Marine biological responses to climate change

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Although the fossil record of the Antarctic marine faunas is far from complete, there is growing evidence to suggest that a distinctive, temperate, shallow benthos has characterised the southernmost high latitudes since at least the late Palaeozoic Era (Crame, 1994[1]). Such fauna, which were not necessarily continuous through time, show two consistent features: they are invariably less diverse than their lower latitude counterparts (Crame, 2001[2]), and they are characterised by bipolar elements (Shi and Grunt, 2000[3]). By the Late Cretaceous the Antarctic shallow marine fauna formed part of a distinctive Weddellian Province that could be traced around the southern Gondwana margins from Patagonia, through West Antarctica, to New Zealand and south-eastern Australia (Zinsmeister, 1982[4]). There is no doubt that it was affected by the mass extinction event at the end of the Cretaceous, but precisely to what extent is still uncertain. The late Paleocene-early Eocene fossil record of Antarctica is incomplete, but by the Middle Eocene it is apparent that benthic molluscan diversity had more than recovered to its pre-mass extinction levels. The prolific middle-late Eocene La Meseta Formation of Seymour Island has now yielded in excess of 170 molluscan taxa, with more than half of these being bivalves (Stilwell and Zinsmeister, 1992[5]). Thereafter shallow-marine benthic molluscan diversity was substantially reduced to its present day levels. Whether this was a gradual process or perhaps punctuated by further mass extinctions is unknown. Bivalves appear to have been particularly badly hit in the intervening 35 Ma and it is possible that this happened for a variety of reasons.

The broad history of continental glaciation in Antarctica is reasonably well established (Barrett, 2008[6]). However, the details that are important to an understanding of the evolution of the Antarctic marine fauna are still lacking. The important question in terms of the evolutionary history of the Southern Ocean shallow water marine fauna is to what degree fluctuations in sea level, and the extent of the continental ice-sheet, have driven changes in the depth and area of habitat on the continental shelves around Antarctica (Clarke and Crame, 1989[7]). Although there is clear geophysical evidence for extensions of the ice-sheet having reduced considerably the area of continental shelf at least once in the past, we cannot yet say how often this has occurred in the past or how widespread these extensions might have been (see Convey et al., submitted.).

What we can assume from these constraints for the evolution of Antarctic species is that natural climate change has always played an important and multi-fold role. The genesis of the circumpolar current together with the cooling of the Southern Ocean isolated most populations from those living farther north, creating a state in which Antarctica is sometimes considered an “evolutionary incubator”. This isolation was associated with an increase in invertebrate diversity, but other factors were also involved. First of all, some animal groups became extinct during the cooling and left ecological niches unoccupied. Others survived with very few representatives that provided the seeds to radiate into many new species. Other groups were pre-adapted, e.g. isopods and amphipods, by their breeding behaviour, but they continued to evolve and adapted to the new Antarctic habitats and food sources. The glaciation of the continent prevented terrestrial fluvial river run-off and, consequently, supported in many places the growth and development of filter feeders. Despite the availability of some information about the food preferences and life cycles of selected species, e.g. amphipods, our knowledge of the occupation of specific ecological niches or, alternatively, broadly overlapping environmental demands, especially among filter feeders, is still very poor. The slow growth of filter feeders, encouraged among other factors by the low temperature, can explain why rather few species might have been historically outcompeted (Gutt, 2006[8]). As a consequence, modern filter feeders are rich in species, provide microniches for a species associated mobile fauna and large benthic predators are comparatively scarce. This image of the modern Antarctic shelf benthos was interpreted as the result of a mainly convergent development of Palaeozoic and modern communities (Gili et al., 2006[9]) and reminds regionally due to its 3-D structure that of a modern coral reefs. During glacial maxima, most species that survived on the shelf or upper slope, especially those being dependant on phytodetritus, had to adapt to a low food supply (Bonn et al., 1998[10]). During summers of interglacial periods these animals might experience a clear food surplus. The moderate number of benthic species compared to global numbers could be explained by this switching back and forth from conditions with low food supply, creating high diversity, to conditions with a high food supply, supporting high competition pressure.

