An Historical Phytogeography of the High Andean Flora*

Revista Chilena de Historia Natural 56: 109-122, 1983 An Historical Phytogeography of the High Andean Flora*

Fitogeograffa hist6rica de la Flora Altoandina

BERYL B. SIMPSON

Department of Botany, University of Texas, Austin, TX 78712, U.S.A:

ABSTRACT Palynological and geological evidence have shown that the Andes were uplifted to their present elevations only within the last 5 million years. Consequently, the floras of all of the high Andean habitats (those above treeline) must be very young and have ultimately been derived from older, lower elevation habitats. However, some low elements which colonized high elevation habitats subsequently underwent authochthonous radiations giving rise to endemic groups. This study examines the relative contributions of the I) initial source pool, 2) habitat severity, and 3) in situ speciation to modern levels of species diversity within the major phytogeographical regions of the high Andes (páramo, puna, austral alpine). It is suggested that initial floristic differences along the Andes were due to receipt of propagules from dissimilar regions and differential survival of immigrants. The Northern Andes received a more diverse array of colonizing elements than any of the other high elevation regions and at the same time provided a habitat that was conducive to establishment and persistence. Consequently, during the period of their formation, the northern Andes became increasingly diverse compared to montane regions farther south. Superimposed on these Tertiary factors were the effects of the Pleistocene climatic events which were of major importance in determining the level of autochthonous speciation. A combination of Tertiary and Pleistocene, ecological and geological factors are thus needed to explain the modern patterns of diversity seen throughout the high Andean habitats. Various phytogeographical classifications proposed for the Andes are compared to floristic regions expected on the basis of ecological and historical events. Key words: Biogeography, Evolution of Andean Flora, Paleoclimates.

RESUMEN Las evidencias palinol6gicas y geol6gicas han mostrado que los Andes se levantaron hasta sus altitudes actuales solamente a partir de los ultimos 5 millones de años. En consecuencia, la flora de todos los hábitats altoandinos (aquellos por encima del limite arb6reo) debe ser muy joven yen ultima instancia habr!a derivado de los habitats de menor altura. Sin embargo, algunos de los elementos que colonizaron los hábitats altoandinos experimentaron radiaci6n aut6ctona, originando grupos endemicos. En este trabajo se examinan: 1) la fuente inicial de la biota, 2) el rigor del hábitat, y 3) la especiaci6n in situ hasta los niveles modernos de la diversidad de especies dentro de las principales regiones fitogeográficas de los altos Andes (páramo, puna, austral-alpina). Se sugiere que las diferencias florísticas iniciales a lo largo de los Andes se deben a la recepci6n de propagulos desde regiones distintas y sobrevivencia diferencial de los inmigrantes. Los Andes septen- trionales recibieron una gama más diversa de colonizadores que cualquiera de las otras regiones altas, y al mismo tiempo proporcionaron habitats más adecuados para el establecimiento y sobrevivencia. Consecuentemente, durante el período de su formaci6n llegaron a ser mucho más diversos en compa- raci6n a las regiones montaiiosas más meridioriales. En forma adicional a los factores terciarios, los efectos de los eventos climaticos pleistocenicos fueron de gran importancia en la determinacion de los niveles de especiaci6n aut6ctona. Por lo tanto, se requiere una combinaci6n de factores terciarios y pleis- tocénicos, geol6gicos y ecol6gicos para explicar los patrones modernos de diversidad existentes actual- mente en los habitats altoandinos. Se comparan varias clasificaciones fitogeográficas propuestas para los Andes con las regiones florísticas esperadas sobre la base de eventos geol6gicos y ecol6gicos. Palabras claves: Biogeografla, Evoluci6n Fiora Andina, Paleoclimas. * Paper presented in the Symposium "Biogeography and Evolution of the Andean Flora" held during the IV Meeting of the Botany Section, Sociedad de Biologia de Chile, 7-10 september, 1982, Antumapu, Santiago. (Received 24 May 1983, Accepted 30 September 1983) 110 SIMPSON

