Climate-dependent evolution of Antarctic ectotherms: An integrative analysis

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Abstract

The paper explores the climate-dependent evolution of marine Antarctic fauna and tries to identify key mechanisms involved as well as the driving forces that have caused the physiological and life history characteristics observed today. In an integrative approach it uses the recent concept of oxygen and capacity limited thermal tolerance to identify potential links between molecular, cellular, whole-organism, and ecological characteristics of marine animal life in the Antarctic. As a generalized pattern, minimization of baseline energy costs, for the sake of maximized growth in the cold, appears as one over-arching principle shaping the evolution and functioning of Antarctic marine ectotherms. This conclusion is supported by recent comparisons with (sub-) Arctic ectotherms, where elevated levels of energy turnover result at unstable, including cold temperatures, and are related to wide windows of thermal tolerance and associated metabolic features.

At biochemical levels, metabolic regulation at low temperatures in general, is supported by the cold compensation of enzyme kinetic parameters like substrate affinities and turnover numbers, through minute structural modifications of the enzyme molecule. These involve a shift in protein folding, sometimes supported by the replacement of individual amino acids. The hypothesis is developed that efficient metabolic regulation at low rates in Antarctic marine stenotherms occurs through high mitochondrial densities at low capacities and possibly enhanced levels of Arrhenius activation energies or activation enthalpies. This contrasts the more costly patterns of metabolic regulation at elevated rates in cold-adapted eurytherms.

Energy savings in Antarctic ectotherms, largely exemplified in fish, typically involve low-cost, diffusive oxygen distribution due to high density of lipid membranes, loss of haemoglobin, myoglobin and the heat shock response, reduced anaerobic capacity, large myocytes with low ion exchange activities, and the use of lipid body stores for neutral buoyancy. Important trade-offs result from obligatory energy savings in the permanent cold: low metabolic rates support cold-compensated growth but imply narrow windows of thermal tolerance and reduced scopes for activity. The degree of thermal specialization is not uniformly defined by cold temperature but varies with life style characteristics and activity levels and associated aerobic scope. Trade-offs for the sake of cold compensated growth parallel reduced capacities for exercise performance, exacerbated by the effect of high haemolymph magnesium levels in crustaceans and, possibly, other invertebrates. High magnesium levels likely exclude the group of reptant decapod crustaceans from Antarctic waters below 0 °C.

The hypothesis is developed that energy savings imposed by the permanent cold bear specific life history consequences. Due to effects of allometry, energy savings are exacerbated at small body size, favouring passive lecithotrophic larvae. At all stages of life history, reduced energy turnover for the sake of growth causes delays and low rates in other higher functions, with the result of late maturity, fecundity and offspring release, as well as extended development. As a consequence, extended life spans evolved due to life history requirements. At the same time, polar gigantism is enabled by a combination of elevated oxygen levels in cold waters, of reduced metabolism and of extended periods of growth at slow developmental rates.

Introduction

It has been well documented that decadal-scale variations in the coupled ocean-atmosphere system impact animal communities and populations in marine ecosystems (Cushing, 1982; Beamish, 1995; Bakun, 1996; Finney et al., 2002). Similarly, current analyses of the effects of climate change on marine ecosystems have revealed that present-day effects of global warming on the biosphere are associated with shifts in the geographical distribution of ectothermic animals along a latitudinal cline or with pole-ward or high-altitude extensions of geographic species ranges (Walther et al., 2002; Parmesan and Yohe, 2003; Root et al., 2003). However, the level of significance of such observations is under debate partly due to the lack of comprehensive cause and effect understanding (Clarke, 1996; Jensen, 2003). Nonetheless, temperature means and variability as associated with the climate regime can be interpreted as major driving forces setting the large scale biogeography of marine water breathing animals.

On the cold side, temperature variability is currently lowest in the marine Antarctic with temperature maintained close to freezing in several areas (Clarke, 1988, Clarke, 1998; Peck, 2005). At the same time, Antarctic marine ectotherms live at the low end of the temperature continuum in marine environments, and are considered highly stenothermal (Somero and De Vries, 1967; Peck and Conway, 2000; Somero et al., 1996, Somero et al., 1998; Pörtner et al., 1999a, Pörtner et al., 2000; Peck et al., 2002). Temperature means and variability in relation to the climate regime may thus exert key influences in shaping survival and functional adaptation to temperature. These patterns are paralleled by a specialization of animals on limited thermal windows. The present paper tries to develop a comprehensive picture of thermal adaptation and limitation from molecular to ecosystem levels and thereby, identify the forces and benefits of thermal specialization from an integrative point of view.

