Stressors, vitality impairment, and survival of fishes

Developing rapid visual in situ trait assessment (reflex actions, injury) associated with vitality impairment.

Video slideshow (2:06) discussing stressors, vitality impairment, and survival of fishes in fisheries contexts.

Why observe several reflex actions together to measure animal vitality?

Philipchircop 2012

Why observe several reflex actions together to measure animal vitality? The short answer is that animals are whole beings; a summary collection of component parts and their interactions in response to stimuli.

Animals are constructed of biochemical and behavioral components that interact to form a whole; capable of responding to stressors. The interactions of stressors and behavior are also important for prediction of vitality impairment and survival. Reflex actions are fixed behavior patterns that include biochemical, muscle, organ, and nerve functions.

Efforts to identify factors that can control vitality and predict post-release survival and mortality of captured animals generally strive to identify single important variables. For example, temperature changes, injury, exhaustion, and hypoxia can control vitality and survival. For simplicity, single factors are statistically modeled as predictors for survival. Factor interactions are rarely considered because of their complexity.

Patterns of vitality impairment vary with species and contexts. Observing impairment of several reflex actions and possible injury in a defined context integrates the effects of multiple stressors, contexts, and their interactions on animal impairment and survival. Measurement of single reflex action impairment can miss the range of vitality that spans from excellent to moribund. 

Stoner 2012 (crabs)

Below are several examples of the cascading nature of impairment observed as individual reflex actions cease to function in a spectrum of stressor intensities. Reflex actions with higher proportion of impairment are impaired before those with lower percentage. Note that patterns of impairment vary with taxa and context.

Davis 2010 (walleye pollock, coho salmon, northern rock sole, Pacific halibut)

Stoot et al. 2013 (turtles)

Uhlmann et al. 2016 (plaice, sole)

Forrestal 2016 (triggerfish)

Forrestal 2016 (yellowtail snapper)

Danylchuk et al. 2014 (lemon shark)

McArley and Herbert 2014 (snapper)

Sampson et al. 2014 (mottled mojarra)

Stoner 2009 (Tanner crab, snow crab)

Stoner 2012 (spot prawn)

What is RAMP: reflex action mortality predictor?

Reflex actions and injury traits in crab scored for impairment (Stoner 2012, Yochum et al. 2015).

Reflex actions and injury traits in sharks scored for impairment (Danylchuk et al. 2014).

Reflex actions and injury traits in fish scored for impairment (Davis 2010, McArley and Herbert 2014).

Reflex actions and injury traits in turtles scored for impairment (LeDain et al. 2013, Stoot et al. 2013).
Photos; crab - Farm to Market, shark -  Swell Brains, fish - DEEP, turtle - Aquatica.

Any animal has reflex actions and potential injury traits; see diamonds in figures. These fixed traits can be observed, scored present or absent, and summed to form an animal vitality impairment score. Animal vitality is a gestalt of reflex and injury traits that we can observe as a whole animal, active and responding to stimuli. Vitality impairment and mortality are correlated and this relationship is expressed as RAMP, reflex action mortality predictor.

Impairment of well-defined reflex actions and injury types may differ for each species, dependent upon their natural history and phylum.  These species traits of reflex actions and injury types can be scored and combined to express the percentage of whole animal impairment. No impairment represents a healthy animal with all actions present and all injury absent. Increasing absence of reflex actions and presence of injury types is increasing impairment and is correlated with mortality.

Sublethal and lethal zones associated with reflex action impairment scores (RAMP) in walleye pollock, rock sole, sablefish, and Pacific halibut (Davis and Ottmar 2006). For these species at specific transition impairment values, a rapid rise in mortality is observed after a small increase in reflex impairment. 

These curves illustrate the expression “you are alive until you are not”. Animals live in various states of vitality impairment that are correlated with stress. Above a quantifiable level of vitality impairment, animals begin to show mortality, correlated with continued increase for impairment. The distribution of reflex impairment and injury in a group of animals is a measure of population vitality. 

For fish species (Davis 2010, McArley and Herbert 2014), animals have several types of reflex actions which can be secondary or primary. One action group contains secondary peripheral actions that are part of swimming and defensive behavior (fin erection and startle). Impairment of these reflex actions generally indicates sublethal stress effects and is associated with increasing stressor intensity (duration or strength). A second action group contains primary body functions (orientation and coordinated breathing). Impairment of primary body functions generally indicates delayed mortality after stress induction. In the same way, for crustacean species (Stoner 2012, Yochum et al. 2015), loss of leg reflex actions are associated with sublethal stress effects. Loss of eyestalk and mouth actions are associated with delayed mortality after stress induction.

