American eel (Anguilla rostrata) substrate selection for daytime refuge and winter thermal sanctuary
J. P. N. Tomie A D , D. K. Cairns B F , R. S. Hobbs C , M. Desjardins C , G. L. Fletcher C and S. C. Courtenay A EA Fisheries and Oceans Canada at the Canadian Rivers Institute, Biology Department, University of New Brunswick, Fredericton, NB, E3B 5A3, Canada.
B Fisheries and Oceans Canada, Box 1236, Charlottetown, PE, C1A 7M8, Canada.
C Department of Ocean Sciences, Memorial University of Newfoundland, St John’s, NL, A1C 5S7, Canada.
D Present address: Atlantic Coastal Action Program Cape Breton, 582 George Street, Sydney, NS, B1P 1K9, Canada.
E Present address: Department of Environment and Resource Studies, University of Waterloo, 200 University Avenue W, Waterloo, ON, N2L 3G1, Canada.
F Corresponding author. Email: david.cairns@dfo-mpo.gc.ca
Marine and Freshwater Research 68(1) 95-105 https://doi.org/10.1071/MF15102
Submitted: 7 March 2015 Accepted: 30 November 2015 Published: 11 February 2016
Abstract
We addressed hypotheses that anguillid eels use mud as a substrate refuge only in the absence of substrate cavities, and that the winter distribution of eels in coastal bay and estuarine habitat is limited to waters warmer than the freezing point of fish tissue (~–0.7°C). In the seasonally ice-covered southern Gulf of St Lawrence, Canada, locations of summer fyke and winter spear fisheries indicate that American eels (Anguilla rostrata) are widely distributed in both summer and winter in shallow soft-bottomed bay and estuarine habitat. Captive eels in fresh water preferred mud substrates during summer, during pre-winter cooling and during post-winter warming periods, but in winter chose mud and cobble substrates at approximately equal frequencies. Plasma antifreeze was not detected in blood sampled from eels speared in mud under winter ice. Winter bottom water temperatures in an eel wintering site were below the approximate freezing point of fish tissue 29.9% of the time. Mud of eel wintering grounds is warmer than overlying water and appears to serve as a thermal sanctuary that allows eels to safely overwinter under ice-covered waters. American eels in the southern Gulf of St Lawrence spend ~67% of their annual cycle within the substrate.
Additional keywords: antifreeze proteins, aquatic infauna, burrows, substrate cavities.
References
Aoyama, J., Shinoda, A., Sasai, S., Miller, M. J., and Tsukamoto, K. (2005). First observations of the burrows of Anguilla japonica. Journal of Fish Biology 67, 1534–1543.| First observations of the burrows of Anguilla japonica.Crossref | GoogleScholarGoogle Scholar |
Atkinson, R. J. A., and Taylor, A. C. (1991). Burrows and burrowing behaviour of fish. Symposia of the Zoological Society of London 63, 133–155.
Atlantic States Marine Fisheries Commission (2012). American Eel Benchmark Stock Assessment. Stock Assessment Report number 12-01. Atlantic States Marine Fisheries Commission, Washington, DC.
Baras, E., Jeandrain, D., Serouge, B., and Philippart, J. C. (1998). Seasonal variations in time and space utilisation by radio tagged yellow eels Anguilla anguilla (L.) in a small stream. Hydrobiologia 371/372, 187–198.
| Seasonal variations in time and space utilisation by radio tagged yellow eels Anguilla anguilla (L.) in a small stream.Crossref | GoogleScholarGoogle Scholar |
Byrne, J. V., and Kulm, L. D. (1962). A lightweight and inexpensive piston corer. Limnology and Oceanography 7, 106–108.
| A lightweight and inexpensive piston corer.Crossref | GoogleScholarGoogle Scholar |
Cairns, D. K., Shiao, J. C., Iizuka, Y., Tzeng, W. N., and MacPherson, C. D. (2004). Movement patterns of American eels in an impounded watercourse, as indicated by otolith microchemistry. North American Journal of Fisheries Management 24, 452–458.
| Movement patterns of American eels in an impounded watercourse, as indicated by otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Cairns, D. K., Dutil, J. D., Proulx, S., Mailhiot, J. D., Bédard, M. C., Kervella, A., Godfrey, L. G., O’Brien, E. M., Daley, S. C., Fournier, E., Tomie, J. P. N., and Courtenay, S. C. (2012). An atlas and classification of aquatic habitat on the east coast of Canada, with an evaluation of usage by the American eel. Canadian Technical Report of Fisheries and Aquatic Sciences, number 2986. Fisheries and Oceans Canada. Available at http://www.dfo-mpo.gc.ca/Library/345546.pdf [Verified 4 December 2015].
