Abstract
Understanding how elasmobranchs respond to stressors is imperative so that effective measures to reduce mortality be employed, whether in commercially captured animals or sharks and rays maintained in human care. Currently, reflex action mortality predictors (RAMPs) are the most reliable proxies to indicate an animal's condition state, commonly employed for both teleost and elasmobranchs. As our understanding of mortality predictors is evolving, is it necessary that traditional indicators be constantly reviewed and new proxies proposed, in order to improve the tools available for the best possible evaluation of a stressed individual. In this context, this review aimed to compile data on behavioral and visual proxies, along with the proposition of new proxies to guide professionals and assist them in identifying signs associated with alarming situations that might potentially result in the death of highly stressed individuals or sub-lethal effects at population level (migration, reproduction) that may seriously compromise the success of release measures.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abel DC, Grubbs RD (2020) Shark biology and conservation: essentials for educators, students and enthusiasts. Johns Hopkins University Press, Baltimore
Adams KR, Fetterplace LC, Davis AR et al (2018) Sharks, rays and abortion: the prevalence of capture-induced parturition in elasmobranchs. Biol Conserv 217:11–27. https://doi.org/10.1016/j.biocon.2017.10.010
Aines AC, Carlson JK, Boustany A et al (2018) Feeding habits of the tiger shark, Galeocerdo cuvier, in the northwest Atlantic ocean and gulf of Mexico. Environ Biol Fish 101:403–415. https://doi.org/10.1007/s10641-017-0706-y
Amlacher E (2012) Rigor mortis in fish. In: Borgstrom G (ed.) Fish as food, pp 385–409
Andrews PLR, Young JZ (1993) Gastric motility patterns for digestion and vomiting evoked by sympathetic nerve stimulation and 5-hydroxytryptamine in the dogfish Scyliorhinus canicula. Philos T R so Lond B 342:363–380. https://doi.org/10.1098/rstb.1993.0165
Aursand IG, Erikson U, Veliyulin E (2010) Water properties and salt uptake in Atlantic salmon fillets as affected by ante-mortem stress, rigor mortis, and brine salting: a low-field 1H NMR and 1H/23Na MRI study. Food Chem 120:482–489. https://doi.org/10.1016/j.foodchem.2009.10.041
Baremore IE, Hale LF (2012) Reproduction of the sandbar shark in the western north Atlantic ocean and gulf of Mexico. Mar Coast Fish 4:560–572. https://doi.org/10.1080/19425120.2012.700904
Bell J, Satchell G (1963) An undescribed unilateral ocular reflex in the dogfish Squalus acanthias. Aust J Exp Biol Med 41:221–234. https://doi.org/10.1038/icb.1963.22
Benoît HP, Hurlbut T, Chassé J et al (2012) Estimating fishery-scale rates of discard mortality using conditional reasoning. Fish Res 125–126:318–330. https://doi.org/10.1016/j.fishres.2011.12.004
Borgstrom G (ed) (2012) Fish as food V1: production, biochemistry, and microbiology. Elsevier, Amsterdam
Bouyoucos IA, Simpfendorfer CA, Rummer JL (2019) Estimating oxygen uptake rates to understand stress in sharks and rays. Rev Fish Biol Fisher 29:297–311. https://doi.org/10.1007/s11160-019-09553-3
Boylan SM, Harms CA, Waltzek T et al (2011) Clinical report: hyperplastic adipose lids in mackerel scad, Decapterus macarellus (Cuvier): hyperplastic adipose lids in mackerel scad. J Fish Dis 34:921–925. https://doi.org/10.1111/j.1365-2761.2011.01306.x
Braccini M, Van Rijn J, Frick L (2012) High Post-Capture Survival for Sharks, Rays and Chimaeras Discarded in the Main Shark Fishery of Australia. PLoS ONE 7:e32547. https://doi.org/10.1371/journal.pone.0032547
