ICES Journal of Marine Science (2016), 73(9), 2356–2363. doi:10.1093/icesjms/fsw087

Original Article An assessment of post-release mortality for a commonly discarded deep-sea isopod (Bathynomus giganteus) using Downloaded from reflex impairment

Brendan Talwar1,*, Edward J. Brooks2,‡, and R. Dean Grubbs1

1Florida State University Coastal and Marine Laboratory, 3618 Hwy 98, St Teresa, FL 32358, USA http://icesjms.oxfordjournals.org/ 2Shark Research and Conservation Program, Cape Eleuthera Institute, PO Box EL-26029, Eleuthera, The Bahamas *Corresponding author: tel: þ5027770847; e-mail: [email protected] ‡C/O Cape Eleuthera Island School, PO Box EL-26029, Rock Sound, Eleuthera, The Bahamas and USA Talwar, B., Brooks, E. J., and Dean Grubbs, R. An assessment of post-release mortality for a commonly discarded deep-sea isopod (Bathynomus giganteus) using reflex impairment. – ICES Journal of Marine Science, 73: 2356–2363. Received 4 January 2016; revised 20 April 2016; accepted 25 April 2016.

Estimates of post-release mortality (PRM) rates for discarded bycatch are largely unknown across marine fisheries and represent a substantial at East Carolina University on September 29, 2016 source of uncertainty when estimating total fishery mortality. One way to predict PRM is through the use of reflex action mortality predictors (RAMP), whereby the presence or absence of target reflexes and known post-release fate are used to create a delayed mortality model. We employed reflex impairment assessments in concert with post-capture caging and video monitoring to predict 5-d PRM rates for the deep- sea giant isopod Bathynomus giganteus, a common bycatch species in numerous deepwater fisheries worldwide, and also considered the fac- tors contributing to mortality. Mortality rates 5 d post-capture ranged from 50 to 100% and both RAMP scores and time at the surface were significant predictors of mortality, although our conclusions regarding the effect of surface time are limited. In-cage video documented little movement within the 24-h monitoring period following capture, and it appeared that surviving individuals often fed within the holding period after cage deployment. Our results suggest that PRM in B. giganteus is common and that this unaccounted source of mortality should be quantified for other deep-sea captured as bycatch. Keywords: Bathynomus giganteus, bycatch, deep-sea, discard mortality, isopod, post-release mortality, RAMP, reflex action mortality predictor, reflex impairment, the Bahamas.

Introduction taxa in question (Davis, 2002). In general there is a lack of data Bycatch, defined as non-target species that are discarded or un- regarding the contribution of discard mortality to total fishery managed, makes up an estimated 40.4% of total catches for global mortality, which poses a serious challenge to marine fisheries marine fisheries (Davies et al., 2009), and represents a threat to management (Hall et al., 2000; Davis, 2002). the sustainable management of marine ecosystems (Crowder and Increasingly, commercial fisheries are expanding to the deep- Murawski 1998; Harrington et al., 2005, Kelleher, 2005). As a re- sea (Morato et al., 2006; Watson and Morato, 2013) where species sult of low economic value or harvest prohibitions (Harrington are generally highly susceptible to overexploitation due to their et al., 2005), many individuals caught as bycatch are discarded very conservative life histories (Large et al., 2003; Simpfendorfer alive with unknown post-release mortality (PRM) rates which and Kyne, 2009; Norse et al., 2012). Individuals captured at depth often vary drastically depending on the fishery, gear type, and undergo a forced ascent from hundreds of metres deep to the

