AASP Primary Records Program

THE ANSWER IS BLOWIN' IN THE WIND ...
Valedictory oration read by Henk Visscher, on retiring as Professor in Palaeobotany and Palynology at the University of Utrecht, June 5, 2002.

'Phytocentric' ..., 'ecological crisis' .... These topics appear to have determined my scientific image. At least, if one can put faith in the announcement, earlier today, of a Symposium [on these topics] dedicated to me. Therefore, I want to tell how I happened to develop an interest in fossil plants, and in the mass extinctions that caused upheavals from time to time in Earth's history. I'll show how the subject of my doctoral thesis happened to play an important role in this. I also hope to demonstrate that it is never too late to propose an alternate interpretation of the data presented in that doctoral thesis.

Let us revisit the early 60's -- a dynamic period for a geology student during which the concept of plate tectonics was developed. When studying towards obtaining one's BSc, one was taught that there was no acceptable physical model for the drift of continents. But a few years later, when being examined for the Master's or Doctor's degree you "had always known" that parts of the Earth's crust could have migrated thousands of miles. It thus became clear that effects of geological processes like mountain building, erosion or sedimentation should be analyzed, as accurately as possible, in their historical context. The necessity of a better understanding of the time factor was not only discussed in the lecture halls, but also, e.g., on the public radio, where Bob Dylan almost daily asked the question:
'How many years can a mountain exist before it is washed to the sea?'

The first time my nose was rubbed in this question was during fieldwork in southern Spain. In those days, the Spanish mountain ranges were scrupulously divvied up among geological institutes: the Sierras of southern Spain (the Betic Cordillera) were studied mainly by groups from Amsterdam, Paris and Bonn. Students from Utrecht were not to show their faces there - they had their own playground in the Pyrenees.

However, the Utrecht Professor Rutten had started to write his book 'The geology of western Europe'; and while documenting the chapter on southern Spain, he ran into contradictory interpretations. According to published reports, there was a drastic change in geological structure that 'coincidentally' was conterminous with the boundary between the French and German study areas.

This boundary was delineated by the river Guadalhorce. North of Malaga, near the village of El Chorro, it runs through a spectacular 400 m deep gorge. Around 1920, hydroelectric projects were started in this area. In conjunction with this construction, a footpath was carved out along one wall of the gorge. At several places this path is no more than a narrow ridge on a vertical wall, about 100 m above water level. At the occasion of one of these power stations being visited by King Alfonso XIII, this path was named 'El camino del Rei' - 'the King's path.'

The King's path still exists, but it has deteriorated to the point that only thrill seekers make use of it. Parts of the railing are gone, and there are gaping holes through which you can see the water below. But, in the early 60s the path was still in good shape. This was observed by Frank Sinatra, during the filming of Ryan's Express, a war movie set in Italy, in which the Camino del Rei was used to introduce some extra adrenalin. And this I also observed, after Rutten dispatched me as student with the vague instruction: "Go have a look to see if the French and German notions on the geological structure of this locality could be brought into harmony." The King's path was a convenient and safe connector between the northern and southern parts of my mapping area.

The steep walls of this gorge are vertical beds of limestone. The age of these rocks are not a problem -- marine fossils place them accurately in the geological column: they are of Jurassic age. Especially the ammonoids contained in them allow the dating of some of these beds with an accuracy of about 1 million years. So far so good.

[Here follows a brief intro in the origins of Palynology and pollen analysis, and the ensuing development of paleo-ecology. Visscher cites the work by Weber in the late 19th century. as well as the patent on Palynology long ago granted to Standard Oil (ESSO). Klaus had demonstrated the use of pollen in correlating Permian and Triassic strata in Austria. That was why Utrecht Prof Jonker, Visscher's mentor and predecessor, saw the correlation of Triassic salt deposits in the Netherlands as a means to put his newly established research institute on the map.

