Growth and Population Dynamics of Espeletia (Compositae) in the Venezuelan Andes

SMITHSONIAN CONTRIBUTIONS TO BOTANY NUMBER 48

Alan P. Smith

SMITHSONIAN INSTITUTION PRESS City of Washington 1981 ABSTRACT Smith, Alan P. Growth and Population Dynamics of Espeletia (Compositae) in the Venezuelan Andes. Smithsonian Contributions to Botany, number 48, 45 pages, 19 figures, 20 tables, 1981.-Espeletia (Compositae, Heliantheae) is a major component of alpine and subalpine plant communities in the Venezu- elan Andes. A detailed analysis of population dynamics was undertaken for Espeletia species representing the arborescent, caulescent rosette, and acaulescent rosette forms. Mortality, growth, and reproduction were recorded during a 15-month period for E. schultzii, and E. lutescens (caulescent rosette species), E. fzoccosa and E. atropurpurea (acaulescent rosette species), and E. humbertii (an arborescent species of treeline forests). Espeletia floccosa is obligately semelparous; all other study species are iteroparous. Microenvironmental variables were measured at all sites.

OFFICIALPUBLICATION DATE is handstamped in a limited number of initial copies and is recorded in the Institution's annual report, Smithsonian Year. SERIESCOVER DESIGN:Leaf clearing from the katsura tree Cercidiphyllum japonicum Siebold and Zuccarini.

Library of Congress Catalogingvv in Publication Data Smith,'Alan P.-

Growth and DoDulation dvnamics of EsDeletia ComDositae)\I in the Venezuelan Andes. (Srnithsonian' cbntributions to botany ;'no. 48) Bibliography: p. 1. Espeletia. 2. Growth (Plants) 3. Plant populations-Andes. 4. Plant populations-venezuela. 5. Alpine flora-Andes. 6. Alpine flora-Venezuela. 7. Botany-Andes-Ecol- ogy. 8. Botany-Venezuela-Ecology. I. Title. 11. Series. QKl.S2747 no. 48 [QK495.C74] 581s 81-607061 [583'.55] AACR2 Contents

Page Introduction ...... 1 Acknowledgments ...... 4 General Methods ...... 4 Research Design ...... 4 Plot Design ...... 6 Environmental Measurements ...... 7 The Phramo Environment ...... 7 Studies of Juveniles ...... 10 Recruitment ...... 10 Size Class Distribution ...... 11 Growth ...... 12 Mortality ...... 14 Studies of Adults ...... 19 Size Class Distribution ...... 19 Growth ...... 20 Rosette Turnover Time ...... 26 Mortality ...... 26 Reproductive Phenology ...... 29 Effects of Slope Aspect on Growth and Population Density ...... 33 Experimental Study of Growth ...... 35 Discussion ...... 35 Relationship between Growth Form and Population Dynamics .... 35 Population Control and Stability ...... 38 Summary: Tables ...... 38 Appendix: Tables ...... 40 Literature Cited ...... 44