Cairns, D. K., Chaput, G., Poirier, L., Avery, T., Castonguay, M., Mathers, A., Casselman, J., Bradford, R., Pratt, T., Verreault, G., Clarke, K., Veinnot, G., and Bernatchez, L. (2014). Recovery potential assessment for the American eel (Anguilla rostrata) for eastern Canada: life history, distribution, reported landings, status indicators, and demographic parameters. Research Document 2013/134, Fisheries and Oceans Canada, Canadian Science Advisory Secretariat, Ottawa ON. Available at http://www.dfo-mpo.gc.ca/Csas-sccs/publications/resdocs-docrech/2013/2013_134-eng.pdf [Verified 4 December 2015].
Caron, F., and Verreault, G. (1997). Le réseau sentinelle de l’anguille. In ‘The American Eel in Eastern Canada: Stock Status and Management Strategies. Proceedings of Eel Management Workshop’, 13–14 January 1997, Quebec City, QC. (Ed. R. H. Peterson.) Canadian Technical Report of Fisheries and Aquatic Sciences, number 2196, pp. 144–160. (Fisheries and Oceans Canada: St Andrews, NB, Canada.) Available at http://www.dfo-mpo.gc.ca/Library/223402.pdf [Verified 4 December 2015].
Chadwick, E. M. P., Cairns, D. K., Dupuis, H. M. C., Ewart, K. V., Kao, M. H., and Fletcher, G. L. (1990). Plasma antifreeze levels reflect the migratory behaviour of Atlantic herring (Clupea harengus) in the southern Gulf of St Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 47, 1534–1536.
| Plasma antifreeze levels reflect the migratory behaviour of Atlantic herring (Clupea harengus) in the southern Gulf of St Lawrence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitFansw%3D%3D&md5=a787cb0bef90591f80a81445a545453cCAS |
Clay, D. (1991). Seasonal distribution of demersal fish (Osteichthyes) and skates (Chondrichthyes) in the southeastern Gulf of St Lawrence. Canadian Special Publication of Fisheries and Aquatic Sciences, number 113, pp. 241–260. Fisheries and Oceans Canada.
Clément, M., Chiasson, A. G., Veinott, G., and Cairns, D. K. (2014). What otolith microchemistry and stable isotope analysis reveal and conceal about anguillid eel movements across salinity boundaries. Oecologia 175, 1143–1153.
| What otolith microchemistry and stable isotope analysis reveal and conceal about anguillid eel movements across salinity boundaries.Crossref | GoogleScholarGoogle Scholar | 24889970PubMed |
COSEWIC (2012). ‘COSEWIC Assessment and Status Report on the American Eel (Anguilla rostrata) in Canada.’ (Committee on the Status of Endangered Wildlife in Canada: Ottawa.)
Costa-Dias, S., and Lobon-Cervia, J. (2008). Diel feeding activity and intensity in the European eel Anguilla anguilla (L.) during an annual cycle in a Cantabrian stream. Knowledge and Management of Aquatic Ecosystems 390–391, 01.
| Diel feeding activity and intensity in the European eel Anguilla anguilla (L.) during an annual cycle in a Cantabrian stream.Crossref | GoogleScholarGoogle Scholar |
Damjanović, I., Byzov, A. L., Bowmaker, J. K., Gacic, Z., Utina, I. A., Maximova, E. M., Mickovic, B., and Andjus, R. K. (2005). Photopic vision in eels: evidences of color discrimination. Annals of the New York Academy of Sciences 1048, 69–84.
| Photopic vision in eels: evidences of color discrimination.Crossref | GoogleScholarGoogle Scholar | 16154922PubMed |
Dorgan, K. M., Jumars, P. A., Johnson, B. D., and Boudreau, B. P. (2006). Macrofaunal burrowing: the medium is the message. Oceanography and Marine Biology – an Annual Review 44, 85–121.