VC International Council for the Exploration of the Sea 2016. All rights reserved. For Permissions, please email: [email protected] Assessment of PRM for a commonly discarded deep-sea isopod 2357 surface facing extreme thermal (17–30 C), barometric unpublished data) and stomach content analysis has suggested a (>80 atm), and photic stress (Brooks et al., 2015) and, if dis- rather wide diet for a strict scavenger (Briones-Fourzan and carded alive, must return to depth after experiencing a suite of Lozano-Alvarez, 1991; Barradas-Ortiz et al.,2003). sub-lethal impairments that may increase the chance of PRM or Here, we quantify PRM of B. giganteus and assess reflex im- predation (Wilson et al., 2014). These sub-lethal effects can in- pairment to create a framework for predicting discard mortality clude physiological disturbance and/or physical injury, which can for this common bycatch species in deep-sea fisheries. We also affect behaviour, growth, reproduction and immune function, ul- identify factors contributing to PRM, investigate the effect of timately reducing fitness in the long term (reviewed by Wilson emersion on PRM, and provide insights into the post-release et al., 2014). In invertebrates, the magnitude of these sub-lethal locomotion and feeding behaviours of individuals in experimen- effects often depends on gear type, capture duration, emersion tal enclosures at the seafloor. time, and temperature (Giomi et al., 2008; Haupt et al., 2006; Ridgway et al., 2006; Wilson et al., 2014). In deep-water fisheries, Methods the combined effect of high magnitude stressors experienced dur- ethics ing capture, ascent, and descent is likely to result in higher PRM Research was carried out under the Cape Eleuthera Institute (CEI)

