Marine Biology

, Volume 160, Issue 12, pp 3221–3232 | Cite as

Energy demand of larval and juvenile Cape horse mackerels, Trachurus capensis, and indications of hypoxia tolerance as benefit in a changing environment

  • Simon Joscha Geist
  • Werner Ekau
  • Andreas Kunzmann
Original Paper

Abstract

Trachurus capensis is an important fisheries resource in the degraded Namibian upwelling ecosystem. Food supply and shoaling of hypoxic zones are hypothesised to influence the species’ recruitment success. This paper is the first to quantify energy requirements and hypoxia tolerance of larval and juvenile stages of a Trachurus species. We measured normoxic respiration rates of T. capensis with a size range from 0.001 to 20.8 g wet mass (WM) collected off Cape Town (33.9°S, 18.5°E, 12/2009) and in the northern Benguela (17–24°S, 11–15°E, 02/2011). Routine metabolic rate (RMR) and standard routine rate (SRR) (mg O2 h−1) followed the allometric functions RMR = 0.418 WM0.774 and SRR = 0.275 WM0.855, respectively. Larvae and juveniles had comparatively high metabolic rates, and the energy demand of juveniles at the upper end of the size range appeared too high to be fuelled by a copepod diet alone. T. capensis’ early life stages showed a high tolerance to hypoxic conditions. RMR in larvae did not change until 30 % O2sat at 18 °C. In juveniles, critical oxygen saturation levels were low (PC for SRR = 11.2 ± 1.7 % O2sat and PC for RMR = 13.2 ± 1.6 % O2sat at 20 °C) and oxy-regulation effective (regulation index = 0.78 ± 0.09). A high hypoxia tolerance may facilitate the retention of larvae in near-shore waters providing favourable feeding conditions and allowing juveniles to exploit food resources in the oxygen minimum zone. These mechanisms seem to well adapt T. capensis to a habitat affected by spreading hypoxic zones and probably enhance its recruitment success.

Supplementary material

227_2013_2309_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 17 kb)
227_2013_2309_MOESM2_ESM.docx (31 kb)
Supplementary material 2 (DOCX 31 kb)