Dutil, J.-D., Proulx, S., Galbraith, P. S., Chassé, J., Lambert, N., and Laurian, C. (2012). Coastal and epipelagic habitats of the estuary and Gulf of St Lawrence. Canadian Technical Report of Fisheries and Aquatic Sciences, number 3009, Fisheries and Oceans Canada. Available at http://www.dfo-mpo.gc.ca/Library/347185.pdf [Verified 4 December 2015].
Evans, R. P., Hobbs, R. S., Goddard, S. V., and Fletcher, G. L. (2007). The importance of dissolved salts to the in vivo efficacy of antifreeze proteins. Comparative Biochemistry and Physiology 148, 556–561.
| The importance of dissolved salts to the in vivo efficacy of antifreeze proteins.Crossref | GoogleScholarGoogle Scholar | 17707669PubMed |
Ewart, K. V., and Fletcher, G. L. (1990). Isolation and characterization of antifreeze proteins from smelt (Osmerus mordax) and Atlantic herring (Clupea harengus harengus). Canadian Journal of Zoology 68, 1652–1658.
| Isolation and characterization of antifreeze proteins from smelt (Osmerus mordax) and Atlantic herring (Clupea harengus harengus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtlyhsL8%3D&md5=85decbf4d65a0715a28505dd1111926dCAS |
Fletcher, G. L. (1977). Circannual cycles of blood plasma freezing point and Na+ and Cl– concentrations in Newfoundland winter flounder (Pseudopleuronectes americanus): correlation with water temperature and photoperiod. Canadian Journal of Zoology 55, 789–795.
| Circannual cycles of blood plasma freezing point and Na+ and Cl– concentrations in Newfoundland winter flounder (Pseudopleuronectes americanus): correlation with water temperature and photoperiod.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXks1Gms7k%3D&md5=8a951ff76f82ec8a2d488270dfd7013dCAS | 871990PubMed |
Fletcher, G. L., Hew, C. L., and Davies, P. L. (2001). Antifreeze proteins of teleost fishes. Annual Review of Physiology 63, 359–390.
| Antifreeze proteins of teleost fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKmtLY%3D&md5=c44ad7e3712e2498093a7ea71b3bf255CAS | 11181960PubMed |
Fujino, K., Lewis, E. L., and Perkin, R. G. (1974). The freezing point of seawater at pressures up to 100 bars. Journal of Geophysical Research 79, 1792–1797.
| The freezing point of seawater at pressures up to 100 bars.Crossref | GoogleScholarGoogle Scholar |
Gans, C. (1975). Tetrapod limblessness: evolution and functional corollaries. American Zoologist 15, 455–467.
| Tetrapod limblessness: evolution and functional corollaries.Crossref | GoogleScholarGoogle Scholar |
Glova, G. J. (1999). Cover preference tests of juvenile shortfinned eels (Anguilla australis) and longfinned eels (A. dieffenbachii) in replicate channels. New Zealand Journal of Marine and Freshwater Research 33, 193–204.
| Cover preference tests of juvenile shortfinned eels (Anguilla australis) and longfinned eels (A. dieffenbachii) in replicate channels.Crossref | GoogleScholarGoogle Scholar |
Glova, G. J. (2002). Density effects on juvenile shortfinned eel (Anguilla australis) cover preferences in replicate channels. New Zealand Journal of Marine and Freshwater Research 36, 483–490.
| Density effects on juvenile shortfinned eel (Anguilla australis) cover preferences in replicate channels.Crossref | GoogleScholarGoogle Scholar |
Gray, J. S., and Elliott, M. (2009). ‘Ecology of Marine Sediments: from Science to Management’, 2nd edn. (Oxford University Press: Oxford, UK.)
Greene, K. E., Zimmerman, J. L., Laney, R. W., and Thomas-Blate, J. C. (2009). Atlantic coast diadromous fish habitat: a review of utilization, threats, recommendations for conservation, and research needs. Atlantic States Marine Fisheries Commission, Habitat Management Series number 9. Available at http://www.asmfc.org/files/Habitat/HMS9_Diadromous_Habitat_2009.pdf [Verified 4 December 2015].