Another effect of the cooling of the Antarctic continent and surrounding waters is a similarity of environmental conditions and, consequently, of the fauna, between habitats on the Antarctic shelf, at its continental slope and in the adjacent deep-sea. Independently of whether deep-sea animals colonized the Antarctic shallow waters or vice versa, this long-term dispersal shows that Antarctic benthic life is not as isolated from northerly adjacent areas as is the open ocean ecosystem by the Antarctic Convergence.

Adaptation of algae

Macroalgae from the Antarctic show an adaptation to considerably lower temperatures compared with Arctic species (Wiencke et al., 1994[11]). This difference is the result of the different times of exposure of these groups to low temperatures, 14 million years in the Antarctic compared with 3 million years in the Arctic. The northern distribution limit of endemic Antarctic species is mainly set by the temperature requirements for macroscopic growth (Wiencke and tom Dieck, 1989). In the ecologically important brown macroalgae (Desmarestiales), the northern distribution limit is determined by the temperature requirements for growth of the macroscopic stages (sporophytes). These species are only found in areas south of the Antarctic convergence with temperatures < 5°C. During the ice ages the coastline of the Antarctic continent was probably mostly inhospitable for macroalgae, and suitable refuges were probably provided by some of the sub-Antarctic islands and/or southernmost South America. At the LGM the northern boundary of the Antarctic region just touched South America. However, habitats as far south as the South Shetland Islands may have served as refuges (Bischoff-Bäsmann and Wiencke, 1996[12]). Species with relatively high temperature demands were able to extend their northern distribution limit to lower latitudes during the ice ages. Species or species pairs with a bipolar distribution such as Desmarestia viridis/confervoides (Peters and Breeman, 1992[13]), Acrosiphonia arcta (Bischoff and Wiencke, 1995b[14]) and Urospora penicilliformis (Bischoff and Wiencke, 1995a[15]) probably drifted across the equator during the Pleistocene decline in water temperatures in the tropics (Wiencke et al., 1994[11]). The most resistant developmental stages of these species tolerate 25-27°C, temperatures slightly above the minimum equatorial sea surface temperatures during the last glaciation (23-25°C). Ice recrystallization inhibition proteins (IRIPs) and freeze tolerance have recently been discovered in the cryophilic Antarctic hair grass by John et al. (2009[16]) and ice-binding face of a plant antifreeze protein e.g. by Middleton et al. (2009[17]) and Janech et al. (2006[18]).

The evolution of Antarctic fish

Much of our knowledge of the effects of the environment on vertebrate physiology and evolution has come from fish, which share many basic physiological mechanisms with humans. The close physical and physiological interaction with the aquatic environment makes them sensitive sentinels of environmental challenge and offers important advantages for defining the organism-environment interface and the mechanisms of temperature adaptation. Fish have developed cellular and molecular mechanisms of cold adaptation, and these are fully representative of the suite of strategies adopted by organisms under strong evolutionary pressure. In the course of evolution, Antarctic fish have developed specialised adaptations, some of which characterise these organisms as unique. In strong contrast to the continental shelf faunas elsewhere, the fish fauna of the Southern Ocean around Antarctica is also unique in being overwhelmingly dominated by the single, highly endemic group of Notothenioidei. From many viewpoints Notothenioidei are the best characterised group of fish in the world. The dominance by a single taxonomic group of fishes provides a simplified natural laboratory for exploring the wealth of their physiological, biochemical and ecological adaptations, and of their evolution. Understanding the patterns of adaptation can tell us much about the process of evolution, and on the impact of climate change on a highly specialised group of fish. Notothenioids are the best example of adaptive radiation by a vertebrate group in the sea; they provide a truly unique opportunity to study the evolution of a single group of fishes in a known thermal and tectonic context, and also to study reactions of highly specialised organisms to anthropogenic changes. The amount of information available on cold adapted polar fish will provide invaluable clues on the development, impact and consequences of climate challenges, with powerful implications for the future of the Earth.