Brooks EJ, Sloman KA, Liss S et al (2011) The stress physiology of extended duration tonic immobility in the juvenile lemon shark, Negaprion brevirostris (Poey 1868). J Exp Mar Biol Ecol 409:351–360. https://doi.org/10.1016/j.jembe.2011.09.017
Brownscombe JW, Danylchuk AJ, Chapman JM et al (2017) Best practices for catch-and-release recreational fisheries—angling tools and tactics. Fish Res 186:693–705. https://doi.org/10.1016/j.fishres.2016.04.018
Bruce B (1992) Preliminary observations on the biology of the White Shark, Carcharodon carcharias, in South Australian waters. Mar Freshwater Res 43:1. https://doi.org/10.1071/MF9920001
Brunnschweiler JM, Andrews PLR, Southall EJ et al (2005) Rapid voluntary stomach eversion in a free-living shark. J Mar Biol Ass 85:1141–1144. https://doi.org/10.1017/S0025315405012208
Brunnschweiler JM, Nielsen F, Motta P (2011) In situ observation of stomach eversion in a line-caught Shortfin Mako (Isurus oxyrinchus). Fish Res 109:212–216. https://doi.org/10.1016/j.fishres.2011.02.005
Buddington RK, Krogdahl Å (2004) Hormonal regulation of the fish gastrointestinal tract. Comp Biochem Phys A 139:261–271. https://doi.org/10.1016/j.cbpb.2004.09.007
Butler EC, Childs A-R, Parkinson MC et al (2017) An assessment of the health and survival of fishes caught-and-released in high-energy surf zones during a South African competitive angling event. Fish Res 195:152–168. https://doi.org/10.1016/j.fishres.2017.07.002
Campbell MJ, McLennan MF, Courtney AJ et al (2018) Post-release survival of two elasmobranchs, the eastern shovelnose ray (Aptychotrema rostrata) and the common stingaree (Trygonoptera testacea), discarded from a prawn trawl fishery in southern Queensland Australia. Mar Freshwater Res 69:551. https://doi.org/10.1071/MF17161
Carrier JC, Musick JA, Heithaus MR (eds) (2012) Biology of sharks and their relatives. CRC Press, Boca Raton
Castro JI, Sato K, Bodine AB (2016) A novel mode of embryonic nutrition in the tiger shark, Galeocerdo cuvier. Mar Biol Res 12:200–205. https://doi.org/10.1080/17451000.2015.1099677
Cavalcante DG, Gallo H, de Sousa OM et al (2016) Aspectos da reprodução e primeiro registro de distocia em raia-ticonha (Rhinoptera bonasus). Bol Inst Pesca 42:710–718. https://doi.org/10.20950/1678-2305.2016v42n3p710
Chang C-H, Chiao C-C, Yan HY (2009) The structure and possible functions of the milkfish Chanos chanos adipose eyelid. J Fish Biol 75:87–99. https://doi.org/10.1111/j.1095-8649.2009.02266.x
Charbeneau GREG (2004) Physiological and behavioral changes to elasmobranchs in controlled environments. In: Smith M, Warmolts D, Thoney D, Hueter R (eds) Elasmobranch husbandry manual: captive care of sharks, rays, and their relatives. Ohio Biological Survey, Columbus, pp 261–270
Christie BL (2012) Intestinal eversion in the atlantic sharpnose shark, Rhizoprionodon terraenovae, a behavior ubiquitous among elasmobranch fishes. Gulf Mexico Sciente 30:50–53. https://doi.org/10.18785/goms.3001.08
Clark E, von Schmidt K (1965) Sharks of the central gulf coast of florida. B Mar Sci 1:13–83
Clark TB, Papastamatiou YP, Meyer CG (2007) Intestinal eversion in a free-ranging manta ray (Manta birostris). Coral Reefs 27:61–61. https://doi.org/10.1007/s00338-007-0305-z
Cliff G, Dudley SFJ (1992) Sharks caught in the protective gill nets off Natal, South Africa. 6. The copper shark Carcharhinus brachyurus (Günther). S Afr J Mar Sci 12:663–674. https://doi.org/10.2989/02577619209504731
Cliff G, Thurman GD (1984) Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp Biochem Phys A 78:167–173. https://doi.org/10.1016/0300-9629(84)90111-7
