A Word about Cryptic Refugia

Dryas Octapetalus - Mountain Avens
namesake of the Young Dryas

Temperate species expanded and contracted with temperature fluxes during glacial cycles. Many cold-tolerant species that survived in northern cryptic refugia had larger distributions: the Arctic Fox (Alopex lagopus), the reindeer (Rangifer tarandus) the little white flower Dryas octapetala (pictured left) and dwarf birch (Betula nana). These species expanded during glacials and contracted during interglacials.   With impending global warming, their contracted distributions may well retreat into isolated cooler refugia just as the reverse is true for heat-loving plants.  Recent phylogeographic studies have given support to the existence of previously unknown, or cryptic, refugia during the LGM  Provan (2008)

        The Arctic Fox (Alopex lagopus)

Phylogeographic evidence indicates there was a major northern refugium for a variety of taxa in the area around the Carpathians, with divergent lineages in the region, many predating the LGM.

The existence of a Carpathian refugium characterized by mixed deciduous and coniferous woodland, often on milder south facing slopes is supported by the fossil record and palyncological studies.  Its role in the postglacial colonization of Northern and Western Europe has only become apparent with genetic analysis. 

The Carpathian Mountains  

The Carpathians were a cryptic refugium for Carpathians Regions of mixed coniferous and deciduous woodland as well as Microtus agrestis (field vole) Jaarola (2008), Clethriononys glareolus (bank vole), Kotlik (2006) Vipera berus (adder) Ursenbacher (2006), Triturus spp. (newts) Babik (2005)  Rana arvalis (moor frog).  

The Carpathians are a chain of mountains stretching in an arc from the Czech Republic, Slovakia, Poland, Hungary, Ukraine to Romania. The highest range is theTatras Mtns on the border of Poland and Slovakia.  

Northern North America ice-free regions in the Canadian high Arctic and between the Laurentide and Cordilleran ice sheets was a cryptic refugia for Dryas integrifolia (plant) Tremblay (1999), Ovis spp. (mountain sheep), Loehr (2006) Lagopus mutus (rock ptarmigan), Holder (2000) Dicrostonyx groenlandicus (collared lemming) Federov (2002) and Packera spp. (plants) Golden (2000) .

In the English Channel, the Hurd Deep, or surrounding trenches, which might have
persisted as ‘marine lakes’ were the cryptic refugia for Ascophyllum nodosum (seaweed), Olsen (2010)  Fucus serratus (seaweed) (Coyer, 2003) Palmaria palmata (seaweed) Provan (2005)

In the last few years,  many pieces of the European Cryptic Refugia puzzle have come from phylogeoraphic research by many dedicated scholars -  associating patterns of gene geneology with geographic distributions. 

Fish migrate south to warmer waters during the LGM

Archaeozoological finds  of marine and amphihaline fish remains from the Last Glacial Maximum (LGM)  show evidence of very different species ranges compared to the present.

An ecological niche model based on paleoclimatic reconstructions of sea surface temperatures and bathymetry have been used to effectively predict the spatial range of marine fish during the LGM. The results indicate that the ranges of marine fish species now in northwestern Europe were displaced significantly southwards from the modern distribution, challenging an existing paradigm of marine glacial refugia. 

The model presents strong evidence of an invasion of important fish through the Straits of Gibraltar in glacial times, where they were exploited by Palaeolithic populations around the western Mediterranean Sea. Kettle (2010)

The Megalodon Megaselachus megalodon was an enormous shark. It first appeared around 18 million years ago and was found in all oceans of the world from the Miocene until the Mid-Pleistocene.  It became extinct around 1.5 million years ago. It evolved from the Isurus during the Eocene (around 50 million years ago). The first true ancestor was the Carcharocles auriculatus, which was rather smaller. People used to see the Megalodon as ancestor of the modern white shark. It is however, more likely that the Megalodon belongs to a separate genus and is just a distant relative of the modern white shark.

Reconstructed megalodon skeleton 
on display at the Calvert Marine Museum
Solomon, Maryland, USA

This animal dominated the oceans and is regarded one of the largest and most powerful predators of all vertebrate animals to have ever lived. He could reach a length up to 18 metres, dilate its mouth about 2 metres with tail fins  over 4 metres in length and a dorsal fin could reach a length of 2 metres. He had a cosmopolitan distribution, which means that its habitat was spread throughout the entire world, in (almost) every ocean. 