A suborder of Perciformes, Notothenioidei comprise 8 families with 44 genera and 129 species (Eastman, 2005[19]). Notothenioids represent 35% of all species in the Southern ocean and 76% of all species in the shelf waters of Antarctica (90-95% of the fish biomass). The majority of the species are endemic to the Antarctic waters, where they have successfully diversified into several ecological niches. As for other examples of adaptive radiation, this was made possible by the isolation of Antarctic coastal waters and its separation from other continents by large and deep water masses, with no shallow water connections (undersea mountain ridges or plateaus). The presence of the Antarctic Polar Front, which acts as an oceanographic barrier (albeit perhaps “leaky” (Clarke et al., 2005[20])), further reduces the exchanges between Antarctic and sub-Antarctic waters. As described earlier, this isolation was established after the opening of the Drake Passage (Scher and Martin, 2006[21]) and the Tasman gateway (Stickley et al., 2004[22]).

The subzero water temperatures and the progressive extension of ice sheets likely determined the extinction of most of the temperate fish fauna, leaving space to those species that evolved some adaptation to the freezing conditions. Antarctic notothenioids are stenothermal, and their ability to cope with the ongoing increases in environmental temperatures might be reduced, due to losses in the level of temperature-mediated gene expression, including the absence of a heat-shock response (Hofmann et al., 2005[23]; Somero, 2005[24]) described above. Thus, the question to what extent Antarctic fish may adapt to environmental change becomes a very important issue.

Three mechanisms will be mentioned below in some detail: the first two of which are development of antifreezes and hematological features. Polar fish are the only vertebrates endowed with these two specialisations. Both have required costly and complex anatomical, ecological, physiological and biochemical adjustments and compensations, and both have tight links with the temperature of the environment. Hence warming, albeit small, may have a significant impact. The third mechanism is ecological adaptation to the new habitat.

Another physiologically relevant peculiarity of Antarctic fish is the high content of mitochondria in slow muscle fibres, towards the upper end of the range reported for teleosts with similar lifestyles, and up to 50% higher in Channichthyidae (Johnston, 2003[25]). The phyletically basal bovichtids, pseudaphritids and eleginopids do not possess antifreeze glycoprotein gene sequences in their genomes (Cheng et al., 2003[26]).

  1. Antifreeze compounds in polar fish: Most invertebrate species have body fluids whose osmotic pressure is the same as seawater so that they do not freeze unless the water around them freezes. Freezing is generally unlikely for organisms inhabiting depths more than a few metres below the intertidal. Fish, on the other hand, have body fluids less concentrated than seawater, usually around 300–600 mOsm per litre, and must invest the costs associated with production of antifreeze glycoproteins (AFGPs) year-round to avoid freezing (Devries, 1971[27]; 1982; Clarke, 1998[28]; Cheng and Chen, 1999[29]). The importance of this attribute is underlined by the large number of copies of antifreeze genes in the genome of Antarctic notothenioids (Wang et al., 1995[30]; Cheng and Detrich III, 2007), and the fact that the trait has evolved on several separate occasions (Chen et al. 1997a[31],b[32]; Cheng and Chen, 1999[29]) and meets the criteria for a “key innovation” (Eastman, 2005[19]). Biochemical and cellular adaptations showing strong temperature compensation of functional capability have been identified in polar marine species, and these include changes in enzyme isoforms or activation energies (Clarke, 1998[28]; Vetter and Buchholz, 1998[33]), adaptation of rate of microtubule assembly (Detrich et al., 1989[34]), and mitochondrial proliferation in red muscles of polar fish (Johnston et al., 1998[35]). These adaptations all allow specific intracellular processes to proceed at rates similar to those in temperate species. However, these are rarely, if ever translated into whole-animal compensation, because metabolic activity and growth rates are predominantly slower in polar marine environments (Peck et al., 2002[36]). That some cellular functions are cold-compensated and proceed at rates similar to those from other latitudes supports the argument that slow growth, development and metabolic rates are dictated by resource considerations (Clarke, 1991a[37],b[38]), and that these characteristics all reduce ATP demand in the face of seasonally or ecologically reduced resource availability (Clarke, 1998[28]).