INTRODUCTION regions they ultimately drew the majority of their floras. In a sense, therefore, this Phytogeography, the study of the geogra- kind of analysis allows predictions to be phical distributions of plants, can consist made about types of vegetation in, and the of static descriptions of species that occur floristic affmities of, various regions of the in particular areas, or it can include an Andes. analysis of the development of vegetative In tracing the history of the high Andean patterns. Most phytogeographers have an vegetation, I first examine the effects of insatiable desire to explain the evolution geological, and consequently climatic, of modern floras, and it is the historical changes on the original, low elevation aspects of plant geography that interest me communities present at the beginning of most. Consequently when asked to present the Tertiary. I then discuss why, during the an overview of the phytogeography of the course of the Cenozoic, these climatic Andes, I decided to trace the evolution of changes caused the percentages of the the modern vegetation types of the high floras derived from various source areas to (supraforest) regions. change in predictable ways along the cordi- Many con temporary ecologists (following llera. Finally, I examine the effects of the MacArthur and Wilson 196 7) are prone to Pleistocene in shaping the modern high state that the number of species in an area Andean floras. I then assess various phyto- is determined by: the time available for geographical classifications previously colonization, the size of the area to be proposed for the high Andes in light of the colonized, the biotic interactions between historical development of the vegetation. species, the number of potential colonizers, and the distance over which colonizers THE EFFECTS OF UPLIFT must travel. These factors are indeed of major importance in explaining diversity The geological events that resulted in the within communities, but any model that raising of the Andes to their present relies on these criteria alone, assumes that elevations did not happen instantaneously the areas under consideration are all within (even in geological time). Supra-forest the same climatic zone, have the same habitats were not suddenly created and diversity of habitats per unit area, and can ready for colonization, even though it is all draw from the same pool of colonizers. easy to speak of them as if they were Attempts to explain the diversity of (Simpson 1975). Moreover, the rise of the organisms within a community by only Cordillera over the 6 5 odd million years these factors also assumes that the areas from the end of the Cretaceous to the end under consideration have been stable of the Pliocene was correlated with a (climatically and edaphically) over the time progressive generation of climatic zonality spans involved. For the most part, these from the equator to the poles and of the are unrealistic assumptions. During the development of intracontinental patterns time over which the Andes were colonized, of aridity. conditions within the high elevation Consequently, as the Andes rose, the habitats were continually changing and effects of altitude were confounded by constantly altering the pools of "potential" factors that produced a disparity in colonizers. climatic conditions from north to south What I would like to do here, therefore, along the Andes and from low to high is present a dynamic picture of the develop- elevations within particular latitudes (Figs. ment of the modern floras of the high 1, 2). Figure 3 schematically indicates the Andes and show how and why the supra- relative elevations of the north, central, forest habitats of the Andes differentiated and southern parts of western South Ame- into the main types of vegetation we now rica during the middle Eocene, the middle see. For these reconstructions, I examine Miocene, and at the end of the Pliocene, not only the effects of area and absolute and suggests the kinds of vegetation that time of availability for colonization, but would have been present in these regions also the effects of changing climate. By at these times. The elevations suggested for tracing their histories, we can see why all of the periods except the end of the different areas of the high Andes would Pliocene are speculative, but are suggested necessarily develop certain vegetative by fossil evidence from Patagonia (Patterson structures and from what extra-Andean & Pascuall972), Bolivia (Ahlfeld & Branisa HISTORICAL PHYTOGEOGRAPHY OF THE HIGN ANDEAN FLORA 111

Fig. 1: Development of the latitudinal thermal gradient during the Tertiary. a) During the Eocene there was very little difference in temperatures between the equator and poles. The rotation of the earth did cause an upwelling on the western side of the continent that would have affected coastal regions. b) By mid-Miocene, there was ice in Antarctica and there was a definite equator to pole thermal gradient. The modern wind and current systems would have been more or less developed and the Andes were high enough to cause some rainshadow effects. c) By the end of the Pliocene, the modern climatic pattern of South America was established. Desarrollo del gradiente latitudinal termico durante el terciario. a) Durante el eoceno hubo una diferencia muy pequefia de temperaturas entre el ecuador y los palos. La rota ción de la Tierra provoc6 corrientes ascendentes en el sector occi- dental del continente que habr{an afectado las regiones litorales. b) En el mioceno media, bubo hielo en la Antártica y un gradiente termico definido desde el ecuador hacia los palos. Los sistemas de vientos y corrientes habr{an estado más o menos desarrollados y los Andes alcanzaron una altitud suficiente como para condicionar algún efecto de "som- bra de lluvias". c) AI termino del plioceno se establecieron los patrones climaticos modernos de Sudamerica.

COSMOPOLITAN AND ", HOLARCTIC ELEMENTS I a b

TROPICAL FOREST o•

TRQptCAL FOREST

OPEN OPEN FOREST SAVANNA

\SAVANN SOME 1 TEMPERATE TEMPERATE ELEMENTS ELEMENTS) > <> <> AUSTRAL.: EOCENE ·ANTARCTIC MIOCENE ELEMENTS

Fig. 2: Effects on the vegetation of the climatic developments of the Tertiary indicated in Fig. 1. a) Eo- cene. b) Mid-Miocene. c) End of the Pliocene. Also indicated are the various source areas of propagules that began to be important in the Miocene. Efectos sobre la vegetaci6n de los eventos climaticos del terciario sefialados en la Fig. 1. a) Eoceno. b) Mioceno media. c) Finales del plioceno. Tambien se indican las diversas áreas de origen de propagulos que llegaron a ser importantes en el mioceno. 112 SIMPSON

a c PLIO-PLEISTOCENE EOCENE MIOCENE

Montane- Forest rainfores Tropical

semi dry valleys

Forest 16ºS Montane scrub

subtropical mont ane Tropical or est Forst matorra

Warm Temperate Alpine Forest Forest

Fig. 3: Schematic cross-sections at various latitudes across the Andes showing possible elevations and vegetation types during the a) Eocene; b) mid-Miocene; c) end of the Pliocene. Secciones transversales esquematicas a varias latitudes a traves de los Andes mostrando las posibles altitudes y tipos de vegetacion durante el: a) eoceno; b) mioceno medio, y c) finales del plioceno.