References

  1. Auel H, Verheye HM (2007) Hypoxia tolerance in the copepod Calanoides carinatus and the effect of an intermediate oxygen minimum layer on copepod vertical distribution in the northern Benguela Current upwelling system and the Angola-Benguela Front. J Exp Mar Biol Ecol 352:234–243CrossRefGoogle Scholar
  2. Bakun A (2010) Linking climate to population variability in marine ecosystems characterized by non-simple dynamics: conceptual templates and schematic constructs. J Mar Syst 79:361–373CrossRefGoogle Scholar
  3. Bakun A, Babcock EA, Lluch-Cota SE, Santora C, Salvadeo CJ (2010a) Issues of ecosystem-based management of forage fisheries in “open” non-stationary ecosystems: the example of the sardine fishery in the Gulf of California. Rev Fish Biol Fish 20:9–29CrossRefGoogle Scholar
  4. Bakun A, Field DB, Redondo-Rodriguez A, Weeks SJ (2010b) Greenhouse gas, upwelling-favorable winds, and the future of coastal ocean upwelling ecosystems. Glob Change Biol 16:1213–1228CrossRefGoogle Scholar
  5. Bartholomae CH, van der Plas AK (2007) Towards the development of environmental indices for the Namibian shelf, with particular reference to fisheries management. Afr J mar Sci 29:25–35CrossRefGoogle Scholar
  6. Behrens JW, Steffensen JF (2007) The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785). Mar Biol 150:1365–1377CrossRefGoogle Scholar
  7. Bertrand A, Barbieri MA, Gerlotto F, Leiva F, Cordova J (2006) Determinism and plasticity of fish schooling behaviour as exemplified by the South Pacific jack mackerel Trachurus murphyi. Mar Ecol Prog Ser 311:145–156CrossRefGoogle Scholar
  8. Bertrand A, Gerlotto F, Bertrand S, Gutierrez M, Alza L, Chipollini A, Díaz E, Espinoza P, Ledesma J, Quesquén R, Peraltilla S, Chavez FP (2008) Schooling behaviour and environmental forcing in relation to anchoveta distribution: an analysis across multiple spatial scales. Prog Oceanogr 79:264–277CrossRefGoogle Scholar
  9. Bochdansky AB, Leggett WC (2001) Winberg revisited: convergence of routine metabolism in larval and juvenile fish. Can J Fish Aquat Sci 58:220–230Google Scholar
  10. Buckley LJ, Lough R, Peck MA, Werner FE (2000) Comment: larval Atlantic cod and haddock growth models, metabolism, ingestion, and temperature effects. Can J Fish Aquat Sci 57:1957–1960CrossRefGoogle Scholar
  11. Capossela KM, Brill RW, Fabrizio MC, Bushnell PG (2012) Metabolic and cardiorespiratory responses of summer flounder Paralichthys dentatus to hypoxia at two temperatures. J Fish Biol 81:1043–1058CrossRefGoogle Scholar
  12. Chapman LJ, McKenzie DJ (2009) Chapter 2 Behavioral responses and ecological consequences. In: Richards JG, Farell AP, Brauner CJ (eds) Fish Physiology Series 27, Hypoxia. Academic Press, Amsterdam, pp 25–77Google Scholar
  13. Chekunova VI, Naumov AG (1978) Energy metabolism of the horse mackerel, Trachurus murphyi, and the butterfish, Stromateus maculatus, from the South-Eastern part of the Pacific Ocean. J Ichthyol 18:468–474Google Scholar
  14. Clark TD, Seymour RS (2006) Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi). J Exp Biol 209:3940–3951CrossRefGoogle Scholar
  15. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  16. Couturier CS, Rouault A, McKenzie D, Galois R, Robert S, Joassard L, Claireaux G (2007) Effects of water viscosity upon ventilation and metabolism of a flatfish, the common sole Solea solea (L.). Mar Biol 152:803–814CrossRefGoogle Scholar
  17. Cury P, Shannon L (2004) Regime shifts in upwelling ecosystems: observed changes and possible mechanisms in the northern and southern Benguela. Prog Oceanogr 60:223–243CrossRefGoogle Scholar
  18. Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293CrossRefGoogle Scholar
  19. Daoud D, Chabot D, Audet C, Lambert Y (2007) Temperature induced variation in oxygen consumption of juvenile and adult stages of the northern shrimp, Pandalus borealis. J Exp Mar Biol Ecol 347:30–40CrossRefGoogle Scholar