With that background, Visscher decided to try to test the applicability of Permian-Triassic palynology to solve the apparently insolvable problems in dating the Spanish strata underlying the limestones in the Camino del Rei. Jonker made it possible for him to learn the methods from Klaus in Austria, where he went to work a stage in the thousand-year old salt mines of Hallstatt, in the Austrian Alps. These beds had been thought to be Triassic, but Klaus demonstrated that they actually were of Permian age. Visscher then did a Master's study dating the Triassic salt from cores from the eastern parts of Holland. Following that, he completed a doctoral study on the (red and gypsum bearing) Permo-Triassic strata of Dun a'Ri (Kingscourt), again from outcrop and core samples.]

Through my doctoral study in Ireland, but also later in cooperation with a large number of students and doctoral candidates, I have shown that the distinction between Permian and Triassic beds is fairly simple. The compositions of Permian and Triassic floras are so clearly different and characteristic, that the associated spore/pollen assemblages form a practical basis for dating and subdividing the strata in which they are found. This works in all of Europe, including Spain (as we found when we returned there many years later).

During my graduate study, I noticed how some groups of pollen grains from the youngest Permian show wide morphological variation. Types that at first glance appear quite distinct, nevertheless can be linked via gradual changes. This happens especially to coniferous pollen. Similar variability has been demonstrated as well in pollen derived from fossil coniferous cones.

A prime example of this phenomenon is Lueckisporites, a pollen later recognized as having been produced by the Family Majonicaceae, which are extinct conifers. I tried to express the differences within the natural variation pattern of this pollen as "norms" of a number of morphological variants. The most distinct differences were seen in the so-called 'air sacs' or 'sacci'. Norm A has sacci not unlike those of extant spruces or pines. Norm B has (strongly) reduced sacci. By analyzing the percentages of these norms in a number of successive populations, gradual changes appeared to occur as we looked at younger populations. Most notably, Norm B seemed to increase at the expense of Norm A. I interpreted this morphological trend as an indication for the existence of gradual evolutionary developments in the conifers that produced the Lueckisporites-type pollen.

However! Morphological data don't speak for themselves; then, they were interpreted as affirming a theory. In hindsight, I could see later that, in the interpretation of the morphological trends in the Lueckisporites 'norms,' I had become biased by expecting that plant-microfossils could offer a possibility to confirm the gradualism of evolutionary changes.

In the 1960's, the problem of gradualism was a fundamental challenge for paleontology. In Utrecht, [the micropaleontologist] Drooger and his graduate students stressed the possibility of reconstructing variation patterns in series of successive populations of unicellular foraminifers. Commonly, it was accepted that such series of successive populations indicated gradual changes. I considered that a similar analysis of plant microfossils might show gradual evolution in land plants; that, even if we didn't know the complete plant, or even part of it, gradual change in the pollen might be an expression of new plant types being formed.

Further down in this address I'll revisit this situation, when I'll try to re-interpret the variation in Lueckisporites from the perspective of the ecological crisis at the end of the Permian.

In the last 600 million years of geological history, there have been some five periods of mass extinction. By far the most disastrous was the one ending the Permian period. The marine ecosystems were totally devastated. Half of the number of families of marine invertebrates were lost at the Permian-Triassic transition. The percentage of species lost at this time was 85-95%. These included corals, bryozoans, brachiopods and cephalopods, as well as unicellular organisms like foraminifers and radiolarians.

On dry land there also were significant changes: the diversity of insects was drastically reduced. In addition, the "mammalian-type vertebrates" show an abrupt interruption in their explosive evolution and diversification.

However, for a long time it was thought that plant life was not severely affected by this crisis. Indeed, the numbers of plant families below and above this boundary do not show much of a decline. Yet, this is in contradiction to the picture painted by palynological data, which show remarkable differences between Permian and Triassic pollen assemblages. In my doctoral thesis I didn't pay this much attention, although I did forecast that changes in the land floras might turn out to be as fundamental as those in the marine realm.