1960) and Colombia (Van der Hammen with the Eocene appearance of Nothofagus 1974). in Patagonia (Archangelsky & Romero At the beginning of the Tertiary, fossil 1974) (Figs. 1-3). By the Oligocene, the floras (Gerth 1941, Patterson and Pascual surface waters of the Antarctic Ocean were 1972, Archangelsky and Romero 1974, cold and by the mid-Miocene, transient Báez and Gasparini 1979) indicate that glaciations occurred on the Antarctic there was some, but very little zonation continent (Kennett 1977, Kerr 1982). across the latitudes spanned by South Ame- Thus, by at least 14 million years ago, the rica even though the continent was in its modern thermal gradient between the present position. Most of the continent, at equator and the poles was in place. least most of the exposed western portions, These changes would have had pro- appear to have been forested, with a slight nounced effects on the emerging Andes. gradation from tropical rainforest in Once the low to high latitude thermal equatorial latitudes to subtropical forest gradient had been established, the modern in the extreme south. In the Eocene, the system of heat balance (or a similar .one) first indications of temperate forest have would have been created. The earth's pattern been found (Archangelsky & Romero of heat balance, or latitudinal energy 1974). Oxygen isotope data from the An- contrasts, combined with the rotation tarctic Ocean indicate cooling of the effects of the planet cause the modern bottom water by mid-Eocene (Kennett wind and pressure systems. Consequently, 1977). This marine data correlates well the establishment of a thermal gradient not HISTORICAL PHYTOGEOGRAPHY OF THE HIGH ANDEAN FLORA 113 only dictated that the high latitudes would linear (Whittaker. 1975, Whittaker and be colder than the low latitudes, but also Marks 1975). The most conspicuous that the high and low latitudes would be elevation at which productivity declines is under different wind and pressure regimes. treeline. Most of the area of South America north of In temperate regions, treeline usually the Tropic of Capricorn came to lie within occurs at elevations at which the ground the influence of the trade winds and the is permanently frozen below 20-30 em area south of the Tropic within the because trees are not able to absorb enough westerly wind zone. Once this global moisture from the soil to sustain their large circulation pattern developed, the Andes biomasses. When air temperatures reach themselves began to play an increasingly ooc, the xylem can be frozen with the important role in the climate of South result that water lost from exposed branches America because the mountains created (or leaves) by inadvertent transpiration can rainshadows to the lee side of the prevailing not be replaced. If not reversed rapidly winds. enough, death of the exposed plant parts It is well known (Humboldt 1817, Troll occurs. The "hardening" of plants before 1959, Walter 1979) that mountains within the winter freezes in cold temperate regions a given biome have a sequence of altitudi- serves to protect trees from this kind of nal belts reflecting changes in vegetation. damage, but at high enough elevations, This change is caused, all other factors (e.g., conditions eventually become too severe total precipitation) being equal, by the even for hardened tissues to withstand the decrease in temperature, increase in direct low temperatures if exposed. Plants that irradiation, and decrease in diffuse are low growing and protected under the irradiation with elevation. The rate of tem- snow cover avoid this sort of frost damage. perature decrease with increasing elevation In high elevation tropical habitats, stress is called the lapse rate. The average lapse conditions leading to the reduction and rate is considered to be about .65ºC/100 m finally elimination of plant growth are rise in elevation. However, in practice, the somewhat different. There is no temperature seasonality, but as elevations become rate is often not linear and it can vary from higher and higher, there is a more and more place to place. For example, in the north pronounced diurnal fluctuation in tem- central Andes of Peru and Ecuador, the peratures (Hedberg I 964, Monasterio lapse rate between sea level and 1000 m is 1979) (Fig. 4). As elevations increase up to about normal. From 1000 to 2500 m, the rate is only .32ºC/100 m rise in elevation. Between 2500 and 4500 m elevation the decrease is relatively linear and approaches ºC the average value of .65°C. Above this 15 elevation, on clear nights, the rate can be as E G high as 1º C/100 m (Johnson 1976). z A Eventually an elevation is reached where R P. 10 the temperature decreases to ooc. The M E actual altitude of this zero degree isotherm T varies with latitude and with the season of ' ILY ' the year. Likewise, there is an elevation DA ' ' above which temperatures never rise above 5 ' z 0°C. This constitutes permanent snow or A E frost line. Since the average annual tem- M perature at the base of a mountain in high latitudes is much lower than that at the 0 base of a tropical mountain, the elevations 0 30 60 of the zero degree isotherms and permanent LATITUDE snowlines are much higher in the tropics than in high latitudes. Fig. 4: The diurnal change in temperature plotted against latitude for several high elevation stations. Reduction in plant growth expressed as (Redrawn from Barry 1979). reduction in productivity, has been shown Cambios diurnos de las temperaturas graficadas en rela- to follow altitudinal decreases in tem- ción con Ia latitud para varias estaciones de alta-monta- perature, although the decrease is not ña. (Redibujadas de Barty 1979). 114 SIMPSON