Triage for captured and released fisheries species: research and survival

Will they survive? (The Guardian, 2013)

Vitality impairment can be linked to post-capture mortality in fisheries bycatch. Vitality impairment can be estimated by direct observation of animal activity, responsiveness, and injury. For each critical fisheries species in crabs, fishes, sharks, and turtles, reflex actions that are consistently present in healthy, uninjured individuals are listed as control levels. Impairment is signified by loss of reflex action types and addition of injury types after capture.  

Reflex actions are fixed, consistent animal behavior patterns that can be triggered by perception of external stimuli (light, sound, smell, gravity, touch). Stimulation of reflex actions is not controlled by body size, motivation, strength of stimulus, or fear. Reflex action traits summed as a whole animal can be an expression of vitality (Davis 2010). In contrast, volitional behavior can be altered by body size, motivation, strength of stimulus, fear, cognition, and as such is not a controlled measure of vitality.

With the species reflexes and potential injury lists, observations of captured animals can be made in commercial and sport fisheries. Patterns of significant impairment can be determined and related to fishing context and species (Raby et al. 2015). These patterns help identify the relative effects of fishing gears, handling, and physical factors (air, temperature, light, pressure) on impairment and potential survival and mortality.

Figure shows overlap between information on animal physiology and fisheries biology, adapted from Horodysky et al. 2015 and modified to show vitality information. Measures of vitality include reflex impairment and injury, which are whole animal measures that are ecologically relevant, linking physiological and population level research and hypothesis testing. Volitional behavior is coordinated whole animal movements beginning with perception and motivation, followed by attraction and aversion to various stimuli (injury, threat, food, shelter, species mates, migration).

Patterns of vitality impairment can guide research questions and priorities to triage fisheries for treatment of bycatch mortality and enhancement of survival. Vitality impairment can measure the efficacy of engineering fishing gears to increase bycatch survival. 

Observing vitality impairment

Animal vitality can be measured by observing species traits associated with activity, responsiveness, and injury. For each species, a group of reflex actions can be observed that are consistently present in healthy animals. As vitality becomes impaired, reflex action traits disappear and injury traits may begin to appear. 

Activity, responsiveness, and injury for measurement of vitality impairment (Benoît et al. 2010). 

Fisheries show gradients of stressors associated with capture, handling, and release or escape. Discard mortality, survival, and vitality impairment are controlled by stressor gradients.

Gradients of mortality and simulated stressors in sablefish fisheries; water temperature and gear type including trawl (time), longline, pot. Smaller fish are more sensitive to stressors (AFSC).

Vitality impairment gradients are associated with stressors and can be used to predict survival and delayed mortality for populations of impaired animals. Vitality impairment gradients can be measured by identifying classes of health condition; excellent, good, poor, and moribund based on rapid observation and impression of animal injury and activity (Benoît et al. 2015). 

The resolution for observations of vitality impairment gradients can be increased by including more information. RAMP is an example of this approach (Davis and Ottmar 2006, Davis 2010). A list can be made of reflex actions present in control animals and possible injuries. Then presence or absence of listed traits is observed after exposure to stressors. Increasing impairment is associated with stress effects and morbidity.

Reflex actions observed in snapper by McArley and Herbert 2014.

Relationships between vitality impairment and survival or delayed mortality can be experimentally determined. Then predictions of stress effects in other settings with similar stressors can be made by measuring vitality impairment associated with stressors, without the need to hold or tag animals. Vitality impairment can be rapidly observed in sampled populations as an additional factor to evaluate stressor effects and is a useful indicator of animal health and stress status, that can be validated experimentally.

Reflex impairment and mortality for individuals (A) and groups (B) of Atlantic cod with 95% confidence intervals (Humborstad et al. 2009). 

Fisheries studies that have used and documented reflex actions or injury for vitality impairment testing

The table presents selected examples of reflex action & injury vitality impairment testing.

See also a list of reflex actions and injury that may be scored for vitality impairment.

Citations:

AFSC, Alaska Fisheries Science Center 2014 Observer Sampling Manual.

Fisheries Monitoring and Analysis Division, North Pacific Groundfish Observer Program. Seattle, WA.

Barkley, A.S. & Cadrin, S.X. 2012. Discard mortality estimation of yellowtail flounder using reflex action mortality predictors. Trans. Am. Fish. Soc. 141:638-644.

Benoît, H.P., Hurlbut, T., and Chassé, J. 2010. Assessing the factors influencing discard mortality of demersal fishes using a semi-quantitative indicator of survival potential. Fish. Res. 106:436-447.