The enormous triangular teeth, with a length of 15 cm (enamel + crown),that have been found, were first believed to be derived from snakes and dragons. It was discovered in 1667, they were in fact, shark teeth.   

Megalodon Tooth

Most fossils are teeth or vertebral columns. Fossils of Megaselachus megalodon have been found near St. Maria Island, the Azores. Avila (2012)

The Sabre-Toothed Salmon (Oncorhynchus rastrosus)
 first appeared near the coast of modern California, during the Miocene, disappearing during the Pleistocene. They travelled up the rivers from the sea to breed. This extinct fish was about 250-300 cm in length. Characteristic for this animal were its fangs, sticking out the tip of its snout. Besides these fangs, the fish had relatively little teeth, which suggests that it ate plankton.

For the eel, this refugium was probably on the Atlantic coasts of Portugal and Morocco.Kettle (2008)  The glacial refuge of the shad is unclear, but remains have been discovered on the upper Tagus River system at Aridos-1 from the Mindel-Riss interglacial approximately 300 ka BP  and  it is likely to have survived the glacial maximum around the Iberian Peninsula and northwest Africa. 

In Southern Spain, the boreal gadid species, haddock Melanogrammus aeglefinus) and pollock (Pollachius pollachius) have been reported for the Cueva de Nerja near Malaga dating to the LGM:  significant because these species are currently found in Northwest Europe, and the southernmost range for haddock and pollock is currently the Bay of Biscay and northern Portugal, respectively. Whitehead (1986)

The most recent analyses of the LGM deposits from the Cueva de Nerja have revealed that the northern gadids (including saithe Pollachius virens, cod Gadus morhua, and ling Molva molva) make up more than 30% of the identified fish remains and thus represented a significant presence among the  fish exploited by Paleolithic hunters with the exploitation of gadids continuing for an extended period of time after the LGM until the early Holocene as sea levels were returning to present levels and sea surface temperatures approached present values.

Atlantic Salmon (Salmo salar)

Among the most spectacular  species range shifts  have been reports of  of Atlantic salmon (Salmo salar) remains in archaeological sites from the Mediterranean drainage basins of France, Spain, and Italy dating from the LGM up to the early Holocene. Additional small art objects unambiguously depicting salmon have been located at the Grand Grotte de Bize on a Mediterranean drainage basin with reports from late Palaeolithic–early Mesolithic sites in France, Spain, and Italy) suggesting  the presence of resident salmon populations in the western Mediterranean Sea.  However recent genetic analysis has shown a mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium.

Consuegra (2002)

The current southernmost range of Atlantic salmon in Northwest Europe is Northern Portugal, which indicates that immigrant populations would have had to pass through the Straits of Gibraltar when temperatures in Southern Spain during the LGM were similar to  present day Northern Europe. However, the archaeozoological evidence is contested. Many  sites in southern France are in proximity to Atlantic drainage basins, and it is possible that the Atlantic salmon remains in the Mediterranean watersheds may have been transported as part of a seasonal migration of fishermen.

Europe: Trees or No Trees? A New Emerging Synthesis

The study of biodiversity during the Pleistocene offers many opportunities to assess the impacts of climate change.  

GOAT WILLOW (Salix Caprea) now believed to
have had wide boreal distribution during the LGM

Scientists are fascinated by distributions of European trees in the coldest stages of the last full glacial, especially at isolated locations where some species survived to influence their long-term ancestry and current distributions. For fauna and flora species, the location of their European refugium during the coldest glacial maximum remains a teasing puzzle.  

Emerging evidence from fossil proxies, paleoclimatic modelling and genetic research suggests the traditional paradigm of trees being restricted to S. Europe, especially the 3 southern peninsulas (Iberian, Balkan and Italian) is questionable.  

Evidence includes 151 carbon-14 dated and identified pieces of macrofossil charcoal wood from 40 sites in central and eastern Europe that suggest that during the last full glacial, there were populations of conifers with some deciduous trees growing much further north and east than previously believed.  

