Faunal microfossils: Indicators of Holocene ecological change in a saline Antarctic lake

Palaeogeography, Palaeoclimatology, Palaeoecology 221 (2005) 83 – 97 www.elsevier.com/locate/palaeo

Faunal microfossils: Indicators of Holocene ecological change in a saline Antarctic lake Louise Cromera, John A.E. Gibsona,b,T, Kerrie M. Swadlinga, David A. Ritza a School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania 7001, Australia Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart, Tasmania 7001, Australia

b

Received 30 April 2004; received in revised form 30 January 2005; accepted 3 February 2005

Abstract The sediment record of the fauna of Ace Lake, a saline meromictic lake in the Vestfold Hills, Antarctica, consists of copepod eggs, spermatophores and exoskeletal fragments, rotifer and tintinnid loricae, and foraminiferal and folliculinid tests. The relative abundance of these remains, along with other characteristics of the core, allows the development of a coherent picture of the progress of Ace Lake from a species-poor, freshwater lake early in the Holocene to a biodiverse marine basin following a marine transgression. Subsequent sea level fall reformed Ace Lake as a saline lake and productivity initially increased after isolation. After a major event, possibly associated with overturn of the meromictic lake, biodiversity and productivity decreased, and have continued to do so until the present. D 2005 Elsevier B.V. All rights reserved. Keywords: Antarctica; Palaeozoology; Invertebrate remains; Saline lake; Climate change; Isostatic rebound; Ace Lake; Vestfold Hills; Meromictic

1. Introduction Palaeolimnology has been a consistent theme in Antarctic lake studies since the mid-1980s (e.g., Pickard et al., 1986; Bjo¨rck et al., 1996; Roberts and McMinn, 1999; Hodgson et al., 2001; Wagner et al., 2004). Application of a range of techniques—

T Corresponding author. Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart, Tasmania 7001, Australia. Tel.: +61 3 6226 2428; fax: +61 3 6226 2973. E-mail address: [email protected] (J.A.E. Gibson). 0031-0182/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2005.02.005

mainly chemical and biological—has enabled an understanding of the evolution of many lake basins to be developed. In early studies, the question answered was often about the basic history of a lake in terms of its isolation from the ocean (Pickard et al., 1986) or its interaction with physical processes such as glacier retreat and advance (Bjo¨rck et al., 1996). It was soon recognised that the sediments of many lakes, particularly the abundant meromictic (permanently stratified) lakes, provided superb records of wellpreserved microfossils, notably diatoms, which could be used indirectly as indicators of palaeo-climate change (e.g., Bronge, 1992; Bjo¨rck et al., 1996;

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Roberts et al., 1999, 2001). Recently, more attention has been given directly to the palaeoecology of Antarctic lakes (e.g., Squier et al., 2002; Verleyen et al., 2004). In many cases, these studies still focus on secondary proxies, in that they examine chemical or genetic signatures of a particular class of organism (e.g. microalgae or phototrophic sulphur bacteria), but, by consideration of a suite of indices, a view of the development of the ecology of a lake can be obtained. Comparative studies of the development of lake ecology through sediment records have been made in Greenland, where most of the lakes are thought to have appeared early in the Holocene (Funder and Fredskild, 1989; Bennike, 1999; Bjo¨rck and Bennike, 2002). In these studies, the colonisation of the Greenland lakes by crustacea was documented, including the arrival during the mid-Holocene climate optimum of an ostracod that is no longer found on the island (Bennike, 2000). The relative paucity of species in these lakes, particularly the absence of large benthic grazers, makes them amenable to such studies. The fauna of many Antarctic lakes is similarly depauperate and, thus, a systematic approach that involves the study of how lake ecology has changed through time should be feasible. In this article, we present the results of the first systematic study of the palaeofauna of a continental Antarctic lake: Ace Lake, in the Vestfold Hills, East Antarctica. This study revealed that major changes have occurred in the biology and productivity of the lake during its development. We use these data, along

with previously-published sediment records, to describe changes in the lake’s ecology. The changes in the ecology recorded in the sediments of Ace Lake provide a model for the ecological development of similar marine-derived saline lakes that occur both elsewhere in the Vestfold Hills (Pickard et al., 1986; Gibson, 1999) and in other regions of Antarctica (Tominaga and Fukui, 1981; Roberts et al., 2004; Verleyen et al., 2004).

2. Study site Ace Lake is situated in the Vestfold Hills, East Antarctica (68828.31V S, 78811.27V E) (Fig. 1). The lake is meromictic and saline, with a limited flora and fauna (for a review, see Rankin et al. (1999)). Physical characteristics of Ace Lake are summarised in Table 1. The lake is located less than 200 m from the nearest marine inlet, Long Fjord, and the sill connecting the lake to the fjord is only marginally above current lake level. The surface level of the lake increased by approximately 2 m between 1978 and 1994, with a concomitant decrease in surface salinity (Gibson and Burton, 1996), indicating the potential for relatively rapid changes in the lake environment. The salinity of Ace Lake increases with depth, with a series of haloclines occurring within the water column (Gibson and Burton, 1996; Gibson, 1999; Rankin et al., 1999). The evolution of Ace Lake has been complex, due in part to the balance between eustatic sea level rise

Fig. 1. Bathymetric map of Ace Lake, showing the approximate location of the core site (star). The left panel shows the position of the lake in the Vestfold Hills (unstippled) and the polar ice sheet (stippled), and the location of the Vestfold Hills on a map of Antarctica. Previously studied cores mentioned in the text were collected in the vicinity of the core site for this study, but the precise locations are uncertain.