5200 m and above, the number of hours of during the Tertiary and the Andes progres- freezing per day increases to the point at sively rose, we would therefore expect which the ground becomes permanently that there was a gradual development of a frozen and growth for rooted plants gradient in productivity from low to high becomes impossible. Below this zone, there latitudes and from low to high elevations. is often freezing at the soil surface, reducing Correlated with these trends in productivity, the amount of water that can be absorbed. we would expect a progressive decrease in Mean night minima are normally about numbers of species in high latitudes and -lOºC on the altiplano (Johnson 1976). high elevations from that present in the Temperatures of 1 to 4ºC are supposed to same terrestrial localities in the Eocene. In be lethal for tropical forest plants (Bielb effect, the development of global thermal 1965). In addition, above 2500-3000 m in zonality and increased elevations both had tropical regions, rainfall decreases relative the same effect, the reduction in primary to lower elevations. It is not clear whether productivity and the elimination of species the limit of tree growth in high tropical (reduction in diversity). Where these effects regions is determined by aridity, the large are strongest, as in the high vegetation number of hours during which freezing can zones of the southern Andes, reductions occur, or both, but the fact that treeline in would have been most severe. By the time the tropics is higher in valleys than on the latitudinal thermal gradient became a ridges suggests that drought is the dominant strong force in the mid-Miocene, the south- factor. Although trees can not grow under em Andes would have been raised to eleva- such conditions, shrubs, grasses, and tions of at least 1500 m, sufficiently high p'erennial herbs can grow well. Obviously, for the development of an alpine type of plants can not become dormant each day, vegetation (Fig. 3 ). The northern Andes but must still deal with the problem of would have also been raised to similar nightly freezes. The most general solution elevations, but the temperatures at low to avoid the effects of short bouts of elevations would have been much higher freezing temperatures is to insulate the than those at the southern end of the living tissues (Hedberg 1964 ). If properly Andes. Following the lapse rate up the insulated against damage that could be tropical Andes shows that elevations of caused during the few hours of freezing 1500 m are too low for temperatures to each night, and if sufficient soil moisture decrease to the point at which trees can is present, "caulescent" herbs can grow no longer grow. Evidence for the lack of in these habitats. Such plants constitute supra-forest habitats before the end of the a vegetation stratum that is lacking in high Pliocene (3-5 million years ago) in Colom- elevation arid regions and alpine meadows bia has been presented by Vander Hammen and, as such, add to the diversity of (summarized in Van der Hammen 1974). tropical humid versus tropical dry or Van der Hammen's data suggest that the temperate high elevation habitats. Eastern Cordillera of Colombia did not It has been shown that, across biomes, rise above 2000 m before the end of the diversity varies predictably in the same way Pliocene and, until that time, was covered as productivity. Diversity decreases from with montane forest. Open habitats at the tropics to the poles and from the elevations above 3500 m, became available bases to the summits of mountains (cf., and were colonized in Colombia only MacArthur 1972). The reasons for these within the last 5 million years. In terms patterns have been debated for years of time, therefore, the oldest kind of (Pianka 1966), but one argument supra-forest habitat in the Andes is the (MacArthur 1969, Connell and Orias austral-alpine. However, any advantage 1964) relates differences in diversity directly of being available for colonization at to differences in primary productivity. As an earlier time than other Andean regions conditions become so severe so as to permit would have been negated by the extreme the growth of fewer and fewer individuals, selection exerted by the combination the maintenance of populations of sufficient of temperateness and high elevation. size for reproduction becomes a problem. The development of a tropics to pole The species that dominate at environmental thermal gradient was not the only climatic extremes are those that are able successfully change that occurred during the Tertiary. to maintain effective breeding populations. For certain regions of the Andes, As the equator-pole gradient increased concomitant changes in precipitation were HISTORICAL PHYTOGEOGRAPHY OF THE HIGH ANDEAN FLORA f15

