Impacts of instrumental period climate change on invertebrates

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This page is part of the topic Marine biology in the instrumental period

Decadal-scale variations in the coupled ocean-atmosphere system have an impact on animal communities and populations in marine ecosystems (Cushing, 1982[1]; Beamish, 1995[2]; Bakun, 1996[3]; Finney et al., 2002[4]). Present-day effects of global warming on the biosphere are associated with shifts in the geographical distribution of ectothermic (cold-blooded) animals along a latitudinal cline or with poleward or high-altitude extensions of geographic species ranges (Walther et al., 2002[5]; Parmesan and Yohe, 2003[6]; Root et al., 2003[7]). Temperature means and variability associated with the climate regime can be interpreted as major driving forces on the large scale biogeography of marine water breathing animals. These relationships lead us to expect that climate warming will have a significant impact on ecosystems at both poles.

The marine Antarctic has cold temperatures that are close to freezing in several areas, and which have the lowest temperature variability at high latitudes (Clarke, 1998[8]; Peck, 2005[9]). Thus, Antarctic marine ectotherms live at the low end of the aquatic temperature continuum and within a narrow temperature window (making them highly stenothermal) (Somero and DeVries, 1967[10]; Peck and Conway, 2000[11]; Somero et al., 1996[12], 1998[13]; Pörtner et al., 1999[14], 2000[15]; Peck et al. 2002[16], 2006[17]). Climate-induced changes in mean temperature and its variability should influence the survival of such organisms. That begs the questions – (i) to what extent has stenothermy in Antarctic species and phyla been overestimated? and (ii) how may species differ with respect to their respective levels of stenothermy and their capacities to acclimate to thermal change? Recent data show that Antarctic fish can undergo thermal acclimation and shift their physiological characters accordingly, e.g. in a zoarcid (Lannig et al., 2005[18]) and a notothenioid (Seebacher et al., 2005[19]).

A comparison of the mechanisms characterizing thermal intolerance between and within species of marine invertebrates and fish has led to the development of a unifying physiological concept of thermal limitation and adaptation. The first line of thermal intolerance in animals, which restricts performance in behaviour, growth and reproduction, is the limit on the capacity of oxygen supply mechanisms (Pörtner, 2001[20], 2002[21]; Pörtner et al., 2001[22]). Thermally induced reduction in oxygen supply capacity can take place at both high and low temperature extremes, before any biochemical stress indicators are affected. Between these extremes is a temperature window in which there is maximum scope for the aerobic activity and associated performance needed for successful survival in the wild. These thresholds were defined as critical temperatures (Tc) (see review by Pörtner, 2001[20]). At more extreme low and high temperatures, there is a transition to anaerobic mitochondrial metabolism as the capacity for oxygen supply diminishes. This is seen in crustaceans (Frederich and Pörtner, 2000[23]) and other invertebrate phyla (Pörtner, 2001[20], 2002[21]), in temperate and Antarctic fish like zoarcids (temperate Zoarces viviparus, Antarctic Pachycara brachycephalum) and in sub-Arctic fish like Atlantic cod (G. morhua) (Mark et al., 2002[24]; Zakhartsev et al., 2003[25]; Lannig et al., 2004[26]) (see also Van Dijk et al., 1999[27]; Pörtner et al., 2004[28]).

4.49 Temperature effects on aquatic animals. The thermal window of aerobic performance (left) display optima and limitations by pejus (“turning worse”), critical, and denaturation temperatures, when tolerance becomes increasingly passive and time-limited. Seasonal acclimatization involves a limited shift or reshaping of the window by mechanisms that adjust functional capacity, endurance, or protection. Positions and widths of windows on the temperature scale shift with life stage (right). Synergistic stressors like ocean acidification and hypoxia narrow thermal windows according to species-specific sensitivities (broken line), further modulating biogeographies, coexistence ranges, and other interactions. From: Pörtner, H.-O. and Farrel, A.P. (2008) Pysiology and Climate Change. Science 322:690-692; reprinted with permission from AAAS.

Recent evidence demonstrated the ecological relevance of oxygen limited heat tolerance through its effect at ecosystem level (Pörtner and Knust, 2007[29]). Heat stress in the wild reduced performance (Pörtner and Farrell, 2008[30], Figure 4.49) and enhanced mortality even before critical temperatures were reached. These findings emphasize the early effect and crucial role of limitation in oxygen supply in compromising fitness.

4.50 Acute temperature influences on Antarctic invertebrates. Survival and ability to ‘right’ (turn back over) of the Antarctic limpet Nacella concinna. Data from Peck (2005[9], unpublished).