Cliff G, Dudley SFJ, Davis B (1990) Sharks caught in the protective gill nets off Natal, South Africa. 3. The shortfin mako shark Isurus oxyrinchus (Rafinesque). S Afr J Mar Sci 9:115–126. https://doi.org/10.2989/025776190784378808
Colbachini H, Gutierrez RC, Pizzutto CS et al (2018) A new report on the clasper movements of a captive Sand Tiger Shark Carcharias taurus (Lamniformes: Odontaspididae) and a possible reason for the behaviour. J Threat Taxa 10:12577–12581. https://doi.org/10.11609/jott.3852.10.11.12577-12581
Cooke SJ, Bergman JN, Madliger CL et al (2021) One hundred research questions in conservation physiology for generating actionable evidence to inform conservation policy and practice. Conserv Physiol 9:coab009. https://doi.org/10.1093/conphys/coab009
Cortés Enric, Papastamatiou Yannis, Carlson John, Ferry-Graham Lara, Wetherbee Bradley (2008) An overview of the feeding ecology and physiology of elasmobranch fishes. In: Kapoor B (ed) Feeding and digestive functions in fishes. Science Publishers, pp 393–443. https://doi.org/10.1201/b10749-10
Crooks N (2011) Sexual and seasonal dimorphisms in the dermal, dental, and ampullary structures of the lesser-spotted catshark, Scyliorhinus canicula. Dissertation, University of Portsmouth
Crow GL, Howe JC, Uchida S et al (1990) Protrusion of the valvular intestine through the cloaca in sharks of the family carcharhinidae. Copeia 1990:226. https://doi.org/10.2307/1445839
Crow GL, Brock JA, Howe JC et al (1991) Shark bite wounds of the valvular intestine: the cause of an acute mortality syndrome of captive blacktip reef sharks, Carcharhinus melanopterus. Zoo Biol 10:457–463. https://doi.org/10.1002/zoo.1430100604
Cusack L, Field CL, Hoopes L et al (2016) Comparison of pre- and postquarantine blood chemistry and hematology values from wild-caught Cownose rays (Rhinoptera bonasus). J Zoo Wildl Med 47:493–500. https://doi.org/10.1638/2015-0267.1
Danylchuk AJ, Suski CD, Mandelman JW et al (2014) Hooking injury, physiological status and short-term mortality of juvenile lemon sharks (Negaprion bevirostris) following catch-and-release recreational angling. Conserv Physiol 2:036–036
Dapp DR, Walker TI, Huveneers C et al (2016) Respiratory mode and gear type are important determinants of elasmobranch immediate and post-release mortality. Fish Fish 17:507–524. https://doi.org/10.1111/faf.12124
Davis MW (2007) Simulated fishing experiments for predicting delayed mortality rates using reflex impairment in restrained fish. ICES J Mar Sci 64:1535–1542. https://doi.org/10.1093/icesjms/fsm087
Davis MW (2010) Fish stress and mortality can be predicted using reflex impairment. Fish Fish 11:1–11. https://doi.org/10.1111/j.1467-2979.2009.00331.x
Dean MN, Motta PJ (2004) Feeding behavior and kinematics of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Zoology 107:171–189. https://doi.org/10.1016/j.zool.2004.04.002
Doherty PD, Enever R, Omeyer LC et al (2022) Efficacy of a novel shark bycatch mitigation device in a tuna longline fishery. Curr Biol 32(22):R1260–R1261. https://doi.org/10.1016/j.cub.2022.09.003
Dudley SFJ, Cliff G (1993) Sharks caught in the protective gill nets off Natal, South Africa. 7. The blacktip shark Carcharhinus limbatus (Valenciennes). S Afr J Mar Sci 13:237–254. https://doi.org/10.2989/025776193784287356
Dudley S, Cliff G, Zungu M et al (2005) Sharks caught in the protective gill nets off KwaZulu-Natal, South Africa. 10. The dusky shark Carcharhinus obscurus (Lesueur 1818). Afr J Mar Sci 27:107–127. https://doi.org/10.2989/18142320509504072
Ellis JR, McCully Phillips SR et al (2016) A review of capture and post-release mortality of elasmobranchs: capture mortality of elasmobranchs. J Fish Biol 90:653–722. https://doi.org/10.1111/jfb.13197