Plotted against a new high-resolution millennial time-scale for the interval ∼32–∼16 ka BP in Greenland our evidence shows that coniferous as well as some broadleaf trees were continuously present throughout those interstadial/stadial cycles for which there are adequate data.Willis (2004)

Southern vs. northern refugia hypotheses were investigated by estimating the potential LGM distributions of 7 boreal and 15 nemoral widespread European tree species using species distribution modelling. The models were calibrated using data for modern species distributions and climate and projected onto two LGM climate simulations for Europe. Five modelling variants were implemented.

Broadly consistent results were obtained irrespective of the climate simulation and modelling variant used. Results indicated that LGM climatic conditions suitable for boreal species existed across Central and Eastern Europe and into the Russian Plain. 

In contrast, suitable climatic conditions for nemoral tree species were largely restricted to the Mediterranean and Black Sea regions. Large proportions of these northern and southern regions would have been suitable for a number of boreal or boreal plus nemoral tree species, respectively.

Synthesis:  It is clear that the view of the LGM landscape in Europe as largely treeless, especially north of the Alps, needs to be revised. Trees were probably much more widespread during the LGM than hitherto thought, although patchily distributed at low densities due to low atmospheric CO₂ concentrations and high wind-speeds. 

The findings presented here help explain the occurrence of mammal assemblages with mixtures of forest, tundra and steppe species at many localities in southern Central and Eastern Europe during the LGM, as well as the phylogeographic evidence for the extra-Mediterranean persistence of many boreal species.
Svenning (2008)

Trembling Aspen - Populus Tremuloides propagates by root sprouts, to form enormous clone coloni of one single organism  - Utah's Pando Populus colony has the distinction of being both the oldest (80,000 years old) and heaviest living organism at 6 million kg. 

The northern refugia hypothesis is that trees were distributed much more widely in Europe during the LGM.  According to this hypothesis, trees occurred not only across Southern Europe, but also in the southern parts of Central Europe, a proposal is mainly based on evidence from pollen and plant macrofossil evidence but is also receiving support from phylogeographic studies of certain species (e.g. Silver Burch (Betula pendula and Betula pubescens), Trembling Aspen (Populus tremuloides, and willow (Salix caprea).  These species all show wide boreal pleistocene distributions.  

Betula Pendula -Tiver, Russia

The phylogeographic evidence for nemoral (woodland) tree species appears to be more consistent with the southern refugia hypothesis.

Survival for the non-boreal beech tree Fagus sylvatica  as far north as the Carpathians has been suggested. Late-glacial and post-glacial increases in the number of pollen sites where Fagus was locally present suggests that the area occupied by beech populations expanded exponentially from the glacial refugia for a duration of over 10,000 years, until about 3500 years before present.  Magri (2008)

Glacial refuge areas should be expected to harbor a large fraction of the intraspecific biodiversity of the temperate biota. Chloroplast DNA variation was studied in 22 widespread European trees and shrubs sampled in the same forests. Most species had genetically divergent populations in Mediterranean regions, especially those with low seed dispersal abilities. Petit (2003)

Glacial Refugia were hot spots but not melting pots of genetic diversity .... genetically most diverse populations were not located in the south but at intermediate latitudes, a likely consequence of the admixture of divergent lineages colonizing the continent from separate refugium.

Multispecies genetic divergence of each of the 25 European forests studied. Higher than average values in black circles, lower than average, white circles.  For all forests, divergence levels represented by connecting lines, with continous black lines indicating comparatively high divergence, dotted lines, intermediate divergence.  Altitude is indicated by grey shading (lightest gray 250-500 m with gray intensifying as altitude increases from 500-1000 and over 1000 m).  Past sea levels are indicated by black dotted lines Petit (2003)

Mangroves Marching North

MANGROVE "ISLAND"

Mangroves are unique trees with saline adapted roots that play an important role as land-builders and stabilizers of substrates derived from sedimentation processes in tropical coastal regions. Carlton, 1974   

Found in versatile forms from low shrubby plants to majestic forest canopies reaching 30-40 m. Tomlinson, 1986 , mangroves and their habitats have generated so much interest from scientists and researchers that currently there are over 6000 scholarly references on the subject.