Braccini, M., Van Rijn, J., and Frick, L. 2012. High post-capture survival for sharks, rays and chimaeras discarded in the main shark fishery of Australia? PLoS ONE 7: e32547.

Brownscombe, J.W., Thiem, J.D., Hatry, C., Cull, F. Haak, C.R., Danylchuk, A.J., and Cooke, S.J. 2013. Recovery bags reduce post-release impairments in locomotory activity and behavior of bonefish (Albula spp.) following exposure to angling-related stressors. J. Expt. Mar. Biol. Ecol. 440:207-215.

Brownscombe, J.W., Nowell, L., Samson, E., Danylchuk, A.J., & Cooke, S.J. 2014. Fishing-related stressors inhibit refuge-seeking behavior in released subadult Great barracuda. Trans. Am. Fish. Soc. 143:613-617.

Campbell, M.D., Patino, R., Tolan, J., Strauss, R., and Diamond, S.L. 2010.

Sub-lethal effects of catch-and-release fishing: measuring capture stress, fish impairment, and predation risk using a condition index. ICES J. Mar. Sci. 67:513-521. 

Campbell, M.D., Tolan, J., Strauss, R., and Diamond, S.L. 2010. Relating angling-dependent fish impairment to immediate release mortality of red snapper (Lutjanus campechanus). Fish. Res. 106:64-70.

Danylchuk, A.J., Suski, C.D., Mandelman, J.W., Murchie, J.W., Haak, Brooks, A.M.L., and Cooke, S.J. 2014. Hooking injury, physiological status and short-term mortality of juvenile lemon sharks (Negaprion bevirostris) following catch-and-release recreational angling. Cons. Physiol. 2:cot036.

Davis, M. W. 2007. Simulated fishing experiments for predicting delayed mortality rates using reflex impairment in restrained fish. ICES J. Mar. Sci. 64:1535-1542.

Davis, M.W. & Ottmar, M.L. 2006. Wounding and reflex impairment may be predictors for mortality in discarded or escaped fish. Fish. Res. 82:1-6.

Depestele, J., Buyvoets, E., Calebout, P., Desender, M., Goossens, J., Lagast, E., Vuylsteke, D., and Vanden Berghe, C. 2014. Calibration tests for estimating reflex action mortality predictor for sole (Solea solea) and plaice (Pleuronectes platessa): preliminary results. ILVO-communication. Report nr. 158. 30p. 

Diamond, S.L. & Campbell, M.D. 2009. Linking “sink or swim” indicators to delayed mortality in red snapper by using a condition index. Mar. Coast. Fish.: Dynamics, Manag. Eco. Sci. 1:107-120.

Donaldson, M.R., Hinch, S.G., Raby, G.D., Patterson, D.A., Farrell, A.P., and Cooke, S.J. 2012. Population-specific consequences of fisheries-related stressors on adult sockeye salmon. Physiol. Biochem. Zool. 85:729-739.

Hammond, C.F., Conquest, L.L., and Rose, C.S. 2013. Using reflex action mortality predictors (RAMP) to evaluate if trawl gear modifications reduce the unobserved mortality of Tanner crab (Chionoecetes bairdi) and snow crab (C. opilio). ICES J. Mar. Sci. 70:1308-1318.

Hannah, R.W. and Matteson, K.M. 2007. Behavior of nine species of Pacific rockfish after hook-and-line capture, recompression, and release. Trans. Amer. Fish. Soc. 136:24-33.

Humborstad, O-B., Davis, M.W., and Løkkeborg, S. 2009. Reflex impairment as a measure of vitality and survival potential of Atlantic cod (Gadus morhua). Fish. Bull. 107:395-402. 

McArley, T.J. & Herbert, N.A. 2014. Mortality, physiological stress and reflex impairment in sub-legal Pagrua auratus exposed to simulated angling.  J. Expt. Mar. Biol. Ecol. 461:61-72.

Raby, G.D., Donaldson, M.R., Hinch, S.G., Patterson, D.A., Lotto, A.G., Robichaud, D., English, K.K., Willmore, W.G., Farrell, A.P., Davis, M.W., and Cooke, S.J. 2012. Validation of reflex indicators for measuring vitality and predicting the delayed mortality of wild coho salmon bycatch released from fishing gears. J. Appl. Ecol. 49:90-98.

Stoner, A.W. 2012. Assessing stress and predicting mortality in economically significant crustaceans. Rev. Fish. Sci. 20:111-135.