Antarctic marine invertebrates may be more thermally sensitive than fish (Pörtner et al., 2007[31]). The critical temperature in the infaunal bivalve Laternula elliptica lies at about 6°C (Pörtner et al., 1999[14]; Peck et al., 2002[16]). Before reaching that temperature this species develops systemic hypoxia (hypoxemia), which reduces whole organism performance. Early reductions in aerobic scope include a complete loss of ability to burrow in L. elliptica or to self-right in the limpet Nacella concinna at 5°C (Figure 4.50), and a 50% loss of capability at temperatures between 2°C and 3° C (Peck et al., 2004[32]). The scallop, Adamussium colbecki was even more thermally constrained, being totally incapable of swimming when temperatures rose to 2°C. The early loss of performance and a progressive reduction in haemolymph oxygenation suggests that thermal thresholds are close to 0°C in L. elliptica (Peck et al., 2004[32]; Pörtner et al., 2006[33]). The thermally most sensitive Antarctic invertebrate to date is the bivalve Limopsis marionensis from the Weddell Sea, with a critical temperature of 2°C (Pörtner et al., 1999[14]). Mortality tests confirm the fatal effect of oxygen limited thermal tolerance and the inability of invertebrates to acclimate to higher temperatures. In epifaunal scallops (A. colbecki), half of the specimens died after 19 days at 4°C (D. Bailey, pers. commun.). In infaunal clams (L. elliptica), half died in 2 months at 3°C, and in the brittle star Ophionotus victoriae half died in less than 1 month at 3°C (L. Peck, pers. obs.). It appears that Antarctic stenotherms, especially among the invertebrates, live close to their thermal optimum, while others, like Antarctic fish, may live permanently below their optimum. For example, the Antarctic eelpout (P. brachycephalum) grows optimally at around 5°C, well above ambient temperatures (Brodte et al., 2006[34]), in accordance with its ability to acclimate to warmth (Lannig et al., 2005[18]).

Several Antarctic marine invertebrate species dwell in the intertidal zone and may experience elevated temperatures in summer. They likely use metabolic depression strategies and anaerobic metabolism to survive in response to temperature-induced hypoxemia (Pörtner, 2002[21]). A role for hypoxia in metabolic depression was also evident during the winter season (Morley et al., 2007[35]) and is known in temperate zone invertebrates (Grieshaber et al., 1994[36]).

Under field conditions, the loss of aerobic performance capacity at higher temperatures limits the survival of invertebrates in warmer summers. Data from physiological and other laboratory studies suggests that further warming of the marine environment by as little as 1°C will exceed the thermal tolerance of some marine invertebrate species. These polar ectotherms clearly do not have the opportunity to retreat to cooler, i.e. higher latitude waters, which leads to the expectation of fatal consequences not only for individual species but possibly also for characteristic properties of ecosystem structure and functioning. While the apparent stability of Antarctic foodweb structures in response to potential species losses may at least temporarily buffer such changes (Jacob, 2006[37]), it cannot prevent the potential loss of typical Antarctic fauna.

Functional or physiological aspects of meiofauna in general, and nematodes in particular, remain poorly known. Studies of the trophic position of meiobenthos in temperate and tropical areas have led to conflicting results (van Oevelen et al., 2006[38] and references therein) and studies in Antarctic and sub-Antarctic sediments are preliminary and restricted to a limited number of habitats (Moens et al., 2007[39]). Biomarker analysis of bulk sediment organic matter and of nematodes in different regions and sediment types was carried out to assess the energy source of meiobenthic fauna in Antarctic shelf sediments (Moens et al., 2007[39]). The results of this study suggested substantial selectivity of the metazoan meiobenthos for specific components of the sedimented organic matter, such as ice algae or flagellates, with this selectivity differing between sites and sediments. Laboratory experiments on a number of selected species from temperate regions showed that reproductive success, growth and metabolic activity of nematodes largely depend on temperature, the quality and quantity of food, and to a lesser extent salinity, with different species thriving under different conditions (Moens and Vincx, 2000a[40],b[41]). A better understanding of the current functionality of the meiobenthic communities in different habitats is needed, and will allow for assessment of how these processes can be affected by changes in the environment. These changes might also impact structural aspects of the meiobenthic, and more specific the nematode communities, such as community composition and diversity, but also densities and biomass.

4.51 Daily growth rates of krill in the Scotia Sea/South Georgia region measured in January-February, and having been adjusted for effects of variable food availability and krill size via a mixed model (re-drawn from Atkinson et al., 2006[42]). Each point represents a growth experiment derived for a swarm of krill, sampled across nearly the full range of summer surface temperatures that they occupy.