rates in these taxa than in their shallower counterparts. research permit numbers MAF/FIS/17 and MAF/FIS/34 issued by Downloaded from To predict the PRM rates of crustaceans, recent field studies the Bahamian Department of Marine Resources and in accordance have been successful in using reflex action mortality predictors with the CEI animal care protocols developed within the guidelines (RAMP) (Stoner et al., 2008; Stoner, 2009, 2012a,b; Urban, 2015) of the Association for the Study of Animal Behaviour and the whereby the presence or absence of reflexes at-vessel can be used Animal Behaviour Society (Rollin and Kessel, 1998). to quickly gauge an individual’s probability of survival. Reflex im- Field work was conducted May–June 2015 in northeastern pairment scores (the sum of negative reflexes for a single assess- Exuma Sound, 2.5 km west of Powell Point on Eleuthera, The http://icesjms.oxfordjournals.org/ ment) are robust in that they reflect the cumulative effects of Bahamas (24.541N, 76.121W), where water >1000 m deep is various types of stressors to multiple bodily systems (Stoner, accessible within 4 km of shore (Brooks et al., 2015). One trap 2012a,b). After fitting delayed mortality curves to the observa- and cage trial were conducted every 7 d across the study period. tions, which describe the relationship between reflex impairment scores and PRM rates (reviewed by Stoner, 2012a), RAMP can be Evaluating reflexes employed to predict mortality without containment, tagging, or Bathynomus giganteus were routinely captured in ongoing trap tracking, as long as relevant stressors are comparable (Barkley surveys between 800 and 1000 m deep at our capture site and im- and Cadrin, 2012; Yochum et al., 2015). Although reflex impair- mediately examined to identify reflexes that were lost over time ment scores generated from RAMP assessments are a common while submerged in deck tanks prior to the initiation of this at East Carolina University on September 29, 2016 tool used to predict mortality across a wide range of marine spe- study. Target reflexes were chosen based on being (i) quickly and cies such as decapod crustaceans (Stoner et al., 2008, Stoner, easily tested in the field, (ii) consistent and stereotypic, (iii) able 2012b, Urban, 2015), teleosts (Davis and Ottmar, 2006, Davis, to be scored as binary positive or negative responses, and (iv) un- 2007, 2010, Raby et al., 2012), and elasmobranchs (Danylchuk ambiguous across experimenters. Based on these criteria, six et al., 2014; Gallagher et al., 2014), no methods to predict mortal- reflexes were selected for field trials (Table 1). ity have been previously tested for deep sea taxa or for marine isopods despite their prevalence as bycatch in emerging deep-sea fisheries (e.g. Perez and Wahrlich, 2005). Field trials The deep dwelling giant isopod Bathynomus giganteus is the pri- Individuals were captured in a circular 2.5 m diameter trap mary bycatch species in the trap fishery for golden crabs (Chaceon made of 3.8 3.8 cm polyvinyl chloride (PVC)-coated wire fenneri)(Perry et al., 1995; Harper et al., 2000) and common mesh. A rectangular bait cage filled with 1.4 kg of miscellaneous bycatch in the deep trawl fishery for rock shrimp (Sicyonia brevir- fish parts and/or little tunny (Euthynnus alletteratus)wassus- ostris) and royal red shrimp (Hymenopenaeus robustus)inthe pended in the center of the trap and multiple layers of fine wire northern Gulf of Mexico (D. Grubbs, pers. obs.)aswellasthe mesh prevented captured individuals from accessing the bait. A monkfish (Lophius gastrophysus) gillnet fishery in southern Brazil single trap per trial (n ¼ 4) was attached to 1000 m of line and (Perez and Wahrlich, 2005). It has also been documented as set for 24 h before being hauled to the surface at 0.3 m/s. bycatch in Brazilian deep water shrimp trawl fisheries (Perez et al., Bathynomus giganteus capture density varied from 15 to 43 indi- 2013) while a close relative, Bathynomus doederleini,iscommon viduals per trap. bycatch of Taiwanese hagfish (Eptatretus spp./Paramyxine spp.) Once on the boat, isopods were transferred to coolers filled with trap fisheries (Soong and Mok, 1994). Bathynomus giganteus has water at ambient sea surface temperature (26–28 C) in full sun- also been recently targeted in Japanese fisheries to fuel a new de- light. They were then randomly sorted into two treatment groups: mand for isopod-infused rice crackers (D. Grubbs, pers. obs.). The those exposed to 15 min of air at 27–28 C and those retained in species inhabits depths from 359 to 1050 m off of the Yucatan the coolers with water changes every 5 min (hereafter termed ‘con- Peninsula, Mexico (Barradas-Ortiz et al.,2003), 349–733 m in the trols’). During this period, we placed unique combinations of southern Gulf of Mexico (Briones-Fourzan and Lozano-Alvarez, multi-coloured 15 cm zip ties on the pereopods of each individual 1991), 594–1415 m in northeastern Exuma Sound, The Bahamas for identification. Zip ties were affixed with the minimal tightness (M. Violich, unpublished data) and to at least 1,735 m in the required to avoid tag loss and tag ends were removed to allow for northern Gulf of Mexico (D. Grubbs, unpublished data). Although freedom of movement and pereopod extension. B. giganteus primarily scavenges on fish and squid remains RAMP assessments were then conducted on randomly selected (Barradas-Ortiz et al.,2003), active predation of a small squaloid individuals, alternating between an animal exposed to air fol- shark has been observed in an experimental enclosure (B. Talwar, lowed by a control individual. Once the six reflexes (Table 1) 2358 B. Talwar et al.