Enever R, Catchpole TL, Ellis JR et al (2009) The survival of skates (Rajidae) caught by demersal trawlers fishing in UK waters. Fish Res 97:72–76. https://doi.org/10.1016/j.fishres.2009.01.001
Favaro B, Cote IM (2015) Do by-catch reduction devices in longline fisheries reduce capture of sharks and rays? A Global Meta-Anal Fish Fish 16(2):300–309. https://doi.org/10.1111/faf.12055
Forlano PM, Maruska KP, Sower SA et al (2000) Differential distribution of gonadotropin-releasing hormone-immunoreactive neurons in the stingray brain: functional and evolutionary considerations. Gen Comp Endocr 118:226–248. https://doi.org/10.1006/gcen.2000.7467
Frick LH, Reina RD, Walker TI (2009) The Physiological response of port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity. N Am J Fish Manage 29:127–139. https://doi.org/10.1577/M08-031.1
Friedman MHF (1935) The function of the claspers and clasper-glands in the skate. J Biol Board Can 1:261–268. https://doi.org/10.1139/f35-010
Fuller LN (2019) Description and alleviation of the stress response in Atlantic sharpnose sharks (Rhizoprionodon terraenovae), white-spotted bamboo sharks (Chiloscyllium plagiosum), and golden shiners (Hotemigonus crysoleucas). Dissertation, University of Mississippi
Gallagher A, Serafy J, Cooke S et al (2014) Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release. Mar Ecol Prog Ser 496:207–218. https://doi.org/10.3354/meps10490
George RH, Steeil J, Baine K (2017) Diagnosis and treatment of common reproductive problems in elasmobranchs. In: Smith M, Warmolts D, Thoney D, Hueter R, Murray M, Ezcurra J (eds) The elasmobranch husbandry manual ii recent advances in the care of sharks, rays and their relatives. Ohio Biological Survey, Columbus
Gervais CR, Brown C (2021) Impact of conspecific necromones on the oxygen uptake rates of a benthic elasmobranch. Anim Behav 174:1–8. https://doi.org/10.1016/j.anbehav.2021.01.009
Gilbert PW, Oren ME (1964) The selachian nictitans and subocular fold. Copeia 1964:534. https://doi.org/10.2307/1441519
Gordon I (1993) Pre-copulatory behaviour of captive sandtiger sharks, Carcharias taurus. In: Wourms JP, Demski LS (eds) The reproduction and development of sharks, skates, rays and ratfishes. Springer, Dordrecht, pp 159–164
Grande M, Murua J, Ruiz J et al (2019) Bycatch mitigation actions on tropical tuna purse seiners: best practices program and bycatch releasing tools. IATTC 9th meeting of the working group on bycatch. Inter-American Tropical Tuna Commission, San Diego California
Grigg GC (1970) Water flow through the gills of port jackson sharks. J Exp Biol 52:565–568. https://doi.org/10.1242/jeb.52.3.565
Gruber SH, Keyes RS (1981) Keeping sharks for research. In: Hawkins AD (ed) Aquarium system. Academic Press, Harcourt Brace Jovanovich, London United Kingdom, pp 373–402
Gruber SH, Schneiderman N (1975) Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris). Behav Res Meth Instr 7:430–434. https://doi.org/10.3758/BF03201554
Hallett C (2003) The diet of Etmopterus baxteri and Etmopterus species B (Squalidae) from waters off Tasmania. Dissertation, Bangor
Hammerschlag N, Sulikowski J (2011) Killing for conservation: the need for alternatives to lethal sampling of apex predatory sharks. Endang Species Res 14:135–140. https://doi.org/10.3354/esr00354
Harrison IJ (2002) Order Mugiliformes, Mugilidae. In: Carpenter KE, De Angelis N (eds) The living marine resources of the western central Atlantic. Food and Agriculture Organization of the United Nations, Rome