Examining physiological responses to temperature change is difficult for free-swimming pelagic organisms such as Antarctic krill, which do not behave naturally in captivity. For krill an alternative approach has been taken to look at temperature effects. Somatic growth rates can be determined in a manner largely free from laboratory artefacts, making them useable as a field-derived index of physiological health (Atkinson et al., 2006[42]). By performing many such experiments across krill’s temperature range during the summer growth period, the various factors affecting growth (chiefly food, krill size and temperature) can be teased apart. These results showed that, having adjusted for food and krill size, growth was highest at low temperatures and decreased substantially above 3°C (Figure 4.51). This stenothermy has implications for krill at their northern limits, for example at South Georgia. Surface layer temperatures have already warmed there by about 1°C in the last 80 years (Whitehouse et al., 2008[43]) and future increases could make this region increasingly unsuitable for krill in summer.

References

  1. ↑ Cushing, D.H. 1982. Climate and Fisheries. Academic Press, London.
  2. ↑ Beamish, R.J. 1995. Climate Change and Northern Fish Populations. Canadian Special Publication of Fisheries and Aquatic Science, 121, 739 pp.
  3. ↑ Bakun, A. 1996. Patterns in the Ocean-Ocean Processes and Marine Population Dynamics. California Sea Grant College System, La Jolla.
  4. ↑ Finney, B.P., Gregory-Eaves, I., Douglas, M.S.V. and Smol, J.P. 2002. Fisheries productivity in the northeastern Pacific Ocean over the past 2,200 years, Nature, 416, 729-733.
  5. ↑ Walther, G-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C, Fromentin, J-M., Hoegh-Guldberg, O. and Bairlein, F. 2002. Ecological responses to recent climate change, Nature, 416, 389-395.
  6. ↑ Parmesan, C. and Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems, Nature, 421, 37-42.
  7. ↑ Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. and Pounds, J.A. 2003. Fingerprints of global warming on wild animals and plants, Nature, 421, 57-60.
  8. ↑ Clarke, A. 1998. Temperature and energetics: a review of cold ocean physiology. In Cold Ocean Physiology (eds HO Pörtner, RC Playle), Soc. Exp. Biol. Seminar Ser., 66, 3-30.
  9. ↑ 9.0 9.1 Peck, L.S. 2005. Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature change, Antarctic Sci., 17, 497-507.
  10. ↑ Somero, G.N. and Devries, A.L. 1967. Temperature tolerance of some Antarctic fishes, Science, 156, 257-258.
  11. ↑ Peck, L.S. and Conway, L.Z. 2000. The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In Harper E, Tatlor JD, Crame JA (eds). Evolutionary biology of the bivalvia, 177. Geol Soc Special Publications, London, 441-450.
  12. ↑ Somero, G.N., Dahlhoff, E. and Lin, J.J. 1996. Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In: Johnston IA, Bennett AF (Eds) Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge University Press, Cambridge, 53-57.
  13. ↑ Somero, G.N., Fields, P.A., Hofmann, G.E., Weinstein, R.B. and Kawall, H. 1998. Cold adaptation and stenothermy in Antarctic notothenioid fishes: what has been gained and what has been lost. In: di Prisco G, Pisano E, Clarke A, (Eds), Fishes of Antarctica: a Biological Overview. Springer, Milano, 97-109.
  14. ↑ 14.0 14.1 14.2 Pörtner, H.O., Peck, L., Zielinski, S. and Conway, L.Z. 1999. Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature, Polar Biology, 22, 17-30.
  15. ↑ Pörtner, H.O., Van Dijk, P.L.M., Hardewig, I. and Sommer, A. 2000. Levels of metabolic cold adaptation: tradeoffs in eurythermal and stenothermal ectotherms. In: Davison W, Williams CW (Eds) Antarctic Ecosystems: Models for a Wider Understanding, Caxton Press, Christchurch, New Zealand, 109-122.
  16. ↑ 16.0 16.1 Peck, L.S., Pörtner, H.O. and Hardewig, I. 2002. Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula elliptica, Physiol. Biochem. Zool., 75, 123-133.
  17. ↑ Peck, L.S., Convey, P. and Barnes, D.K.A. 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability, Biol. Rev., 81, 75-109.
  18. ↑ 18.0 18.1 Lannig, G., Storch, D. and Pörtner, H.O. 2005. Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation, Polar Biol., 28, 575-584. DOI: 10.1007/s00300-005-0730-9.
  19. ↑ Seebacher, F., Davison, W., Lowe, C.J. and Franklin, C.E. 2005. A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fish, Biol. Lett., 2, 151-154.