as important as increases in elevation for not become extremely dry until very late the historical development of the vegetation. in the Tertiary, pockets of arid habitats Unlike temperature, the rainfall patterns developed relatively early in interandean developed were not correlated in a straight- valleys. These valleys formed a scattered forward manner with latitude. Changes network from the northernmost regions occurred not only in the total amount of of Colombia to central Chile and Argenti- precipitation that was received, but also in na. It is difficult to assign an absolute age the dispersion of the precipitation over the to any of the interandean valleys, but some year. The rainfall pattern developed by the of them must have existed since Miocene end of the Tertiary showed a decrease in times when the first major upthrusts of the total precipitation from the northern most of the Andean units occurred. These Andes to the southern end of the altiplano valleys were undoubtedly of importance in and then a gradual increase in total annual providing migration routes for some of the precipitation toward southern Chile. In taxa preadapted to arid conditions that addition, a seasonality of rainfall developed eventually colonized the dry regions of the from Colombia south to the same region. altiplano. Within the Central Andes a gradient of precipitation from semi-arid to extremely POTENTIAL COLONIZERS arid developed from east to west across the altiplano (Figs. 1-3). The development We mentioned above that the number of of these patterns of rainfall was gradual species in an area (and, of course, the kinds over the first half of the Tertiary as of species) are dependent in part on the latitudinal thermal gradient set into motion number of potential colonizers. Usually, the major wind patterns we now see. The all individuals of neighboring "source areas" extremes of aridity that resulted in the are considered potential colonizers. The western part of the central Andes was, source areas of colonists for all of the high however, a consequence of the final montane regions would originally have uplift of the Eastern Cordillera and been the tropical and subtropical forests probably did not exist in its present form that covered them and which now abut until very late in the Pliocene. The aridity most of the high tropical Andes. In a sense, in this region is now so severe that it these taxa would never have been colonists produces one of the driest deserts in the and any modern elements derived from world. them are actually natives rather than As in the case of increased temperateness immigrants. As so often happens, however, and the attainment of very high elevations, in the onslaught of changing conditions, the formation of desertic conditions had most of the original inhabitants were the effects of reducing total productivity replaced by successful alien colonists. The (Murphy 1975) and of reducing diversity most successful of these immigrants came by eliminating more and more of the from areas ecologically similar to the new species that had grown in the Andean kinds of habitats being created. regions when they were low, warm, and Some Neotropical elements did respond humid. Within the tropics there is a to the selection pressures exerted by altitude progression of vegetation types across and/or aridity and became incorporated aridity gradients. Forest gives way to grass- into the high elevation floras, but although land, grassland to scrub, and scrub to selection over time can modify the tolerance barren soil with no perennial biomass. In limits of many species, whether or not such the high Andes, the first, forest, stage is not changes occur depends on the original present, but the remainder of the sequence amount of variation present in a species, is followed with one notable difference in the severity of the selection, the time span the last stages. Annuals never become as over which selection has to act, and important in the extremely dry regions of competition from other taxa. In the case of high elevations as they are in low, equally the central, and to some extent the dry, elevation deserts. Solifluction (freezing southern, high Andes, selection was strong, and thawing of the surface layers of the time was short, and the demands made of soil) strongly inhibits seedling establishment species adapted to life in the lowland and makes the annual habit a precarious humid tropics were beyond the limits of one. variation present in most of them. As While the central Andes probably did conditions became more and more disparate 116 SIMPSON from lowland tropical conditions, fewer groups that ultimately became cosmopolitan and fewer species of the original lowland because of their colonization abilities. vegetation survived. The highest number Since, in general, we expect the number survived in those high elevation habitats of propagules received to be inversely most similar to their lowland counterparts related to distance, it seems clear that the and fewest survived in the vastly different northern Andes would have received more high elevation arid and temperate habitats. propagules from North America than any Consequently, we expect the fewest Neo- other Andean region. Yet, if we could tropical elements in the high arid habitats make predictions as to the relative and the supra forest habitats of the austral contributions of the various sources of regions, and the most in the high elevation species that populated in the high elevation humid tropical habitats. habitats by the end of the Tertiary, we As the mountains rose and conditions mtgh t predict that the northern high changed, other sources of colonists besides Andes would have the largest absolute the lowland or montane forests became number of taxa derived from North Ameri- increasingly important (Fig . 2). Among can stocks, but it terms of percentages of these were open habitats in various parts the floras of various regions, Holarctic taxa of the Neotropics and the interandean dry might constitute higher percentages of the regions, both of which provided taxa pre- central and southern Andean floras than of adapted to arid or semi-arid conditions. the northern regions. Likewise, weedy While the Patagonian flora is often cosmopolitan elements would probably considered to be a "source" area for Andean constitute greater percentages of the floras elements, it is equally probable that Patago- of the Central Andes than of the northern nia was colonized by taxa that had become Andes. In the southermost Andes, we also adapted to open, cold environments in the expect a high percentage of cosmopolitan Andes. North America likewise provided elements, austral elements and, although a source of taxa pre-adapted to cool distances from North America are great, conditions because of its well developed a significant proportion of widespread non-forest temperate biota. temperate elements that colonized via Colonization by Nearctic species probably North America. occurred gradually from the mid Miocene onward. The final closing of the Panama gap per se about 3.5 million years ago EFFECTS OF THE PLEISTOCENE would actually have had little effect on the colonization rate of the supraforest habitats By the end of the Pliocene, we would of the Andes since the uplift of the lowland expect that the northern Andes would connection between Colombia and Panama have had the richest floras of any of the would not have changed the distance high elevation habitats and would have between montane peaks. The fact that contained a high percentage of Neotropical most of the colonization of the high Andes elements. During the Pleistocene, the occurred after the middle of the Pliocene differences between the floras of the is due to the final raising of these habitats northern, central, and southern Andes were at that time, not the production of a magnified. This intensification of patterns continuous lowland connection between Pa- already laid down by the end of the nama and Colombia. Relative to North Tertiary was caused by the promotion of America or Eurasia, South America did not speciation within the high elevation zones develop a sizable non-forest temperate flora of the northern Andes and the further because the continent lacks a large reduction of species diversity in the temperate land mass. There were, of course, extreme south. In the central Andes, the some native austral herbaceous elements Pleistocene was a time of differentiation and many of these would have served as the of some taxa, but the effects were not as original colonizers of the sou them Andes pronounced as in the north. when they rose to heights above which· In the Colombian Andes, Van der trees could survive. Nevertheless, it is likely Hammen (1974 and references therein) that many of the propagules that successfully has shown that by the beginning of the colonized the southern open, high elevation Pleistocene, a flora similar to the modern habitats would have arrived via long distance high elevation flora existed. During the dispersal and would have belonged to Pleistocene his studies have documented HISTORICAL PHYTOGEOGRAPHY OF THE HIGH ANDEAN FLORA 117

