capture and post-release survival for any holocephalan species, including elephant fish, is unknown. A recent review on capture and post-release mortality done by Ellis et al. (2017) covered only elasmobranch species. The importance of physiological and biochemical studies is fundamental as they provide a basis for determining the probability of fish survival from capture in fishing gear and discarding by fishers (Walker, 2007).
The objective of the present study was to determine the physiological changes and post-release survival of captured elephant fish to better understand the effects of capture in fishing gear and handling on this species. This information can be used in fishery stock assessment and provide a measure of post-capture mortality, which is a key component of ecological risk assessment for effects of fishing (Hobday et al., 2011; Stobutzki et al., 2002; Walker, 2005) needed for effective conservation and management of elephant fish populations. Hence we measured immediate and delayed secondary responses to stress (i.e. primary responses to stress were not studied due to the difficulty in measuring them in chondrichthyan species (Pankhurst, 2011)), recovery and mortality of elephant fish following experimental simulated fishing capture and handling in the laboratory and monitored their condition during a 72-h blood monitoring period.
Section snippets
Collection and husbandry of animals
Elephant fish were caught using rod and reel in Western Port Bay (Victoria, Australia) and transported to research facilities in Queenscliff (Victoria, Australia) in a circular 2500-L truck-mounted fish transport tank containing seawater aerated with pure oxygen. Capture and transport were described in detail by Boisvert et al. (2015). The animals were transferred to circular 19,000-L holding tanks (4.6 m diameter and 1.2 m high) connected to a flow-through seawater system running at ambient
Control treatments
A total of 21 animals were used in the control treatments. Mean plasma lactate concentration increased and mean haematocrit decreased significantly over time for all three control treatments (Table 1). Plasma lactate increased significantly between the first (pre-treatment) and second (0 h) blood sample for all control treatments, and it remained significantly different at 3 h before returning to baseline levels (Table 2 and Fig. 1). Haematocrit decreased between 3 h and 24 h, returning to
Discussion
In general, experimental simulation of capture in fishing gear and handling as performed in the present study resulted in elevated plasma lactate, potassium and osmolality and immediately depressed plasma glucose. Gillnet caused higher physiological disturbance than longline and angling. Mortality was observed after gillnet and longline captures. Low plasma glucose concentration, red eyes (blood-shot), pale skin and impaired swimming were good indicators of poor condition in elephant fish.
Conclusions
Capture in fishing gear changes the physiological condition of elephant fish as indicated by increases in levels of plasma lactate, potassium and osmolality, and haematocrit, and decreases in levels of plasma glucose. However, measurements of these indicators immediately after capture (at 0 h) do not show the full extent of the physiological responses to capture stress. As in elasmobranch species, the usual pattern for these blood variables is to continue rising rapidly after capture, peak, and
Acknowledgments
Research was conducted under scientific permits issued by Fisheries Victoria (RP1000), and approved by the Animal Ethics Committee of Monash University (BSCI/2009/16, BSCI/2009/29). Research was funded by grants from the Australian Research Council (grant number LP 110200572 to RDR). Acknowledgments are due to the Department of Environment, Land, Water and Planning, Victoria, Australia, for logistic support; J. D. Bell, J. A. Van Rijn, C. A. Boisvert, L. H. Frick, R. Watson and S. Hyodo for
References (60)
- et al.
Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids
Ann. Rev. Fish Dis.
(1991) - et al.
Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of the sandbar shark (Carcharhinus plumbeus, Nardo)
J. Exp. Mar. Biol. Ecol.
(2008) - et al.
At-vessel mortality and blood biochemical status of elasmobranchs caught in an Australian commercial longline fishery
Global Ecol. Conserv.
(2015) - et al.
Elevation of plasma glucose by catecholamines in elasmobranch fish
Gen. Comp. Endocrinol.
(1978) - et al.
Stress related physiological changes and post-release survival of Port Jackson sharks (Heterodontus portusjacksoni) and gummy sharks (Mustelus antarcticus) following gill-net and longline capture in captivity
J. Exp. Mar. Biol. Ecol.
(2010) - et al.
Trawl capture of Port Jackson sharks, Heterodontus portusjacksoni, and gummy sharks, Mustelus antarcticus, in a controlled setting: effects of tow duration, air exposure and crowding
Fish. Res.
(2010) - et al.
Immediate and delayed effects of gill-net capture on acid-base balance and intramuscular lactate concentration of gummy sharks, Mustelus antarcticus
Comp. Biochem. Physiol. – Mol. Integr. Physiol.
(2012) - et al.
Ecological risk assessment for the effects of fishing
Fish. Res.
(2011) Metabolic effects of epinephrine and norepinephrine in the eel Anguilla anguilla L
Gen. Comp. Endocrinol.
(1973)Changes in the blood sugar of the cod, sculpin, and pollock during asphyxia
J. Biol. Chem.
(1927)
The endocrinology of stress in fish: an environmental perspective
Gen. Comp. Endocrinol.
Comparison of some hormonal effects on carbohydrate metabolism in an elasmobranch (Squalus acanthias) and a holocephalan (Hydrolagus colliei)
Gen. Comp. Endocrinol.
The physiological response to anthropogenic stressors in marine elasmobranch fishes: a review with a focus on the secondary response
Comp. Biochem. Physiol.
Distribution of leukocytes as indicators of stress in the Australian swellshark, Cephaloscyllium laticeps
Fish Shellfish Immunol.
Oxygen binding by the blood and hematological effects of capture stress in two big game fishes mako shark Isurus oxyrinchus and striped marlin Tetrapturus audax
Comp. Biochem. Physiol.
Post-capture survival and implications for by-catch in a multi-species coastal gillnet fishery
PLoS One
Reproduction and Ageing of Australian Holocephalans and White-Fin Swell Shark. PhD Thesis
Capture, transport, and husbandry of elephant sharks (Callorhinchus milii) adults eggs, and hatchlings for research and display
Zoo Biol.
Evaluation of the Effects of Targeting Breeding Elephant Fish by Recreational Fishers in Western Port
High post-capture survival for sharks, rays and chimaeras discarded in the main shark fishery of Australia?
PLoS One
Summary of Tag Releases and Recaptures in the Southern Shark Fishery
Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus
Comp. Biochem. Physiol.
Strategies for quantifying sublethal effects of marine catch-and-release angling: insights from novel freshwater applications
Am. Fish. Soc. Symp.
Respiratory mode and gear type are important determinants of elasmobranch immediate and post-release mortality
Fish
Key principles for understanding fish bycatch discard mortality
Can. J. Fish. Aquat. Sci.
Capture, care, and behavioral observations of two species of chimeroid fishes: Hydrolagus colliei and Callorhinchus milii
Chondros
Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimaeroidei)
Am. Mus. Novit.
A review of capture and post-release mortality of elasmobranchs
J. Fish Biol.
New Zealand shark fisheries: development, size and management
Mar. Freshw. Res.
The physiological response of Port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity
North Am. J. Fish. Manage.
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