Griffith, R. W. (1981). Composition of the blood serum of deep-sea fishes. The Biological Bulletin 160, 250–264.
| Composition of the blood serum of deep-sea fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktl2gtLY%3D&md5=b6083a31ae80272c7fe79bea5097f61bCAS |
Hammond, S. D., and Welsh, S. A. (2009). Seasonal movements of large yellow American eels downstream of a hydroelectric dam, Shenandoah River, West Virginia. American Fisheries Society Symposium 58, 309–323.
Hedger, R. D., Dodson, J. J., Hatin, D., Caron, F., and Fournier, D. (2010). River and estuary movements of yellow-stage American eels Anguilla rostrata, using a hydrophone array. Journal of Fish Biology 76, 1294–1311.
| River and estuary movements of yellow-stage American eels Anguilla rostrata, using a hydrophone array.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvpsFSgtQ%3D%3D&md5=846578e953221a64f9b0fa09af0d8026CAS | 20537015PubMed |
Herrel, A., Choi, H. F., De Schepper, N., Aerts, P., and Adriens, D. (2011). Kinematics of swimming in two burrowing anguilliform fishes. Zoology 114, 78–84.
| Kinematics of swimming in two burrowing anguilliform fishes.Crossref | GoogleScholarGoogle Scholar | 21392954PubMed |
Higgins, R. P., and Thiel, H. (1988). ‘Introduction to the Study of Meiofauna.’ (Smithsonian Institution Press: Washington, DC.)
Jacoby, D. M. P., Casselman, J. M., Crook, V., DeLucia, M. B., Ahn, H., Kaifu, K., Kurwie, T., Sasal, P., Silfvergrip, A. M. C., Smith, K. G., Uchida, K., Walker, A. M., and Gollock, M. J. (2015). Synergistic patterns of threat and the challenges facing global anguillid eel conservation. Global Ecology and Conservation 4, 321–333.
| Synergistic patterns of threat and the challenges facing global anguillid eel conservation.Crossref | GoogleScholarGoogle Scholar |
Jessop, B. M., Shiao, J. C., Iizuka, Y., and Tzeng, W. N. (2004). Variation in the annual growth, by sex and migration history, of silver American eels Anguilla rostrata. Marine Ecology Progress Series 272, 231–244.
| Variation in the annual growth, by sex and migration history, of silver American eels Anguilla rostrata.Crossref | GoogleScholarGoogle Scholar |
Jessop, B. M., Cairns, D. K., Thibault, I., and Tzeng, W. N. (2008). Life history of American eel Anguilla rostrata: new insights from otolith microchemistry. Aquatic Biology 1, 205–216.
| Life history of American eel Anguilla rostrata: new insights from otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Lamson, H. M., Shiao, J. C., Iizuka, Y., Tzeng, W. N., and Cairns, D. K. (2006). Movement patterns of American eels (Anguilla rostrata) between salt- and freshwater in a coastal watershed, based on otolith microchemistry. Marine Biology 149, 1567–1576, 1587–1588.
| Movement patterns of American eels (Anguilla rostrata) between salt- and freshwater in a coastal watershed, based on otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Medcof, J. C. (1969). Fishermen’s reports of freshwater and saltwater migrations of Nova Scotia eels (Anguilla rostrata). Canadian Field-Naturalist 83, 132–138.
Ménard, A., Turgeon, K., and Kramer, D. L. (2008). Selection of diurnal refuges by the nocturnal squirrelfish, Holocentrus rufus. Environmental Biology of Fishes 82, 59–70.
| Selection of diurnal refuges by the nocturnal squirrelfish, Holocentrus rufus.Crossref | GoogleScholarGoogle Scholar |
Meysman, F. J. R., Middelburg, J. J., and Heip, C. H. R. (2006). Bioturbation: a fresh look at Darwin’s last idea. Trends in Ecology & Evolution 21, 688–695.
| Bioturbation: a fresh look at Darwin’s last idea.Crossref | GoogleScholarGoogle Scholar |
National Research Council of Canada (2015). Sunrise/sunset calculator. Available at http://www.nrc-cnrc.gc.ca/eng/services/hia/sunrise-sunset.html [Verified 4 February 2015].