Table 1. Candidate reflexes identified for assessing condition of trap-caught Bathynomus giganteus. Reflex Test Orientation Positive response Negative response Leg retraction Extend first paired In water, ventral Pereopods resist extension and/or Pereopods fall limply back into the pereopods side up retract strongly to the start start position and present no position resistance to extension Mouth closure Open mandibles with a In water, ventral Mandibles resist opening and, upon Mandibles fall limply into the start blunt probe, then side up removal of probe, close quickly position and show no resistance remove the probe and tightly or open and close to opening rapidly Pleopod Brush the pleopods with In water, ventral Pleopods undulate or, if contracted Pleopods fall limply to rest flat movement a blunt probe towards side up inward towards the midline of against the body and show no the mouth the carapace, resist stimulation movement Pereopod Manually stimulate the Out of water, Pereopods move spontaneously Pereopods are motionless after movement pereopods with a ventral side up when stimulated stimulation blunt probe Antennae Manually extend both Out of water, Antennae move after stimulation or Antennae hang limply and exhibit Downloaded from extension antennae straight out ventral side up rapidly return to the start no response to stimulation in front of the body position Telson flexion Pull the telson downward Out of water, Telson resists the flattening motion Telson exhibits no resistance or until it is at a > 180 ventral side up and/or curls upward past the upward motion angle to the body original start postion The test for each reflex is the action required to elicit a given response (i.e. positive or negative) within 5 seconds of testing, listed in the same order as they http://icesjms.oxfordjournals.org/ were conducted in the field. were assessed, each animal was assigned a carapace redness score A generalized linear model with a binomial probability distribu- from 0 to 2, which was previously hypothesized to vary with con- tion and a logit link function was fitted to the data using Firth ad- dition, and examined for physical injury. justed maximum likelihood estimation (Firth, 1993) with total 5-d While tagging procedures and RAMP assessments were con- mortality as the binary response variable (either dead or alive) and ducted, the trap was converted into a cage by sealing the two en- nine possible explanatory variables included as predictors. trances with 1 1 cm wire mesh. The bait cage was also opened Categorical variables included emersion, sex, carapace redness to allow access to the fish remains. Last, two programmable white score (0, <10% red; 1, between 10 and 60% red; 2, between 60 and at East Carolina University on September 29, 2016 LED lights (“Lanternfish”, Blue Turtle Engineering, Florida, 100% red), and physical injury (present or absent). Continuous United States) and a GoPro Hero 3 White Edition camera pro- variables included surface time (the time interval between a trap grammed with a Time Lapse Intervalometer (Cam-Do, United reaching the boat and the associated cage being lowered to depth States) in a Scout Pro H3 deep-sea housing (Group B from the surface), reflex impairment score (i.e. sum of negative Distribution Inc, Florida, United States) were synced to record reflexes that were selected using contingency analysis), carapace for 4 min every half hour for 24 h and attached to the inside of total length (TL), and the interactions between both surface time the cage before deployment. and reflex impairment score and TL and reflex impairment score. Three 5 lb floats were attached via stainless steel longline snaps These parameters were evaluated using the Shapiro-Wilk test for at 20, 60, and 80 m above the cage and an archival temperature normality and outliers identified and removed using diagnostic and depth recorder (Lotek LAT1400, Newfoundland, Canada) in- plots. The order of RAMP assessments across individuals was not side of a PVC housing was attached just above the cage bridle included in the model as were chosen haphazardly and as- prior to cage deployment at the capture location. Floats prevented sessments were brief (<1 min). A maximal model including all ex- the line from tangling with the cage or getting stuck on the bot- planatory variables was fitted and non-significant factors were tom while the TDR recorded temperature and depth every 4 s for removed in stepwise fashion while evaluating the increases in devi- roughly 30 h allowing for the calculation of descent and ascent ance and Akaike Information Criterion (AIC) with each removal. rates. The model was reduced until the minimal adequate model re- After 5 d at the seafloor, cages were hauled to the surface and mained, which included only significant terms or terms that, once isopods were assessed for mortality and condition using the same removed, caused a significant increase in AIC or deviance (see reflex impairment assessments as described previously before Crawley, 2007). A Student’s t-test was used to look for differences being euthanized. Last, animals were inspected for physical inju- between reflex impairment scores before and after caging. All of ries caused by the caging process and dissected to assess feeding. the analyses were performed using JMP 7.0.1 (SAS Institute, Cary, NC, United States) and R Programming Language (R Data analysis Development Core Team, 2008) and the level of