... 111

Growth and Population Dynamics of Espeletia (Compositae) in the Venezuelan Andes

Alan P. Smith

Introduction accurate description of spatial relationships because each plant’s location can be described as a The presence of perennial caulescent rosette point on an “X-Y” coordinate system, a tech- plants differentiates many high elevation ecosys- nique far less appropriate for plants with assy- tems in the tropics from alpine comunities of the metrical canopies; plants can be easily manipu- temperate latitudes (Cuatrecasas, 1968; see also lated for experimental studies; associated plants Figure 1). Such plants are characterized by ro- are also small in stature, facilitating characteri- settes of large leaves supported by unbranched or little-branched stems. Immature leaves form a zation of competitive neighborhoods; many giant dense bud around the apical meristem. Dead rosette species are abundant, permitting adequate leaves are often persistent, forming a thick cylin- replication of measurements. der around the stem. This form has evolved in- This paper describes seasonal variation in dependently in the alpine regions of the East growth, mortality, and reproduction in relation Africa (Senecio, Carduus and Lobelia), South Amer- to environment for Espeletia species of contrasting ica (Puya and Espeletia), Hawaii (Argyroxiphium), growth forms. Long-term studies of year-to-year New Guinea (Cyathea), and the Canary Islands variation in population dynamics are continuing, (Echium), but is absent in extra-tropical alpine and will be presented in later papers. This re- regions. It is therefore assumed that the form is search is part of a larger study of convergent an adaptive response to tropical alpine environ- evolution among tropical alpine giant rosette spe- ments (Hedberg, 1964; Mabberly, 1973). Ecolog- cies of the New and Old World tropics. ical studies of these plants may help us under- Espeletia (Compositae, Heliantheae) is endemic stand plant forms characteristic of high tropical to the Andes of Venezuela, Colombia, and north- mount ains. ern Ecuador. The genus probably evolved in The giant rosette form is particularly well place from the genus Polymnia, which occurs in suited for studies of plant population biology: tropical montane forests (J. Cuatrecasas, pers. plants are small enough to make thorough growth comm., Mar 1973). At least 90 species are recog- measurements feasible, yet large enough to permit nized, of which 45 occur in Venezuela (Cuatre- precise measurements; the rosette form permits casas, 1954, 1977; Aristeguieta, 1965). The most Alan P. Smith, Smithsontan Tropical Research Institute, Post Office “primitive” member of the genus is probably E. Box 2072, Balboa, Panama. nerifolia Sch. Bip., a very widely distributed ar-