At the evolutionary level, antifreeze compounds enabled the ancestral notothenioid to fill the many ecological niches made available by ice-driven extinctions. Indeed, estimates obtained using “molecular clock approaches” indicate that the main notothenioid diversification started 23-15 Ma (Bargelloni et al., 1994[39]; Near, 2004[40]), in parallel with the establishment of permanent sea ice.

  1. The molecular evolution of hemoglobins in polar fish: Specialised hematological features are among the most striking adaptations developed by the Antarctic ichthyofauna during evolution. Antarctic waters are cold and oxygen-rich. Oxygen binding is generally favoured at low temperature. The metabolic demand of fish for oxygen is relatively low, the solubility of oxygen in the plasma is high, but the energetic cost associated with circulation of a highly corpuscular blood fluid is also large (Wells, 1990[41]; di Prisco et al., 1991[42]; Eastman, 1993[43]). Notothenioids have evolved reduced hematocrits, hemoglobin concentration/multiplicity and oxygen affinity. The growing knowledge of the phylogenetic relationships among the notothenioid families (Eastman, 1993[43]; Bargelloni et al., 1994[39]; Bargelloni et al., 2000a[44],b[45]; Eastman, 2000[46]; Near et al., 2003[47]; Dettaï and Lecointre, 2004[48]; Near, 2004[40]; Near et al., 2004[49]; Eastman, 2005[19]; di Prisco et al., 2007[50], Near and Cheng, 2008[51]; Negrisolo et al., 2008[52]; Verde et al., 2008b[53],c[54]; Giordano et al., 2009a[55],b[56]) is producing compelling evidence to answer some questions about thermal adaptation. Certainly the identification of the sister group of the suborder will be necessary to understand how these species have achieved adaptations to temperature and how they have been affected by climate change in the late Eocene (38-35 Ma is the time of widespread continental glaciation and sharp drops in Southern Ocean surface temperatures (di Prisco et al., 1991[42]; Eastman, 1993[43]; Clarke, 1998[28]). Bovichtidae, Pseudaphritidae, Eleginopidae, Nototheniidae, Harpagiferidae, Artedidraconidae, Bathydraconidae and Channichthyidae (icefishes) are the families of the suborder, thought to have arisen in Antarctica through adaptive radiation from the single ancestral stock. Seven families have hemoglobin (Hb)-containing erythrocytes in the blood, whereas Channichthyidae (the crown group) are devoid of Hb (Ruud, 1954[57]; Cocca et al., 1995[58]; Zhao et al., 1998[59]). Bovichtidae (only one out of ten species is Antarctic) and monotypic Pseudaphritidae and Eleginopidae presumably diverged during the Eocene and became established in waters around areas that now correspond to New Zealand, Australia and high-latitude South America.
3.30 Icefishes: Chionodraco hamatus. Photo: G. di Prisco

The globin-gene status in notothenioids, leading to the unique vertebrate specialisation in the hemoglobin-less family Channichthyidae (Figure 3.30), has been studied in detail (Cocca et al., 1995[58]; Zhao et al., 1998[59]; di Prisco, 2000[60]; di Prisco et al., 2002[61]; Hudson and Coyne, 2002[62]; Near et al., 2006[63]). Why have icefishes alone taken such a radical course leaving the other Antarctic families with only partial reductions in hemoglobin? Does hemoglobin remain absolutely vital for adequate oxygen transport in the other Antarctic notothenioids, or is it a vestigial relict which may be redundant under stress-free conditions? Are the hematological features of the modern families a result of life-style adaptation to extreme conditions? What is the sensitivity of this specialised oxygen-transport system to warming?