L. Cromer et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 221 (2005) 83–97 Table 1 Present day physical and chemical characteristics of Ace Lake (data from Zwartz et al., 1998; Rankin et al., 1999; Gibson, 1999) Area Surface level Sill height Maximum depth Mean depth Salinity range Temperature range Depth of oxic–anoxic interface Ice cover maximum thickness Ice cover duration

18 ha 8.73 m above mean sea level (1997) 9 m above mean sea level 25 m 8.1 m 7–43 g L 1 1–11.4 8C 12 m 1.8–2.0 m 11–12 months per year

and isostatic rebound of the land during the Holocene (Zwartz et al., 1998). Analysis of a series of variables in the lake’s sediment, including stable isotopes, microfossils, pigments from microalgae and photosynthetic sulphur bacteria, and cell-membrane lipid components and genetic signatures of methanogenic archaea, has allowed an outline of the lake’s history to be developed (Volkman et al., 1985; van den Hoff et al., 1989; Bird et al., 1991; Fulford-Smith and Sikes, 1996; Zwartz et al., 1998; Roberts and McMinn, 1999; Roberts et al., 1999; Coolen et al., 2004). The development of the lake can be summarised briefly as follows: after retreat of the polar ice sheet between 13,000 and 10,400 cal years BP (Roberts and McMinn, 1999; Coolen et al., 2004), the lake basin was filled with glacially-derived fresh water, forming bPalaeoQ-Ace Lake. Relative sea level rise resulted in the invasion of the basin by seawater approximately 9400 cal years BP. The marine phase lasted until about 5100 cal years BP, when sea level fell beneath the sill between the lake and the ocean, forming modern Ace Lake and trapping saline water in its basin. Since then, at least two periods of meromixis have occurred, interspersed by periods of holomixis (Burton and Barker, 1979). Further details of the lake’s history are given in the discussion below. The fauna of Ace Lake has been incompletely recorded. The only metazoan regularly recorded in the water column of the lake is the abundant calanoid copepod Paralabidocera antarctica (Bayly and Burton, 1987; Swadling and Gibson, 2000). Ciliates and heterotrophic dinoflagellates have also been recorded (Perriss and Laybourn-Parry, 1997). The main locality of animal biodiversity within the lake is in the verdant

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microbial mats that occur to a depth of at least 10 m. These mats contain cyanobacteria, macro- and microalgae, including diatoms (Roberts and McMinn, 1996), and provide food for a harpacticoid copepod (Idomene scotti: Rankin et al., 1999), three rotifers (Encentrum spatitium, Encentrum salinum and Notholca sp. affin. verae: Dartnall, 1997, 2000), two nematode species and a platyhelminthe (Dartnall, 2000). Dartnall (2000) also recorded the presence of a large, tube-dwelling ciliate, Magnifolliculina sp. The benthic community within the lake is spatially heterogeneous, and a complete inventory of the animal species present has yet to be made.

3. Materials and methods A 185 cm sediment core was collected from the deepest section of Ace Lake in November 1994 using a 3.5 cm diameter Glew corer (Glew, 1989). The core was sectioned into 1 cm segments that were stored in Whirlpak bags at 4 8C for transportation to the University of Tasmania. Salinity of sediment porewater (F 1 g L 1) was measured using a hand-held refractometer after filtration. Water content was determined by drying at 60 8C overnight and measuring the weight loss. The dried samples were then heated to 525 8C overnight and reweighed to determine loss on ignition (LOI). Faunal remains in the sediment were analysed at 5 cm intervals from the surface down to 50 cm, then every 10 cm from 50 to 170 cm, and every 5 cm from 170 cm to the base of the core. Sediment samples were treated as follows to facilitate isolation of faunal remains: 10 ml of a 20% solution of the detergent Calgon was added to approximately 4 g wet sediment in a glass crystallising dish. A few drops of a 1% solution of Rose Bengal were added to stain zooplankton remains and make them more visible under the microscope. The sample was then agitated gently to break up large fragments of organic-rich sediment, and the dish was stored overnight at 4 8C. Faunal remains were isolated by passage of the treated sediment through 200 Am, 100 Am and 44 Am sieves. The samples were washed through the sieves with seawater previously filtered through a glass fibre filter with nominal pore size 0.7 Am. The material retained in each sieve was viewed through a dissecting

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microscope, sorted and counted. The size, shape, colours and any markings of the faunal remains found in the sediment were recorded for identification. Due to the large amount of algae and other decayed organic matter in the sediments, the 44 Am sieve sample often contained too much material to be processed efficiently. A plankton splitter was used to sub-sample this fraction. All abundances given in this article are on a per gram dry weight basis.

4. Results 4.1. Physical and chemical characteristics of the sediment core The sediment core could be separated into six distinct units based on colour, texture, percentage water and LOI (Fig. 2): Unit 1. 177–185 cm. Grey-brown, sandy sediment with low water content (b60%) and LOI (b 12%). Unit 2. 156–177 cm. Red-brown, sandy sediment with water content increasing to 87% and LOI increasing to 19.5%. Unit 3. 67–156 cm. Diffusely banded green sediment with near constant high water content (average 90.4%, SD 1.2%) and high LOI (17.5–22%), except for two horizons with markedly higher values. Unit 4. 51–67 cm. Dark brown-green sediment with a transition to slightly but distinctly lower water content (87–82%) and LOI (N20% to b 17.5%). Unit 5. 25–51 cm. Sediment similar in appearance to Unit 4, but with markedly lower water content (58–64%) and variable LOI (16–25%). Unit 6. 0–25 cm. Reddish-brown sediment containing occasional thin carbonate bands. The water content was similar to Unit 5 (60– 64%), but the LOI was generally lower (12–20%). Sediment porewater salinity also varied markedly throughout the core (Fig. 2). Of particular note were the salinity maxima early in Unit 2 and near the interface between Units 4 and 5.

4.2. Dating of the sediments No radiocarbon dates were obtained in the current study. Previous studies, notably those of Bird et al. (1991), Zwartz et al. (1998), Roberts and McMinn (1999), and Coolen et al. (2004), have provided dates for other cores from Ace Lake, and a reasonably consistent temporal framework for major events in the history of Ace Lake has been built up (Fig. 3). Considerable variation occurs in the sedimentation rate in the three cores studied previously, but the clear transitions in sediment characteristics that occurred at depths of 51 and 156 cm in the core described in this study were evident in the earlier studies, allowing direct comparison of results. A further difficulty is the estimation of the Antarctic reservoir effect that results from the incorporation of old carbon in marine waters into modern material. Roberts and McMinn (1999) estimated a reservoir effect of 974 years and Coolen et al. (2004) 115 years. The most thorough dating of a core from Ace Lake was by Coolen et al. (2004) (Fig. 3), and we use their dating framework in our discussion. 4.3. Faunal diversity and total abundance Animal-derived objects identified in the sediment of Ace Lake were from three distinct classes: animal remains; eggs and spermatophores; and faecal pellets (Fig. 4). Animal remains included calanoid and harpacticoid copepod exoskeletal fragments; tintinnid loricae; rotifer loricae; ciliate tests; and foraminiferal tests. Sixteen different egg types were recorded; of these, only the eggs of Paralabidocera antarctica were positively identified by comparison to modern material. Pictures of egg types not shown in Fig. 4 are available at http://www.xxx. Copepod spermatophores were also abundant at some depths, and appeared identical to those produced by Paralabidocera antarctica. Spermatophores from other species were also likely to be present. Faecal pellets were remarkably well preserved in the sediments (Fig. 4). Intact pellets were recovered from throughout the core with the exception of Unit 1. The species responsible for production of these pellets could not be identified with certainty, but most pellets were identical in shape and size to those produced by Paralabidocera antarctica (Tanimura et al., 1984).