Inhabiting the upper inter-tidal zone of sheltered shores in the tropics, they are seldom found outside inter-tidal areas and mostly occur between mean sea level and the level of mean high water spring tides.  Mangrove ecosystems are well established as they are sediment traps that maintain the quality of coastal waters, serving to protect coastlines from erosion during storms, habitats for rare fauna and nurseries for commercial fish and crustaceans.  Ellison (1990)  

Mangroves in the Ice Ages - On the front lines of Climate Fluctuations

From a geological perspective, mangroves came and went at considerable speed having undergone almost chronic disturbance as a result of fluctuations in sea-level during the Ice Ages. 

However they show considerable resilience over timescales commensurate with shoreline evolution. This notion is supported by evidence that soil accretion rates in mangrove forests are currently keeping pace with mean sea-level rise. Further support for their resilience comes from patterns of recovery from natural disturbances (storms, hurricanes) which coupled with key life history traits, suggest pioneer-phase characteristics. Alongi (2008)  

For example, Anak Krakatoa, a volcanic island off the Sunda shelf that first appeared in 1927 already has a colony of pioneer mangroves fringing its shoreline.

Mangroves growing in coastal regon of Anak Krakatoa.

With a warming climate today, Mangroves are now marching north.....

Florida Everglade Mangrove Forest pushing further north as climate warms

Along a 50-mile stretch of the central Florida coast south of St. Augustine, mangrove forests doubled between 1984-2011, according to recent analysis of satellite imagery.  
Mangroves are very sensitive to temperature and with the disappearance of winter freezing, mangroves are now displacing marsh grasses.  

Scientists report it is not a small rise in average temperatures but the disappearance of cold winter nights that limited the growth of cold-sensitive species.   

Given that the earth has only warmed by 1.5 degrees Fahrenheit since the 19th century, the pace and scale of some recent developments have been surprisingly fast Cavanaugh (2014)  

Mangroves  that fringe shorelines in the tropics are among the earth’s environmental treasures, yet in many places, mangroves are critically endangered by shoreline development and other human activities.  Perhaps a change in climate that allows mangroves to thrive in new areas might well be seen as a happy development. 

Unfortunately they are displacing salt marshes, which are also ecologically valuable and also under threat from development. Their ecology is markedly different from that of mangroves, raising new questions about what will be lost if marsh grasses are killed off by the invading trees.

So why is the topic of glacial refugia so important?

The winners and losers in the gamble of life - from a climate change perspective

Since late 20th century with scientific recognition of glacial-interglacial shifts during the Pleistocene, there has been a revolution in understanding of the impermanence of vegetation patterns. Today it is known that until mid-latitude cooling and reduced CO2 levels during the Pliocene, tropical flora flourished at high latitudes from the time of the dinosaurs. 

Oxygen isotope analysis of foraminafera in ocean sediment cores revealed the connection between rapid changes in ice volume and sea surface temperatures Shackleton (1967), later confirmed by Greenland ice core records Dansgaard (1993), and still later by Antarctic ice cores Barnola (1987).  With this historic sequencing established, pollen analysis from anaerobic lake sediment cores continues to contribute vital information regarding prehistoric vegetation patterns.

Northern Hemisphere Glaciation

The transient nature of vegetation is impacted by earth-sun orbital cycles Milankovic (1941).  Seasonality is a major control of vegetation - the axial tilt of the earth or obliquity as it called in astronomical terms, between 21.8 - 24.4 degrees over a period of 41,000 years affects the strength of seasonality affecting the amount of insolation received in summer and winter.  A 2nd astronomical orbital forcing called Precession with a 27,000 year cycle - akin to the gyrations of a spinning top - alters the distance between the earth and the sun - modifying the dates of perihelion and aphelion, earth-sun distances between December and June. Together, enhanced by earth system feedbacks, these orbital forcings have a subtle yet profound impact on vegetation patterns. 

Naturalists such as F. E. Clements (1874-1945)  believed dynamic vegetation patterns were based on succession to a mature state of vegetation best suited to local conditions, an idea that at best is only partly correct. Today there is heated debate over the extent of prehistoric burning by early hunter gathers that may have altered the prehistoric landscape worldwide. 

