Evolution of the Austral-Antarctic fl ora during the Cretaceous : New insights from a paleobiogeographic perspective

Fores t environments have continuously existed in Antarctica since the late Paleozoic and only disappeared from this continent since the Neogene. Nevertheless, the structure of these forests underwent substantial evolutionary changes. During the late Cretaceous, forests dominated by conifers and pteridophytes were gradually replaced by angiospermdominated forests. Elements common to these Antarctic forests are important constituents of the recent Valdivian Forest. During the Turonian stage of the Late Cretaceous, the Antarctic Peninsula and Patagonia were reconnected by a land bridge after a separation since the end of the Jurassic. Using biogeographic tools applied to the palynological and leaf imprint record, outcrops of Campanian-Maastrichtian age were studied from the Snow Hill, James Ross and Seymour (Marambio) Islands in the James Ross basin, Antarctica; Skua Bay, Half Three Point, Price Point and Zamek Hill on King George Island, Antarctica, and Rocallosa Point, Cerro Guido, Las Chinas, Dorotea Hill, Cazador Hill and La Irene in Chilean-Argentinian Patagonia, comparing the current distribution and the paleogeography, as well as the infl uence of potential areas of endemism and vicariants events. The analysis indicates that vegetation evolved under environmental conditions subject to intense volcanic and climatic disturbances, with changes from a period with extreme greenhouse climate (Turonian-Campanian) to strong cooling during the Maastrichtian. We suggest that a continuous forest existed in southern South America and Antarctica, which was shaped during the Latest Cretaceous by the presence of marine basins and and intermittent connection and disconnection of the fl ora.


INTRODUCTION
Forest ecosystems have existed in Antarctica since the Late Paleozoic (Axelrod 1984, Hunt & Poole 2003, Taylor et al. 1992) evolving mainly in conditions warmer than the present, until the Neogene (Cantrill 2001, Francis & Poole 2002), when a sharp drop in temperature occurred at the Oligo-Miocene boundary.The structure of vegetation, however, under went considerable changes, from forests dominated by conifers and pteridophytes during the Early Cretaceous (Falcon-Lang et al. 2001) to forests dominated by angiosperms, similar to Valdivian forests of southern Chile.These last conditions gradually established during the Late Cretaceous, after the massive radiation of angiosperms throughout Gondwana.Common elements of these Upper Cretaceous fl oras of Antarctica are now well represented in different types of modern Chilean forests (Dutra & Batten 2000, Poole et al. 2001, Cantrill & Poole 2002, Leppe et al. 2007).Deposits of Late Cretaceous and Paleogene age are well recorded from the James Ross Basin and the Fildes Peninsula Group, King George Island, as well as from the Magallanes basin in southern Patagonia (Cantrill 1997, 2000, Torres et al. 1997, Césari et al. 1999).Paleoecological reconstructions indicate that fl oristic casts have evolved in the context of environments under intense volcanic disturbance (Poole et al. 2001).Climatically, the Late Cretaceous was one of the warmest periods of the Phanerozoic, with warm pulses during the Turonian and cold events during the Maastrichtian (Huber 1998).Low temperatures near to the end of the Cretaceous were again followed by an increase in temperature, or climatic optimum, during the Paleocene and Eocene (Upchurch et al. 1998).
A ter r estrial connection during the Campanian-Maastrichtian between South America and Antarctica is crucial to understand the establishment of a new structure in the austral vegetation.Upper Jurassic-Lower Cretaceous taxa evolved isolated in both Antarctic and Patagonian communities until the reestablishment of a terrestrial bridge between both landmasses during the Turonian (Pankhurst & Smellie 1983, Smellie et al. 1984).During the Campanian-Maastrichtian this connection led to a new mixed Antarctic-Patagonian biota predecessor of moder n southern South American temperate forests.Recently, new arguments have extended the discussion about the origins and persistence of these southern temperate biota, particularly of the Valdivian forest, a broadleaf and mixed forest ecoregion on the west coast of southern South America, mostly in Chile and western Argentina (Poole et al 2003, Povilauskas et al. 2008).Several authors have pointed out that the Valdivian forest is the closest equivalent to Upper Cretaceous-Paleogene forests from Antarctica (Axelrod 1984, Francis & Poole 2002, Cantrill 2001, Poole et al. 2003), but this hypothesis was based only on a few taxa or localities.During the past 10 years, however, enor mous volumes of multidisciplinar y data were published on paleomagnetism, sedimentar y provenance, paleobiogeography, molecular phylogeny and paleoecology, among many other disciplines.These datasets offer alter native or complimentar y explanations to the complex relationship between the geological and biological evolution of the Antarctic-Patagonian region, from which integrated studies have been scarce.