1 2 SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE1.-Study species: .4.E. humbertzi on talus slope at 3500 m: plant is approximately 4 m tall; B? E. schulltiz at 3600 m on leeward slope; C. E. schultzii at 4200 m: D. E. schultzii at 3000 m, showing insect damage to leaves: E, E. jloccosa at 3600 m. an acaulescent, monocarpic species: F, E. atropurpurea at La Aguada at 3400 m, an acaulescent, glabrous-leaved species; G, E. lutesrens at 4200 m; largest plant is approximately 1.5 m tall: H, longitudinal section of E. schultrii plant at 3600 m. borescent species of subalpine forests (Cuatreca- rescent species occur at elevations of about 2600 sas, 1954; Chardon, 1951; Smith and Koch, m to 3600 m in elevation. 1935). There are 15 other arborescent species, all The majority of Espeletia species occurs in the occupying restricted geographical ranges. Arbo- paramo (alpine and/or subalpine) zone. Most NUMBER 48 3 paamo species have the caulescent rosette growth diurnal temperature fluctuations (Smith, 1974a, form, but there are also several acaulescent par- 1974b, 1979). The arborescent form persists in amo species. Caulescent and acaulescent rosette Espeletia species of subalpine forests. A similar species occur at elevations of about 2700 m to evolutionary pattern has been proposed for the 4600 m. Nomenclature of Espeletia spp. is that of genus Senecio in the East African high mountains Aristeguieta (1965); for other plants, Vareschi (Mabberley, 1973). (1970) is followed. Only one previous study has dealt with growth Montane forest tree line occurs between 2700 and population dynamics of Espeletia. Pannier m and 3400 m in the Venezuelan Andes around (1969) grew E. schultzii under phytotron condi- Merida, Estado Merida (9’N), depending on ex- tions. He found that germination percentage was posure and degree of human disturbance. Pockets increased by wetting and drying cycles, and that of woodland extend up to 4200 m in sheltered the degree of seed dormancy varied seasonally. valleys and on talus slopes. Forests have been Leaf color and amount of leaf pubescence varied eliminated altogether in many areas, so that par- with the temperature regime under which the amo vegetation merges gradually with manmade plants were grown, suggesting a high degree of montane pastures. The upper limit of vascular phenotypic plasticity. Pannier recorded mortality plants occurs at approximately 4800 m,just below of E. schultzii seedlings in a 1 m2 plot in the snowline. paramo at 3600 m. Highest mortality occurred in The Andes began to rise during the Cretaceous, the dry season. Baruch (1972) studied water re- reaching their present height during the Pliocene lations in E. neriiflia under both field and phy- and the Pleistocene (Vuillemier, 197 1). Pleisto- totron conditions. He found that increased leaf cene glaciations caused fluctuations of climatic pubescence and density thickness (dry weight per zones (Van der Hammen, 1968). Glaciers ex- cm2 of leaf surface) is correlated with reduced tended downward to approximately 2600 m in transpiration. the Andes around Merida (R. Giegengack, pers. The anatomy of Espeletia has been studied by comm., Feb 1974). Modern snowline occurs at Carlquist (1958), Roth (1973), Weber (1956), and approximately 4850 m and, in Venezuela, apparently is retreating. Anecdotal accounts suggest Rock (pers. comm., May 1972). Powell and Cua- that in the early 20th century snowline occurred trecasas (1970) found that 30 Espeletia species all at approximately 4400 m to 4500 m (R. Giegen- had a chromosome number of N= 19. gack, pers. comm., Feb 1974). Observations on the distribution, growth form, Sierran “islands” with alpine or subalpine en- and anatomy of certain Afroalpine caulescent vironments were produced as the Andes rose. The rosette species (Lobelia spp. and Senecio spp.) were invasion of these islands by Espeletia-presumably made by Cotton (1943), Hauman (1934, 1935), by genotypes of arborescent forest species similar and Mabberley (1973), but no quantitative eco- to E. neriifolia-produced numerous isolated pop- logical data were collected. Hedberg (1964) and ulations. This comparative isolation, combined Coe (1967) found that nyctinastic leaf movement with new selective forces imposed by the paramo and retention of dead leaves on the stem in these environment, apparently contributed to extensive species result in maintenance of tissue tempera- speciation (Chardon, 195 1; J. Cuatrecasas, pers. tures above ambient at night. Hedberg (1969) comm., March 1973). The