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  22. ↑ Pörtner, H.O., Berdal, B., Blus, R., Brix, O., Colosimo, A., De Wachter, B., Giuliani, A., Johansen, T., Fischer, T., Knust, R., Naevdal, G., Nedenes, A., Nyhammer, G., Sartoris, F.J., Serendero, I., Sirabella, P., Thorkildsen, S. and Zakhartsev, M. 2001. Climate effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus), Continental Shelf Res., 21, 1975-1997.
  23. ↑ Frederich, M. and Pörtner, H.O. 2000. Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in the spider crab Maja squinado, Amer. J. Physiol., 279: R1531-R1538.
  24. ↑ Mark, F.C., Bock, C. and Pörtner, H.O. 2002. Oxygen limited thermal tolerance in Antarctic fish investigated by magnetic resonance imaging (MRI) and spectroscopy (31P-MRS), Amer. J. Physiol., 283, R1254-R1262.
  25. ↑ Zakhartsev, M.V., De Wachter, B., Sartoris, F.J., Pörtner, H.O. and Blust, R. 2003. Thermal physiology of the common eelpout (Zoarces viviparus), J. Comp. Physiol. B, 173, 365-378.
  26. ↑ Lannig, G., Bock, C., Sartoris, F.J. and Pörtner, H.O. 2004. Oxygen limitation of thermal tolerance in cod, Gadus morhua L. studied by non-invasive NMR techniques and on-line venous oxygen monitoring, Amer. J. Physiol., 287, R902–R910.
  27. ↑ Van Dijk, P.L.M., Tesch, C., Hardewig, I. and Pörtner, H.O. 1999. Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae), J. Exp. Biol., 202, 3611-3621 .
  28. ↑ Pörtner, H.O., Mark, F.C. and Bock, C. 2004. Oxygen limited thermal tolerance in fish? Answers obtained by Nuclear Magnetic Resonance techniques, Resp. Physiol. Neurobiol., 141, 243-260.
  29. ↑ Pörtner, H.O. and Knust, R. 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance, Science, 315, 95-97.
  30. ↑ Pörtner, H.O. and Farrell, A.P. 2008. Physiology and Climate Change. Science, 322, 690-692.
  31. ↑ Pörtner, H.O., Peck, L.S. and Somero, G.N. 2007. Thermal limits and adaptation: an integrative view (Antarctic Ecology: From Genes to Ecosystems), Phil. Trans. R. Soc. B, 362, 2233-2258.
  32. ↑ 32.0 32.1 Peck, L.S., Webb, K. and Bailey, D. 2004. Extreme sensitivity of biological function to temperature in Antarctic marine species, Functional Ecology, 18, 625-630.
  33. ↑ Pörtner, H.O., Peck, L.S. and Hirse, T. 2006. Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance, Polar Biol., 29, 688-693 .
  34. ↑ Brodte, E., Knust, R. and Pörtner, H.O. 2006. Temperature dependent energy allocation to growth in Antarctic and boreal eelpout (Zoarcidae), Pol. Biol., 30, 95-107.
  35. ↑ Morley, S.A., Peck, L.S., Miller, A.J. and Pörtner, H.O. 2007. Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics, Oecologia, 153, 29-36.
  36. ↑ Grieshaber, M.K., Hardewig, I., Kreutzer, U. and Pörtner, H.O. 1994. Physiological and metabolic responses to hypoxia in invertebrates, Rev. Physiol. Biochem. Pharmacol., 125, 43-147.
  37. ↑ Jacob, U. 2006. Trophic dynamics of Antarctic shelf ecosystems – food webs and energy flow budgets, PhD thesis, AWI Bremen University.
  38. ↑ Van Oevelen, D., Moodley, L., Soetaert, K., Middelburg, J.J. 2006. The trophic significance of bacterial carbon in a marine intertidal sediment: Results of an in situ stable isotope labeling study, Limnology and Oceanography, 51, 2349-2359.
  39. ↑ 39.0 39.1 Moens, T., Vanhove, S., De Mesel, I., Kelemen, B., Janssens, T., Dewicke, A. and Vanreusel, A. 2007. Carbon sources of Antarctic nematodes as revealed by natural carbon isotope ratios and a pulse-chase experiment, Polar Biol., 31 (1), 1-13.
  40. ↑ Moens, T. and Vincx, M. 2000a. Temperature and salinity constraints on the life cycle of two brackish-water nematode species, Journal of Experimental Marine Biology and Ecology, 243, 115-135.
  41. ↑ Moens, T. and Vincx, M. 2000b. Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments, Journal of Experimental Marine Biology and Ecology, 243, 137-154.
  42. ↑ 42.0 42.1 Atkinson, A. Shreeve, R.S, Tarling, G.A., Hirst, A.G., Rothery, P., Pond, D.W., Murphy, E.J. and Watkins, J.L. 2006. Natural growth rates of Antractic krill (Euphausia superba): II: Predictive models based on food, temperature, body length, sex, and maturity stage, Limnology and Oceanography, 51, 973-987.
  43. ↑ Whitehouse, M.J., Meredith, M.P., Rothery, P., Atkinson, A., Ward, P. and Korb, R.E. 2008. Rapid warming of the ocean at South Georgia, Southern Ocean during the 20th Century: forcings, characteristics and implications for lower trophic levels, Deep-Sea Research I, 55, 1218-1228.
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