Pathways of research in cold-adapted organisms and climate change

This page is part of the topic Marine biology over the next 100 years

The development of research on biological adaptations to polar environmental conditions is relatively recent. Adaptations of the polar ichthyofauna in response to environmental change are commanding attention, and the effects of climate change on biodiversity are increasingly considered. There is ample evidence that recent climate changes already caused physiological problems to a broad range of species, drive evolutionary responses (Thomas C D et al., 2001, 2004; Walther et al., 2002), and produce micro-evolutionary changes in some species (Rodriguez-Trelles and Rodriguez, 1998). But species do not live in isolation and it is necessary to evaluate their responses at community and ecosystem levels. Ecologists and physiologists are thus faced with the difficult challenge of predicting the effect of warming not only on individual species, but also on whole communities. For instance, ice-shelf collapse increases the number of icebergs, enhancing the impact by scouring on benthic biodiversity as well as on the food web by altering regional and local current patterns. Although changes in sea temperature are as yet small, increased warming may cause sub-lethal effects on physiological performance and potential disruption in ecological relationships (Clarke et al., 2007).

Most of the work at the molecular and ecological levels in cold-adapted habitats has concentrated on Antarctic fish species. Understanding the impact of past, current and predicted environmental change on biodiversity and the consequences for Antarctic-ecosystem adaptation and function is a primary goal. Examination of Antarctic ecosystems undergoing change provides a major contribution to the understanding of evolutionary processes relevant to life on Earth. Key questions include: “How well are Antarctic organisms able to cope with daily, seasonal and longer-term environmental changes?” and ”Will climate change result in either relaxation of selection pressure on genomes, or tighter constraints and ultimately the extinction of species and populations?”

Many of the same questions are being asked for the Arctic, not least through pressure from commercial fishing. Geography, oceanography and biology of species inhabiting Arctic and Antarctic polar regions have often been compared (e.g. Dayton et al., 1994) to outline the differences between the two ecosystems. The northern polar region is characterised by extensive, shallow shelf seas surrounding a largely land-locked ocean, whereas the southern polar region comprises a dynamic and open ocean and a very deep continental shelf (Smetacek and Nicol, 2005). The sea north of the Arctic Circle is almost completely enclosed and influenced by large human populations in extensively colonised terrestrial areas, as well as by industrial activities. The exchange of seawater through the passage between Greenland and the Svalbard Islands was not possible until 27 Ma (Eastman, 1997). The Arctic region was in a high-latitude position by the early Tertiary, but the climate remained temperate with water temperatures of 10-15°C. During the Miocene, about 10-15 Ma ago, Arctic land masses reached their current positions and it is thought that only at that time temperatures dropped below freezing (“unipolar ice-sheet mode)”]. Some studies indicate that glaciation events in the Arctic began 10-6 Ma ago, whereas in Antarctica glaciation started much earlier (Eastman, 1977). However, recent evidence revises the timing of the earliest Arctic cooling events, strongly supporting the indication of a “bipolar symmetry” in climate cooling. This suggests simultaneous evolution of ice at the poles and therefore a bipolar transition from “greenhouse” to “icehouse”, pointing out the importance of greenhouse-gas changes in driving global climate patterns. According to this revision, the earliest Arctic cooling events are dated much earlier, to approx. 45 Ma.

Although high latitudes and cold climates are common to both the Antarctic and the Arctic, in many respects the two regions are more dissimilar than similar. The modern polar faunas differ in age, levels of endemism, taxonomic composition, zoogeographic distinctiveness, and in the range of physiological tolerance to various environmental parameters. Because of the isolating barrier of the Polar Front, the climatic features of the Antarctic waters are more extreme and constant than those of the Arctic, where the range of temperature variation is wider, thus facilitating migration and redistribution of the fauna.