arborescent type was found that annual height increase in Senecio ken- apparently ancestral to the more compact caules- iodendron was approximately 2.5 cm. Studies of the cent rosette form, which requires lower energy population biology of the alpine Senecio species allocation for nonphotosynthetic support tissue were initiated in 1977 and are continuing (Smith, and provides greater buffering against intense unpublished data). Less extensive, but similarly 4 SMITHSONIAN CONTRIBUTIONS TO BOTANY long-term studies of growth, mortality, and re- 35733 to W. D. Billings and GB 28950 to the cruitment for alpine Cyathea species on Mount Southeastern Plant Environment Laboratory at Wilhelm were initiated in 1975 (Smith, unpub- Duke University, a Duke University Graduate lished data). School Research Award, a Duke University Dis- Information on within- and between-species sertation Travel Award, and by the Smithsonian variation in population dynamics is essential for Tropical Research Institute. an interpretation of growth form patterns in Es- peletia. Data on net growth rate and longevity are General Methods necessary in order to determine the immediate causes of trends in plant height. It is also necessary RESEARCHDEsIGN.-The research provided (1) to determine which environmental factors reduce elevational comparisons within a wide-ranging growth and reproduction and increase mortality; caulescent rosette species (E. schultzii), (2) com- the capacity of the caulescent rosette growth form parisons within E. schultzii at an intermediate to moderate the effects of these specific factors elevation along a topographic gradient, and (3) can then be evaluated. comparisons among Espeletia species representing Knowledge of population dynamics in Espeletia different growth forms. All sites were located in is also essential for an understanding of the func- the Andes near Merida, Estado Merida, Vene- tioning of alpine and subalpine ecosystems of the zuela (Figure 2). north tropical Andes, where Espeletia is a domi- Elevational Comparisons: Elevat ional comparisons nant component of the community. for E. schultzii were made among sites at 3000 m ACKNOWLEDGMENTS-Iam grateful to Dr. W. (Zerpa site), 3600 m (Mucubaji site), and 4200 m D. Billings for his encouragement and advice (Aguila site). Espeletia schultzii is abundant at 3000 throughout this study. m and 3600 m, growing in dense stands from Logistical support in Venezuela was kindly ridge tops to bog edges. At 4200 m, at the upper provided by the Instituto Silvicultura, Facultad limit of its range, E. schultzzi occurs primarily in de Ciencias Forestales, and the Centro de Estu- gently sloping, rocky drainage areas. These three dios Forestales de Postgrado, Universidad de 10s sites were all on gentle slopes exposed to the Andes, Merida; the Instituto Forestal Latino- prevailing NE winds. The 3000 m and 3600 m American0 de Investigaction y Capitacion, Mer- sites were located on morainal deposits. The 4200 ida; the Herbarium of the Facultad de Ciencias m site was never glaciated. Forestales and the Herbarium of the Facultad de Topographic Comparisons: Comparisons within E. Farmacia, Universidad de 10s Andes, Merida. schultzii were made along a small morainal ridge- Dr. Jose Cuatrecasas and Dr. Federico Pannier bog gradient at 3600 m (Mucubaji). The total generously provided me with information on the relief from ridge to bog was about 10 m. Sites ecology and distribution of Espeletia. were located at the base of the slope; on a mid- I am grateful to Mrs. Shirley M. Billings for slope exposed to the prevailing NE winds; at the much advice and assistance on financial and top of the slope, also exposed to the wind; and on logistical matters, and to David Hanselmann, a leeward midslope. Some data were also col- Marilyn Loveless, Zdravko Baruch, Juliana Mul- lected on plants growing on the edge of the bog roy, and Sr. Faustino Diaz and his family for (Figure 3). This gradient was in a fenced research their cooperation in the field. I thank Drs. Beryl area referred to as the “upper exclosure.” B. Simpson and Egbert G. Leigh for useful com- Three other sites at 3600 m were used for ments on the manuscript, and Mrs. Arilla H. studies of E. schultzii: (1) a steep xeric slope of a Kourany for editorial assistance. terminal moraine north of Laguna Mucubaji Financial support was provided by National (Figure 2); (2) a gently sloping talus slope at 3600 Science Foundation grants GB 34882 and GB m; (3) a series of windward and leeward slopes in NUMBER 48 5