Henningsen AD (1999) Levels of recirculating reproductively-related steroid hormones in female elasmobranchs. Implications for reproduction in a captive environment. Aquarium Sci Conserv 2:97–116
Henningsen AD, Whitaker BR, Walker ID (2005) Protrusion of the valvular intestine in captive smalltooth sawfish and comments on pristid gastrointestinal anatomy and intestinal valve types. J Aquat Anim Health 17:289–295. https://doi.org/10.1577/H04-063.1
Horodysky AZ, Graves J (2005) Application of pop-up satellite archival tag technology to estimate postrelease survival of white marlin (Tetrapturus albidus) caught on circle and straight-shank (“ J”) hooks in the western North Atlantic recreational fishery. Fish Bull 103(1):84
Hughes GM (1960) A comparative study of gill ventilation in marine teleosts. J Exp Biol 37(1):28–45. https://doi.org/10.1242/jeb.37.1.28
Jerome JM, Gallagher AJ, Cooke SJ et al (2018) Integrating reflexes with physiological measures to evaluate coastal shark stress response to capture. ICES J Mar Sci 75:796–804. https://doi.org/10.1093/icesjms/fsx191
Jung-Schroers V, Hellmann J, Steinhagen D (2015) Birth complications and cesarean section in a blacktip reef shark (Carcharhinus melanopterus). Austin J Vet Sci Anim Husb 2:1017
Kabasakal H (2010) Post-release behavior and anthropogenic injuries of the bluntnose sixgill shark, Hexanchus griseus (Bonnaterre, 1788) (Chondrichthyes: Hexanchidae) in Turkish waters. Ann Ser Hist Nat 20:39
Kerstetter DW, Graves JE (2006) Survival of white marlin (Tetrapturus albidus) released from commercial pelagic longline gear in the western North Atlantic. Fish Bull 104(3):434
Knotek RJ, Rudders DB, Mandelman JW et al (2018) The survival of rajids discarded in the New England scallop dredge fisheries. Fish Res 198:50–62. https://doi.org/10.1016/j.fishres.2017.10.015
Laptikhovsky VV (2004) Survival rates for rays discarded by the bottom trawl squid fishery off the Falkland Islands. Fish Bull 102:757–759
Leite RD, Wosnick N, Giareta EP et al (2020) Evidence of dystocia in a free-ranging cownose ray Rhinoptera bonasus (Elasmobranchii, Rhinopteridae). Bol Lab Hidrobiol. https://doi.org/10.18764/1981-6421e2020.13
Levine RP, Monroy JA, Brainerd EL (2004) Contribution of eye retraction to swallowing performance in the northern leopard frog, Rana pipiens. J Exp Biol 207:1361–1368. https://doi.org/10.1242/jeb.00885
Litvinov FF (2006) On the role of dense aggregations of males and juveniles in the functional structure of the range of the blue shark Prionace glauca. J Ichthyol 46:613–624. https://doi.org/10.1134/S0032945206080091
Long JA, Mark-Kurik E, Johanson Z et al (2015) Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517:196–199. https://doi.org/10.1038/nature13825
Luer CA, Gilbert PW (1985) Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Raja eglanteria. Environ Biol Fish 13:161–171. https://doi.org/10.1007/BF00000926
Mahon J, Chua F, Newman P (2001) Successful spotted Eagle Ray (Aetobatus narinari) breeding program and details of an assisted birth. Drum Croak Spec Edit 2:104–107
Mandelman JW, Cicia AM, Ingram GW et al (2013) Short-term post-release mortality of skates (family Rajidae) discarded in a western North Atlantic commercial otter trawl fishery. Fish Res 139:76–84. https://doi.org/10.1016/j.fishres.2012.09.020
Markaida U, Sosa-Nishizaki O (2010) Food and feeding habits of the blue shark Prionace glauca caught off Ensenada, Baja California, Mexico, with a review on its feeding. J Mar Biol Ass 90:977–994. https://doi.org/10.1017/S0025315409991597
Martin RA (2007) A review of shark agonistic displays: comparison of display features and implications for shark–human interactions. Mar Freshw Behav Phy 40:3–34. https://doi.org/10.1080/10236240601154872