Global climate change late in the Eocene epoch (about 35 million years ago) started to shape the characteristics of marine Antarctic ecosystems. This was the beginning of the transition from a cool-temperate climate in Antarctica to the polar climate that exists there today (for review see Clarke and Crame, 1992; Crame, 1993; Clarke, 1996). However, for a long time, temperatures remained close to 4 or 5 °C and only during the last 4–5 million years cooling continued and reached the low temperatures that characterize extant Antarctic waters (Fig. 1). The cooling trend strongly influenced the structure of shallow-water, Antarctic marine communities, and these effects are still evident in modern Antarctic communities. Current evidence suggests a long evolutionary history in situ for much of the Southern ocean fauna, with a large degree of endemism but some exchange via the deep sea (Clarke and Crame, 1989). Cooling reduced the abundance and diversity of fish and crabs, gastropods and bivalves, which in turn reduced skeleton-crushing predation on invertebrates. Reduced predation allowed dense populations of ophiuroids and crinoids to appear in shallow-water settings at the end of the Eocene and these communities are persistent today (Aronson et al., 1997). Nonetheless, temperature oscillations have occurred repeatedly on timescales of several thousands of years during recent Antarctic climate history. As an example, Antarctic surface waters were warm (at 4–5 °C close to Bouvet island) and ice free between 10,000 and 5000 yr B.P. About 5000 yr B.P., sea surface temperatures cooled by 2–3 °C, sea ice advanced, and the delivery of ice-rafted detritus to the sub-Antarctic South Atlantic increased abruptly (Hodell et al., 2001).

Despite some variability the unique features of long-term stable cold temperatures throughout the whole year in the marine Antarctic contrast the relative thermal instability and young age of the marine Arctic (Overpeck et al., 2003; Schauer et al., 2004; Maslowski et al., 2004) as well as the large temperature fluctuations in temperate climates. Comparison of fauna from these diverse climates has served to identify and characterize the special physiological characters of Antarctic fauna. For large-scale studies of marine biogeography and evolution, animals from marine Antarctic ecosystems, especially those at highest latitudes and with the largest degree of stenothermy, might thus be considered as a reference point in the long-term stable cold.

Studies within the EASIZ (Ecology of the Antarctic Sea Ice Zone) program have provided key perspectives for crucial relationships between physiological characteristics and ecological features of various Antarctic invertebrates and fish (Clarke, 1988, Clarke, 1998; Pörtner et al., 2000; Peck, 2002). These studies also have helped to unravel some of the mechanisms and trade-offs, which define the benefits of thermal specialization and their potential ecological consequences, for example, the reduced diversity of crabs and fish. Considering recent progress in the physiology of thermal tolerance a cause and effect understanding currently emerges of how fluctuations in body temperature depending on the climate regime, features of cellular design and the levels of energy turnover and performance in animals are interrelated (Pörtner, 2002a).

Key questions are whether, and how, the key functional properties and limits of Antarctic ectotherms have been shaped by adaptation to the permanent cold? The present study assumes that this process is crucial, while extreme seasonalities in light conditions or food availability may play a lesser role. In support of this assumption, eurythermal life forms with contrasting patterns of high energy turnover are found at similarly high latitudes under similar patterns of seasonality but more variable climate and temperature regimes of the North Atlantic. However, the thermal environments even of Antarctic oceans are not uniform, with different temperature means and variability, e.g. in the Bellingshausen Sea, the Weddell Sea, the Northern Antarctic peninsula or at various water depths (Kaplan et al., 1997, Kaplan et al., 1998; Vaughan et al., 2001; Vogt, 2004; Fahrbach et al., 2004). The question then arises; to what extent the stereotype of a “good” Antarctic ectotherm does exist. It will be discussed whether Antarctic marine life rather should be interpreted to be located to variable degrees at the extreme end of a continuum of life forms in various climates. This is a general question beyond more specific ones, e.g., the limited diversity of the impoverished Antarctic fish fauna due to requirement and evolution of antifreeze proteins (Chen et al., 1997) or the special sensitivity of the crustacean fauna to high magnesium levels in cold ocean waters, which excluded the reptant decapods from the marine Antarctic below 0 °C (Frederich et al., 2001, see below). Another more general question would be why evolution excluded expensive lifestyles and physiologies from the marine Antarctic (cf. Clarke, 1988, Clarke, 1998).

