Hagfish feeding habits along a depth gradient inferred from stable isotopes

Marine Ecology Progress Series

Volumn 485, Issue , 2013, Pages 223-234

  Zintzen, Vincent ^a   Rogers, Karyne M ^b   Roberts, Clive D ^a   Stewart, Andrew L ^a   Anderson, Marti J ^c  

^a MUSEUM OF NEW ZEALAND TE PAPA TONGAREWA   (New Zealand)

^b GNS SCIENCE   (New Zealand)

^c MASSEY UNIVERSITY   (New Zealand)

Author keywords

Body condition index; Carbon; Ecology; Eptatretus; Fish; Lipid content; Neomyxine; Nitrogen

Indexed keywords

BODY CONDITION; CARBON; FEEDING BEHAVIOR; HABITAT TYPE; LIPID; MUSCLE; NITROGEN; SPECIALIZATION; STABLE ISOTOPE; TROPHIC LEVEL;

NEW ZEALAND;

EID: 84879614450     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10341     Document Type: Article

References (62)

1. Alfaro AC, Thomas F, Sergent L, Duxbury M (2006) Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar Coast Shelf Sci 70: 271-286
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46
3. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-525
4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to Software and Statistical Methods
5. Bailey TG, Robison BH (1986) Food availability as a selective factor on the chemical-compositions of midwater fishes in the eastern North Pacific. Mar Biol 91: 131-141
6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917
7. Choy CA, Davison PC, Drazen JC, Flynn A and others (2012) Global trophic position comparison of two dominant meso pelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS ONE 7: e50133
8. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/Tutorial. PRIMER-E, Plymouth, UK Cox GK
9. Sandblom E, Richards J, Farrell A (2011) Anoxic survival of the Pacific hagfish Eptatretus stoutii. J Comp Physiol B 181: 361-371
10. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197: 261-263
11. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45: 341-351
12. Deschner T, Fuller BT, Oelze VM, Boesch C and others (2012) Identification of energy consumption and nutritional stress by isotopic and elemental analysis of urine in bonobos (Pan paniscus). Rapid Commun Mass Spectrom 26: 69-77
13. Downing SW, Spitzer RH, Koch EA, Salo WL (1984) The hagfish slime gland thread cell. I. A unique cellular system for the study of intermediate filaments and intermediate filament-microtubule interactions. J Cell Biol 98: 653-669
14. Drazen JC (2007) Depth related trends in proximate composition of demersal fishes in the eastern North Pacific. Deep-Sea Res I 54: 203-219
15. Drazen JC, Popp BN, Choy CA, Clemente T, De Forest L, Smith KL (2008) Bypassing the abyssal benthic food web: Macrourid diet in the eastern North Pacific inferred from stomach content and stable isotopes analyses. Limnol Oceanogr 53: 2644-2654
16. Drazen JC, Yeh J, Friedman J, Condon N (2011) Metabolism and enzyme activities of hagfish from shallow and deep water of the Pacific Ocean. Comp Biochem Physiol A Mol Integr Physiol 159: 182-187
17. Emdin SO (1982) Effects of hagfish insulin in the atlantic hagfish, Myxine glutinosa-The in vivo metabolism of [14C]glucose and [14C]leucine and studies on starvation and glucose-loading. Gen Comp Endocrinol 47: 414-425
18. Evans K, Hindell MA (2004) The diet of sperm whales (Physeter macrocephalus) in southern Australian waters. ICES J Mar Sci 61: 1313-1329
19. Flood PR (1998) The skeletal muscle fibre types of Myxine glutinosa. In: Jorgensen JM, Lomholt JP, Weber RE, Malte H (eds) Biology of hagfishes. Chapman & Hall, London, p 173-202
20. Forrest BM, Gillespie PA, Cornelisen CD, Rogers KM (2007) Multiple indicators reveal river plume influence on sediments and benthos in a New Zealand coastal embayment. NZ J Mar Freshw Res 41: 13-24
21. Gaskin DE, Cawthorn MW (1967) Squid mandibles from the stomachs of sperm whales (Physeter catodon L.) captured in the cook strait region of New Zealand. NZ J Mar Freshw Res 1: 59-70
22. Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect ?13C and ?15N values in carp: implications for food web studies. Oecologia 138: 175-183
23. Gómez-Villota F (2007) Sperm whale diet in New Zealand. Master of Applied Science, Auckland University of Technology
24. Graves GR, Newsome SD, Willard DE, Grosshuesch DA, WurzelWW, Fogel ML (2012) Nutritional stress and body condition in the Great Gray Owl (Strix nebulosa) during winter irruptive migrations. Can J Zool 90: 787-797
25. Hatch KA, Crawford MA, Kunz AW, Thomsen SR, Eggett DL, Nelson ST, Roeder BL (2006) An objective means of diagnosing anorexia nervosa and bulimia nervosa using 15N/14N and 13C/12C ratios in hair. Rapid Commun Mass Spectrom 20: 3367-3373
26. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian-tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95: 388-394
27. Hobson KA, Sirois J, Gloutney ML (2000) Tracing nutrient allocation to reproduction with stable isotopes: a preliminary investigation using colonial waterbirds of Great Slave Lake. Auk 117: 760-774