The different phylogenetic histories of polar fish depend on the differences in the respective habitats. As a result of isolation, the genotype of Notothenioidei diverged with respect to other fish groups in a way interpreted as a giant species flock (Eastman and McCune, 2000[64]). The Arctic ichthyofauna is thriving in a much more complex ocean system than the Antarctic one. Antarctic waters are dominated by a single taxonomic group; Arctic waters are instead characterised by high diversity. This is reflected in phylogeny, as shown for instance by the amino-acid sequences of globins (Eastman, 1997[65]; Verde et al., 2002[66], 2006a[67],b[68],c[69]; Giordano et al., 2007[70]; Verde et al., 2007[71]; Dettaï et al., 2008[72]; Verde et al., 2008a[73],b[53],c[54]; Verde et al. 2009[74]).

  1. Heat shock proteins: Protein synthesis at low temperature may be difficult and hence costly, which may restrict the amount of useful protein available for growth (Fraser et al., 2002[75]). This factor would again be a limitation of resource, or energy available for growth and development, rather than a direct limitation of rate by reduced temperature. Hofmann et al. (2000[76]) have shown that there is no classic heat shock response in the Antarctic fish Trematomus bernacchii, although the position is more complex than this in other species. Some Antarctic marine invertebrates express heat shock genes when temperatures are elevated experimentally to over 10°C, although this is not something they ever experienced in nature (Clark et al., 2008a[77]), whereas other invertebrates appear to be similar to the fish data reported by Hofmann et al. (2000[76]) in having no heat shock proteins (HSP) response to elevated temperature (Clark et al., 2008b[78]). Surprisingly, in the context of laboratory studies, where there was no induction of response in the limpet Nacella concinna until 15°C, wild intertidal populations do show a heat shock response when emersed, even though foot temperatures do not exceed 3°C (Clark et al., 2008a[77]). It is not known whether the lack of a heat shock response in some Antarctic species is due to the deletion or dysfunction of genes, instability of messenger RNAs, the absence of a functional heat shock factor, or some other character. The loss of this response is, however, a large energetic cost saving, and could only be successful in an environment with very stable temperatures over long evolutionary periods. Such cost-saving adaptations as the loss of a heat shock response contrast markedly with adaptations developed in the much more variable terrestrial environment.
  2. Ecological adaptation of notothenioid fish: Isolation and extinctions, together with the evolution of AFGPs and reduction of reliance on hemoglobin provided the opportunity for notothenoids to radiate, but alone cannot explain the great number of species. Additional adaptations or modifications led to notothenioid radiation. The ancestral notothenioid was a benthic fish, yet acquisition of neutral buoyancy allowed the repeated colonisation of pelagic habitats (pelagic, epipelagic, cryopelagic). Even for truly benthic species, diversification occurred through partition of depth range, from very shallow waters (0-30 m) to great depths (2,950 m, Bathydraco scotiae). Variation in body size (from the few centimetres of Pleuragramma antarcticum to close to two metres of the large pelagic predator Dissostichus mawsoni) and diverse feeding habits further contributed to diversification among notothenioid species. Besides niche partitioning, habitat fragmentation provided the means for species divergence, as often observed in adaptive radiations. Recent studies have demonstrated reduced gene flow between populations of notothenioid fish distributed around the continent, even in the presence of homogenising circumpolar currents (Patarnello et al., 2003[79]; Zane et al., 2006[80]). Speciation was also promoted by the presence of sub-Antarctic islands and archipelagos (e.g. South Georgia, Kerguelen Islands).

A clear example of how all the above described factors shaped the evolution of notothenioids is provided by Chen et al. (1998[81]). These authors mapped ecological and geographic distributions of the species belonging to a notothenioid family, Channichthyidae, onto a molecular phylogenetic tree. It emerged that speciation was always associated either with a shift in ecological habits (feeding behaviour, depth range) or with disjunct geographic distribution. The evolution of notothenioids represents an extraordinary example of adaptive radiation in the marine environment, with all the canonical characteristics of this mode of speciation (isolation, mass extinctions, key adaptations, ecological shifts and habitat fragmentation).