Martins MF, Rolim FA, Gadig OBF (2020) Report on fetal mummification in the scalloped hammerhead shark Shyrna lewini. J Fish Biol 97:309–313. https://doi.org/10.1111/jfb.14368
Mas D, Domenech B, Espinosa J et al (2010) Noninvasive measurement of eye retraction during blinking. Opt Lett 35:1884. https://doi.org/10.1364/OL.35.001884
Matsumoto R, Matsumoto Y, Ueda K et al (2019) Sexual maturation in a male whale shark (Rhincodon typus) based on observations made over 20 years of captivity. Fish Bull 117:78–86. https://doi.org/10.7755/FB.117.1-2.9
Morales P, Dunker F (1999) Suspected intestinal torsion in a blacktip reef shark (Carcharhinus melanopterus). J Zoo Wildl Med 30:170–172
Musyl MK, Gilman EL (2018) Post-release fishing mortality of blue (Prionace glauca) and silky shark (Carcharhinus falciformes) from a Palauan-based commercial longline fishery. Rev Fish Biol Fish 28(3):567–586. https://doi.org/10.1007/s11160-018-9517-2
Musyl MK, Brill R, Curran DS et al (2011) Postrelease survival, vertical and horizontal movements, and thermal habitats of five species of pelagic sharks in the central pacific ocean. Fish Bull 109:341
Myrberg AA, Gruber SH (1974) The behavior of the bonnethead shark. Sphyrna Tiburo Copeia 1974:358. https://doi.org/10.2307/1442530
Noakes DE, Parkinson TJ, England GC et al (2001) Arthur’s veterinary reproduction and obstetrics. Saunders Elsevier, London, p 844
Poisson F, Séret B, Vernet A-L et al (2014) Collaborative research: development of a manual on elasmobranch handling and release best practices in tropical tuna purse-seine fisheries. Mar Pol 44:312–320. https://doi.org/10.1016/j.marpol.2013.09.025
Poscai AN, de Sousa RB, da Silva Casas AL et al (2017) Microscopic aspects of the nictitating membrane in Carcharhinidae and Sphyrnidae sharks: a preliminary study. Zoomorphology 136:359–364. https://doi.org/10.1007/s00435-017-0351-1
Prado AC, Wosnick N, Adams K et al (2021) Capture-induced vulnerability in male Shortnose guitarfish during their reproductive period. Anim Conserv 25:233–243. https://doi.org/10.1111/acv.12734
Pratt HL, Carrier JC (2001) A Review of Elasmobranch Reproductive Behavior with a Case Study on the Nurse Shark, Ginglymostoma cirratum. Env Biol Fish 60:157–188. https://doi.org/10.1023/A:1007656126281
Randall J (1977) Contribution to the biology of the withetip reep shark (Triaenodon obesus). Pac Sci 31:143–164
Rangel BS, Castro Ribeiro D, Chagas JMA et al (2020) Effects of biological traits on capture-induced parturition in a freshwater stingray and perspectives for species management. J Fish Biol 97:546–551. https://doi.org/10.1111/jfb.14412
Rangel BS, Vignoli R, Xavier N et al (2021) New records on intestinal eversion in a free-ranging nurse shark (Ginglymostoma cirratum) and a free-ranging, breaching-spotted eagle ray (Aetobatus narinari). Environ Biol Fish 104:1353–1357. https://doi.org/10.1007/s10641-021-01160-1
Razzaque SA, Khan MM, Shahid U (2020) Safe handling & release for gillnet fisheries for whale shark, manta & devil rays and sea turtles. IOTC-2020-WPEB16–26_Rev1. Indian Ocean Tuna Commission
Revill AS, Dulvy NK, Holst R (2005) The survival of discarded lesser-spotted dogfish (Scyliorhinus canicula) in the western English channel beam trawl fishery. Fish Res 71:121–124. https://doi.org/10.1016/j.fishres.2004.07.006
Rincon G, Vooren CM (2007) A record of abortion in the school sharks Galeorhinus galeus (Carcharhiniformes, Triakidae) captured on the continental shelf off southern Brazil. PANAMJAS 2:53–54