28. Hoffman JC, Sutton TT (2010) Lipid correction for carbon stable isotope analysis of deep-sea fishes. Deep-Sea Res I 57: 956-964
29. Hückstädt LA, Koch PL, McDonald BI, Goebel ME, Crocker DE, Costa DP (2012) Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169: 395-406
30. Jaquet N, Dawson S, Slooten E (2000) Seasonal distribution and diving behaviour of male sperm whales off Kaikoura: foraging implications. Can J Zool 78: 407-419
31. Johnson EW (1994) Aspects of the biology of Pacific (Eptatretus stouti) and Black (Eptatretus deani) hagfishes in Monterey Bay, California. Master thesis, Fresno California State University, CA
32. Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing ?13C values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43: 1213-1222
33. Knapp L, Mincarone MM, Harwell H, Polidoro B, Sanciangco J, Carpenter K (2011) Conservation status of the world's hagfish species and the loss of phylogenetic diversity and ecosystem function. Aquatic Conserv Mar Freshw Ecosyst 21: 401-411
34. Kolasinski J, Frouin P, Sallon A, Rogers K, Bruggemann HJ, PotierM(2009) Feeding ecology and ontogenetic dietary shift of yellowstripe goatfish Mulloidichthys flavolineatus (Mullidae) at Reunion Island, SW Indian Ocean. Mar Ecol Prog Ser 386: 181-195
35. Korneliussen H, Nicolaysen K (1973) Ultrastructure of four types of striated muscle fibers in the atlantic hagfish (Myxine glutinosa, L.). Z Zellforsch Mikrosk Anat 143: 273-290
36. Lachenbruch PA, Mickey MR (1968) Estimation of error rates in discriminant analysis. Technometrics 10: 1-11
37. Logan JM, Lutcavage ME (2008) A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Commun Mass Spectrom 22: 1081-1086
38. Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical ex traction and modelling methods. J Anim Ecol 77: 838-846
39. Lusseau SM, Wing SR (2006) Importance of local production versus pelagic subsidies in the diet of an isolated population of bottlenose dolphins Tursiops sp. Mar Ecol Prog Ser 321: 283-293
40. Martini FH (1998) The ecology of hagfishes. In: Jorgensen JM, Lomholt JP, Weber RE, Malte H (eds) Biology of hagfishes. Chapman & Hall, London, p 57-77
41. McConnaughey T, McRoy CP (1979) Food-Web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53: 257-262
42. McLeod RJ, Wing SR (2007) Hagfish in the New Zealand fjords are supported by chemoautotrophy of forest carbon. Ecology 88: 809-816
43. Mellgren SI, Mathisen JS (1966) Oxidative enzymes, glycogen and lipid in striated muscle-A histochemical study in Atlantic hagfish (Myxine glutinosa (L)). Z Zellforsch Mikrosk Anat 71: 169-188
44. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18: 293-320
45. Pinnegar JK, Polunin NVC (2000) Contributions of stableisotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122: 399-409
46. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179-189
47. Powell ML, Kavanaugh SI, Sower SA (2005) Current knowledge of hagfish reproduction: implications for fisheries management. Integr Comp Biol 45: 158-165
48. R Development Core Team (2012) R: A language and environment for statistical computing. www.R-project.org
49. Richardson LR, Jowett JP (1951) A new species of Myxine (Cyclostomata) from Cook Strait. Zoology Publications from Victoria University College 12: 1-5
50. Rodgers KL, Wing SR (2008) Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from ?13C and ?15N. Mar Ecol Prog Ser 359: 239-248
51. Rogers KM (2009) Stable isotopes as a tool to differentiate eggs laid by caged, barn, free range, and organic hens. J Agric Food Chem 57: 4236-4242
52. Rueda FM, Martinez FJ, Zamora S, Kentouri M, Divanach P (1998) Effect of fasting and refeeding on growth and body composition of red porgy, Pagrus pagrus L. Aqua-cult Res 29: 447-452
53. Shelton RGJ (1978) On the feeding of the hagfish Myxine glutinosa in the North Sea. J Mar Biol Assoc UK 58: 81-86
54. Smith CR (1985) Food for the deep-sea: utilization, dispersal, and flux of nekton falls at the Santa Catalina Basin floor. Deep-Sea Res I 32: 417-442
55. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol Annu Rev 41: 311-354
56. Strahan R (1963) The behaviour of myxinoids. Acta Zool 44: 73-102
57. Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20: 595-601
58. Tamburri MN, Barry JP (1999) Adaptations for scavenging by three diverse bathyla species, Eptatretus stouti, Neptunea amianta and Orchomene obtusus. Deep-Sea Res I 46: 2079-2093
59. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11: 107-184
60. Weatherley AH, Gill HS (1981) Recovery growth following periods of restricted rations and starvation in rainbow trout Salmo gairdneri Richardson. J Fish Biol 18: 195-208
61. Zintzen V, Roberts CD, Anderson MJ, Stewart AL, Struthers CD, Harvey ES (2011) Hagfish predatory behaviour and slime defence mechanism. Scientific Reports 1:131, doi: 10. 1038/srep00131
62. Zintzen V, Anderson MJ, Roberts CD, Harvey ES, Stewart AL, Struthers CD (2012) Diversity and composition of demersal fishes along a depth gradient assessed by baited remote underwater stereo-video. PLoS ONE 7: e48522