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Fig. 2. Water content (%), loss on ignition (%), porewater salinity (x), and abundances of remains (number per gram dry weight) recorded in the core. Also shown are the total abundance and diversity of remains at each sample depth, and the number of faecal pellets, which are not included in either the total abundance or diversity plots. The sedimentary units described in the text are also given.

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Fig. 3. Comparison of previously published characteristics of cores from Ace Lake with those of the core used in the present study. The initial freshwater stage is indicated in each core by diagonal hatching; the marine phase by small carets; and the saline lake phase by dotted fill. The positions of the lacustrine–marine and marine–lacustrine interfaces are shown (tie lines). The total length of each core is indicated at the base of each column. Also shown for the core used in the current study are the boundaries between the initial seasonally isolated marine basin (SIMB) phase and open marine conditions, and between the second SIMB phase and the saline lake. Also shown are the calibrated radiocarbon dates of Coolen et al. (2004) as well as earlier data (see the original references for further details).

Total abundance of remains (exclusive of faecal pellets) varied significantly with depth (Fig. 2). At the base of the core, 670 remains were recorded per gram dry sediment. Abundance dropped to less than 200 g 1 through Unit 2, but increased again to 300–1100 g 1 before dropping close to the upper limit of Unit 3. Unit 4 was characterised by generally rising abundance that continued in Unit 5, reaching more than 10,000 g 1 at 30 cm. Remain diversity was low at the base of the core, with only a single remain type present in Unit 1 (Fig. 2). Diversity increased markedly in Unit 2, where seven remain types were recorded, and the number of remain types remained in the range 4–9 throughout Unit 3. Diversity was lower in Unit 4, but then increased again in Units 5 and 6. Maximum diversity occurred at 37 cm in Unit 5. 4.4. Distributions and abundances of individual remain types Loricae of the rotifer Notholca sp. affin. verae were the only faunal remains identified in the oldest sediment of the core, and were characteristic of Unit 1 (Fig. 2). Abundance dropped rapidly, and this species was absent from the first sediment segment in which other remains were observed. Loricae were absent

throughout Units 3 and 4, but reappeared in Unit 5, reaching maximum abundance at 27 cm. They continued to be recorded in Unit 6 until the most recent sediments, albeit in reduced numbers. Tests of the ciliate Magnifolliculina sp. were first recorded at low abundance at 173 cm in Unit 2. This small peak was followed by the complete disappearance of the tubes until Unit 5, whereupon they gradually increased to a peak at 26 cm near the boundary with Unit 6. Abundances were lower in the more recent sediments. Tintinnid loricae first appeared in Unit 2. A local maximum in abundance occurred early in Unit 3, but abundance then decreased to near zero throughout the central portion of the unit. Tintinnids again became a major component of the fauna late in Unit 3, and were present through Units 4 and 5. They were absent from Unit 6. More than one species of tintinnid was possibly present in the sediment (L. Cromer, unpublished observation), though for the purposes of this study they were treated as a single remain type. Tests of the foraminiferan Portatrochammina weisneri were recorded at low abundance at one depth in Unit 3, became significantly more abundant in Units 4 and 5, but were absent from Unit 6. Copepod exoskeletal remains were found in Unit 2 at low abundance (4 g 1 at 173 cm), but were absent throughout Unit 3. They reappeared at far higher

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Fig. 4. Light and SEM micrographs of (a) lorica of the rotifer Notholca sp. affin. verae (length 180 Am); (b) tests of the ciliate Magnifolliculina sp. (length 200 Am), (c) copepod exoskeletal remains (breadth 150 Am); (d) egg type AC4 (diameter 120 Am); (e) faecal pellet recovered from 22 cm (scale bar 100 Am); (f) faecal pellet recovered from 122 cm (scale bar 100 Am).

abundances in Unit 5, before disappearing abruptly. No exoskeletal remains were recovered from Unit 6. The species represented by these remains were difficult to determine, as many were only small portions of the entire exoskeletons. Most of the more complete exoskeletons belonged to harpacticoid copepods, but further identification was impossible. The distribution of spermatophores was very similar to that

of the exoskeletal remains. They were largely absent from Units 1– 3 (a single spermatophore was observed at 85 cm), but became more common at the top of Unit 4. Peak abundance occurred just below the boundary between Units 5 and 6. Of the sixteen different egg types observed, only one, designated AC1 and identical to those of modern Paralabidocera antarctica, was positively identified.

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This egg type was present sporadically and at low abundance through Units 2 and 3. It became more abundant at the top of Unit 4, reaching a peak around the boundary between Units 5 and 6. A second egg type, AC2, displayed morphological similarities to those of Paralabidocera antarctica, but was slightly smaller. AC2 was present in Units 2 and 3, being consistently present at moderate abundances throughout the latter unit. It was nearly absent throughout Unit 4, but was the dominant egg type at 37 cm, a depth at which egg type AC1 was nearly absent. The remaining 14 egg types varied significantly in size and other characteristics. The maximum abundance of any of these egg types was 300 g 1 (AC3 at 37 cm), and none of the others exceeded 40 g 1. Faecal pellets were absent from the oldest sediments. They were initially observed in Unit 2 and continued to be present at moderate abundances throughout most of Unit 3, though becoming rare by the top of the unit and at the base of Unit 4. Maximum abundance occurred in Unit 5.

5. Discussion In order to be preserved in lacustrine sediments, animal remains must either be pre-adapted to preservation (e.g., resting and diapause eggs), or contain some body parts resistant to degradation under both oxic and anoxic conditions. The degradation rate of remains, which are made up of complex organic material such as chitin, will be slower under anoxic conditions as the bacteria present are able to utilise a smaller range of organic molecules than those in oxygenated conditions. Preservation of remains under methanogenic conditions will be even better, as methanogens metabolise an even more limited range of simple organic molecules. The small area of the sediment sampled when collecting a core may not reflect the biota at other sites in the lake. In particular, collection of a core from beneath the oxic–anoxic interface of a meromictic lake requires that organisms associated with the benthic microbial mats in the areas of the lake in which the surface sediment is oxygenated must be transported to the core site. Thus, the absence of a particular species from a sediment sample does not necessarily imply its absence from the lake.