significance for Contingency analysis was used to model reflex presence/absence the aforementioned tests was a < 0.05. against mortality for animals pooled from both control and air exposed groups. Pearson’s Chi Square tests were then used to test Results the null hypothesis that the distribution of positive or negative Capture characteristics reflexes was equal. Those reflexes that were distributed signifi- A total of 100 isopods of a mean TL of 28 cm (64.7 SD) were cap- cantly differently than expected (using an alpha value of a < 0.1) tured during four trials, including 77 males and 23 females. Traps were used in all other analyses for predicting mortality. were set at a mean depth and temperature of 845 m (627.5 SE) Assessment of PRM for a commonly discarded deep-sea isopod 2359 and 7.5 C(6 3.7 SE) on a muddy bottom with no benthic Post-capture behaviour structure. Across the four cage deployments, only seven individuals were Physical injury was uncommon, occurring in only 13% of indi- observed moving during the 24-h video monitoring periods. The viduals prior to caging, and did not appear significant. Of these inju- first observed movements were always either pleopod or pereopod ries, nine were broken pereopod or antennae tips, three were slight twitching. During one deployment, five animals started to move carapace breaks along the margins, and one was a small tear to a sin- within 2 h of reaching the sea floor, and one individual even began gle pleopod. No at-vessel mortality was observed prior to caging. scavenging on a dead conspecific and on fish remains shortly thereafter. The only other two isopods that exhibited any life were Reflex action mortality predictors observed moving after 8.5 and 10 h had elapsed during two other Presence or absence of the antennae extension and pleopod cage deployments. Swimming behaviours were irregular, if they movement reflexes could not differentiate between survivors and occurred at all, and were characterized by an inability to orient ef- mortalities based on Contingency Analysis (x2 ¼ 2.336, p > 0.1 fectively before landing inverted on the cage floor after a short for antennae extension; x2 ¼ 1.597, p > 0.1 for pleopod move- burst of activity. Furthermore, recovery from capture appeared ment), and were thus not included in the reflexes used to predict very slow, with only 24% of surviving isopods exhibiting any sign mortality or in comparisons between control and treatment of movement within the first 24 h following cage deployment. Downloaded from groups. In all trials, small (<5 cm) isopods entered the cage through Animals exposed to 15 min of air were more impaired than the mesh walls within the first hour and swam haphazardly those not exposed (Table 2); however, there was no significant throughout the cage, settling on both the bait cage and less fre- difference in 5-d mortality rates between these groups. Across quently on unmoving B. giganteus. Live, non-caged B. giganteus subgroups, the most commonly lost (i.e. negatively scored) also appeared on the outside of the cage within 3 h and appeared http://icesjms.oxfordjournals.org/ reflexes were pereopod movement and mouth closure, followed highly active, regularly swimming or crawling on the cage walls by telson flexion and leg retraction. Leg retraction was therefore with constant antennae movement and normal, highly oriented the least sensitive reflex to capture stress and the combination of swimming behaviour. Many were also observed excavating in the capture and emersion stress. muddy benthos in an attempt to access fish remains or dead iso- 2 Presence or absence of mouth closure (x ¼2.908, p ¼ 0.08), pods from beneath the cage floor, at times concentrating around 2 2 leg retraction (x ¼7.059, p ¼ 0.008), telson flexion (x ¼ 8.554, clusters of unmoving isopods within the cage. None showed signs 2 p ¼ 0.003), and pereopod movement (x ¼ 10.005, p ¼ 0.001) of aversion to the lights. These high levels of activity are in con- could differentiate between survivors and mortalities and were trast to caged individuals, which moved very little, if at all, during thus used to create a mortality curve based on the sum (0–4) of the 24-h post-capture observation period. lost reflexes (Figure 1). This curve predicts PRM rates of 50– Stomachs were present in 71% (n ¼ 71) of individuals after at East Carolina University on September 29, 2016 100% depending on impairment score. the 5-d period, while 29% (n ¼ 29) were completely devoid of stomachs or internal organs, suggesting that they were scavenged Factors affecting mortality or preyed upon. Of the 71 isopods with stomachs, 42% (n ¼ 29) Logistic regression suggested that a model including only surface survived the trials and 64% (n ¼ 45) had stomach contents time and reflex impairment score provided the best fit to binomial (Figure 2). Of the 29 that survived, 93% (n ¼ 27) had stomachs mortality data (AICfull model ¼ 118.6, AICminimal model ¼107.7), contents. while sex, physical injury, TL, carapace redness score, and emer- sion were poor predictors of 5-d mortality (Tables 3 and 4). Mean surface time was 56 min, and ranged from 30 to 81 min across tri- als. Although reflex impairment scores and surface time were cor- related (r2 ¼ 0.32, d.f. ¼ 99, p < 0.01) and TL and reflex impairment scores were weakly correlated (r2 ¼ 0.05, d.f. ¼ 99, p ¼ 0.01), the interactions between these terms were not signifi- cant and were subsequently removed from the model.