the occurrence of several glacial advances Consequently, species distributions are that lowered snow and vegetation lines usually determined by climatic, rather than about 2000 m. Overlapping with these geographical factors. During the Pleistocene, periods of cold were periods alternately ranges across the altiplano were undoubtedly more, then less, humid than modern times. also modified (Simpson 197 5, 1979) and The combined effects of the various some elements that now have restricted climatic oscillations would have been ranges would have experienced times of expansions of ranges of almost all of the conditions favorable for range expansion. kinds of plants present in the high northern On the other hand, even at times when Andes. Van der Hammen's pollen profiles conditions were most different from now, (Van der Hammen 1974) clearly show that when lakes dissected the altiplano, and at some times, Polylepis greatly expanded glaciers wiped out populations and severed its range and at other times the areas connections between populations to the dominated by grasses increased in size. This north and south of Lake Titicaca, there multiple and. varied set of opportunities for would never have been the kind of isolation expansion followed inevitably by that now exists (and existed during restrictions would have provided perfect previous interglacials) in the northern conditions for speciation. Some groups Andes. Consequently, differentiation was such as Espeletia, Diplostephium, and Lori- not as common, nor in most cases, as caria emerged from the Pleistocene as complete as, that in the northern Andes. speciose groups with almost all of their Some authochtonous speciation would species endemic to the high elevations of have occurred, but not on the scale of that the northern Andes. This same pattern, but to the north. to a lesser extent, would have affected the In the southernmost Andes, supraforest mountain tops of the ·Ecuadorian and habitats are distributed along the edges of northern Peruvian Andes. the large glaciers in the extreme south and The Central Andes would have been atop peaks to the north of the ice fields. affected somewhat differently. First, the al- Consequently, these habitats are tiplano is a large expanse of high elevation distributed in part in an island-like fashion habitat. There are not a series of isolated similar to the northern high elevation "islands" of habitat in this region. habitats (Fig. 5). As in the northern Andes,

-34º

-38º

50º-

Fig. 5: The distribution of Austral-alpine (stippled) habitats at the present time (a) and during the maxi- mum glaciation (b) in southern South America. Distribucion de los hábitats austral-alpinos (punteados) en Ia actualidad (a) y durante Ia máxima glaciacion (b) en el sur de Sudamerica. 118 SIMPSON

Pleistocene glacial events lowered snow and PHYTOGEOGRAPHICAL CLASSIFICATIONS vegetation zones and hence expansion lati- OF THE HIGH ANDES tudinal, and longitudinally of high elevation zones. The extent to which this occurred, ho- The previous analysis would lead us to wever, differed greatly from that in the believe that different types of vegetation northern Andes. In southernmost South developed in the northern, central, and America, glaciations effectively wiped out southern Andes. That this did, in fact, all of the alpine habitats south of 44ºS. Al- happen is reflected in the common pine elements could have existed north of recognition of three major high Andean Chiloe Island, along the base of the Andes phytogeographical units, the Páramo, Puna, in Argentina and at lowered elevations and Austral-alpine. Still, various authors between the latitudes of 32º and 42º in have classified the vegetation in different south-central Chile (Fig. 5). While there is ways. some evidence that suggests vegetation Perhaps the most generalized phytogeo- zones moved north in Chile, the movement graphical scheme proposed for the high was not great and when climatic conditions Andean flora is that of Cabrera and Willink changed, islands of alpine habitat were not (1973) (Fig. 6). These authors have placed left behind. The effect of the habitat the high Andean vegetation within a larger changes would have 'been extinction and unit they call the Andean-Patagonian Do- the promotion of some differentiation, but minion which includes all the high eleva- not an extreme proliferation of species. tion vegetation types from Venezue-