Ritter E, Compagno L (2013) Clasper Flaring: Maintenance Behavior, or a Normally Hidden Feature of Male Whitetip Reef Sharks, Triaenodon obesus? TOFISHSJ 6:10–12. https://doi.org/10.2174/1874401X01306010010
Rodrigues AFS, de Rangel B, Wosnick N et al (2019) Report of injuries in batoids caught in small-scale fisheries: implications for management plans. Oecol Aust 23(01):78–89. https://doi.org/10.4257/oeco.2019.2301.07
Rosa-Molinar E, Williams CS, Collard S (1983) Fetal mummification in the sandbar shark, Carcharhinus plumbeus (Nardo, 1827). J Wildl Dis 19:156–158. https://doi.org/10.7589/0090-3558-19.2.156
Sandoval-Castillo J, Villavicencio-Garayzar C (2008) Fetal mummification in silky shark (Carcharhinus falciformis) from the Gulf of California, Mexico. Braz Arch Biol Technol 51:551–554. https://doi.org/10.1590/S1516-89132008000300015
Saygu I, Deval MC (2014) The post-release survival of two skate species discarded by bottom trawl fisheries in Atalya bay, eastern Mediterranean. Turk J Fish Aquat Sci 14(4):947–953. https://doi.org/10.4194/1303-2712-v14_4_14
Schaller P, Dunker F (2005) Use of contrast radiograph to determine trauma to the valvular intestine in the blacktip reef shark (Carcharhinus melanopterus). Drum Croak 36:23–28
Schwab IR (2003) Janus on the mudflats. Brit J Ophthalmol 87:13–13. https://doi.org/10.1136/bjo.87.1.13
Sims DW, Andrews PLR, Young JZ (2000) Stomach rinsing in rays. Nature 404:566–566. https://doi.org/10.1038/35007149
Smale M (2005) The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the Eastern Cape, South Africa. Afr J Mar Sci 27:331–335. https://doi.org/10.2989/18142320509504091
Smith M, Warmolts D, Thoney D et al (2004) The elasmobranch husbandry manual: captive care of sharks, rays and their relatives. Spec Publ Ohio Biol Surv 589:145
Stedman NL, Garner MM (2018) Chondrichthyes. In: Terio K, Mcaloose D, Leger JS (eds) Pathology of wildlife and zoo animals. Academic Press Elsevier, Cambridge, p 1136p
Stevens JD (1984) Biological observations on sharks caught by sport fishermen off new south wales. Aust J Mar Feshw Res 35:573–590. https://doi.org/10.1071/MF9840573
Stevens J, Wiley P (1986) Biology of two commercially important carcharhinid sharks from northern Australia. Mar Freshw Res 37:671. https://doi.org/10.1071/MF9860671
Stevens GMW, Hawkins JP, Roberts CM (2018) Courtship and mating behaviour of manta rays Mobula alfredi and M. birostris in the Maldives. J Fish Biol 93:344–359. https://doi.org/10.1111/jfb.13768
Stibbe EP (1928) A comparative study of the nictitating membrane of birds and mammals. J Anat 62:159
Takatsuka V, Costa DGC, Oliveira NY et al (2019) Use of eugenol for anesthesia of lesser guitarfish Zapteryx brevirostris (Rhinobatidae). Braz J Biol 79:516–520. https://doi.org/10.1590/1519-6984.186755
Tomita T, Murakumo K, Miyamoto K et al (2016) Eye retraction in the giant guitarfish, Rhynchobatus djiddensis (Elasmobranchii: Batoidea): a novel mechanism for eye protection in batoid fishes. Zoology 119:30–35. https://doi.org/10.1016/j.zool.2015.09.004
Tomita T, Murakumo K, Komoto S et al (2020) Armored eyes of the whale shark. PLoS ONE 15:e0235342. https://doi.org/10.1371/journal.pone.0235342
Tricasa TC, Michael SW, Sisneros JA (1995) Electrosensory optimization to conspecific phasic signals for mating. Neurosci Lett 202:129–132. https://doi.org/10.1016/0304-3940(95)12230-3
Tuttle AD, Burrus O, Burkart MA et al (2008) Three cases of gastric prolapse through the gill slit in sand tiger sharks, Carcharhinus taurus (Rafinesque). J Fish Dis 31:311–315. https://doi.org/10.1111/j.1365-2761.2007.00881.x