After my graduation, my scientific activities were determined by new priorities quite different from the Permian-Triassic crisis. Nevertheless, the problem remained in the back of my consciousness. And, little by little, in the last 30 years we managed to make botanical contributions to the discussions involving this crisis. For a long time the Dolomites were our main source of information. Later, other regions were added, and especially data from East-Greenland spurred our scientific interests. While acknowledging the efforts of pre-grad and graduate students, I'll acquaint you with some of our latest results. I also want to thank our colleagues studying organic-geochemistry- originally working out of Delft, later out of Texel and Utrecht -- who always made certain that we could integrate the analysis of molecular plant fossils with our other research. A fundamental problem in determining degrees of variation of land plants remains the identification of natural species, genera and even families based on fossil plant remains. As well, little attention is being paid to the recognition of families in the systematics of fossil plants.

The so-called 'meso-fossils' (plant fragments of a few millimeters to several centimeters) are a rich source of information on the diversity of late Permian flora in Europe. In several localities in the Dolomites, unlimited quantities of such fragments can be obtained. For the most part these consist of cuticles; i.e, the external waxy layers covering the epidermis (the outermost cell layer) of all green parts of land plants. Cuticles carry a perfect imprint of the cell pattern of the epidermis, as well as of the stomata and guard cells. Stomata are the openings regulating the in- and outflow of gasses and water.

These cell patterns commonly are characteristic of a plant species. Via cuticle analysis it is possible to correlate leaf fragments, seed-bearing cones and polliniferous cones, and thus to describe new natural species of fossil plants. Now, the fossil conifers are among the best-defined and best-known plants from the youngest Permian. By isolating pollen from the fossil cones they can be correlated with dispersed grains. Pollen-morphological characteristics provide understanding of the reproduction biology of the extinct plants. One of the reconstructed conifer families was found to possess prepollen. In contrast to pollen of recent seed plants, prepollen did not produce a pollen tube to facilitate fertilization. This primitive property did not survive the Permian-Triassic crisis. (American fans gave a name to this family: the Utrechtiaceae!)

In the analysis of the Permian-Triassic crisis, much emphasis is placed on the massive extinction of diverse animal groups. However, as we became more and more involved with the changes in the flora, it dawned upon us that it was not so much mass extinction of the land plants, but their expiring en masse that provided understanding of the true nature of the crisis; and from that, possibly into the causes and effects of this world-wide ecological disaster.

Palynological analysis of the development of the vegetation shows that we are dealing with an ecological crisis. The most detailed data of the nature of the crisis was found in shallow marine beds from East-Greenland. It is our good fortune that these beds were marked by a high rate of deposition. While in many regions the whole crisis is documented in strata less than 1 m thick, in Greenland the crisis is recorded in more than 15 m stratigraphic thickness.

From the pollen and spore record, we recognize three phases:
-- first there is a collapse of the ecosystem, in which closed forests quickly gave way to an open vegetation dominated by soft herbaceous plants, mostly lycopodiophytes;
--secondly, there is a re-colonization by a number of woody shrubs;
-- finally there is the extinction of the tree species that earlier had dominated the late Permian forest vegetation.

It seems clear that the most significant happening in this scenario was not this delayed extinction, but rather the collapse of the forest ecosystem. In other parts of the world, a similar scenario now is beginning to be recognized, irrespective of climate zones or plant-geographic provinces. From the beginning of the Carboniferous, the biomass on earth was totally dominated by the wood of trees and shrubs. Thus, the worldwide dying of forests, without the formation of any new compensating equivalent biomass, was bound to have a dramatic effect on the carbon cycle. For an extended period, more organic material was being destructed than was being made by photosynthesis. Wood is broken down in particular by fungi. A strong increase in the activity of fungi is being confirmed by high concentrations of fungal remains in palynological assemblages in the youngest Permian. This 'fungal event' is now recognized from Arctic Canada to Australia.