By the time Europeans arrived in the Americas, there had been extensive alteration of the landscape by fire: the Central Valley grasslands may have been oak forests that were burned by native American groups in order to facilitate hunting and clear forests of decaying matter.  Only since the late 20th century has there been recognition by the U.S. National Park Service of the contribution of fire to reinvigorate decaying and diseased vegetation.  When the Spanish arrived in California, they banned Native Americans from setting fires, although  burning through the late 19th century was recorded by missionaries and explorers.    

Unraveling prehistoric vegetation patterns today is aided by genetic analysis which can pinpoint movements down to the subspecies.  Pollen analysis is restricted to taxa.

Plant Succession during Deglaciation at Glacier Bay, Alaska which was ice covered until  around 300 years ago Chapin (1994)

Map of Glacier Bay, Alaska 

The remarkable Rosebay Willow Herb that covered London bomb sites and was a pioneer species during the deglaciation of Glacier Bay, Alaska 

1st came Rosebay Willow Herb, with Alder trees next and with Dryas Octapetalus 
growing in ring formation (asexually). Then Spruce and Hemlock (that prefers a shadier site – came later in the sequence after 250 years). In process succession – how important is the soil? Interestingly, alders are well-known as nitrogen-fixing plants that  enrich the soil and as the amount of nitrogen in the soil increases through time, then other plants could come in.


Today we live in the Holocene Interglacial.  Due to human industry, global warming will bring unprecedented changes and the onset of the next NH glaciation will be delayed.   

Current vegetation patterns are expected to shift, particularly within areas of the subtropics such as SW North America, India and Africa where increased aridification is predicted in future decades.  Clearly there will  be some winners - plants  enjoy enhanced CO2 and more warm, humid weather - so many heat-loving plants may thrive.

The Pallid Bat

In a world of climate change, there will no doubt be some losers -  bat populations already being driven to extinction by White Nose Syndrome (WNS)  Lorch (2011) will be further threatened by climate change impacts on echolation - (echo - location) to identify prey by emitting a high frequency ultrasonic squeak, listening for the echo back of the location of a juicy insect for dinner.  Unfortunately increased humidity and warmth attenuates the high frequency sound, lessening the range of echolation effectiveness of bats attuned to high frequencies to locate food sources Luo (2013).  

Coast redwoods (Sequoia sempervirens) distributed along a narrow band of California's northern coast could possibly turn out to be winners as the climate warms (Professor A. Roger Byrne, U.C. Berkeley personal communication).  During the Northern California summer, these red giants take advantage of the coastal fog to capture water out of the air— summer is the critical growing season for the trees, despite being California's dry season.  Future warming temperatures may possibly bring the fog belt further inland extending the habitat of the world's tallest trees, the Coastal redwoods, Sequoia sempervirens.

Sequoia Sempervirens bathed in its life-giving fog

Tenaghi Philippon, N.E. Greece - A 1.35 million Year Pollen Sequence

 Ruins from Philippi on the Aegean

The longest continuous European pollen record comes from the site of Philippi, in eastern Macedonia, N.E. Greece, established by Philip II in 356 B.C. but abandoned in the 14th Century after the Ottoman conquest.  It is now a UNESCO site for its Greek and Roman ruins.  Evaluation of the original age model using calibration based on vegetation changes and March and June perihelion configurations  suggests that the base of the pollen extends back to 1.35 million years.  

The pollen sequence from the Philippi basin provides the opportunity to examine long-term vegetation and individual taxa trends within the context of global climate changes.  Interestingly although this pollen sequence shows no changes in the magnitude of interglacial tree populations after the Mid-Brunhes climatic event around 430,000 years before present.  Instead the Tenaghi Philippon pollen sequence suggests major vegetation shifts in the composition of  interglacial cycles after MIS 16, which was a strong amplitude glacial which resulted in reduced diversity and a more 'modern' appearance of subsequent vegetation distributions.  