Geological setting
Movements of two major plates of the former Gondwana continent, South America and Antarctica, control the moder n tectonic scenario in the region.These are in turn linked to four minor plates: Scotia, Drake, South Sandwich and South Shetland (Augusto et al. 2007).The Late Cretaceous was the time when the final breakup of Gondwana occurred and led to the isolation of Antarctica.Paleontological data indicate that the Antarctic Peninsula was adjacent to southern South America during almost all of the Mesozoic, allowing for an active migration and exchange of terrestrial faunal and floral assemblages.This interchange between South America and the Antarctic Peninsula ceased during the Paleogene when a shallow seaway developed, but the fi nal continent separation did not occur until the early Neogene with the development of deep sea conditions in the Drake passage (Zinsmeister 1987).
The Austral Basin is located in southern South Patagonia and is composed of three sub-basins (Suarez et al. 2009).The Rocas Verdes Basin was active during the Late Jurassic and Early Cretaceous and was formed by an extensional tectonic regime associated with the separation of southern Gondwana (Dalziel & Cor tés 1972, Suarez 1979, Dalziel 1981).The closure of the Rocas Verdes Basin during the mid-Cretaceous was accompanied by the collision of the Cape Horn Microplate with South America (Dalziel 1981).This is the moment when deposition star ted in the Magallanes Basin (Suarez et al. 2009).The Magallanes Basin was initially fi lled with turbiditic siliciclastic sediment (Natland et al. 1974, Fildani et al. 2007, Pardo et al. 2012), with the proto-Andes as the main source of sediment infi ll (Fildani et al. 2007).The Upper Cretaceous sediment sequence of the Magellanes basin the Última Esperanza Province refl ects gradual shallowing towards slope and subsequently to shallow marine environments prograding to the south.Deltaic environments fi rst occured in the Lago Argentino area.An example of the massive retrogradational marine deposits in the Magallanes Basin is exposed in the Tres Pasos Formation, Última Esperanza Province, equivalent to Rosa and Fuentes Formations in the Seno Skyring and Brunswick Peninsula area (Fig. 1).In this region deep marine environments were gradually replaced by shallow marine and fi nally alluvial fan deposits known as Dorotea Formation, in Chile, or Cerro Cazador Formation in Argentina (Macellari et al. 1989, Malumián & Caramés 1997).These formations were assigned to the Upper Campanian-Maastrichtian based on ammonite occur rences (Macellari 1988, Macellari et al. 1989, Malumián & Caramés 1997).The top of the sediment sequence is still known as Cerro Dorotea Formation in Chile, while coeval sediments on the Argentinian side adjacent to the northern border of the Última Esperanza Province are known as the La Irene Formation.This latter unit corresponds to sandstone and conglomerate deposited in a meandering river environment.The Calafate Formation unconformably overlies the La Irene Formation (Macellari et al. 1989) and is now also considered to be Maastrichtian in age (Marenssi et al. 2004).This unit represents alluvial to estuarine deposits and is equivalent to the top of the sediment sequence known from Cerro Guido and Las Chinas in the Última Esperanza Province.
The Antarctic Peninsula allocates the remnants of a continental margin to the southeast and of a magmatic arc of Meso-Cenozoic age to the nor thwest, the latter resulting from the subduction of oceanic plate  Macellari 1988, Macellari et al. 1989, Malumián et al. 1997, Birkenmajer & Zastawniak 1989, Birkenmajer 2001, Hathway 2000, Elliot 1988, Crame et al. 1991, Riding & Crame 2002and Pirrie et al. 1997.Correlación de las principales formaciones del Cretácico superior de la Cuenca de Magallanes (considerando la nomenclatura chilena y argentina) y la Península Antártica (considerando la cuenca de James Ross y la isla Rey Jorge).Macellari 1988, Macellari et al. 1989, Malumián et al. 1997, Birkenmajer & Zastawniak 1989, Birkenmajer 2001, Hathway 2000, Elliot 1988, Crame et al. 1991, Riding & Crame 2002and Pirrie et al. 1997.beneath the Paleopacifi c margin (Fig. 2).The magmatic arc, as well as accretional complexes reflecting forearc and back-arc conditions, preser ves a variety of paleoenvironments, many of which contain fossil plants (Poole & Cantrill 2006).Plant-bearing units include the Half Three Point Formation (Shen 1994) of Late Campanian or Campanian-Maastrichtian age (Cao 1992), a lacustrine deposit refl ecting a subtropical humid climatic inter val (Shen 1994).Campanian-Maastrichtian plants are also known from Price Point, presenting a dominance of angiosperms, and from Skua Bay where the megafl ora, though poorly preserved, is dominated by ferns.The Skua Bay fl ora may be slightly younger than assemblages identifi ed in other Upper Cretaceous localities on King George Island, and they are markedly different to assemblages of the Zamek Hill Formation at Admiralty Bay, which is exceedingly rich in Nothofagus (Dutra & Batten 2000).In contrast, the James Ross Basin in the nor theastern par t of the Antarctic peninsula (Figs.1-2) developed in a back-arc location in response to the south-eastward-directed subduction of proto-Pacifi c oceanic lithosphere beneath the Antarctic Peninsula magmatic arc (Pirrie et al. 1997).The basin fi ll constitutes a regressive megasequence (Nelson 1975, Ineson et al. 1986, Crame et al. 1991).For instance, the Aptian-Turonian of the basin is characterized by submarine fan deposits, whereas the Snow Hill Island Formation of late Campanian-early Maastrichtian age reflects a shallow shelf environment based on mollusc assemblages including the ammonite Gunnarites antarcticus.The Snow Hill Island Formation unconformably underlies the Maastrichtian López de  Ber todano Formation, which is restricted to the nor thern tip of Snow Hill Island, to Seymour Island, and to a small exposure on Vega Island (Pir rie et al. 1997).This sequence thus represents one of the most complete Upper Cretaceous sections in the Southern hemisphere, with a wide record of paleoenvironments and diverse biota.
Here we suggest that biogeographic bridges connected Patagonia and the Antarctic Peninsula during the last interval of the Late Cretaceous (Fig. 2), generating one or more ancestral biota.The geographic continuity of Patagonia and the Antarctic Peninsula, currently disjointed by the Drake Passage, may partly explain the vicariant pattern and areas of endemism, but weather patterns differing between the western and eastern side of the isthmus may also have played in important role.