Nyman, L. (1972). Some effects of temperature on eel (Anguilla) behaviour. Report number 52 of the Institute of Fresh-water Research, pp. 90–102, Institute of Fresh-water Research, Drottningholm, Sweden.
Owens, E. H., and Bowen, A. J. (1977). Coastal environments of the Maritime provinces. Maritime Sediments 13, 1–31.
Petrie, B., Drinkwater, K., Sandstrom, A., Pettipas, R., Gregory, D., Gilbert, D., and Sekhon, P. (1996). Temperature, salinity and sigma-t atlas for the Gulf of St Lawrence. Canadian Technical Report of Hydrography and Ocean Sciences, number 178. Available at http://www.dfo-mpo.gc.ca/Library/198079.pdf [Verified 4 December 2015].
Pratt, T. C., Bradford, R., Cairns, D. K., Castonguay, M., Chaput, G., Clarke, K., and Mathers, A. (2014). Recovery potential assessment for the American eel (Anguilla rostrata) in eastern Canada: functional description of habitat. Research Document 2013/132, Fisheries and Oceans Canada, Canadian Science Advisory Secretariat, Ottawa ON. Available at http://www.dfo-mpo.gc.ca/Csas-sccs/publications/resdocs-docrech/2013/2013_132-eng.pdf [Verified 4 December 2015].
Sharp, G., Semple, R., Connolly, K., Blok, R., Audet, D., Cairns, D. K., and Courtenay, S. C. (2003). Ecological assessment of the Basin Head Lagoon: a proposed Marine Protected Area. Canadian Manuscript Report of Fisheries and Aquatic Sciences, number 2641. Fisheries and Oceans Canada. Available at http://publications.gc.ca/collections/collection_2007/dfo-mpo/Fs97-4-2641E.pdf [Verified 4 December 2015].
Smith, M. W., and Saunders, J. W. (1955). The American eel in certain fresh waters of the maritime provinces of Canada. Journal of the Fisheries Research Board of Canada 12, 238–269.
| The American eel in certain fresh waters of the maritime provinces of Canada.Crossref | GoogleScholarGoogle Scholar |
Sorensen, P. W., Bianchini, M. L., and Winn, H. E. (1986). Diel foraging activity of American eels, Anguilla rostrata (Lesueur), in a Rhode Island estuary. Fish Bulletin 84, 746–747.
Spares, A. D., Stokesbury, M. J. W., O’Dor, R. K., and Dick, T. A. (2012). Temperature, salinity and prey availability shape the marine migration of Arctic char, Salvelinus alpinus, in a macrotidal estuary. Marine Biology 159, 1633–1646.
| Temperature, salinity and prey availability shape the marine migration of Arctic char, Salvelinus alpinus, in a macrotidal estuary.Crossref | GoogleScholarGoogle Scholar |
Tesch, F. W. (2003). ‘The Eel’, 3rd edn. (Blackwell: Oxford, UK.)
Thibault, I., Dodson, J. J., and Caron, F. (2007). Yellow stage American eel movements determined by microtagging and acoustic telemetry in the St Jean River watershed, Gaspé (Quebec, Canada). Journal of Fish Biology 71, 1095–1112.
| Yellow stage American eel movements determined by microtagging and acoustic telemetry in the St Jean River watershed, Gaspé (Quebec, Canada).Crossref | GoogleScholarGoogle Scholar |
Tomie, J. P. N., Cairns, D. K., and Courtenay, S. C. (2013). How American eels Anguilla rostrata construct and respire in burrows. Aquatic Biology 19, 287–296.
| How American eels Anguilla rostrata construct and respire in burrows.Crossref | GoogleScholarGoogle Scholar |
Watling, L. (1975). Analysis of structural variations in a shallow estuarine deposit-feeding community. Journal of Experimental Marine Biology and Ecology 19, 275–313.
| Analysis of structural variations in a shallow estuarine deposit-feeding community.Crossref | GoogleScholarGoogle Scholar |
Wentworth, C. K. (1922). A scale of grade and class terms for clastic sediments. The Journal of Geology 30, 377–392.
| A scale of grade and class terms for clastic sediments.Crossref | GoogleScholarGoogle Scholar |