Stoner, A.W., Rose, C.S., Munk, J.E., Hammond, C.F., and Davis, M.W. 2008. An assessment of discard mortality for two Alaskan crab species, Tanner crab (Chionoecetes bairdi) and snow crab (C. opilio), based on reflex impairment. Fish. Bull. 106:337-347.

Szekeres, P., Brownscombe, J.W., Cull, F., Danylchuk, A.J., Shultz, A.D., Suski, C.D., Murchie, K.J., and Cooke, S.J. 2014. Physiological and behavioural consequences of cold shock on bonefish (Albula vulpes) in The Bahamas. J. Expt. Mar. Biol. Ecol. 459:1-7.

Trumble, R.J., Kaimmer, S.M., and Williams, G.H. 2000. Estimation of discard mortality rates for Pacific halibut bycatch in groundfish longline fisheries. N. Amer. J. Fish. Manag. 20:931-939.

Yochum, N., Rose, C.S., and Hammond, C.F. 2015. Evaluating the flexibility of a reflex action mortality predictor to determine bycatch mortality rates: A case study of Tanner crab (Chionoecetes bairdi) bycaught in Alaska bottom trawls. Fish. Res. 161:226-234.

Human delayed mortality can be predicted using olfactory impairment

Olfactory impairment in humans was measured by error rate in olfaction tests. Increasing number of errors in olfaction tests were related to increasing 5-year mortality rates in a logistic regression (PLoS ONE). 

The human logistic relationship between olfactory impairment and 5-year delayed mortality is a powerful method for predicting delayed mortality and is similar to other animal RAMP relationships between reflex impairment, injury, and delayed mortality. Olfactory impairment can be easily measured in human and animal clinical settings and can easily and automatically be measured in aquaculture contexts by analysis of animal distributions and activity in rearing facilities. Given the fundamental nature of olfaction, one would expect the relationship between olfactory impairment and delayed mortality to be generally present among animal phyla and this can be tested in clinical and field settings.

Pinto et al. 2014 state, “We are the first to show that olfactory dysfunction is a strong predictor of 5-year mortality in a nationally representative sample of older adults. Olfactory dysfunction was an independent risk factor for death, stronger than several common causes of death, such as heart failure, lung disease and cancer, indicating that this evolutionarily ancient special sense may signal a key mechanism that affects human longevity. This effect is large enough to identify those at a higher risk of death even after taking account of other factors, yielding a 2.4 fold increase in the average probability of death among those already at high risk (Figure 3B). Even among those near the median risk, anosmia increases the average probability of death from 0.09 (for normal smellers) to 0.25. Thus, from a clinical point of view, assessment of olfactory function would enhance existing tools and strategies to identify those patients at high risk of mortality.”

(PLoS ONE)

The human study controlled for the mortality effects of age, gender, socioeconomic status, and race. Additionally, “We excluded several possibilities that might have explained these striking results. Adjusting for nutrition had little impact on the relationship between olfactory dysfunction and death. Similarly, accounting for cognition and neurodegenerative disease and frailty also failed to mediate the observed effects. Mental health, smoking, and alcohol abuse also did not explain our findings. Risk factors for olfactory loss (male gender, lower socioeconomic status, BMI) were included in our analyses, and though they replicated prior work [41], did not affect our results.” Note that the study did not control for effects of possible episodic exposure to toxins or injury that may result in temporary or permanent olfactory impairment not related to death.

Olfactory response is an involuntary response to a stimulus, and may be considered a reflex action. In the human study, presence or absence of smell detection for rose, leather, orange, fish, and peppermint were summed and related to delayed mortality. Olfactory responses to various substances can be scored as present or absent and summed to predict delayed mortality. In the same way, the RAMP method is an example of presence-absence scoring with summation of reflex impairment and injury scores to predict delayed mortality.  Measuring and summing whole animal responses, i.e., olfaction, reflex actions, and injury to stimuli is a powerful method for observing the effects of stressors and aging on delayed mortality.   

“We believe olfaction is the canary in the coal mine of human health, not that its decline directly causes death. Olfactory dysfunction is a harbinger of either fundamental mechanisms of aging, environmental exposure, or interactions between the two. Unique among the senses, the olfactory system depends on stem cell turnover, and thus may serve as an indicator of deterioration in age-related regenerative capacity more broadly or as a marker of physiologic repair function [13].”

Clearly, measurement and summation of presence-absence for whole animal involuntary characteristics (olfaction, reflex actions, and injury) is a powerful way to predict delayed mortality in humans and other animals.

Making and Using RAMP in Fisheries

A video is available that explains making and using RAMP in fisheries.

Why is vitality impairment related to mortality?