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Fig. 6: Phytogeographical schemes proposed for the high Andean vegetation. a) The most generalized scheme proposed by Cabrera and Willink (1973). b) A composite scheme combining. studies of We- berbauer (1945), Cabrera (1951, 1968), Troll (1959), Van der Hammen (1974), Simpson (1975). Esquemas fitogeográficos propuestos para la vegetaci6n altoandina. a) El esquema más usual propuesto por Cabrera yWillink (1973). b) Un esquema compuesto combinando estudios de Weberbauer (1945), Cabrera (1951, 1968), Troll (1959), Vander Hammen (1974), Simpson (1975). HISTORICAL PHYTOGEOGRAPHY OF THE HIGH ANDEAN FLORA 119 la to Tierra del Fuego, the coastal deserts and the Thorn or Dry Puna the high of Peni and Chile, and the Patago- elevation vegetation types dominated by nian steppes of Neuquen, western Rio shrubs. Troll (1959) based his divisions on Negro, Chubut, and Santa Cruz in Argenti- climate and the structure of the vegetation. na. Within this dominion, they He differentiated Paramo from Puna on the circumscribed a High Andean Province basis of the presence of a pronounced dry extending across all the high elevations of season in the latter with the transition Venezuela, Colombia, and Ecuador, the occurring in northern Peru. Across the eastern and western edges of the altiplano Puna from northeast to southwest there is and all of the supra-forest habitats south of an increase in the length of the dry season. the altiplano to the tip of the continent. Although the reduction in precipitation They also delineated a second province, the and increase in seasonality is gradual across Puna Province which included the central this expanse, there are areas where the portions of the altiplano. Physiognomically structure of the vegetation and the floristic this scheme has some merit because it composition undergoes anoticeable change. lumps all of the grass-perennial forb The break between a predominantly grass associations and separates out the arid steppe to an open shrubland constitutes the shrub-dominated types of vegetation. Yet, boundary between Troll's Wet and Dry Puna. Sarmiento (1975) has shown that parts of Cabrera later (1968) further divided the the Puna (the "high Andean desert" of Sar- Dry Puna of Troll into Wet Puna, Dry miento) has a higher floristic similarity Puna, and Desert Puna (Fig. 6). Vegetation with Patagonia than with the Puna proper. that falls under Troll's classification of Salt Likewise, Cleef (1979) has shown that Puna is scattered about the western altipla- almost half of the Paramo flora is derived no in saline areas. Salt Puna is therefore an from local tropical taxa and that almost edaphically, and not a climatically, half of these are monotypic genera. determined vegetation type. Floristically, therefore, the Puna of Cabrera It is unfortunate that Troll did not travel and Willink (1974) seems to be composed in the southern Andes because the high of more than one natural vegetation type elevation flora there has been little studied and the Páramos appear distinct from the as a unit compared to the Paramo or Puna. other grass-dominated high Andean Most workers are content simply to call vegetation types. everything south of the Puna, "high Hueck and Siebert ( 1972) divided the Andean vegetation". The few attempts to high altitude vegetation of the Andes into subdivide the vegetation phytogeogra- Paramo, Puna, Salar vegetation, and "High- phically have been done on a limited scale. Andean Vegetation without Major There are numerous other phytogeogra- Classification". They used the term Paramo phical schemes portions of the high Andean to refer to areas in which Espeletia grows. vegetation but these finer subdivisions have The "unsubdivided" high elevation usually been made by workers within parti- vegetation included everything else from cular countries or for a region of a country Venezuela to Tierra del Fuego that was not with little attempt to relate their schemes Puna (altiplano scrub) or Salar vegetation. to those proposed for the same kind of While this scheme does recognize the vegetation in a contiguous country. In the Paramo vegetation as distinct, it is hard to Paramos, for example, Cuatrecasas early understand the existence of a high-Andean ( 1958) subdivided the Colombian vegetation non-Paramo type of vegetation in Colombia above treeline into altitudinal zones which and Venezuela. Species that Hueck and he designated SubParamo, Paramo proper, Siebert (1972) listed as characteristic of and SuperParamo. These distinctions have this kind of vegetation are all either been followed by recent workers in Colom- widespread taxa or groups restricted to bia (cf. Van der Hammen 1974, Cleef the central Andes. 1978). In Venezuela a different set of Many other authors (cf. Walter 1971) vertical belts was worked out by Vareschi have followed Troll (1959) and divided (1970) and still a third by Monasterio the tropical Andes into Paramo and Puna, (1980). but subdivided the Puna into Wet Puna, In Ecuador, perhaps because of the lack Dry or Thorn Puna and Salt Puna. The Wet of in depth studies, there has been little Puna included all of the grass and forb controversy about the name for the vegeta- dominated parts of the high central Andes tion of the high elevations and few 120 SIMPSON attempts have been made to subdivide it. vegetation province, but he subdivided this The term Paramo is applied without into a northern, central and southern problems by botanists and local inhabitants component. The northern extended from alike to all of the vegetation above treeline Jujuy to La Rioja (22-290 S), the central with the exception of isolated "bosques de from the soutltern part of San Juan across quinoales" (Polylepis) that appear in Mendoza to the northern part of Neuquen scattered localities. In Peru, Weberbauer (30º to about 380 S), and the southern (1945) used the term Jalca for the southern fromsouthern Neuquen across the western extension of the Paramo, but he clearly part of Rio Negro, Chubut, Santa Cruz and indicated that he considered it Páramo and Tierra del Fuego. It appears to me that the stated that it differed from the Puna to flora of the Andes south of the altiplano the south because it received a larger amount of precipitation and a greater consists of a gradual transition from dry proportion of the precipitation in the form Puna vegetation to austral alpine vegetation of sleet than the Puna. The southern limit in much the same way as the high of the Paramo he indicated was at 8º30' S mountains of southern Ecuador and latitude in the region west of the Marafion northern Peru form a bridge between the Valley. Paramo and the Puna. South of 8-90 S in Peru, the Puna begins. Weberbauer did not subdivide the Peruvian CONCLUSIONS Puna into smaller vegetation units either altitudinally or latitudinally and he thus How one determines phytogeographic did not distinguish between the kind of regions is a matter, to some degree, of vegetation south of the Jalca but north of personal preference. Some authors rely 13ºS and the vegetation of the