Deforestation causes soil erosion. Organic material from eroded soils is carried by rivers far into the sea. Marine sediments from the Permian/Triassic crisis interval often are enriched in microscopic organic debris that might have been derived from soils. The proof of this hypothesis was provided by analysis of the fossil organic molecules. Application of organic-geochemical analysis of marine 'crisis sediments' from the Dolomites demonstrated the presence of aromatic hydrocarbon compounds which characteristically are known to be formed from cellulose derived from decaying plant tissues. Increase in soil erosion also provides an increase in mineral nutrients into the marine environment. This type of eutrophication resulted in explosive algal growth. In the Permian/Triassic crisis interval, we find clear indication of extreme algal activity. Throughout the world we observe high concentrations of acritarchs (i.e. organic fossil phytoplankton of uncertain, but probably algal, affinity). Regions in which trees are exterminated soon are colonized by opportunistic weed-like plants. In this crisis interval all over the world Selaginella and related plants were playing an important role in the pioneer communities. (Selaginella is still known as a plant able to find solutions for surviving extreme changes in its environment. For example, the 'Rose of Jericho' or 'Resurrection plant,' living in the desert, looks like a cluster of dead leaves; but with a bit of moisture it transforms into a fresh green plant. No wonder that Selaginella has survived 300 million years worth of geological history.)

[Consequences of the mass dying of forests are simple to predict; even the delayed extinctions follow patterns seen in model studies in population dynamics. Demanding and strongly competitive species, dominant in the undisturbed environment, do not die off all at once as their environment is attacked. Rather, they disappear one after the other, over an extended period, while their places are taken over by a variety of invading forms. Only after a long time will a new equilibrium establish itself.]

Let us return to the Permo/Triassic assemblages of Eastern Greenland. Remarkably, many spores of the lycopodiophytes occur as tetrads; particularly so immediately after the collapse of the forest eco-system. We are presently focusing our research on this phenomenon, but I shall tell you in which direction we are looking. Spores and pollen grains result from the reduction division of a mother cell, in which the number of chromosomes in four resulting daughter cells is half that of the mother cell. As long as the spores remain attached to each other, they form a 'tetrad.' Generally, the four cells detach, and are dispersed individually (as spores or pollen). Sometimes, though, the tetrad connection is maintained permanently. The genetic basis of the permanence of tetrads was uncovered recently during the molecular-genetic analysis of Arabidopsis thalania; in certain mutants of this species the pollen persists as permanent tetrads. Other irregularities also may occur during the reduction division: these show up e.g. as abnormal size, or wall thickness, or they may form permanent dyads. Knowledge of mutant genes that hinder a normal development during or following the reduction division is increasing rapidly. However, we also gain more insight in the cause of the formation of these genetic abnormalities. Environmental stress appears to be a crucial factor. Particularly in the former 'east block countries' there are many investigations on the influence of air- and soil-pollution on the development of pollen. Field studies and laboratory experiments have shown that strong acidification and heavy metal pollution particularly disturb the normal development of pollen. This results in sterility and abnormally high variability of pollen.

However, natural environmental stress may result in similar mutagenesis. An example is Cupressus dupreziana, the Sahara cypress, a nearly-extinct conifer from Southern Algeria. Its current distribution covers no more than 200 km2, where 153 trees, all more than 100 years in age, grow under extreme drought conditions. Their seedlings are doomed, because the groundwater table is beyond the reach of their roots. This species also shows irregularities in the reduction division; and its pollen shows great morphological variability.

The reproduction of the Sahara cypress is not easily studied in nature. Studies on specimens grown in nurseries, though, gave strong indication that reproduction is mostly apomictic. (Apomixis is vegetative reproduction, in which seeds or spores will grow into new plants without any sexual fertilization having taken place.) Apomixis is not uncommon in land plants. The mechanism is also genetically steered, and is stimulated by environmental stress. In apomictic plants, the normal development of spores or pollen often is disturbed. A good example is again Selaginella, some species of which reproduce virtually exclusively apomictically. Especially species of Arctic and high-Alpine environments show permanent tetrads and deviant spores.