8O50’ N

KM BELOW 3000M ABOVE 4000M

FIGURE2.-Map of research sites (numbers = study site numbers given in Appendix (Table A; X = locations of government weather stations; triangle = Pic0 Mucunque, 4765 m). the “lower exclosure,” a fenced research area from it in growth form. An arborescent species, adjacent to Laguna Mucubaji(Figure 2). E. humbertii Cuatrecasas, was studied at Laguna Interspec@ Comparisons: Espeletia schultzii was Negra, approximately 1 km southeast of the Mu- compared with several other species differing cubajitopographic site, at 3500 m (Figure 2). 6 SMITHSONIAN CONTRIBUTIONS TO BOTANY

WIND L

WEATHER STATION

FIGURE3.-Topographic gradient used for study of E. schultzii at 3600 m (numbers = site numbers in Appendix Table A).

Populations were located on a talus slope, in a cies to find the reproductive adult with the small- closed forest, and in a treefall in an otherwise est rosette diameter. A reproductive adult was closed forest. defined as any plant with new or old flower stalks. A semelparous acaulescent rosette species, E. This minimum rosette diameter was then used to floccosa, was studied at 3600 m (Mucubaji). Pop- distinguish between adults and juveniles. For E. ulations were small and were located on rocky schuftzii this critical diameter is 25 cm, for E. windward slopes, surrounding by E. schuftzii. A fluccosa it is 10 cm, and for E. futescens it is 40 cm. study plot was established in such a population For E. humbertii it was not necessary to distinguish (Mucubaji), approximately 300 m from the main between adult and juvenile stages: the large plots topographic site used for E, schultzii and a few used for surveys of adults were also used for meters above the E. schuftzii plot located on talus. complete counts of juveniles, because juvenile An acaulescent, glabrous-leaved species, E. atro- densities were low at most sites. purpurea, was studied at La Aguada, a station on Sampling was initiated on the north edge of a the Merid a Teleferico (cable car) at 3400 m. Data given 10 X 10 m plot. The first 120 adults en- on this species are presented elsewhere (Baruch countered were marked with a metal stake and and Smith, 1979). numbered aluminum tag. If there were fewer A caulescent rosette species, E. lutescens, similar than 120 adults in the plot, the first adults en- to E. schuftzii but much taller, was studied at 4200 countered beyond the plot were tagged in order m (Aguila). It is one of the most widespread to give a uniform sample size from site to site. species at this altitude, occurring from ridge tops to the edges of drainage areas and bogs. A plot These 120 marked adults were used for measure- was established in a population of E. lutescens ment of growth and mortality. Dates for surveys adjacent to the E. schultzii plot at 4200 m. are given in Appendix Tables C and D. Descriptions of all sites are summarized in Ap- Ten I X 1 m quadrats were located at random pendix A. Locations are given in Figure 2. within each 10 X 10 m plot, using coordinates PLOTDESIGN.--IO X 10 m plots were used for from a random number table. Height to highest population studies. Height, stem diameter (for leaf tip, rosette diameter, and distance to nearest arborescent species), rosette or crown diameter, adult neighbor were recorded for every Espeletia and distance to nearest adult neighbor of the juvenile in each quadrat. Each juvenile was same species were recorded for each Espeletia marked with a numbered plastic pot marker. adult within a 10 X 10 m plot. In most cases, 1 Each marker was located 2 cm upslope from its m2 random quadrats, located within the 10 X 10 plant, with the marker edges oriented east-west m plots, were used to sample juvenile plants. A to minimize shading. Great care was taken to preliminary survey was carried out for each spe- locate all juveniles present, including seedlings NUMBER 48 7