By definition, healthy animals have full vitality. Vitality becomes impaired as animals become stressed by capture and handling. Severe vitality impairment can result from the effects of physical injury or other stressors, e.g., fatigue, temperature, light, sea state, and air exposure. Maladaptive stress responses or critical injury associated with severe vitality impairment can result in immediate and delayed mortality.

Why score reflex actions and injury?

Reflex actions are fixed behavior patterns that are directly related to vitality impairment, without control by volitional behavior factors, e.g., motivation, hunger, fear, shelter seeking, migration, and reproduction. Reflex actions reflect the state of neural, muscle, and organ functions.

Injuries are directly related to vitality impairment because they can control neural, muscle, and organ functions.

Scoring vitality impairment in general

Any type of reflex action or injury that is related to vitality can be summed to score vitality impairment. The important point is that a sum of presence/ absence scores for vitality characteristics produces an index of vitality impairment. This vitality index can then be used as a measure of variability for sublethal stressor effects in fisheries, as well as a validated indicator and predictor of mortality and survival.

Steps for making and using RAMP in fisheries.

The importance of vitality in fishing experiments

Key fishing stressor factors, Davis, 2002

Knowledge of key factors controlling fisheries is necessary for sustainable management of fishery stocks. Scientific hypothesis testing in the form of fishing experiments is a necessary component of fisheries knowledge development and validation. Fishing experiments are performed in the field by simulating actual fishing conditions, by actual fishing, and during survey cruises. Fishing experiments can be used to identify key stressor factors that control and contribute to the survival and mortality of captured, discarded, or escaped animals as well as identifying the key factors controlling fishing gear capture efficiency and selectivity.

Trawl captured animals, Robert A. Pawlowski, NOAA Corps

While field fishing experiments represent realistic conditions, they are a matrix of confounded factors which cannot be easily separated into mechanistic hypothesis tests and explanations of factor importance. Effects of factors are often synergistic and prior animal stressor history can alter relative effects of subsequent exposure to factors, e.g., depth changes, injury, elevated temperature, air exposure, and size and species differences.

Flow chart of experimental fishing stressor factors, Davis and Olla 2001

Simulated fishing experiments with factors in controlled laboratory conditions is one way to test hypotheses about mechanistic effects of individual factors and their interactions. However these laboratory experiments are generally viewed as not realistic to field conditions and they are used to identify factors that may be important in the field. Furthermore, modern requirements of animal care laws and committees restrict the use of laboratory fishing experiments by not allowing human application of experimental stressor factors on animals and the use of mortality outcomes. These same laws and committees do not have jurisdiction over field fishing experiments. 

Laboratory trawl tow tank, NOAA RACE

Given that factors are confounded in field fishing experiments, how can we test for effects of factors in the traditional mechanistic hypothesis test? We can test for changes in animal vitality. Since vitality has been shown to be correlated with survival and mortality, it is a useful indicator of animal outcomes before and after exposure to experimental stressor factors. For example, we generally do not know the exposure of animals to stressors prior to experimental manipulation of factors. Not knowing the complete stressor profile is not an obstacle since the animal knows the complete stressor profile and presents vitality levels that have integrated the effects of that profile. Then we can expose animals to additional stressor factors and measure further changes in vitality from their initial levels. 

Important to shift mechanistic thinking from needing to know the effects of individual factors to knowing the effects of fishing variability. Manipulations of time in air and elevated temperature represent differences in fisher sorting and handling behavior on deck and are appropriate for defining the effects of fishing variability. Effects of variation in tow time and catch quantity can be manipulated and are included in the mix of animals landed. The questions of associations among individual fishing stressor factors is left for another day and are more of interest to mechanistic scientists than to managers and fishers. Fishing variability will give a picture of the fishery and its potential effects on animal vitality. By measuring animal vitality, which integrates the effects of stressor factors, you have measured a key master variable that indicates the important effects of fishing.

Vitality is the key variable that can be used to indicate and predict delayed survival and mortality outcomes for discards and escapees from fishing. The relationships between vitality and survival and mortality are defined by captive observation or tagging and biotelemetry experiments. During exposure of animals it is important to insure that all stressor types normally in the fishery in question are present for the population of tested animals (e.g., temperature, air exposure, fatigue, injury) and that a full range (0-100%) of vitality impairment and mortality are observed. Then relationships can be calculated for each species of interest that do not extrapolate beyond available data ranges and that apply to the fishery of interest. These relationships can then be used to predict survival and mortality for animals under any condition of interest in the fishery without the need for further captive observations or tagging.