Table 2. Summary of negatively scored reflexes for emersion (n=50; 15 minutes) and control (n=50) groups of Bathynomus giganteus prior to caging. Air exposure No air exposure Treatment type No. of %of No. of %of negative negative negative negative Reflex responses responses responses responses Leg retraction 15 13.6 9 9.7 Figure 1. Mortality of giant isopods as a function of reflex impairment Telson flexion 26 23.6 23 24.7 score (sum of negative responses from reflex assessments). Each point Mouth closure 28 25.5 25 26.9 represents the calculated 5-d mortality rate for individuals with a given Pereopod movement 41 37.3 36 38.7 impairment score, pooled across treatment groups. The solid line Totals 110 100 93 100.0 shows the curved fit from logistic regression which represents the Number count and proportion of impairment for each reflex are shown as likelihood of mortality for an individual with a given reflex impairment the percentage of total negative responses for each group. score. 2360 B. Talwar et al.

Table 3. Full model and minimal adequate model from backwards stepwise GLM analysis to describe 5-day mortality in Bathynomus giganteus based on seven initial model parameters and two interaction terms. Parameter Estimate S.E. z-value Pr(>jzj) Full model Intercept 0.846 2.315 0.365 0.715 Sex 0.372 0.657 0.567 0.571 Physical injury 0.550 0.853 0.645 0.519 Emersion 0.391 0.560 0.699 0.485 TL 0.039 0.107 0.359 0.719 TL*Reflex impairment score 0.001 0.054 0.019 0.985 Surface Time*Reflex 0.004 0.013 0.301 0.764 impairment score Carapace redness score 0.630 0.503 1.253 0.21 Figure 2. Number of B. giganteus with empty and non-empty Surface time 0.018 0.033 0.552 0.581 stomachs grouped by cage result after 5 d in experimental Downloaded from Reflex impairment score 0.446 1.092 0.409 0.683 enclosures at the seafloor. Most parsimonious model Intercept 1.53 0.631 2.426 ** Surface time 0.028 0.013 2.15 * Reflex impairment score 0.505 2.42 2.089 * http://icesjms.oxfordjournals.org/ Estimates and SEs are on a logit scale. *p < 0.05; **p < 0.02.

Table 4. Akaike Information Criterion (AIC) values and AIC weights (wi) for each GLM used to describe the 5-day mortality of Bathynomus giganteus resulting from stepwise backwards elimination of nonsignificant terms.

Model AIC wi Full model 118.56 0.00 at East Carolina University on September 29, 2016 TL* Reflex impairment score 116.56 0.01 Surface time * Reflex impairment score 114.66 0.01 Sex 112.97 0.03 Figure 3. Sum of negative responses for selected reflexes (mouth Emersion 111.45 0.07 closure, leg retraction, telson flexion, and pereopod movement) Physical injury 109.67 0.17 before and after 5 d of caging at depth for B. giganteus that survived TL 108.72 0.27 experimental trials (n ¼ 29). Carapace redness score 107.77 0.44 Most parsimonious model 107.77 0.44 to capture stress, followed by mouth closure, telson flexion, and leg Reflex impairment score 110.49 0.11 retraction. Telson flexion and leg retraction were maintained most Surface time 110.66 0.10 frequently, and are possible anti-predator responses for an impaired isopod attempting to protect its vulnerable ventral surface.