METHODS
The biogeographic analysis presented here is based on fossil plant associations from Antarctic localities at Snow Hill Island, James Ross Island, Seymour (Marambio) Island, Skua Bay (King George Island), Half Three Point (King George Island), Price Point (King George Island) and Zamek Hill (King George Island), as well as from Patagonian localities at Rocallosa Point (Riesco Island), Guido Hill, Las Chinas, Dorotea Hill in Chile, and and Cazador Hill and La Irene in Argentina (Fig. 2).Las Chinas is a new locality not documented before.Six localities were studied during fi eld campaigns from 2008 to 2011 (Las Chinas, Cerro Guido, Half Three Point, Skua Bay, Price Point and Cerro Dorotea).Distributional data of fossils and localities were obtained from the review of published articles, books and fi eld campaigns (See Appendix).With this information at hand, a georeferenced record database was performed.A geographic distribution map of each taxon was obtained using ArcView GIS 3.2.Altogether, 4044 records were used.A total of 364 taxa were registered, 71 of which correspond to leaf imprints and 293 to palynomorphs.Diagrama de Áreas de consenso (1-28) obtenido por AE.La grilla en cada localidad representa un área de 0.25º x 0.25º.El esquema fi nal muestra las localidades consideradas aquí y relación de áreas obtenidas por PAE, los puntos negros corresponden a la coordenada de la localidad considerada y los grises representan el área considerada en el consenso.