The majority of the animal remains recovered from the most recent sediments are represented by organisms known to live in the lake today. No remains of nematodes, some rotifers or platyhelminthes (Dartnall, 1997, 2000) were recorded, highlighting that the method used here will provide an incomplete representation of the actual faunal community. This problem is also reflected in the presence of three egg types (AC4, AC5 and AC8) in the near-surface sediment that have yet to be attributed to a current lake inhabitant. The problem of egg identification occurs throughout the core, giving indications of at times a more complex community without revealing its components. We are pursuing molecular genetic approaches to identify these unknown components of the community. The sediments of Ace Lake contain a series of animal remains rarely recorded in other Antarctic lakes or in previous sediment studies. This may have been in part the result of the complex history of the lake that resulted in marine organisms being preserved in a lacustrine system. The chemistry (deep-water anoxia), biology (lack of benthic grazers) and physics (low temperature) of the lake would also have aided preservation. The occurrences of rarely recorded types are discussed in the following paragraphs. Skeletal remains of copepods are rarely observed in Quaternary sediments, as they rapidly break down as a result of ingestion by other organisms or bacterial decomposition (Frey, 1964). Spermatophores are far more common in Quaternary sediments (Warner, 1989), and copepod eggs are well preserved (e.g., Bennike, 1998), as they are resistant to breakdown and do not hatch under anoxic conditions (Marcus et al., 1994). The shape and size of the eggs are typically not diagnostic for a particular species, and, unless modern examples can be used for detailed comparison, it is difficult to identify the species that produced them. Copepod skeletal remains were only recorded in this study when egg and spermatophores were abundant, indicating that at these times copepods were present at high densities. Intact copepod faecal pellets have rarely been recorded in lake or marine sediments, as they generally undergo decomposition through coprophagy or microbial processes, either in the water column

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or at the sediment surface. The environments from which they have been reported are typically meromictic, suggesting that rapid transfer to anoxic conditions aids in their preservation (Haberyan, 1985; Dean et al., 2001). The ciliate Magnifolliculina sp. or its close relatives have not been recorded previously from recent sediments. The life-cycle of this ciliate includes a planktonic juvenile stage that eventually settles to the benthos. Folliculinids are epibionts on crustacea or periphyton in marine and fresh waters (Corliss, 1961; Yankovskii, 1998). From the distribution of folliculinid tests in the Ace Lake core, it is apparent that the species prefers conditions in which the basin has only limited exchange with the ocean or when it was completely isolated (see below). This may reflect retention of larval stages within the basin that would allow build up of a significant population, or the enhanced preservation of tests under anoxic conditions. Tintinnids are common components of the pelagic marine ecosystem but are rarely found in pelagic sediment traps or in deep-sea Neogene sediments (W. Howard, personal communication). These ciliates are also relatively common components of the ecosystems of large temperate freshwater lakes, though it has been suggested that they are absent from Antarctic lakes (Bell and Laybourn-Parry, 1999). Fossilised folliculinid tests and tintinnid loricae have been reported in siliceous nodules (possibly Late Cretaceous) from Gabon and in Late Jurassic carbonates from the Mediterranean region respectively (Colom, 1948; Deflandre and Deunff, 1957). Deflandre and Deunff (1957) suggested that the nodules containing the folliculinid fossils were formed in a brackish lagoon. The abundance of subfossil loricae in Ace Lake sediments suggests that shallow, semi-isolated marine systems may be good models for the conditions under which the older fossils originated. Fossil or sub-fossil rotifers have been recorded occasionally; their loricae can be abundant components in fossil peat and gyttja deposits (Frey, 1964; Warner and Chengalath, 1988). The distribution of the rotifer Notholca sp. affin. verae in the sediments of Ace Lake is unusual, in that the species occurs both in the initial freshwater unit, as well as in Units 4–6 when the lake basin contained saline water. Dartnall (2000) reported slight morphological differences

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between individuals of this species found in brackish and saline lakes in the Vestfold Hills, with animals from more saline environments having a slim, Ushaped lorica, while freshwater individuals were more spherical. In Ace Lake sediments, the freshwater form was found in Unit 1, whereas the brackish form was present in Units 4 – 6. Foraminiferans are common in marine ecosystems and are present in some freshwater and saline lakes at lower latitudes (e.g., Holzmann and Pawlowski, 2002), but have not been reported from Antarctic lakes. Portatrochammina weisneri survived in Ace Lake until at least the middle of Unit 5, but appears to be absent from the modern lake. The genus Portatrochammina has been recorded as a component of the benthic fauna of inshore Antarctic marine sediments (Bernhard, 1987), and as an epibiont on an Antarctic bryozoan (Zampi et al., 1997). 5.1. Changes in the ecology of Ace Lake The results of the current study, in conjunction with those of earlier studies, can be used to develop a coherent view of how physical changes have affected the ecology of Ace Lake. In the following paragraphs, the faunal data are integrated with information from previous studies to provide a depiction of how the ecology of Ace Lake has changed with time. The physical changes that have in part driven these changes in the lake’s ecology are illustrated in Fig. 5. 5.1.1. Unit 1—Freshwater lake (N 10,400–9400 cal years BP) The only animal remains recorded in Unit 1 were loricae of the rotifer Notholca sp. affin. verae. Swadling et al. (2001) also reported the presence of empty sheaths of filamentous cyanobacteria, chrysophyte cysts, dinoflagellate cysts and a testate amoeba in this unit. A freshwater diatom flora was present (Roberts and McMinn, 1999), as was the prasinophyte Pyramimonas gelidicola (van den Hoff et al., 1989: note that this study used the same core as that of Bird et al., 1991 and Zwartz et al., 1998). Coolen et al. (2004) concluded that active methane production by freshwater methanogens occurred in the lake sediments during this period. From these observations, it can be concluded that soon after Palaeo-Ace Lake was

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L. Cromer et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 221 (2005) 83–97 Lake level Sea level Unit 1 Freshwater lake ca. 13000 – 9400 cal yr BP Signature species: Notholca Anoxia: absent