Cumulative effects of capture and cage stress Factors affecting mortality Reflex impairment scores were significantly higher after caging Surface time was the only variable other than reflex impairment (mean ¼ 1.9) than they were prior to caging (mean ¼ 1.3) in score that could predict mortality. Its effect was largely driven by those individuals that survived experimental trials (t ¼ 2.39, the extremely high 5-d mortality rate (90%) for individuals that d.f.¼ 28, p < 0.05; Figure 3). After caging, the telson flexion reflex remained at the surface for 81 min, and it should be investigated was lost most often followed by mouth closure, pereopod move- more thoroughly using set increments in the future. Here, its in- ment, and leg retraction. Pereopod movement was the only reflex clusion in the sampling design was largely a result of field con- that was present more often after the trials than before (sum of straints on gear and personnel, and conclusions regarding its negative responses¼ 15 before, 9 after). importance are limited. Surprisingly, emersion (air exposure) had no effect on mortal- Discussion ity, although previous studies have shown that emersion stress, Reflex action mortality predictors which increases with air temperature and duration, can severely Only four of six reflexes that were identified in pre-trial assessments disrupt physiological function in decapod crustaceans (Ridgway were able to differentiate between survivors and mortalities. Although et al., 2006). Ridgway et al. (2006) and Spicer et al. (1990) re- all six were stereotypic and repeatable, rough weather conditions dur- ported that acidemia due to an increase in L-lactate and haemo- ing field trials likely contributed to the inaccurate assessment of re- lymph CO2 during emersion may suggest that the Norway sponses for both pleopod movement and antennae extension. Of the ( norvegicus) cannot maintain an adequate oxygen sup- four remaining reflexes, pereopod movement was the most sensitive ply when exposed to air. Bathynomus giganteus, however, is Assessment of PRM for a commonly discarded deep-sea isopod 2361 particularly adapted to the low-oxygen environment characteris- Post-capture behaviour and cage effects tic of the deep ocean between 400 and 1000 m (Childress and Although recovery was quite slow, a high percentage of surviving Seibel, 1998), and could thus be less sensitive to a limited oxygen individuals had stomach contents, suggesting that many individ- supply. uals recovered to the point of feeding after video monitoring It is possible that temperature could be more detrimental to B. stopped. Still, numerous individuals had non-empty stomachs giganteus than air exposure or desiccation. Indeed, the thermal and did not survive the caging process, suggesting that they had gap experienced by an organism caught in the deep-sea in the failed to evacuate food eaten prior to their initial capture or that sub-tropical summer is exceptionally high (19 C in this study), they had recovered and eaten before they perished. Mortality, and studies on other crustaceans have shown that thermal stress therefore, could have taken place late in the 5-d period as a result does affect survival. For a trawl-caught portunid crab Liocarcinus of confinement stress, delayed effects of capture, or predation depurator, a thermal gap of 12–14 C resulted in 96% mortality from other small isopod species that could fit through the cage whereas a thermal gap of 0–3 C resulted in 2% mortality (Giomi material. et al., 2008). Similarly, in the trawl-caught shrimp Crangon cran- The caging process introduced a number of confounding fac- gon, holding temperatures over 20 C resulted in high mortality tors when estimating PRM rates for each reflex impairment score.