The treatment will conclude with a perspective on how periods with stable versus more unstable climates in earth history may have supported evolutionary progress through progressively enhanced diversification of lifestyles between low and high levels of energy turnover. Thereby, climate variability may have contributed to speciation and radiation and, thus, the setting of biodiversity. Finally, the question arises whether an over-arching conceptual framework is available that leads to a comprehensive understanding of the climate-dependent evolution of marine including Antarctic fauna. Most importantly, such a conceptual framework should integrate information from molecular, cellular, tissue, blood, organismal, population and ecosystem levels of biological organisation. Such integration may include unconventional thinking as required for unravelling the potential interdependence of phenomena at various levels of biological organisation. The conceptual framework can be tested in how it is able to integrate relevant phenomena at various organisation levels. Such a framework also should provide guidance in finding adequate interpretations of individual phenomena.

Section snippets

Oxygen and capacity limited thermal tolerance: evidence from Antarctic species

The concept of oxygen and capacity limited thermal tolerance might provide such an integrative framework (based on Pörtner, 2001, Pörtner, 2002a; Pörtner et al., 2005a). Using the principles of Shelford's law this concept suggests that the first level of thermal intolerance at low and high temperature extremes in metazoa is a loss in whole organism aerobic scope. This relative loss occurs at both, the low and the high borders of the thermal envelope, beyond so-called pejus thresholds (Fig. 2,

Trade-offs in the processes and limits of thermal adaptation

Mechanisms setting aerobic and functional scope especially the adjustment of O2 supply capacity and of the functional capacity of tissues appear crucial in climate-dependent evolution in general (Pörtner, 2001, Pörtner, 2002a, Pörtner, 2004) and also in Antarctic evolution. The underlying systemic to molecular mechanisms of adaptation and the associated tradeoffs (cf. Pörtner et al., 2005c) are thus key to understand the specialization of polar fauna on limited thermal windows. Adjustments in

Trade-offs and savings in energy turnover: life history aspects

There are slow functions not found cold-compensated in Antarctic ectotherms, namely life history functions like reproduction, hatching and larval development (Arntz et al., 1994; cf. Clarke, 1987). In the case of echinoids the slowing of development with falling temperature across latitudes was not linear but rose exponentially (Stanwell-Smith and Peck, 1998) such that the temperature effect was drastic at high polar latitudes (see above). These overarching commonalities elaborated for

Summary and perspectives: pathways of Antarctic evolution

The examples discussed in this paper, drawn from various molecular, physiological and ecological studies, have been interpreted in the light of the integrative concept of oxygen and capacity limitation of thermal tolerance. This analysis has been able to integrate information from various, molecular to ecosystem levels of biological organization that have traditionally been addressed separately. The analysis also has identified crucial links between these levels. A clearer understanding of

Acknowledgements

Supported by the Mar Co Pol I program of the AWI. The author thanks A. Clarke and C. Smith for an excellent symposium.

References (202)

  • S.P. Gieseg et al.

    A comparison of plasma vitamin C and E levels in two Antarctic and two temperate water fish species

    Comparative Biochemistry and Physiology B

    (2000)
  • O. Heilmayer et al.

    Age and productivity of the Antarctic scallop, Adamussium colbecki, in Terra Nova Bay (Ross Sea, Antarctica)

    Journal of Experimental Marine Biology and Ecology

    (2003)
  • D.A. Hodell et al.

    Abrupt cooling of Antarctic surface waters and sea ice expansion in the South Atlantic sector of the Southern Ocean at 5000 cal yr B.P

    Quaternary Research

    (2001)
  • F.B. Johnson et al.

    Molecular Biology of Aging

    Cell

    (1999)
  • R. Acierno et al.

    Myoglobin enhances cardiac performance in Antarctic fish species that express the protein

    American Journal of Physiology

    (1997)
  • I.Y. Ahn et al.

    Lipid content and composition of the Antarctic lamellibranch, Laternula elliptica (King & Broderip) (Anomalodesmata: Laternulidea), in King George Island during an austral summer

    Polar Biology

    (2000)
  • S.D. Archer et al.

    Kinematics of labriform and subcrangiform swimming in the Antarctic fish Notothenia neglecta

    Journal of Experimental Biology

    (1989)
  • W. Arntz et al.

    A case for tolerance in marine ecology: let us not put out the baby with the bathwater

    Scientia Marina

    (2001)
  • W.E. Arntz et al.