Carbon dioxide levels are below 180 parts per million by volume (p.p.m.v.) for a period of 3,000 yr during Marine Isotope Stage 16, possibly reflecting more pronounced oceanic carbon storage. We report the lowest carbon dioxide concentration measured in an ice core, which extends the pre-industrial range of carbon dioxide concentrations during the late Quaternary by about 10 p.p.m.v. to 172–300 p.p.m.v.  Luthi (2008)    

Although species of oak managed to persist in the region, there were many extinctions, including Tsuga (Hemlock), Liriodendrum (Tulip Tree), Parthenocissus (Climbing Grape), Parottia (Persian Ironwood), Cedrus (Cedar), Carya and Eucommia (now native to China) that largely disappeared from the record after MIS 16 which was 650,000 years ago. Tzedakis (2006)

Persian Ironwood that disappeared from Philippi  650,000 years ago

Examples of some tree taxa that went extinct in Europe, and are now only found in S. E. Asia or North America:

Prior to Northern Hemisphere Glaciation, there were many more tropical taxa now only found in S. E. Asia and North America such as  Persimmon (Diospyros), Epipremnum (now only found in tropical forests), Snowbell or Snowdrop tree (Halesca), Karwinskia (Flowering Buckthorn -  Rhamnaceae family), Meliosma, Golden Larch (Pseudo Larix), Stewartia (flowering shrub related to camellia), Actinidia, Magnolia, Prosperpinaca, Fagus (Beech).  

The disappearance of the hardy magnolia from Europe is thought to be related to being out-competed by faster growing and more robust trees during the climate fluctuations of the last 2 million years rather than extinction due to Northern Hemisphere glaciation. Magnolia is a very old plant, considered an evolutionary relict that formerly had widespread distribution and early forms we but today is only found in North America (26 species) and S. E. Asia (80 species).  

As the climate warms, some species will do better:  for example, the horn growth of the endangered Alpine ibex is affected by European springtime temperatures between March and May - with earlier snow melts with more lush alpine grasses and herbs more favorable for the animal's vitality Buntgen (2013).  

Regrettably many other cold loving species will not be so fortunate....

A Tale of Two Extraordinary Adaptations

Desert Rhubarb (Rheum Palaestinum)

EXTREME ADAPTATIONS OF RHUBARB

The Desert Rhubarb (Rheum Palaestinum) in the
Negev Desert possesses unusually large rosette-shaped leaves for a desert plant. Most interestingly, its leaf morphology resembles the slopes it inhabits.  Piqued by this observation, University of Haifa researchers determined that is the only self-irrigating plant in that world known to have this capacity - collecting up to 16 times more water per year than other desert plants in the region.  The study has revealed the plant harvests 4.2 liters per year, akin to the rainfall of a mediterranean climate - in a desert region that receives  only 75 mm of rainfall a year.  Deep depressions in its leaves channel water towards its roots - creating its own mini leaf-oasis.  Yev-Ladun (2009) 



Meanwhile, high in the Himalayas above the treeline at 4000 meters where conditions are so extreme most plants cannot survive, Rheum nobile - the extraordinary Noble Rhubarb stands up to 2 meters tall, a hollow column of overlapping pale-yellow leaves rising from a base of green leaves.  Discovered in the 1840s by Joseph Hooker, Rheum Nobile stands tall on the harsh Himalayan scree-clad slopes withstanding both perishing cold and biting wind as well as an invisible-yet-deadly barrage of ultraviolet light. Amazingly, the translucent column functions as a protective greenhouse, enabling it to grow amazingly large at such an altitude.
A few botanical gardens and amateur enthusiasts grow Rhem nobile but it rarely flowers out of its natural habitat.  The flowers are extraordinary: the hollow columns are actually flower spikes.  Pale yellow leaves "bracts" grow from each spike that surround and hide the flowers inside.  Kew Gardens herbarium head David Simpson says it displays great botanical novelty.  Joseph Hooker noted that in winter, after the fruit and seeds have formed, the dead seed bearing stems are in dismal keeping with the surrounding winter desolation. Nicholls (2013)

In 1964 Sasuke Naoao wrote "the flowers open in a self-made warm room" that boosts pollination, he suggested by providing favorable conditions for insects.

 

Rheum Nobile

                                                   

So even though this blog takes a slight detour from the glacial refugia topic, it is pertinent because it does make one question why if one angiosperm could manage such extreme adaptations, why were there not more? 

Weeds usually are noted for their phenotypic plasticity, but this example of the adaptation of Rhubarb (Rheum ssp) of the polygoniaceae family to survive in both extreme aridity and extreme cold is truly amazing.