This finally brings us back to the Permian-Triassic crisis. In Greenland, we saw that after the disappearance of the forests the landscape was colonized in particular by lycopodiophytes, including Selaginella. Yet, a large proportion of the microspores of these plants occur as tetrads. In tetrads, the germinal apertures of the individual spores are not free - which likely is the reason why these spores could not have played an effective role in sexual reproduction. Apomixis would appear to have been present in this instance. However, not only in Greenland; anywhere in the world, tetrads of the Selaginellales and the related Isoetales are found in the Permian-Triassic crisis interval.

Now that molecular-genetic and ecological studies have put us on the trail of a plausible interpretation of morphologically deviancy of spores and pollen, we have to make sure to revisit Kingscourt. Earlier I said that I had interpreted the increase in Norm B as a reflection of a gradual evolution of the conifers that produced Lueckisporites pollen: a gradual evolution into something new. Now, however, thirty years on, I consider that the morphological trend presages the definite end of the Majonaceae. There is nothing new. A family of conifers expires. All indications seem to suggest that the patterns of variation reflect a mutagenesis caused by extreme environmental stress, possibly including apomixis. Just as in the nearly extinct Sahara cypress.

This afternoon you have been present at the birth of a new phytocentric hypothesis, viz.: that it may be possible to use palynological data to recognize mutagenesis in periods of ecological crisis in the geological past. A hypothesis that needs further support in order to become acceptable.

Environmental stress is a vague concept - too vague to base anything specific on. Before we can base a worldwide mutagenesis on a particular type of stress, we should look for plausible candidates that could have caused the Permian/Triassic crisis.

We do have a working hypothesis: By eliminating other possibilities, we arrived at the concept of a mutagenesis based on excessive ultraviolet irradiation. The cause of such an UV-stress would have to lie in a deterioration of the ozone layer. This would be akin to the current decrease of the ozone layer caused by the release of gasses from our spray cans, deep-freeze boxes and refrigerators. These gasses are referred to as halogen compounds. We have found no spray cans in the Permian. However, volcanoes are natural sources for halogen compounds. In central and western parts of Siberia, massive basalt and tuff layers of Permian-Triassic age that are known as the "Siberian Traps", cover 5.10⁶ km². This is one of the most massive volcanic occurrences in the earth's history. Many researchers consider that it may be possible to link these outflows with the Permian/Triassic eco-crisis. Often the speculation involves hot-house gasses or acid-rain scenarios.

At first glance, an UV hypothesis appears not very plausible. Even the largest volcanoes produce relatively small amounts of halogen gasses. Yet, there is something different and unusual about the Siberian traps: the greatest part of these volcanic rocks exists as 'sills,' that is, they didn't flow over the surface, but intruded in between packets of sedimentary rocks. These sills cause water to be heated, as well as any other chemical enclosed in the sedimentary rock, and thereby facilitate a variety of chemical reactions.

As luck will have it, the Siberian traps coincided exactly with the largest coal deposits, and with the largest salt deposits known on earth. This unique juxtaposition of hot sills, organic carbon and chlorine could well have been responsible for unimaginable large-scale and long-lasting production of organic halogen gasses. These ozone-unfriendly compounds then surfaced via hydrothermal processes. Was Siberia in those days one humungous Yellowstone Park?

Maybe I may cite Bob Dylan once more:

[The oration ended with a discussion of relevancy of paleobotanic study - including palynology - for problems tackled by recent biologists. Not always were relationships harbingers of sweet harmony. Often, the paleobiologists found more support from the geologists, and from stratigraphers of oil companies. The qualities that have kept the paleobotanical lab (LPP) in fighting trim have been its multidisciplinary perspective, openness for renovations, and flexibility. Just recently, in biology circles it is being accepted that geo-biology should occupy itself more with bio-geological questions (or is it the other way around?). This bodes well for the future. But, always remember: When all things have priority, nothing is important.] I hope to stay involved in the future activities of the department, "until (as Drooger once put it so clearly) the moment of becoming totally superfluous."

[Translated by Jan Jansonious, 2003]
posted and last updated 6/7/04 webmaster