Downloaded from rates whereas temperatures between 10 and 20 C resulted in no Caging could have increased the stress on ‘released’ individuals mortality (Gamito and Cabral, 2003). Further research on the ef- and artificially elevated documented PRM rates as suggested by fect of thermal stress is certainly warranted for deep-sea crust- increased reflex impairment for surviving isopods after the se- aceans as the effect of surface time on PRM in this study could be cond haul. Alternatively, the PRM rate could have been underes- driven by this stressor. timated as the cages prevented predation from animals larger Along with thermal stress, deep-sea organisms undergo drastic than the cage mesh. Given that the isopods exhibit extremely lim- http://icesjms.oxfordjournals.org/ changes in pressure and light levels during gear retrieval. ited movement immediately after capture, and that isopods Barometric stress is not typically considered relevant for crust- released at-vessel show little sign of swimming behaviour, des- aceans (Stoner 2012a,b), although it has not been examined for cending over 800 m could take multiple hours. As such, numer- those residing in deep water. Basti et al. (2010), however, did ous predators in the water column attracted by gear retrieval show that increased hauling speed and increased capture depth could easily prey on discarded B. giganteus. Although natural negatively affected the survival of the predators of B. giganteus are not well documented, a tiger shark ( americanus) retrieved from < 200 m. Photic stress can has been found with a giant isopod in its gut (Briones-Fourzan also have deleterious effects in crustaceans (Stoner, 2012a). and Lozano-Alvarez, 1991) and presumably other large bodied Gaten (1988), for instance, showed that deep-dwelling decapods

elasmobranchs and teleosts would prey on impaired isopods in at East Carolina University on September 29, 2016 can experience damage to the photoreceptor layer and are sus- mid-water. ceptible to morphological changes (e.g. cone shape) within the eye after excessive exposure to sunlight. Similar results have been reported by Loew (1976) for the Norway lobster (N. norvegicus) Conclusions and by Meyer-Rochow (1981) for deep-sea Antarctic amphipods. Most importantly, this study found that reflex impairment scores Furthermore, Herring et al. (1999) suggested that exposure to were successful in predicting mortality for the deep-sea giant iso- submersibles’ floodlights could blind shrimp associated with pod after 5 d post-capture, with observed PRM rates ranging be- deep-sea vent communities and Nilsson and Lindstrom (1983) tween 50 and 100%. Furthermore, it suggests that a short reported that exposure to light of 1250 lux (approximately that emersion period may be of little consequence to the post-release of an overcast day) led to complete breakdown of the visual survival of this species. It also highlights the need for additional structures of the deep-sea isopod Natatolana (Cirolana) borealis. research into the effect of surface time on PRM, including a better Chamberlain et al. (1986) described the morphology of the com- understanding of the relative contributions of thermal gap, pound eye of the giant isopod examined here (B. giganteus) and pressure, and light levels on the mortality of discarded deep-sea unsurprisingly suggested any exposure to daylight causes severe crustaceans, particularly as fisheries continue to expand into the and irreversible damage to their photoreceptors. Given the low- deep-sea and bycatch interactions increase. These results further light levels where giant isopod occur, one may predict that vision underscore the prevalence of cryptic discard mortality and em- may not be an important sensory system for such deep-sea spe- phasize the need to better account for it when estimating bycatch cies; however, the complexity of the compound eyes and their mortality. forward orientation suggests they are used not only to detect light but also to estimate distance (Chamberlain et al., 1986). Thus, damage to the visual systems of deep-sea crustaceans and Acknowledgements the resultant loss of orientation could be a major source of We thank Experiment.com crowdfunding donors, the PADI delayed PRM although quantifying its effects in this study was Foundation, and the Sigma Xi Scientific Research Society for their not feasible. financial support. We also thank I Boyoucos, S Burnside, G Due to the relatively benign traps used in this study, physical Burruss, K Durglo, A Feiler, A Gokgoz, K Magnenat, G Neely, O injury was rare after the initial capture event and did not affect O’Shea, C Raguse, M Violich, and C Ward for their numerous mortality. Negative gear interactions would likely be more com- contributions in the field as well as the CEI for logistical support. mon in other capture gears (e.g. trawl or gillnet; Rose, 1999) and Lastly, we greatly appreciate J Travis and D Levitan, as well as an- could result in elevated PRM rates compared with those reported onymous reviewers, for providing welcome feedback on the here. article. 2362 B. Talwar et al.

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