Changes in the marine ecosystem in the Quaternary

Life on the Antarctic shelf in the Quaternary has altered in response to varying degrees of cooling, ice shelf dynamics, isolation and changing oceanography. The major impacts of climate change on glacial timescales in the marine environment have been the glacial-interglacial expansion and contraction of the Antarctic ice sheet across the continental shelf, the consequent loss and recovery of benthic marine habitats, and the interglacial fluctuations in summer and winter maximum sea ice extent. Direct evidence for this can be seen in the marine geological record from the near shore continental shelf off the Windmill Islands (66ºS, 110ºE), in EA, where the expanding ice sheet eliminated habitat, while the shrinking ice sheet led to recolonisation and succession (Hodgson et al., 2003[82]). Maximum expansion of the Antarctic ice sheet to the continental shelf edge at the LGM was diachronous, about 90% of the continental shelf was covered by grounded ice shelves (Harris and O’Brien, 1996[83]), though perhaps not all simultaneously. This ground was therefore unavailable to benthic species. Even so, at any given time refugia were most likely available. This is consistent with molecular evidence that a distinct Antarctic marine biota has survived on the continental shelf, or at the shelf break through multiple glacial cycles. Species richness increased significantly in this phase when populations became isolated during glacial maxima, as antifreeze glycoproteins permitted continued evolution, and, at the end of the glacial period when the populations mixed again, they were unable to interbreed. Such processes are generally termed vicariance events and are described specifically for the Antarctic as a climate-diversity pump (Clarke and Crame, 1989[7]). Relatively high species numbers might also have been supported by low extinction rates, being the result of slow ecological processes reducing the likelihood of competitive displacement (Gutt, 2006[8]). Wherever the benthos lived during glacial periods, its physical and biological environment differed significantly from today’s, especially with regard to food supply (see Bonn et al., 1998[10]). Only during interglacials were the sea-floor and the overlying water column suitable habitats for rich benthic and pelagic communities (Gutt, 2007[84]; Clarke et al., 2004[85]). Within the present Holocene interglacial, physical conditions have been comparatively stable.

Nevertheless, even on Holocene timescales, marine mammal and seabird distributions have been affected by warm periods and expansions and contractions of the sea ice (Hall et al., 2006[86]) ice shelves and possibly epidemic viruses (Nelson et al., 2008[87]). Changes in the Holocene distribution of marine birds can be tracked through the changing distributions of their nesting sites (Emslie and Woehler, 2005[88]; Emslie et al., 2007[89]). Peaks in penguin populations correlate with a period of open water associated with a warm period in the RS between 4 and 3 ka corr.14C BP (Baroni and Orombelli, 1994[90]). Extensive occupation by elephant seals shows the warmest period occurred there between c. 2.3 and 1.1 ka 14C BP (c. 2.6-2.3 and 1.2-0.9 ka BP), correlated with a significant decline in sea ice (Hall et al., 2006[86]). In the Bunger Hills, isotopic concordance between a marine sediment core and fossil stomach oil of snow petrels (mumiyo), and a significant correlation between mumiyo δD and δ13C, suggest that past δ13C variation in plankton was transferred through diet to higher trophic levels and ultimately recorded in the stomach oil of snow petrels (Hiller et al., 1988[91]; Verkulich and Hiller, 1994[92]). Divergence in signals during cold periods may indicate a shift in foraging by the petrels from 13C-enriched neritic prey to normally 13C-depleted pelagic prey, except for those pelagic prey encountered at the productive pack-ice edge during cooler periods, a shift forced by presumed greater sea ice concentration during those times (Ainley et al., 2006[93]). For 13C, both mumiyo and marine sediment were enriched during the warmer ocean conditions experienced during the mid-Holocene (ca. 7.5 to 5.5 cal ka BP) in the Bunger Hills (Ainley et al., 2006[93]). In general most long-term data for high-latitude Antarctic seabirds (Adélie and emperor penguins and snow petrels) indicate that winter sea ice has a profound influence. However, some effects are inconsistent between species and areas, and other effects trend in opposite directions at different stages of breeding and life cycles.


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