Unit 2: Seasonally isolated marine basin 9400 – ca. 9000 cal yr BP Signature species: Tintinnids Anoxia: present

Unit 3: Open marine basin ca. 9000 – 5700 cal yr BP Signature species: Copepods Anoxia: absent

Unit 4: Seasonally isolated marine basin 5700 – ca. 5100 cal yr BP Signature species: Tintinnids Anoxia: present

Unit 5, 6: Saline lake ca. 5100 cal yr BP – Present Signature species: copepods, Notholca and Magnifolliculina Anoxia: present

Fig. 5. Relative lake and/or sea level during the development of Ace Lake. Units 5 and 6 are separated on sediment characteristics (see text). Estimated ages for transitions between units are given, as are the distinctive faunal remains found in the sediment and the probable presence or absence of anoxia within the basin.

formed, a relatively simple freshwater ecosystem consisting of a microbial mat community, planktonic autotrophs and limited grazers developed. The absence of sulphate reduction in the sediments indicates that input of saline water into the basin through seawater incursions had not occurred (the high salinity porewater in this unit (Fig. 2) was the result of displacement of the less dense freshwater after subsequent introduction of seawater into the basin). 5.1.2. Unit 2—Seasonally isolated marine basin (9400–ca. 9000 cal years BP) Sea level has risen by ca. 120 m since the last glacial maximum (Lambeck and Chappell, 2001), but in the Vestfold Hills this has been offset by isostatic rebound in response to a thinning of the Antarctic polar ice sheet. Over the Holocene, this has led to a net decrease in relative sea level relative to the land

(Zwartz et al., 1998). However, the emergence of the land has not occurred uniformly and, around 9400 cal years BP, sea level reached the level of the sill between Ace Lake and Long Fjord (Fig. 1), resulting in seawater entering the lake (Zwartz et al., 1998). There must have been an initial period when the connection between the lake and ocean only occurred during summer, being blocked during winter by the 1.5 m thick ice that typically forms on the lakes. Similar seasonally isolated marine basins (SIMBs) occur in the Vestfold Hills today (Gibson, 1999). Replacement of freshwater would have occurred rapidly (within a few years) as any salt water entering the lake on the inflowing tide would sink under the freshwater layer, and the water lost as the tide ebbed would be less dense freshwater. The salinity of water at the base of modern-day SIMBs can reach over 100 g L 1 as a result of freeze-concentration of brine during winter, especially when there is only limited exchange with the ocean (Gibson, 1999). The high salinity porewater early in Unit 2 is consistent with the formation of a SIMB. The inflowing marine water would carry with it a collection of planktonic organisms that could colonise the basin, and there is clear evidence of this process occurring from the characteristics of the sediment. Firstly, the water content of the core increased to about 84%, indicating a dramatic change in sedimentation conditions from the freshwater lake. Secondly, there is the concerted appearance in the core of the remains from a suite of putatively marine-derived organisms, including copepods (eggs, skeletal remains and faecal pellets), the marine ciliate Magnifolliculina sp., tintinnids, and other, unidentified, eggs. Numerous other species must also have entered the lake, but either were not present at high abundance in the basin, or did not leave identifiable remains. It is probable that the basin was meromictic during this period, as are many modern-day SIMBs (Gibson, 1999). Bird et al. (1991) recorded a maximum in percentage sulphur in the sediment in this unit, consistent with a partially anoxic water column. Increasing sea level would have shortened the period that the basin was isolated until exchange occurred throughout the year. We suggest that the boundary between Units 2 and 3 occurred at this time.

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5.1.3. Unit 3—Marine inlet (ca. 9000–5700 cal years BP) The transition to Unit 3 was indicated by a slight but distinct increase in water content and loss on ignition (Fig. 2), and the disappearance of Magnifolliculina sp. Bird et al. (1991) recorded a drop in percentage sulphur in the sediments, indicating that meromixis broke down and the basin became totally mixed through tidal action. The abundance of faunal remains recorded in Unit 3 was lower than elsewhere in the core even though diversity was quite high (Fig. 2). This might be construed to imply that the basin was less productive, though it is more likely that the paucity of remains reflects active benthic grazing by a community probably similar to that that currently occurs in the inshore marine waters of the Vestfold Hills (Tucker and Burton, 1988) or enhanced bacterial breakdown under oxic conditions. The relative absence of zooplankton eggs could also reflect efficient hatching. If there were no anoxic conditions to inhibit egg hatching (and also to aid their preservation in the sediment), the number of eggs in the sediment would not necessarily reflect total egg production. The diversity of eggs that were preserved in the sediment, however, indicates that the community was quite complex. Early, mid and late marine units can be identified by the relative abundance of tintinnid loricae, which were common early in Unit 3, largely absent through the middle section, and common again late in the unit. Roberts and McMinn (1999) recorded a very similar distribution in the sediments of Ace Lake for a series of diatom species, including Amphora sp. and Cocconeis sp., while other species were more abundant in the middle of the unit (e.g., Chaetoceros spp.). The first two species are benthic, while Chaetoceros spp. are planktonic. These data are consistent with increased water level in the basin and therefore greater tidal mixing during the middle section of Unit 3. Why the tintinnids should be more abundant under protected conditions is uncertain. These ciliates generally live throughout the water column at depths of up to 1000 m, and would therefore seem adapted to a pelagic existence. The absence of tintinnids from the middle part of Unit 3 might indicate removal by grazing, but perhaps also reflects a preference of these animals for a close association with benthic mats.