In summary, the Arctic is the connection between the more extreme Antarctic oceanic system and temperate and tropical systems. Comparison of the ecosystems is likely to provide evolutionary insights into the relationship between environment and evolutionary adaptation. We have a remarkable opportunity to develop comparative studies on evolutionary differences between cold-adapted species and on how organisms from the polar habitats are affected by (and respond to) climate change. Comparing southern and northern polar processes may shed light on evolutionary pressures and provide insight into gene selection.

A detailed assessment of the impacts of climate change in the Arctic has been published (ACIA, 2005). ACCE will hopefully provide a similar contribution for the Antarctic.

Although the impacts of climate change on polar environments are exceeding those envisaged for other regions, and will produce feedbacks with global consequences, they remain difficult to predict because of the complexity of biological responses (Anisimov et al., 2007). Climate change may affect every aspect of an organism's biology, from cellular physiology and biochemistry to food web and habitat. Organisms must alter their physiology and biochemistry to cope with changes in enzyme activity and DNA damage, by means of phenotypic responses (occurring within the lifetime by enzyme activation/inhibition and induction/repression of gene regulation), and genotypic responses (occurring over a much longer timescale through the selection of beneficial mutations). Understanding the adaptation-response mechanisms in species living in both polar habitats may help also to understand change at lower latitudes.

In addition to adaptation, other key research themes include studies of life cycles (tactics and strategies for responding to environment features), micro-evolutionary processes driven by anthropogenic impacts, interactions between changing abiotic conditions (e.g. temperature, UV-B) and biotic responses, modelling interactions between environmental change and organism responses (to facilitate predictions of change), and development of conservation policies in relation to improved understanding of the response of ecosystems to change.

The challenge for the next decade will be to incorporate the physiological/biochemical viewpoint into the field of evolutionary biology. Such integration may provide more detailed answers than we can provide here to the question of how Antarctic and Arctic biota may respond to global warming, and the extent to which they will be able to adjust to it. Another challenge will be to determine the ability of polar species to repair the effects of changes induced by a wide variety of natural and anthropogenic processes, in the general framework of species and ecosystem responses to change.

Intensified communication between scientists should lead to a multidisciplinary approach to studying the ecosystem. Analyses of adaptive evolution across the biological spectrum from molecules to species must integrate physiology, biochemistry/molecular biology, morphology, taxonomy, biogeography, ecology, and ethology. Studying the response of evolutionary processes to changes in selection pressures demands collaboration between biologists, physical scientists and modellers. Investigating changes in the physical environment that have driven evolution over geological time requires collaboration with palaeontologists, paleoclimatologists, geophysicists, glaciologists and oceanographers. Statistical and molecular genetic approaches are needed to monitor changes in biodiversity. The multidisciplinary approach will allow links to be established between tectonics, climate change, glacial processes and evolution. For example, palaeobiological data can be used to assess the age of Antarctic habitats and species; these results can then be combined with molecular estimates of divergence time and disturbances of the mechanisms of adaptation.

The main aim of such cooperation is to identify key ecological processes and their physiological underpinning by using advanced multivariable community analyses and models, as well as mechanistic studies and mechanism-based models. This approach demands an intensive coordination, not only of ongoing, but also of future research activities. Only sound estimation of large-scale biodiversity as a result of evolutionary processes, as well as a synoptic mapping of the most relevant ecological parameters, such as currents, sedimentation, bottom topography, ice cover, will allow verification of different kinds of direct or indirect anthropogenic or natural impacts on benthic and pelagic communities. Physiological studies specify the sensitivities of marine organisms to environmental factors and thereby support a mechanistic understanding of the driving forces behind the patterns observed. Improved communication will help answer questions such as: How will shore systems develop when they no longer experience physical disturbance by sea ice? How will offshore systems change if pelagic algae replace ice-algae - will the zooplankton or the benthos benefit? What are the consequences for apex-predators, e.g. the polar bear in the Arctic?