    Oceanography and marine biology, annual reviews

    Antarctic Zoobenthos

    (1994)
  • R.B. Aronson et al.

    Retrograde community structure in the late Eocene of Antarctica

    Geology

    (1997)
  • A. Astorga et al.

    Two oceans, two taxa and one mode of development: latitudinal diversity patterns of South American crabs and test for possible causal processes

    Ecology Letters

    (2003)
  • Axelsson, M., 2005. The circulatory system and its control. In: Farrell, A.P., Steffensen, J.F. (Eds.), The Physiology...
  • A. Bakun

    Patterns in the Ocean-Ocean Processes and Marine Population Dynamics

    (1996)
  • Beamish, R.J., 1995. Climate Change and Northern Fish Populations. Canadian Special Publication of Fisheries and...
  • J.M. Billerbeck et al.

    Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside

    Oecologia

    (2000)
  • Bluhm, B., 2001. Age determination in polar crustacea using the autofluorescent pigment lipofuscin. Berichte zur...
  • I. Bosch et al.

    Development, metamorphosis and seasona abundance of embryos and larvae of the Antarctic sea urchin, Sterechinus neumayeri

    Biological Bulletin

    (1987)
  • R.G. Boutilier

    Physiological ecology in cold ocean fisheries: a case study in Atlantic cod

  • T. Brey

    Temperature and reproductive metabolism in macrobenthic populations

    Marine Ecology Progress Series

    (1995)
  • T. Brey et al.

    Population dynamics of marine benthic invertebrates in Antarctic and Subantarctic environments: are there unique adaptations?

    Antarctic Science

    (1993)
  • T. Brey et al.

    Growth and production of Sterechinus neumayeri (Echinoidae: Echinodermata) in McMurdo Sound, Antarctica

    Marine Biology

    (1995)
  • J.C. Brodeur et al.

    Myogenic cell cycle duration in Harpagifer species with sub-Antarctic and Antarctic distributions: evidence for cold compensation

    Journal of Experimental Biology

    (2003)
  • G. Chapelle et al.

    Polar gigantism dictated by oxygen availability?

    Nature

    (1999)
  • G. Chapelle et al.

    Amphipod crustacean size spectra: new insights in the relationship between size and oxygen

    Oikos

    (2004)
  • L. Chen et al.

    Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod

    Proceedings of the National Academy of Sciences, USA

    (1997)
  • A. Clarke

    Temperature and embryonic development in polar marine invertebrates

    International Journal of Invertebrate Reproduction

    (1982)
  • A. Clarke

    Temperature, latitude and reproductive output

    Marine Ecology Progress Series

    (1987)
  • A. Clarke

    The influence of climate change on the distribution and evolution of organisms

  • A. Clarke

    Temperature and energetics: an introduction to cold ocean physiology

  • Clarke, A., Crame, J.A., 1989. The origin of the southern ocean marine fauna. In: Crame, J.A. (Ed.), Origins and...
  • A. Clarke et al.

    The Southern ocean benthic fauna and climate change: a historical perspective

    Philosophical Transactions of the Royal Society of London B

    (1992)
  • Clarke, A., Peck, L.S., 1991. The physiology of polar marine zooplankton. In: Proceedings of the Pro Mare Symposium on...
  • A. Clarke et al.

    Scaling of metabolic rate and temperature in teleost fish

    Journal of Animal Ecology

    (1999)
  • J.A. Crame

    Latitudinal range fluctuations in the marine realm through geological time

    Trends in Ecology and Evolution

    (1993)
  • D.H. Cushing

    Climate and Fisheries

    (1982)
  • C. Dahm

    Ophiuroids (Echinodermata) of southern Chile and the Antarctic: Taxonomy, biomass, diet and growth of dominant species

    Scientia Marina (Barcelona)

    (1999)
  • A.L. DeVries et al.

    Physiology and ecology of notothenioid fishes of the Ross Sea

    Journal of the Royal Society of New Zealand

    (1981)
  • C.v. Dorrien

    Ecology and respiration of selected Arctic benthic fish species

    Berichte zur Polarforschung/Reports on Polar Research

    (1993)
  • J.T. Eastman et al.

    Buoyancy studies of notothenioid fishes in McMurdo Sound, Antarctica

    Copeia

    (1982)
  • K.S. Echtay et al.

    Superoxide activates mitochondrial uncoupling proteins

    Nature

    (2002)
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