  20. Drinkwater KF, Beaugrand G, Kaeriyama M, Kim S, Ottersen G, Perry RI, Pörtner HO, Polovina JJ, Takasuka A (2010) On the processes linking climate to ecosystem changes. J Mar Syst 79:374–388CrossRefGoogle Scholar
  21. Dupont-Prinet A, Chatain B, Grima L, Vandeputte M, Claireaux G, McKenzie DJ (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J Exp Biol 213:1143–1152CrossRefGoogle Scholar
  22. Ekau W, Verheye H (2005) Influence of oceanographic fronts and low oxygen on the distribution of ichthyoplankton in the Benguela and southern Angola currents. Afr J Mar Sci 27(3):629–639CrossRefGoogle Scholar
  23. Ekau W, Auel H, Pörtner H-O, Gilbert D (2010) Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 7:1669–1699CrossRefGoogle Scholar
  24. Ekau W, Geist S, von Waldthausen C, Verheye H (2012) 5.7 Ichthyoplankton, fish studies and copepod studies (GENUS SP-4). In: Lahajnar N (ed) RV MARIA S. MERIAN Cruise Report MSM17/L3, Geochemistry and Ecology of the Namibian Upwelling System 2011. DFG Senatskommission für Ozeanographie, Bremen, pp 28–32Google Scholar
  25. FAO (2012) The state of world fisheries and aquaculture 2012. RomeGoogle Scholar
  26. Flynn BA, Richardson AJ, Brierley AS, Boyer DC, Axelsen BE, Scott L, Moroff NE, Kainge PI, Tjizoo MB, Gibbons MJ (2012) Temporal and spatial patterns in the abundance of jellyfish in the northern Benguela upwelling ecosystem and their link to thwarted pelagic fishery recovery. Afr J Mar Sci 34:131–146CrossRefGoogle Scholar
  27. Fry FEJ (1971) 1 The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish Physiology 6. Academic Press, New York, pp 1–98Google Scholar
  28. García HE, Gordon LI (1992) Oxygen solubility in seawater: better fitting equations. Limnol Oceanogr 37:1307–1312CrossRefGoogle Scholar
  29. Geist SJ, Kunzmann A, Verheye HM, Ekau W (2013) Early life history traits determine success of Cape horse mackerel, Trachurus capensis Castelnau, 1861, in the degraded northern Benguela upwelling ecosystem off Namibia ICES J Mar Sci: (under review)Google Scholar
  30. Gilly WF, Beman JM, Litvin SY, Robison BH (2013) Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annu Rev Mar Sci 5:393–420CrossRefGoogle Scholar
  31. Gordon MS (1972a) Comparative studies on the metabolism of shallow-water and deep-sea marine fishes I. White-muscle metabolism in shallow-water fishes. Mar Biol 13:222–237CrossRefGoogle Scholar
  32. Gordon MS (1972b) Comparative studies on the metabolism of shallow-water and deep-sea marine fishes II. Red-muscle metabolism in shallow-water fishes. Mar Biol 15:246–250CrossRefGoogle Scholar
  33. Grantham B, Chan F, Nielsen K, Fox D, Barth J, Huyer A, Lubchenco J, Menge B (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429:749–754CrossRefGoogle Scholar
  34. Herbert NA, Goodman M, Kunzmann A (2012) The low O2 avoidance strategy of the cape silverside Atherina breviceps (Teleostei). Mar Freshw Behav Phy 45:199–208CrossRefGoogle Scholar
  35. Herrmann JP, Enders EC (2000) Effect of body size on the standard metabolism of horse mackerel. J Fish Biol 57:746–760CrossRefGoogle Scholar
  36. Hinrichsen HH, Möllmann C, Voss R, Köster FW, Kornilovs G (2002) Biophysical modeling of larval Baltic cod (Gadus morhua) growth and survival. Can J Fish Aquat Sci 59:1858–1873CrossRefGoogle Scholar
  37. Hjort J (1914) Fluctuations in the great fisheries of northern Europe. Rapp. P.-V. Reun. Cons. Int. Explor. Mer 20:1–228Google Scholar
  38. Houde ED (1987) Fish early life dynamics and recruitment variability. Am Fish Soc Symp 2:17–29Google Scholar
  39. Houde ED (2008) Emerging from Hjort’s shadow. J Northw Atl Fish Sci 41:53–70CrossRefGoogle Scholar
  40. Hutchings L, van der Lingen CD, Shannon LJ, Crawford RJM, Verheye HM, Bartholomae CH, van der Plas AK, Louw D, Kreiner A, Ostrowski M (2009) The Benguela current: an ecosystem of four components. Prog Oceanogr 83:15–32CrossRefGoogle Scholar