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5.1.4. Unit 4—Seasonally isolated marine basin (5700–ca. 5100 cal years BP) As relative sea level decreased Ace Lake would have slowly returned to SIMB status (Fig. 5). Water content and LOI of the sediment dropped, meromixis reformed (Bird et al., 1991) and benthic grazing probably decreased. As the marine influence lessened, a reduction in biodiversity would have occurred as species, notably benthic grazers reliant on the immigration of larval stages into the basin, could no longer maintain populations. Similar loss of biodiversity has been noted in marine lakes formed by isostatic uplift in modern times (Stro¨m and Klaveness, 2003), and other SIMBs in the Vestfold Hills have impoverished zooplankton communities relative to the marine systems to which they are seasonally connected (Bayly, 1986; Eslake et al., 1991). The reduction in grazing pressure and/or competition were probably reasons that remains of a number of species rarely observed throughout Unit 3 were more common in Unit 4. Pyramimonas gelidicola was particularly abundant at times in Unit 4 (van den Hoff et al., 1989), and the absence of cysts, present throughout the marine phase of the lake, possibly indicated a less stressful environment for this species. Pyramimonas gelidicola has been shown to bloom in low salinity water immediately beneath the ice in Ellis Fjord, Vestfold Hills (Gibson, 1998); the reduced tidal action in the basin during this period would allow the build up of such a layer through spring and summer melt at the base of the ice cover and input of freshwater from melting snow banks. The end of Unit 4 was marked by a sharp increase in porewater salinity that mirrored that observed early in Unit 2. The same physical situation was present—limited exchange between the lake and ocean—which resulted in the formation of high salinity water at the base of the water column. The timing of the end of Unit 4 is difficult to determine from the data of Coolen et al. (2004). The estimate given here takes into account the approximate rate of relative sea level change at the time (Zwartz et al., 1998) and the tidal range. 5.1.5. Unit 5—Saline lake (ca. 5100–3000 cal years BP) We interpret the sudden decrease in water content of the sediment at the base of Unit 5 to

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reflect effective cut off of the lake from the marine system. Whether this decrease was the result of cessation of tidal influence, or a change in the chemistry and/or biota, is uncertain. If tidal influence were more important, it is probable that occasional spring tidal input of marine biota, as observed for nearby Lake Fletcher (Eslake et al., 1991), continued for a period until complete separation occurred. The response of the biota to isolation appears to have been an initial decrease in abundance of organisms followed by a dramatic peak both in abundance and diversity. The first species for which there is evidence of an increase was the ciliate Magnifolliculina sp., which appeared in the sediments for the first time since Unit 2. Portatrochammina weisneri then increased in abundance, followed by copepods and Notholca sp. affin. verae. The rotifer had been present at low abundances since the re-isolation of the lake, indicating that the increase in abundance was not due to colonisation of the lake, but rather that conditions for growth were better. During the same period there was a peak in the abundance of Pyramimonas gelidicola (van den Hoff et al., 1989), indicating that the lake became more productive after isolation. There was also a large peak in organic carbon as determined by loss on ignition, also reflecting the greater productivity of the lake. The peak in diversity probably reflected rare species becoming sufficiently common for their remains to be recorded in this study, rather than colonisation of the lake by new species. However, the foram, tintinnids and egg type AC2 disappeared from the core at about the time of maximum remain abundance and diversity, indicating that competition for resources was high. 5.1.6. Unit 6—Saline lake (3000 cal years BP–present) We separate Units 5 and 6 on the basis of the physical characteristics of the sediment, which changed in colour and texture. The interface also coincided with the disappearance of copepod exoskeletons and spermatophores from the core. A clue to the process that occurred at this boundary comes from the work of Coolen et al. (2004), who indicated that an active methane cycle became re-established in the lake at this time. Ace Lake is the only saline lake in the Vestfold Hills in which the low sulphate concen-

tration allows this process to occur. Nearly 80% of the sulphur has been lost from the lake, and sulphur isotopic data are consistent with overturn of a sulphide-rich meromictic lake that resulted in massive venting of gaseous H2S to the atmosphere (Burton and Barker, 1979). That this happened after a particularly productive period in the lake’s history is consistent, as production of H2S in anoxic waters is linked to anaerobic remineralisation of autotrophically-produced organic material by sulphate reducing bacteria (Overmann, 1997). Coolen et al. (2004) also report high concentrations of indicators for photosynthetic sulphur bacteria in this sediment at this depth, consistent with high concentrations of H2S and the positioning of the oxic–anoxic interface quite close to the surface of the lake. Coolen et al. (2004) date this episode at ca. 3000 cal years BP, consistent with a warm phase in the Vestfold Hills recorded by McMinn et al. (2001). The warmer climate increased production through reduced ice cover, and longer ice-free periods facilitated lake turnover. Whole lake mixing may have resulted in the entire water column being anoxic for a period, resulting in the extinction of species that did not have stages that could survive these conditions. In the recent sediments deposited at the top of Unit 6, the abundances of the ciliate, rotifer and copepod eggs have decreased in concert. Pyramimonas gelidicola has also been present at relatively low numbers (van den Hoff et al., 1989), and for the first time since the lake was re-isolated, cysts appear, reflecting greater environmental stress (van den Hoff et al., 1989). This gradual decline is likely to be due to a decrease in nutrient availability as nutrients are buried in the sediment and are not available for further production. Furthermore, the current structure of the lake, in which there is a strong mid-water halocline within the oxic zone (Gibson, 1999), prevents inmixing of nutrient-rich anoxic water into the surface waters where highest light levels, and therefore greatest productivity, occur. The age of this feature is not known, but it has been present in the water column since the lake was first visited in the 1970s (Gibson and Burton, 1996). Significantly lower water level leading to increased surface salinity would be required for the lake to mix through this halocline. The data of Roberts et al. (2001) indicate that such low water level may not have been reached in the last

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650 years. If so, we may be seeing evidence of this block to productivity in the lower abundance of faunal remains in the surface sediments. 5.2. Implications for the future of Ace Lake and other coastal Antarctic lakes The general reduction in the biodiversity of Ace Lake since isolation from the ocean is likely to continue as long as Ace Lake remains separated from the marine environment. The species present will remain in the lake if the physical and chemical conditions remain within their tolerances and while their food sources continue to exist. In the longer term it is likely that further local extinctions will occur as water salinity and temperature rise and fall, or as another species in a trophic web disappears. To balance loss of the strictly marinederived species, new species will disperse to the lake. While there is no evidence for the development of populations of recently-arrived animals in Ace Lake, successful colonisations by metazoa have occurred in nearby, previously saline lakes that have had most of the salt flushed from them (Laybourn-Parry et al., 2002). If sea level were to rise and re-enter Ace Lake and other marine derived lakes, new populations of marine organisms would become re-established within the lake basins. The species that had survived the vicissitudes of changes in the lake environment would now be in competition with less adaptable species that recolonised the basin, though at the same time the long-term survivors would be reinforced by an influx of conspecifics from the marine environment.