This multidisciplinary approach will allow a series of important targets to be tackled including:

1. Links between tectonics, climate evolution, glacial processes and biotic evolution. In particular, we plan to continue to refine our understanding of how the present biota evolved, and why current patterns of biological diversity are what they are. Palaeobiological data can be used to assess the age of Antarctic habitats and species. These results can then be combined with molecular estimates of divergence time to provide a powerful approach to understanding Antarctic biotic evolution (as was used very successfully to determine the history of the notothenioid radiation by the ESF-funded Network on the Biology of Antarctic Fishes). Palaeobiological data can also determine the nature and origin of latitudinal diversity gradients.
2. Links between the physical environment and gene flow. Models of oceanic and atmospheric circulation can be used to predict transport of propagules into (and out of) the Antarctic. Such models can also be used to elucidate advective processes in the Southern Ocean and their impact on gene flow and population dynamics.
3. Links with northern polar studies. Comparison of southern with northern polar processes can elucidate significant evolutionary pressures and provide insight into gene selection.

Organisms have a limited number of responses that enhance survival in changing environments. They can:

1. Use the margins of internal physiological flexibility and capacity to sustain new biological requirements. Species inhabiting coastal seabed sites around Antarctica are thought to have poorer physiological capacities to deal with change than species elsewhere (Peck, 2005; Peck et al., 2007; Pörtner et al., 2007). Experimental data suggest that they die when temperatures are raised by 5–10°C above the annual average, at which point many species lose the ability to perform essential functions, e.g. swimming in scallops or burying in infaunal bivalve molluscs when temperatures are raised only 2–3°C (Peck et al., 2004). In short, the margin range appears narrow, thus the efficiency of this ability may be poor. However, the rate at which the temperatures are increased in laboratory experiments is vastly faster than what occurs in nature, and behavioural change may be quite different at much slower rates of environmental change.
2. Adapt to the new conditions and alter the range of biological capacity. This strategy depends on the magnitude and rate of change, and aquatic habitats change temperature at a far slower rate than terrestrial ones, possibly creating fewer adaptation problems for most marine species. The ability to adapt, or evolve new characters to changing conditions depends on many factors including mutation rate, number of gametes produced per reproductive event, number of reproductive events and generation time. Antarctic benthic species grow more slowly than those from lower latitudes (Barnes et al., 2007; Peck, 2002) and develop at rates often 5 –10 times slower than similar temperate latitude species (Peck, 2002; Peck et al., 2006). They also live to great age, and exhibit deferred maturity (Peck et al., 2006). Data on numbers of embryos produced per reproductive event are scarce. However, there is a cline of increasing size in eggs with latitude (Clarke, 1992). This means fewer eggs are produced per unit effort. Fertilisation kinetic studies also reveal that around two orders of magnitude more sperm are needed for successful fertilisation of eggs of Antarctic marine invertebrates than in temperate species (Powell et al., 2001). From this and the egg data it is clear that fewer embryos are produced per unit reproductive effort by polar species. Longer generation times and fewer embryos reduce the opportunities to produce novel mutations, and result in poorer capacities to adapt to change than in similar species at lower latitudes.
3. Migrate to sites where conditions are favourable for survival. This depends on ability to disperse and availability of suitable sites. Intrinsic capacities to colonise new sites and migrate away from deteriorating conditions depend on adult abilities to travel over large distances, or for reproductive stages to drift for extended periods. Antarctic benthic species with pelagic (swimming or within the water column) phases have extremely long development times compared to lower latitude species (Peck, 2002). This means their larvae spend extended periods in the water column. However, the balance of species with pelagic phases, compared with purely protected development, appears to be significantly lower in some Antarctic groups, especially molluscs. These groups (without pelagic dispersal phases) clearly have lower dispersal capabilities and capacities to migrate. The geographic context is also important here, and whereas most continents have coastlines extending over a wide range of latitude, Antarctica is almost circular in outline, is isolated from other oceans by the circumpolar current, and its coastline covers few degrees of latitude. In a warming environment this geographical constraint could be construed as supplying few places to migrate to. In contrast, Antarctic species do show unusually wide bathymetric ranges. With a deep shelf and strong connectivity with the continental slope, lack of latitudinal scope for migration may be compensated for by bathymetric migration possibilities. On all three major criteria, Antarctic benthic species can appear less capable than species elsewhere of responding to change in ways that can enhance survival. However, evidence of the vulnerability of Antarctic fauna to climate change is not yet clear cut (for arguments see Barnes and Peck, 2008).