  41. Ikeda T (1970) Relationship between respiration rate and body size in marine plankton animals as a function of the temperature of habitat. Bull Fac Fish Hokkaido Univ 21(2):91–112Google Scholar
  42. Ikeda T, Torres JJ, Hernández-León S, Geiger SP (2000) 10 Metabolism. In: Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 455–532CrossRefGoogle Scholar
  43. James AG, Probyn T (1989) The relationship between respiration rate, swimming speed and feeding behavior in the cape anchovy Engraulis capensis Gilchrist. J Exp Mar Biol Ecol 131:81–100CrossRefGoogle Scholar
  44. Killen SS, Costa I, Brown JA, Gamperl AK (2007) Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. P Roy Soc Lond B Bio 274:431–438CrossRefGoogle Scholar
  45. Killen SS, Atkinson D, Glazier DS (2010) The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecol Letters 13:184–193CrossRefGoogle Scholar
  46. Kleiber M (1932) Body size and metabolism. Hilgardia 6:315–351Google Scholar
  47. Kreiner A, Stenevik EK, Ekau W (2009) Sardine Sardinops sagax and anchovy Engraulis encrasicolus larvae avoid regions with low dissolved oxygen concentration in the northern Benguela Current system. J Fish Biol 74:270–277CrossRefGoogle Scholar
  48. Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6:2063–2098CrossRefGoogle Scholar
  49. Ludsin SA, Zhang X, Brandt SB, Roman MR, Boicourt WC, Mason DM, Costantini M (2009) Hypoxia-avoidance by planktivorous fish in Chesapeake Bay: implications for food web interactions and fish recruitment. J Exp Mar Biol Ecol 381:121–131CrossRefGoogle Scholar
  50. Masuda R (2009) Behavioral ontogeny of marine pelagic fishes with the implications for the sustainable management of fisheries resources. Aqua-Bio Science Monographs 2:1–56Google Scholar
  51. Masuda R (2011) Ontogeny of swimming speed, schooling behaviour and jellyfish avoidance by Japanese anchovy Engraulis japonicus. J Fish Biol 78:1323–1335CrossRefGoogle Scholar
  52. McKenzie DJ, Lund I, Pedersen PB (2008) Essential fatty acids influence metabolic rate and tolerance of hypoxia in Dover sole (Solea solea) larvae and juveniles. Mar Biol 154:1041–1051CrossRefGoogle Scholar
  53. Moran D, Wells RMG (2007) Ontogenetic scaling of fish metabolism in the mouse-to-elephant mass magnitude range. Comp Biochem Phys A 148:611–620CrossRefGoogle Scholar
  54. Moss SA, McFarland WN (1970) The influence of dissolved oxygen and carbon dioxide on fish schooling behavior. Mar Biol 5:100–107CrossRefGoogle Scholar
  55. Mueller CA, Seymour RS (2011) The Regulation Index: a new method for assessing the relationship between oxygen consumption and environmental oxygen. Physiol Biochem Zool 84:522–532CrossRefGoogle Scholar
  56. Neill WH, Miller JM, Van Der Veer HW, Winemiller KO (1994) Ecophysiology of marine fish recruitment: a conceptual framework for understanding interannual variability. Neth J Sea Res 32:135–152CrossRefGoogle Scholar
  57. Nelson G, Chabot D (2011) General energy metabolism. In: Farrell AP (ed) Encyclopedia of fish physiology, vol 3. Academic Press, London, pp 1566–1572CrossRefGoogle Scholar
  58. Neuenfeldt S, Andersen KH, Hinrichsen HH (2009) Some Atlantic cod Gadus morhua in the Baltic Sea visit hypoxic water briefly but often. J Fish Biol 75:290–294CrossRefGoogle Scholar
  59. Olivar MP, Fortuño JM (1991) Guide to ichthyoplankton of the southeast Atlantic (Benguela Current region). Sci Mar 55:1–383Google Scholar
  60. Pillar S, Barangé M (1998) Feeding habits, daily ration and vertical migration of the Cape horse mackerel off South Africa. S Afr J Mar Sci 19:263–274CrossRefGoogle Scholar
  61. Pörtner H-O (2010) Oxygen- and capacity limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893CrossRefGoogle Scholar