Consider how scientific peer-reviewers may see this shift from mechanistic thinking and develop thoughts that elaborate the importance of vitality from the animal’s point of view. Some resistance is expected from mechanists who believe that they can attribute cause and effect to individual factors. There is always a matrix of interactions, even under the most restrictive and controlled experimental conditions. There are always interactions and synergisms to account for. As a result, there are associations among factors, rather than cause and effect. In other words, there are causes and conditions associated with effects. 

From the fishing experiment perspective, we set up fishing conditions that are real or that simulate fishing and then measure animal vitality, which is an integrated measure of the effects of interacting factors. It is useful to identify the important stressors by experimentally changing them in fishing experiments; changes in time in air, trawl time, trap retrieval time, depth, season, temperature, catch amount, and injuries. Always remember that there is a hidden context of conditions, i.e., the animals are prestressed by other factors not being controlled. But this hidden context can be accounted for by observing and comparing vitality impairment among animals observed in all treatments, including simply captured animals without additional stressor exposures (using positive controls). This experimental approach is useful both for fishers who wish to modify fishing gear and practices, as well as managers who wish to observe animal vitality and correlate that with mortality and survival.

Allostasis and it's correlate vitality; measured with reflex action impairment and injury

Figure 1. Alternative models of regulation. Homeostasis describes mechanisms that hold constant a controlled variable by sensing its deviation from a “setpoint” and feeding back to correct the error. Allostasis describes mechanisms that change the controlled variable by predicting what level will be needed and then overriding local feedback to meet anticipated demand, Sterling (2003).

Physiological regulation is considered the cornerstone of animal survival and avoidance of death. Inability to regulate is indicated by vitality impairment and causes an animal to exceed its capacity for life. To understand and predict the causes for survival and death, we must be able to measure appropriate state and rate variables involved in regulation. The generally accepted model of physiological regulation is homeostasis, based on the concept of stability through constancy. However homeostasis is unable to explain accumulating medical evidence that physiological variables do not remain constant. Clearly a more comprehensive model of physiological regulation is needed.  

Allostasis is a model of physiological regulation based on the concept of stability through change (Sterling 2003). Allostasis is able to account for evidence that physiological variables are not constant. The allostasis model connects easily with modern concepts in sensory physiology, neural computation, and optimal design, to produce anticipatory regulation. Allostasis was developed with the recognition that the goal of regulation is not constancy, but rather fitness under natural selection, that implies preventing errors and minimizing costs. Both needs are best accomplished by using prior information to predict physiological demand and then adjusting all variables to meet it. In allostasis an unusual variable value is not a failure to maintain a setpoint, but is a response to some prediction made through perception or prior knowledge. Constancy is not a fundamental condition for life. A mean value need not imply a setpoint but rather the most frequent demand.

The brain has close access to essentially every somatic cell through nerve cell connections. The broad metabolic patterns over short and long time scales, and under mild as well as emergency conditions are controlled by the brain. In other words, the brain regulates both physiology and its supporting behavior (Sterling 2003). The use of reflex action impairment to measure vitality and predict survival and mortality is consistent with the allostatic model because it is representative of key elements of physiological regulation; including perception, behavior, and neural control of somatic cell function. Injury also measures vitality impairment because of its direct effects on neural and somatic cell function, hence allostasis. 

Reflex action impairment and injury can measure vitality and predict survival and mortality in taxa ranging from invertebrates to humans. Clearly the presence of higher brain function is not a necessary condition for the allostatic model. Instead, simple interactions of neural and somatic cells can produce allostasis regulation and its correlate, vitality. It remains to elucidate the comparative details of physiological regulation as it developed in new phyla through evolutionary time.

When studying the causes for death, shifting focus from measurement of lower level plasma variables (cortisol, lactate, glucose, O2, pH) to higher level variables (vitality in its various guises) would advance the assessment of physiological regulation and its role in survival and death. Particular values for plasma variables are of secondary importance, until reaching outer limits of operation. The interactions of plasma variables are of primary importance (Ellis and Del Giudice 2014). The homeostatic model fails to capture the importance of stability through change; how animals adapt and ultimately go beyond their physiological limits. The allostatic model addresses stability through change and invites adaption and evolutionary fitness.

Reflex action impairment is probably a biomarker for impairment of physiological regulation and this is why the RAMP curve is non-linear, reflecting the inflection point where physiological regulation is lost and death results. Addition of injury to RAMP adds details of direct injury effects on physiological functioning and regulation, e.g. compromising integument gatekeeping (skin, gut, gill, lung).