Acknowledgements This work was funded by the Australian Antarctic Science Advisory Committee (Projects 706 and 2387). Further funding was obtained through an ARC Discovery Grant and the Transantarctic Association. Peter Sprunk assisted with collection of the sediment core. We thank Professor Pat Quilty for identifying the foraminiferan, and Camille White, Karin Beaumont and E´milie Saulnier-Talbot for some of the photos and general discussion.

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Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/ j.palaeo.2005.02.005. References Bayly, I.A.E., 1986. Ecology of the zooplankton of a meromictic Antarctic lagoon with special reference to Drepanopus bispinosus (Copepoda: Calanoida). Hydrobiologia, 140, 199 – 231. Bayly, I.A.E., Burton, H.R., 1987. Vertical distribution of Paralabidocera antarctica (Copepoda: Calanoida) in Ace Lake, Antarctica, in summer. Australian Journal of Marine and Freshwater Research, 38, 537 – 543. Bell, E.M., Laybourn-Parry, J., 1999. The plankton community of a young, eutrophic, Antarctic saline lake. Polar Biology, 22, 248 – 253. Bennike, O., 1998. Fossil egg sacs of Diaptomus (Crustaceae: Copepoda) in late Quaternary lake sediments. Journal of Paleolimnology, 19, 77 – 79. Bennike, O., 1999. Colonisation of Greenland by plants and animals after the last ice age: a review. Polar Record, 35, 323 – 336. Bennike, O., 2000. Palaeoecological studies of Holocene lake sediments from west Greenland. Palaeogeography, Palaeoclimatology, Palaeoecology, 155, 285 – 304. Bernhard, J.M., 1987. Foraminiferal biotopes in Explorers Cove, McMurdo Sound, Antarctica. Journal of Foraminiferal Research, 17, 286 – 297. Bird, M.I., Chivas, A.R., Radnell, C.J., Burton, H.R., 1991. Sedimentological and stable-isotope evolution of lakes in the Vestfold Hills, Antarctica. Palaeogeography, Palaeoeclimatology, Palaeoecology, 84, 109 – 130. Bjo¨rck, S., Bennike, O., 2002. Chronology of the last recession of the Greenland Ice Sheet. Journal of Quaternary Science, 17, 211 – 217. Bjo¨rck, S., Olsson, S., Ellis-Evans, C., Hakansson, H., Humlum, O., de Lirio, J.M., 1996. Late Holocene palaeoclimatic records from lake sediments on James Ross Island, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology, 121, 195 – 220. Bronge, C., 1992. Holocene climatic record from lacustrine sediments in a fresh-water lake in the Vestfold hills, Antarctica. Geografiska Annaler, 74 (A), 47 – 58. Burton, H.R., Barker, R.J., 1979. Sulfur chemistry and microbiological fractionation of sulfur isotopes in a saline Antarctic lake. Geomicrobiology Journal, 1, 329 – 340. Colom, G., 1948. Fossil tintinnids: loricated infusoria of the order Oligotricha. Journal of Paleontology, 22, 233 – 263. Coolen, M.J.L., Hopmans, E.C., Rijpstra, W.I.C., Muyzer, G., Schouten, S., Volkman, J.K., Sinninghe Damste´, J.S., 2004. Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Organic Geochemistry, 35, 1151 – 1167.

96

L. Cromer et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 221 (2005) 83–97

Corliss, J.O., 1961. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature. Pergamon Press, Oxford. Dartnall, H.J.G., 1997. Three new species of Encentrum (Rotifera) from the Antarctic. Quekett Journal of Microscopy, 38, 15 – 20. Dartnall, H.J.G., 2000. A limnological reconnaissance of the Vestfold Hills. ANARE Research Notes, 141, 1 – 53. Dean, J.M., Kemp, A.E.S., Pearce, R.B., 2001. Palaeo-flux records from electron microscope studies of Holocene laminated sediments, Saanich Inlet, British Columbia. Marine Geology, 174, 139 – 158. Deflandre, G., Deunff, J., 1957. Sur la pre´sence de cilie´s fossiles de la famille des Folliculinidae dans un silex du Gabon. Comptes Rendus de l’Acade´mie des Sciences, 244, 3090 – 3093. Eslake, D., Kirkwood, R., Burton, H., Zipan, Wang, 1991. Temporal changes in zooplankton composition in a hypersaline, Antarctic lake subject to periodic seawater incursions. Hydrobiologia, 210, 93 – 99. Frey, D.G., 1964. Remains of animals in Quaternary lake and bog sediments and their interpretation. Archiv fqr Hydrobiologie Beiheft, Ergebnisse der Limnologie, 2, 1 – 114. Fulford-Smith, S.P., Sikes, E.L., 1996. The evolution of Ace Lake, Antarctica, determined from sedimentary diatom remains. Palaeogeography, Palaeoeclimatology, Palaeoecology, 124, 73 – 86. Funder, S., Fredskild, B., 1989. Palaeofaunas and floras (Greenland). In: Fulton, R.J. (Ed.), Quaternary Geology of Canada and Greenland. Geological Survey of Canada, Ottawa, pp. 775 – 783. Gibson, J.A., 1998. Carbon flow through the inshore marine waters of the Vestfold Hills. ANARE Scientific Reports, 139, 1 – 221. Gibson, J.A.E., 1999. The meromictic lakes and stratified marine basins of the Vestfold Hills, East Antarctica. Antarctic Science, 11, 175 – 192. Gibson, J.A.E., Burton, H.R., 1996. Meromictic Antarctic lakes as indicators of climate change: the structures of Ace and Organic Lakes, Vestfold Hills, Antarctica. Papers and Proceedings of the Royal Society of Tasmania, 130, 73 – 78. Glew, J.R., 1989. A new trigger mechanism for sediment samplers. Journal of Paleolimnology, 1, 241 – 244. Haberyan, K.A., 1985. The role of copepod fecal pellets in the deposition of diatoms in Lake Tanganyika. Limnology and Oceanography, 30, 1010 – 1023. Hodgson, D.A., Noon, P.E., Vyverman, W., Bryant, C.L., Gore, D.B., Appleby, P., Gilmour, M., Verleyen, E., Sabbe, K., Jones, V.J., Ellis-Evans, J.C., Wood, P.B., 2001. Were the Larsemann Hills ice-free through the Last Glacial Maximum? Antarctic Science, 13, 440 – 454. Holzmann, M., Pawlowski, J., 2002. Freshwater foraminiferans from Lake Geneva: past and present. Journal of Foraminiferal Research, 32, 344 – 350. Lambeck, K., Chappell, J., 2001. Sea level change through the last glacial cycle. Science, 292, 679 – 686. Laybourn-Parry, J., Quayle, W., Henshaw, T., 2002. The biology and evolution of Antarctic saline lakes in relation to salinity and trophy. Polar Biology, 25, 542 – 552.