Peruvian al- exclusively on physiognomy as the basis tiplano. He considered that the floristic re- for their division. Others use floristic lationships of the Puna vegetation were with analyses to ascertain relatively coherent the western slopes of the Andes and the groups of species but the Andes as a whole interandean valleys. Pernettya (Ericaceae) are not well enough known floristically to is one of the few dominant Puna elements permit rigorous phytosociological analyses that is clearly derived from the eastern side although such techniques have been used of the Andes. In Bolivia and northern Ar- by several workers in restricted regions gentina, the area covered by Puna vegetation (Oberdorfer 1960, Monasterio 1980, is greatly expanded longitudinally and is Villagrán 1980). In general the phyto- thus affected by the precipitation gradients geographical divisions of the Andes have that lead to the physiognomic and floristic therefore been primarily based on the associations recognized by Troll (1959). presence or absence of certain "key" taxa Floristically as one goes west across the al- such as Espeletia. An examination of the tiplano, the Neotropical-derived taxa drop climates of the mountainous regions of out and the floras correspondingly have a western South America shows that these greater and greater portion of their species physiographic units are correlated with the belonging to widespread temperate or major climatic provinces. An understanding cosmopolitan groups. of the historical development of these South of the Puna, the high elevation climatic provinces allows us to understand vegetation has been divided differently by why and when the major types of Andean botanists depending upon whether they vegetation developed and to predict what were working on the Chilean or the Argenti- future studies will show about the floristic na side of the Andes. Schmithiisen (1956) affinities of different parts of the high delineated a Northern Andean Formation Andes. that extended from the northern limit of It is impossible to test these tentative Chile to 390 S and, south of this, a predictions with any rigor, but a few Southern High Andean Region. The suggestive studies have been made. The first northern part was characterized by having of these by Cleef (1979) is the only in only three "favorable" months for plant depth study. Cleef systematically collected growth. In the southern area, there were over a large number of the colombian Pá- nine "favorable" months. Cabrera (19 51) ramos and examined the taxa in the light placed the Argentine high Andean flora, of their ancestral derivations. Even though other than the Puna, into the Altoandean he sampled only a portion of the total.area HISTORICAL PHYTOGEOGRAPHY OF THE HIGH ANDEAN FLORA 121 covered by Paramo vegetation, he collected normal number for a island of Austral-alpine 259 genera, indicating a very high diversity. habitat. The diversity is again much lower His studies of these genera indicated that than in the north, although in this case, almost half ( 41%) of the genera were only one of the many areas of such derived from tropical elements growing in vegetation was sampled. In terms . of the adjacent regions. Another 10.4% are relationships of these genera, 27% are of related to groups distributed widely South American origin (over one-third are throughout the tropics. Eleven percent of "Andean"), 22% belong to cosmopolitan the genera apparently colonized from groups, 27% belong to widespread, North America (the Holarctic element), primarily temperate groups, and 24% are of 19.6% belonged to widespread temperate austral origin. This flora thus appears to be groups, and 7.7% are cosmopolitan. Most more similar in the origin of its flora to the of these probably also arrived from North Paramos than to the geographically closer America. A small, but significant, Puna. Undoubtedly, this similarity is due to proportion (9 .2%) of the flora is the comparable effective precipitations in apparently of austral origin. the two regions. There are really no other data sets It is thus clear that the floras of the comparable to that of Cleef. Weberbauer various regions of the high Andes have been (1945) lists plants "characteristic of the drawn from different source areas and that Puna", or "plants with their greatest the relative importance of these source development in the Puna", but it is areas depends on the distance from the impossible to ascertain the completeness of source to some extent, but primarily to the the lists. Herzog (1923) enumerates plants degree of ecological similarity of the source of microhabitats at several localities in area and the area under consideration. northern Bolivia, but the brevity of the lists suggests that they contain only the most common species. Two other studies farther south in the Andes contain plants lists that LITERATURE CITED provide a suggestion of what more extensive work in the future might show. The first, a study of the vegetation of AHLFELD F & L BRANISA (1960) Geologia de Bolivia. Institute Boliviano del Petró leo. La Paz. the cordillera of La Rioja, Argentina, by ARCHANGELSKY S & E ROMERO (1974) Los regis- Hunziker (1952) contains an extensive list tros más antiguos del polen de Nothofagus of the plants collected over a wide area (Fagaceae) de Patagonia (Argentina y Chile). of the mountains of La Rioja. Hunziker Boletin de la Sociedad Botanica de Mexico also indicated which species grew at high 33: 13-30. BAEZ AM & ZB DE GASPARINI (1979) The South elevations (Dry Puna). While this study is American herpetofauna: An evaluation of the much less extensive than that of Cleef, the fossil record. In: Duellman WE (ed) The South presence of only 38 genera in Hunziker's American Herpetofauna: Its Origin, Evolution collections from the southern Dry Puna and Dispersal. Museum of Natural History, University of Kansas, Lawrence, Kansas: 29-54. habitats suggests a much lower diversity BARRY RG (1969) High altitude climates. In: PJ Webber than in the north. An analysis of these (ed) High Altitude Geoecology. Westview Press. genera shows that 4 7% are South American Boulder: 55-74. and without exception restricted to the BLIEB R 1965. Temperaturresistenz tropischer Pflanzen Andes or south temperate regions. The auf Puerto Rico. Protoplasma59: 133-156. CABRERA AL (1951) Territories fitogeograficos de la tropical elements so prominent . in the Republica Argentina. Bolet{n de la Sociedad north are completely lacking. Twenty-two Argentina de Botanica 4: 21-65. percent of the genera in the high habitats CABRERA AL (1968) Ecolog{a vegetal de la Puna. In: sampled by Hunziker are cosmopolitan and C. Troll (ed) Geo-ecology of the Mountainous Regions of the Tropical Americas. Colloquium 31 % of widespread distribution in Geographicum. Geographisches Institut der temperate regions. There are no genera of Universität Bonn 9: 91-116. definite austral origin. CABRERA AL & A WILLINK (1973) Biogeografia de The second study by Thomasson (1959) America Latina O.E.A. Washington, D.C. 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