Biogeographical analysis
The floral diversity and relationships among each locality were analysed using the Parsimony Analysis of Endemicity (PAE) and the Analysis of Endemicity (AE).PAE comprises locations, optimizing the correlation between distributional patterns of taxa, using shared taxa among areas according to the most parsimonious solution (Morrone 1994, Posadas 1996).Rosen (1988) coded the presence or absence of taxa in an area as ( 1) or (0), respectively.This method is followed here.Our dataset includes 364 taxa of 13 areas (12 localities + 1 hypothetical area to root the tree) (Appendix).Data were analyzed with NONA 2.0 (Goloboff 1993) and WinClada (Nixon 1999) using a heuristic search (multiple TBR + TBR).The software was allowed to retain a maximum of 10000 trees with 100 replicates of random addition sequence and an initial 100 trees in each replication.Only informative characters were considered.If two or more resulting cladograms were equally parsimonious, a strict consensus cladogram was generated.The areas of endemism identifi ed and the possible relationships between the localities analyzed by PAE were compared with the result of AE.The AE was realized by the method of Szumik et al. (2002) and Szumik & Goloboff (2004).Basically, the method evaluates the consistency of the distribution range of species to a predefined area.The optimality criterion was implemented in NDM/VNDM programs (Goloboff 2005), using default parameters: sets of areas were saved with two or more endemic species (score >2), while sets of <0.90 worst fi t were excluded.Optimal sets were chosen when the number of different endemic species was >40 %.Search for endemism was conducted using different proportions of radius size.The best score for endemicity areas was used (fi ll: X = 90, Y = 90; to assume X = 50, Y = 50).Consensus areas were obtained using 30 % of similarity in species, compared to other areas in the consensus.A fl exible consensus is used when at least 50 % of endemic species are in common.

TABLE 1
Areas of consensus for the analysis of fl ora obtained using, grids of 0.25° x 0.25°.For each area the following parameters are indicated: AI, including individual areas and endemic taxa present.

DISCUSSION
A land bridge between Patagonia and the Antarctic Peninsula is considered to be crucial for the genetic fl ux between the two continents of terrestrial plants It is known that CO 2 reached maximum levels during the early Late Cretaceous and that the region was exposed to westerly winds (Elliot 1988, Del Valle et al. 1992, Hathway 2000).A mountainous terrain is suggested from the proximity to the island arc and may have led to orographic rainfall, moderating temperature extremes and distributing precipitation throughout the year.These were appropriate conditions for the rapid establishment and expansion of a Valdivian type forest.Climatic conditions changed in the Early Campanian and again in the Late Maastrichtian due to the continuous subduction and aggregation of land on the western side of the Antarctic Peninsula (South Shetlands), in addition to a decrease in the global atmospheric Nothofagaceae are known to occur on the Antarctic Peninsula since the Campanian (Zastawniak & Szafer 1990, Francis 1991, Dutra 1997, Dutra & Batten 2000, Dutra 2001, Dutra 2005).The group successfully infi ltrated gymnosperm-dominated forest ecosystems, with some opportunistic species of Nothofagus competing for openings in the canopy.This strategy, commonly known as "gap dynamics" (Veblen et al. 1983, Hill 1992, 1994, Veblen et al. 1996), is currently observed in modern Valdivian forests, especially in Andean forests with repeated volcanic disturbance.Species suppor ting Clades I and II in the present analysis may be related to this strategy, using special microclimatic conditions.From an ecological perspective, both share typical elements of the Valdivian Forests: a canopy dominated by angiosperms and subordinate presence of gymnosperms, and an understory mainly composed of Myrtaceae, Liliaceaea, and Sapotaceae, and ferns such as Blechnaceae and Dicksoniaceae.The sites located in the Tethyan margin, exposed to southern oceanic conditions, are clustered in Clade I and are dominated by angiosperms with subordinated elements of gymnosperms, shrubby ferns and angiosperms.This vegetation significantly differs from the eastern fl ora (Clade II), which exhibits subtropical taxa mixed with cold temperate elements.This contradictory results regarding Clade II may be explained by a difference in climatic conditions, While fl oral assemblages lumped in Clade II were exposed to the South Atlantic-Weddell currents, and, westerly winds and moist or/and a previous vicariant event differentially isolated Patagonian plants of Clade I from the nor thwester n Antarctic Peninsula (South Shetland Islands) and the nor theaster n Antarctic Peninsula (James Ross Basin).Unfor tunately, the subductive activity along the western border of the Antarctic Peninsula may have erased physical evidence for this hypothesis along the western border of the Magallanes Basin.2006), even though their simple type of pollen has frequently been assigned to tree ferns such as Cyathidites and palms.Arecipites is frequently used as a climate proxy indicative of warm conditions and intolerance to long and cold freezing winters (Box 1981).Nevertheless, this interpretation may be erroneous, because other similar families such as Liliaceae, produce structurally identical types of pollen (Erdtman 1971, Skog 1988).Indeed, Palmae have been repor ted in the same area of Antarctica by Askin (1992), even including Monosulcites minutiscabratus (Baldoni & Barreda 1986) and Longaperites (Baldoni & Medina 1989).Modern Palmae are present in cool-temperate Austral ecosystems, among them the Chilean Jubaea chilensis, near Valparaíso, or Rhopalostylis sapida, the Nikau palm, in New Zealand and the Chatham Islands.
In both, PAE and AE analyses, nearby localities such as the Cerro Guido-Las Chinas complex and Dorotea-La Irene show important dif ferences in their floral composition.This reinforces the idea that coeval sedimentar y environments dif fered at shor t distance.Nothofagaceae are completely absent at Cer ro Guido and Las Chinas and are the dominant element in the Dorotea-La Irene assemblages.This important difference may result from diverging microclimates, similar to the differences that today exist between the western and eastern side of the Patagonian Andes.It is nevertheless evident that localities to the west of the hypothetical isthmus between South America and Antarctica are linked, and that a similar link existed between sites located to the east, such as the James Ross Basin, Dorotea and La Irene.However, these biotical dif ferences may reflect another condition: that the outcrops of the Chinas-Cerro Guido may represent the instant before the massive invasion of Nothofagus from Antarctica to Patagonia.Therefore, Dorotea and La Irene outcrops belong to the end-Maastrichtian inter val.Unfortunately, the physical evidence for the western bridge is lost today due to the subduction.The mix of tropical and temperate South American-Australian Antarctic taxa in Maastrichtian localities of northern Magallanes basin is also noteworthy and this area likely represents the "birth place" for the Valdivian forest.