Marcus, N.H., Lutz, R., Burnett, W., Cable, P., 1994. Age, viability, and vertical-distribution of zooplankton resting eggs from an anoxic basin—evidence of an egg bank. Limnology and Oceanography, 39, 154 – 158. McMinn, A., Heijnis, H., Harle, K., McOrist, G., 2001. LateHolocene climatic change recorded in sediment cores from Ellis Fjord, eastern Antarctica. The Holocene, 11, 291 – 300. Overmann, J., 1997. Mahoney Lake: a case study of the ecological significance of phototrophic sulfur bacteria. Advances in Microbial Ecology, 15, 251 – 288. Perriss, S.J., Laybourn-Parry, J., 1997. Microbial communities in saline lakes of the Vestfold Hills (eastern Antarctica). Polar Biology, 18, 135 – 144. Pickard, J., Adamson, D.A., Heath, C.W., 1986. The evolution of Watts Lake, Vestfold Hills, East Antarctica, from marine inlet to freshwater lake. Palaeogeography, Palaeoclimatology, Palaeoecology, 53, 271 – 288. Rankin, L.M., Gibson, J.A.E., Franzmann, P.D., Burton, H.R., 1999. The chemical stratification and microbial communities of Ace Lake: a review of the characteristics of a marine-derived meromictic lake. Polarforschung, 66, 33 – 52. Roberts, D., McMinn, A., 1996. Relationships between surface sediment diatom assemblages and water chemistry gradients in saline lakes of the Vestfold Hills, Antarctica. Antarctic Science, 8, 331 – 341. Roberts, D., McMinn, A., 1999. A diatom-based palaeosalinity history of Ace Lake, Vestfold Hills, Antarctica. The Holocene, 9, 401 – 408. Roberts, D., McMinn, A., Cremer, H., Gore, D.B., Melles, M., 2004. The Holocene evolution and palaeosalinity history of Beall Lake, Windmill Islands (East Antarctica) using an expanded diatom-based weighted averaging model. Palaeogeography, Palaeoclimatology, Palaeoecology, 208, 121 – 140. Roberts, D., Roberts, J.L., Gibson, J.A.E., McMinn, A., Heijnis, H., 1999. Palaeohydrological modelling of Ace Lake, Vestfold Hills, Antarctica. The Holocene, 9, 515 – 520. Roberts, D., van Ommen, T.D., McMinn, A., Morgan, V., Roberts, J.L., 2001. Late-Holocene East Antarctic climate trends from icecore and lake sediment proxies. The Holocene, 11, 117 – 120. Squier, A.H., Hodgson, D.A., Keely, B.J., 2002. Sedimentary pigments as markers for environmental change in an Antarctic lake. Organic Geochemistry, 33, 1655 – 1665. Stro¨m, T.-E., Klaveness, D., 2003. Hunnebotn: a seawater basin transformed by natural and anthropogenic processes. Estuarine, Coastal and Shelf Science, 56, 1177 – 1185. Swadling, K.M., Gibson, J.A.E., 2000. Grazing rates of a calanoid copepod (Paralabidocera antarctica) in a continental Antarctic lake. Polar Biology, 23, 301 – 308. Swadling, K.M., Dartnall, H.J.G, Gibson, J.A.E., Saulnier-Talbot, E´., Vincent, W.F., 2001. Fossil rotifers and the early colonization of an Antarctic lake. Quaternary Research, 55, 380 – 384. Tanimura, A., Minoda, T., Fukuchi, M., Hoshiai, T., Ohtsuka, H., 1984. Swarm of Paralabidocera antarctica (Calanoida, Copepoda) under sea ice near Syowa Station, Antarctica. Antarctic Record, 82, 12 – 19. Tominaga, H., Fukui, F., 1981. Saline lakes at Syowa Oasis, Antarctica. Hydrobiologia, 82, 375 – 389.

L. Cromer et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 221 (2005) 83–97 Tucker, M.J., Burton, H.R., 1988. The inshore marine ecosystem of the Vestfold Hills. Hydrobiologia, 165, 129 – 139. van den Hoff, J., Burton, H.R., Vesk, M., 1989. An encystment stage, bearing a new scale type, of the Antarctic prasinophyte Pyramimonas gelidicola and its palaeolimnological and taxonomic significance. Journal of Phycology, 25, 446 – 454. Verleyen, E., Hodgson, D.A., Sabbe, K., Vanhoutte, K., Vyverman, W., 2004. Coastal oceanographic conditions in the Prydz Bay region (East Antarctica) during the Holocene recorded in an isolation basin. The Holocene, 14, 246 – 257. Volkman, J., Allen, D.I., Stevenson, P.L., Burton, H.R., 1985. Bacterial and algal hydrocarbons in sediments from a saline Antarctic lake, Ace Lake. Organic Geochemistry, 10, 671 – 681. Wagner, B., Cremer, H., Hultzsch, N., Gore, D.B., Melles, M., 2004. Late Pleistocene and Holocene history of Lake Terrasovoje, Amery Oasis, East Antarctica, and its climatic and

97

environmental implications. Journal of Paleolimnology, 32, 321 – 339. Warner, B.G., 1989. Other fossils. Geoscience Canada, 16, 231 – 242. Warner, B.G., Chengalath, R., 1988. Fossil Habrotrocha angusticollis (Rotataria: Bdelloidea) in North America. Journal of Paleolimnology, 1, 329 – 338. Yankovskii, A.V., 1998. Folliculina boltoni in periphyton of Lake Baikal and review of freshwater folliculinids (Ciliophora, Spirotricha). Zoologicheskii Zhurnal, 77, 389 – 396. Zampi, M., Beocci, S., Focardi, S., 1997. Epibiont foraminifera of Sertella frigida (Waters) (Bryozoa, Cheilostomata) from Terranova Bay, Ross Sea, Antarctica. Polar Biology, 17, 363 – 370. Zwartz, D., Bird, M., Stone, J., Lambeck, K., 1998. Holocene sea-level change and ice-sheet history in the Vestfold Hills, East Antarctica. Earth and Planetary Science Letters, 155, 131 – 145.