Measuring reflex action impairment in sole and plaice; preliminary steps to making RAMP

Collection of fish with beam trawl, Jochen Depestele

The beginning steps for measuring reflex action impairment and making a RAMP are detailed in “Calibration tests for identifying reflex action mortality predictor reflexes for sole (Solea solea) and plaice (Pleuronectes platessa): preliminary results” authored by Depestele, J. et al. 2014. Experiments were designed to collect sole and plaice using short hauls of a beam trawl, to test their reflex actions, and to identify consistent reflexes for making RAMP. These experiments followed steps for making RAMP.

A short video demonstrates testing plaice for reflex actions including righting, eye roll (vestibular-ocular response), evade, operculum, mouth, and tail grab. Fish are shown in a series of increasing impairment.

Conclusions from the study included:

Preliminary investigations have been undertaken on-board the RV Belgica to assess the potential presence of a range of reflexes in sole and plaice. A wide range of potential reflexes was investigated prior and during the sea trial, leading to a final selection of seven reflexes with a good potential of being consistently present in fish in a favorably vital condition. Fish in a “perfect” condition could not be retrieved, but 22 individuals of plaice and sole were selected from short hauls and their survival potential was evaluated during 70 hours in on-board holding facilities. Only one sole died, and indicated hence that the control fish for the calibration test serve purpose.

Holding tanks for fish on board RV Belgica, Jochen Depestele

The final selected reflex actions were very similar for sole and plaice, except for one. Forced opening of sole’s operculum did not reveal much resistance of the fish, while holding plaice by its head did not induce curling of the fish. The most consistent reflex actions for sole were called “stabilize, mouth, and tail grab”, followed by the “vestibular-ocular response”. Vital individuals seemingly dig into the sand or stabilize themselves onto the floor of the water-filled box. They also keep their mouth closed when trying to open it with a probe. When fish have stabilized, they respond clearly to grabbing their tail or even tickling it. The “head” reflex was easy to assess, though not always present. However, it is clear that vital soles curled around one’s hand when they had been in holding tanks. This was not that obvious for fish that were just released from the codend. Natural righting was observed regularly, although some individuals remained at their backs for >5 sec and did not return to their natural position at all or only after stimulating them. The consistency could thus be questioned, but good candidate reflexes were proposed for sole, and should be further evaluated. The most consistent reflexes of plaice were the turning of the eyes when the fish was turned around longitudinally. The resistance of plaice to forced opening of the operculum was a clear reaction as well. Not fully consistent, but nevertheless a good indication of the reflexes was the “evade” response and the “tail grab”. When the tail is touched or grabbed in a “good” way (which might require some practice), then the fish swim away, or at least the fins stimulate propulsion. The mouth of plaice was easily opened, but mostly the individuals tried to close it or seemingly opposed to the forced movement.

Our investigations confirmed that on-board holding facilities result in high survival of plaice and sole from very short hauls (<20min). Investigated individuals were non-randomly selected and thus it was not surprising that their physical injuries were limited. These individuals were suitable for developing the reflexes, although they were limited in number (22 for plaice and 22 for sole) and they also did not range over a wide variety of fish conditions (e.g. limited length variability). The seven reflexes from these preliminary investigations are therefore proposed as candidates for the development of a RAMP score for sole and plaice.

The tests of the reflexes were run directly after releasing fish from the codend. When examining the survival from fish that were accommodated for some time (e.g. 48 hours), we noted that they reacted more strongly and had much clearer responses to the reflex tests. In particular the tail grab worked very nicely for sole when their status (alive or dead) was tested. Therefore we suggest that the proposed reflexes are tested once more on surviving individuals of short hauls after an accommodation period of >24hours. Consistency of the outcome of the reflex tests is expected to be improved when the impairment from the catching process is accounting for. Other recommendations for follow-up tests relate to the registration of potential environmental and biological confounding factors.

Survival of the fittest

Bob van Marlen, IMARES

Work is in progress at ICES to define methods for estimating discard survival in reference to the new European Commission Common Fisheries Policy. The ICES newsletter states, “Under the recently reformed European Commission Common Fisheries Policy (CFP), the practice of discarding fish will be phased out, replaced instead with landing obligations. Under the landing obligation, all catches of regulated species must be landed and counted against quotas unless it has been scientifically proven that the species can survive the discarding process. Species that display a high level of discard survivability will be awarded an exemption, meaning that fishers can return these fish to the sea. Unregulated and protected species will continue to be released.”

The ICES WKMEDS focuses on developing guidelines and identifying best practice for undertaking experiments to investigate the survival of organisms discarded from the catches of commercial fisheries. 