Although the absence of wide latitudinal gradients in the Antarctic coastal region minimises the advantage of along-coast migration for survival, it highlights the importance of the sub-Antarctic as a critical research area, largely populated by (eurythermal) fish having a broad temperature tolerance. These fish live in a more variable environment, where changes might be faster and larger than in the High Antarctic. Historically, the sub-Antarctic may have been a site of long-term acclimation, because some cold-adapted notothenioids also inhabit sub-Antarctic waters (e.g. South Georgia, Bouvet), where in shallow waters the temperature may reach +4°C. The same concept can also be applied to invertebrates and warm-blooded animals. Because knowledge of their physiological performance is limited it is not known whether microbes behave in a similar way.

This discussion of latitudinal gradients ignores the fact that both the Ross and Weddell Seas penetrate to high latitudes (close to 85ºS). However, that only becomes significant for most organisms in the event that the ice shelves occupying those shelf seas melt, which is unlikely in the 100 year time scale considered here.

In 2004, to address many of the current questions about the evolution of the biota in the face of climate change, the Scientific Committee on Antarctic Research (SCAR) launched an 8 year international scientific research programme “Evolution and Biodiversity in the Antarctic: the Response of Life to Change” (EBA). EBA integrates research across a wide variety of fields, from functional genomics and molecular systematics to ecosystem science and modelling, and draws on and contributes information to a wide rage of related fields, such as climate modelling and tectonics. Its main goal is to provide a platform for interactions between disciplines and researchers to improve understanding of the role of biodiversity in the Earth System and its responses to change, by offering the Antarctic context, and establishing cross-links with the Arctic, thereby enhancing the knowledge needed to support attempts to achieve a sustainable future for all life. EBA will provide SCAR and the international scientific community with the best possible estimate of the consequences for the Antarctic of continued environmental change.

New information, including the choice of suitable target species, long-term data sets and the concerted efforts from international multidisciplinary programmes, will help EBA to identify the responses of vulnerable species and habitats to climate change. This preliminary step is required to establish efficient strategies aimed at neutralising threats to biodiversity: in particular, before they become hopelessly irreversible, those that are essentially driven by anthropogenic contributions. EBA was selected by ICSU/WMO (the International Council for Science and the World Meteorological Organisation) as a “Lead Project” for the International Polar Year (IPY 2007-2008). This timely programme enabled the scientific community to address the increasing concerns expressed by the Antarctic Treaty Parties about the responses of Antarctic environments to natural and anthropogenic disturbances, and their request for information regarding ways in which these responses can be distinguished and mitigated to ensure long-term conservation of Antarctic environments and their biodiversity.

In summary, areas being investigated and internationally coordinated include:

• Cryptic species: to what extent may we have underestimated the diversity of the Antarctic biota and characteristics of Antarctic species?
• Radiations: when did the key radiations of the Antarctic taxa take place?
• Impact of glaciation at sea (evolutionary links between continental shelf and slope or deep-sea species).
• Phylogeography: geographical and bathymetric structure and relationships in the polar biomes.
• Population structure and dynamics in the context of evolutionary biology.
• Dispersal: immigration and emigration of organisms, dispersal, and role of humans as vectors.
• Genetic structure of populations, and extent to which population structures reflect past evolutionary history.
• The extent to which spatially separated populations of polar organisms interact at some level and, consequently, must be considered as metapopulations.
• The role of advective/transport processes in the gene flow and population structure of marine polar organisms.

In the broader sense such studies will enable biologists:

• To understand the evolution and diversity of life;
• To determine how evolution and diversity have influenced the properties and dynamics of present ecosystems and the global ocean system;
• To make predictions on how organisms and communities are responding and will respond to current and future environmental change.