  62. Post J, Lee JA (1996) Metabolic ontogeny of teleost fishes. Can J Fish Aquat Sci 53:910–923Google Scholar
  63. Rombough PJ (1988) 2 Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XI., The physiology of developing fish, Part A: eggs and larvaeAcademic Press, Burlington, pp 59–161Google Scholar
  64. Schukat A, Auel H, Teuber L, Lahajnar N, Hagen W (2013a) Complex trophic interactions of calanoid copepods in the Benguela upwelling system. J Sea Res (in press). doi:10.1016/j.seares.2013.04.01
  65. Schukat A, Teuber L, Hagen W, Wasmund N, Auel H (2013b) Energetics and carbon budgets of dominant calanoid copepods in the northern Benguela upwelling system. J Exp Mar Bio Ecol 442:1–9CrossRefGoogle Scholar
  66. Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180Google Scholar
  67. Shulman GE, Love RM (1999) Advances in marine biology Vol. 36, The biochemical ecology of marine fishes. Academic Press, LondonGoogle Scholar
  68. Stenevik EK, Skogen M, Sundby S, Boyer D (2003) The effect of vertical and horizontal distribution on retention of sardine (Sardinops sagax) larvae in the northern Benguela—observations and modelling. Fish Oceanogr 12(3):185–200CrossRefGoogle Scholar
  69. Taylor JC, Rand PS, Jenkins J (2007) Swimming behavior of juvenile anchovies (Anchoa spp.) in an episodically hypoxic estuary: implications for individual energetics and trophic dynamics. Mar Biol 152:939–957CrossRefGoogle Scholar
  70. Utne-Palm AC, Salvanes AGV, Currie B, Kaartvedt S, Nilsson GE, Braithwaite VA, Stecyk JAW, Hundt M, van der Bank M, Flynn B, Sandvik GK, Klevjer TA, Sweetman AK, Brüchert V, Pittmann K, Peard KR, Lunde IG, Strandabø RAU, Gibbons MJ (2010) Trophic structure and community stability in an overfished ecosystem. Science 329:333–336CrossRefGoogle Scholar
  71. van den Thillart G, DallaVia J, Vitali G, Cortesi P (1994) Influence of long-term hypoxia exposure on the energy metabolism of Solea solea I. Critical O2 levels for aerobic and anaerobic metabolism. Mar Ecol Prog Ser 104:109–117CrossRefGoogle Scholar
  72. van der Lingen CD, Shannon LJ, Cury P, Kreiner A, Moloney CL, Roux J-P, Vaz-Velho F (2006) 8 Resource and ecosystem variability, including regime shifts, in the Benguela Current system. In: Shannon V, Hempel G, Malanotte-Rizzoli P, Moloney C, Woods J (eds) Large Marine Ecosystems Series 14, Benguela: Predicting a large marine ecosystem. Elsevier, Amsterdam, pp 147–184CrossRefGoogle Scholar
  73. Wardle CS, Soofiani NM, O’Neill FGO, Glass CW, Johnstone ADF (1996) Measurements of aerobic metabolism of a school of horse mackerel at different swimming speeds. J Fish Biol 49:854–862CrossRefGoogle Scholar
  74. Werner T (2012) Trophic positioning, diel vertical migration behavior and physiological traits in euphausiid species of the Namibian Upwelling system. Dissertation, Universität HamburgGoogle Scholar
  75. Werner T, Buchholz F (2013) Diel vertical migration behaviour in Euphausiids of the northern Benguela current: seasonal adaptations to food availability and strong gradients of temperature and oxygen. J Plankton Res 35(4):792–812CrossRefGoogle Scholar
  76. Winberg GG (1956) Rate of metabolism and food requirements of fishes. Belorussian State University, Minsk (translated from Russian by Fish Res Bd Can Transl Ser 194:1-202, 1960)Google Scholar
  77. Yeager DP, Ultsch GR (1989) Physiological regulation and conformation: a BASIC program for the determination of critical points. Physiol Zool 62(4):888–907Google Scholar
  78. Zimmermann C, Kunzmann A (2001) Baseline respiration and spontaneous activity of sluggish marine tropical fish of the family Scorpaenidae. Mar Ecol Prog Ser 219:229–239CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Simon Joscha Geist
    • 1
  • Werner Ekau
    • 1
  • Andreas Kunzmann
    • 1
  1. 1.Leibniz Center for Tropical Marine Ecology (ZMT)BremenGermany

Personalised recommendations