Wada S, Kurata O, Hatai K et al (2010) A Study of the Effects of 2-Phenoxyethanol as a Sedative and/or Anesthetic on Cow-Nosed Ray (Rhinoptera javanica). Jpn J Zoo Wildl Med 15:31–36. https://doi.org/10.5686/jjzwm.15.31
Weber DN, Janech MG, Burnett LE et al (2021) Insights into the origin and magnitude of capture and handling-related stress in a coastal elasmobranch Carcharhinus limbatus. ICES J Mar Sci 78:910–921. https://doi.org/10.1093/icesjms/fsaa223
Weideli OC, Papastamatiou YP (2020) Intestinal eversion in a pelagic shark evokes chase and bite attempts by large-bodied carangid fish. J Ethol 39:125–127. https://doi.org/10.1007/s10164-020-00664-0
Whitney NM, Lear KO, Morris JJ et al (2021) Connecting post-release mortality to the physiological stress response of large coastal sharks in a commercial longline fishery. PLoS ONE 16:e0255673. https://doi.org/10.1371/journal.pone.0255673
Wiersma G, Verhoog P, Fowler S et al (2015) The first field observation of intestinal eversion by a shark (broadnose sevengill, Notorynchus cepedianus). Mar Biodiv 46:17–18. https://doi.org/10.1007/s12526-015-0341-9
Williams HH, Burt MDB, Caira JN (2004) Anthobothrium lesteri n. sp. (Cestoda: Tetraphyllidea) in Carcharhinus melanopterus from Heron Island, Australia, with comments on its site, mode of attachment, reproductive strategy and membership of the genus. Syst Parasitol 59:211–221. https://doi.org/10.1023/B:SYPA.0000048100.77351.9f
Williams GD, Andrews KS, Farrer DA et al (2011) Occurrence and biological characteristics of broadnose sevengill sharks (Notorynchus cepedianus) in Pacific Northwest coastal estuaries. Environ Biol Fish 91:379–388. https://doi.org/10.1007/s10641-011-9797-z
Wosnick N, Rangel BS, Moreira RA, Freire CA (2017) Clasper flaring in a guitarfish (Zapteryx brevirostris Elasmobranchii, Rhinobatidae) under anesthesia. Vet Anaesth Analg 44:976–978. https://doi.org/10.1016/j.vaa.2017.04.001
Wosnick N, Awruch CA, Adams KR et al (2018a) Impacts of fisheries on elasmobranch reproduction: high rates of abortion and subsequent maternal mortality in the shortnose guitarfish. Anim Conserv 22:198–206. https://doi.org/10.1111/acv.12458
Wosnick N, Adams KR, Freire CA (2018b) Ultrasonography as a promising methodology to indicate captured-induced abortion in viviparous elasmobranchs. J Fish Biol 93:1033–1037. https://doi.org/10.1111/jfb.13746
Young FA, Kajiura SM, Visser GJ et al (2002) Notes on the long-term transport of the scalloped hammerhead shark (Sphyrna lewini). Zoo Biol 21:243–251. https://doi.org/10.1002/zoo.10019
Acknowledgements
Authors thank Dr. Hollie Booth for stomach eversion photographic record. This research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) through a post-doctoral fellowship granted to N.W, the Carlos Chagas Filho Foundation for Research Support of the State of Rio de Janeiro (FAPERJ) (R.A.H.D.), a Jovem Cientista do Nosso Estado 2021–2024 grant (process number E-26/201.270/202) and an ARC grant (process number E-26/21.460/2019), as well as through a Brazilian National Council of Scientific and Technological Development (CNPq) productivity grant (Bolsista de Produtividade em Pesquisa 2021–2024) (R.A.H.D.). The implementation of the Projeto Pesquisa Marinha e Pesqueira is a compensatory measure established by the Conduct Adjustment Agreement under the responsibility of the PRIO company, conducted by the Federal Public Ministry—MPF/RJ.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wosnick, N., Leite, R.D., Balanin, S. et al. Behavioral and visual stress-induced proxies in elasmobranchs. Rev Fish Biol Fisheries 33, 175–199 (2023). https://doi.org/10.1007/s11160-023-09757-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-023-09757-8