Importantly ICES states, “Techniques for estimating survival under review include captive observation, vitality assessment, and tagging and biotelemetry, each with its own advantages and disadvantages. By using a combination of techniques, as WKMEDS suggests, clear synergies can be achieved and challenges overcome.”

"It's an exciting time", state the workshop Chairs Michael Breen and Tom Catchpole, "this group will be central to an international community that are working together to address the important issue of discard survival."

The WKMEDS group is producing a synthesis of previous discard survival and mortality research with the goal to develop an integrated approach for estimating discard survival. The integrated approach is designed to guide scientists and managers in their evaluation of potential candidate fisheries and species for discarding exceptions to the landing obligation of the CFP. The integrated approach incorporates information about the role of fishing conditions as stressors, species sensitivity to stressors, vitality impairment of captured species, estimated discard survival rates, and cost-benefit analysis of methods for survival assessment in fisheries as well as impacts of discarding on fisheries stocks.

On the importance of considering sublethal stress and injury effects in discard and escapee survival and fitness

Shark release, NOAA

Sublethal stress and injury are important factors to consider in discard and escapee survival and fitness (Wilson et al. 2014). Fishing gears are often designed to enhance escape of animals that might otherwise become bycatch. Captured animals are discarded from fisheries for economic, regulatory, conservation ethic, and political reasons. Observation of animal impairment (Davis 2010) and immediate mortality for discards on board fishing vessels is straightforward. For animals that are alive when discarded or that escape from fishing gear, the effects of stress and injury can alter behavior, growth, and reproduction, or result in delayed mortality. Delayed mortality of escapees (Suuronen 2005) and discards (Revill 2012) has been documented for commercially important species. However, few studies have measured potential fitness effects of sublethal stress and injury on surviving discards or escapees.

Fig. 1. Conceptual diagram outlining the immediate and long-term effects of escape or release from commercial fishing gear and how it relates to each level of biological organization. Question marks (?) denote areas for which no primary literature exists, and present future avenues of research (Wilson et al. 2014).

Sublethal effects of capture, escaping, and discarding can occur at individual, community, and population levels of organization. For individuals, immediate sublethal effects are physiological responses, injury, and reflex impairment. Delayed sublethal effects are behavioral impairment, altered energy allocation, wound healing, immune function and disease, reproductive success, and offspring quality and performance. Few studies have been conducted for responses at community and population levels, and clearly these are important to consider.

Wilson et al. 2014 summarize:

“The obvious gap that emerges is the lack of research linking at-release measurements with latent sublethal fitness outcomes such as foraging, energetics, growth, reproduction and offspring quality. The dearth of knowledge in this area is likely based on two realities: (1) a justifiable focus on simply quantifying and reducing bycatch mortality, and (2) the difficulty of long-term monitoring of fitness outcomes in wild animals. Of the reviewed studies, several indicated that physiological disturbance, injury or behavioural impairments may have had long-term implications for growth and reproductive fitness. Further study of sublethal effects could clarify previously unaccounted-for population level consequences of fisheries and better conservation practices to mitigate the impacts of fisheries.”

Also of importance to discard survival and fitness is consideration of predation that can occur after escape or discarding of captured animals (Raby et al. in press). Controlling factors for predator-induced mortality include fishery type, stress and injury, barotrauma, predator behavior and abundance, fish size, and temperature. Summary of the Raby et al. review suggests research directions:
  “The important first step is for fishers, managers and researchers to identify systems where predation is likely to be a substantial contributor to unobserved fishing mortality. Most study of capture-and-release mortality involves quantifying the effects of factors such as temperature, capture depth or fight time. Predator type and abundance could be considered new ‘phantom’ factors that are dynamic and would be challenging to incorporate into research. A conservative approach would be to assume a constant level of predation threat for a given fishery and focus on examining the capacity of released fish to evade predators and the accompanying rates of predator-induced mortality. PRP is a unique contributor to mortality because it is probably most often characterized by a short period (minutes or hours) of risk, which could simply be overcome by using pre-release techniques that reduce the impairment of fish being released (Farrell et al. 2001; Broadhurst et al. 2009).”

Future studies that can be used to assess the presence of delayed sublethal fitness effects in fisheries escapees and discards include allostasis, biotelemetry, reproductive success of individuals, measurement of genetic material contributions to next generations, and tank or net pen holding studies to determine behavior, growth rates, and reproduction. In all these types of studies, ongoing collection of fisheries observer data on reflex impairment and injury using a vitality scoring system (RAMP) would be needed to link vitality scores of at-release discards or escapees back to fitness outcomes for individuals.