Fig. 3 :
Fig. 3: Reconstruction of Austral basins of South America and the Antarctic Peninsula modifi ed from Lawver et al. (2009).The continental connection during the Campanian and Maastrichtian is shown as an isthmus between the Antarctic Peninsula and Patagonia.Reconstrucción de la Cuenca Austral modifi cada de Lawver et al. (2009).La conexión durante el Campaniano y Maastrichtiano se muestra como un istmo entre la península Antártica y Patagonia.

Fig. 5 :
Fig. 5: Diagram of consensus areas (1-28) obtained by AE.The grid in each locality represents an area of 0.25º x 0.25º.The diagram shows localities considered here and areas obtained by PAE relationship, black points correspond to localities and gray dots represent the area considered in the consensus.
Editorial responsibility: Álvaro T. Palma ReceivedNovember 18, 2011; accepted August 10, 2012 Clades IA and IB share morphotypes of Sterculiaceae, neotropical trees and shr ubs, which were abundant in Cretaceous Patagonian localities.Clade II clusters the Patagonian localities of Dorotea, La Irene and Cazador Hill with the James Ross Basin localities of Seymour Island, James Ross Island and Snow Hill Island.This clade is suppor ted by a few palynomorphs, with Snow Hill Island and Dorotea sites in a basal position.Seymour Island and James Ross Island are well structured with numerous synapomorphic species of Olacaceae, Proteaceae, Bombacaceae, Podocarpaceae, Aquilafoliaceae and Casuarinaceae.Some are tropical in origin, such as Olacaceae, a Gondwana group of mangroves with a wide record during the Paleogene of South America, New Zealand and Africa (Muller 1981); they indicate megather mal and high rainfall conditions.Other taxa, such as Bombacaceae and Aquilafoliaceae were subtropical to tropical elements of the Maastrichtian-Danian (Prámparo et al. 2007).Proteaceae, as well the conifers Araucariacites, Microcarcharidites and Dacrycarpus, show temperate af finities.Clade IIA also contains Arecipites, a taxon with affi nities to Palmae (Poole et al. 2005), Arecaceae or Liliaceae (Macphail & Cantrill Philosophical Transactions of the Royal Society of London.Series A, Mathematical and Physical Sciences 300: 319-335.DUTRA TL (1997) Composição e história da vegetação do Cretáceo e Terciário da ilha Rei George, Península Antár tica.PhD.Thesis.Instituto Tecnológico em Micropaleontologia, Universidade Federal do Rio Grande do Sul, Por to Alegre,