(cotyledon stages). Dates for surveys of juveniles SW-facing slope (leeward) at 3550 m in the lower are given in Appendix Table E. exclosure (Figure 2). The leeward slope at this The original research design called for a mini- site was far more sheltered from the prevailing mum of two replicate 10 X 10 m plots for each NE wind than was the leeward slope studied in site. However, because insufficient time was avail- the upper exclosure. The lower exclosure site thus able during the initial wet season survey, only provided a clearer demonstration of the effects of one plot per site was established, each divided wind on microclimate. These data were used to into two subplots. interpret patterns of flowering phenology on ENVIRONMENTALMEASUREMENTS.-DeSCrip- windward and leeward slopes. The study was tions of elevational gradients in rainfall and tem- carried out in clear weather on 24-25 Mar 1973. perature are based primarily on data from Ven- Measurement sites were located 6-7 m below the ezuelan government weather stations. These sta- crest. Distance from ridge crest to base of the NE- tions are located at 3100 m (Los Plantios), 1 km facing slope was 13.4 m; distance from crest to from the 3000 m study site; at 3550 m (Mucu- base of the SW-facing slope was 18.0 m. Air baji), 0.5 km from the main Mucubaji study site; temperatures were measured with shaded ther- at 4095 m (Pic0 del Aguila), 5 km from the 4200 mocouples at 50 cm. Wind speed was recorded m study site. These stations are visited daily by with a hand-held anemometer (Deuta-Werke) at government personnel. 1.5 m above the ground. Soil moisture, measured gravimetrically, was For each of seven adult E. schulttii plants on determined periodically for most study sites. each slope, one thermocouple was placed in the Cores of soil were extracted from depths of 0-5, center of the apical bud, a second in the tissue of 5-10, and 10-15 cm for several points around one of the outermost bud leaves on the north side each study plot. Soil moisture content under 15 of the bud, and a third in the tissue of a mature atmospheres pressure was determined in the lab- leaf at a 45' angle on the north side of the rosette. oratory for soil from each site, using the methods of Richard (1949). Weather stations were established at the topo- The Paramo Environment graphic gradient site in the upper exclosure at 3600 m (Figure 3). Each station had a white, Elevational trends in climate are summarized double-roofed, louvered, instrument shelter (Cha- in Table 1. Total annual precipitation decreased bot and Billings, 1972) placed at ground level. from the 3100 m site to the 4095 m site. Wet Each shelter contained a Taylor maximum-min- season soil moisture levels also decreased with imum thermometer. A Bendix-Friez 3-cup ane- increasing elevation (Table 1). Snowfall is rare at mometer was located at 100 cm above the ground 3550 m, but occurs occasionally at 4200 m in the adjacent to each shelter. Weather stations were wet season. There are seldom more than few cm serviced weekly from early June 1972 through of accumulation, and this rarely persists for more mid-January 1973. than 24 hours. Percentage cover by vascular plants, moss, li- Rainfall is strongly seasonal. The dry season chens, rock, litter, and bare soil was estimated for generally lasts from December through March or each 1 m2 random quadrat used for surveys of April. The transition from wet season to dry juveniles. In addition, vegetation cover was esti- season, and from dry season to wet season, can be mated for the area within a 1 cm radius of the very gradual. Rainfall data and other climatic canopy margin of each juvenile present in the 1 variables for Mucubaji (3550 m) are summarized m2 quadrats. in Figure 4. Seasonal precipitation patterns vary A brief microclimatic study was made on a 20' greatly from year to year. Figure 5 summarizes NE-facing slope (windward) and the adjacent 20' 30 years of precipitation data for the months of 8 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE1 .-Elevational differences in environment at re- The effects of topography on microclimate for search location (except where noted, data are from Vene- the primary study site at 3600 m are summarized zuelan government weather stations near Espeletia study in Table 2. The lowest dry season temperatures sites) occurred in the bog, as a result of cold air drain- Factors I 3/00m 3550m 4095m age. Highest dry season temperatures occurred on Mean maximum ternper- 12.6OC 10.5"C 5.2'C2 the leeward slope, because this slope was sheltered ature, 1972 from the wind. Differences between topographic Mean minimum temper- 4.2OC 1.9"C l.l°C2 sites were greatly reduced during the wet season. ature, 1972 Short-term data on wind speed and air tem- Precipitation 1304 mm 1118 mm 980 mm Evaporation, open pan, 108mm 78 mm 74mm perature on a NE-facing (windward) slope and Nov 1970 the adjacent SW-facing (leeward) slope are sum- Soil moisture' marized in Figure 6. Data on tissue temperatures 1 Aug 1972 62% 47% 35% for E. schultzii plants on these slopes are summa- 26 Mar 1973 27% 30% 18% Wilting percentage 18% 18% 11% rized in Figure 7. The slopes were located in the Vegetation cover' 94+2.6% 78+4.0% 38&8.1% lower exclosure at 3550 m (Figure 2). Cover by rock 0% 2+1.0% 37f9.170 Air and plant temperatures early in the morn- ' Data from E. schultrii study plots at 3000 m and 3600 m ing rose faster on the NE-facing slope than they and E. lutescens study plot at 4200 m; soil moisture expressed did on the SW-facing slope because the sun hit on oven-dry weight basis. the NE-facing slope first. However, by 1130 hours Temperature data from June 1968-May 1969. wind speed had increased and the sun was almost directly overhead. By this time, plant temperatures for the more sheltered SW-facing had risen February (mid dry season) and May (early wet above those for the NE-facing slope and remained season) at Paramo de Mucuchies (41 18 m), lo- higher during the afternoon. Soil moisture mea- cated between the 4200 m (Aguila) and 3550 m sured at a depth of 0-15 cm on 25 March 1973 (Mucubaji) research sites. was 28.9% on the NE-facing slope and 16.2% on Mean monthly temperatures are relatively con- the SW-facing slope. stant throughout the year. However, the diurnal Needle ice formation occurred at elevations temperature range is greater in the dry season above 3000 m on bare soil wherever soil moisture than in the wet season (Figure 4). Heavy cloud was high enough. At 4200 m there were extensive cover and frequent fog, as well as rain and snow, are characteristic of the wet season. In the wet areas of bare soil, probably maintained by intense season, clear weather often occurs early in the frost activity; needle ice occurred on most nights. morning but seldom persists beyond 0900 or 1000 At 3600 m there was extensive cover by moss, hours. Completely clear days are common in the lichens, and higher plants, and only small patches dry season. Relative humidity can drop to 15% to of bare soil a few cm2 in size surrounded by 20% at ground level during the dry season but vegetation. Needle ice formation was restricted to often remains near 100%all day in the wet season. these small areas and occurred only on clear Wind is nearly continuous during the day in both nights. Soil frost activity was most intense in the wet and dry seasons. Wind speeds seldom exceeds early dry season when clear nights were common 20 mph, except on high mountain peaks. Highest and soil moisture was still high. By mid dry wind speeds occur in the wet season. Winds are season, soil moisture was too low to permit needle almost entirely from the northeast during the wet ice formation except in wet swales and bogs. season, but occasionally shift to the southwest Cattle and horses graze throughout and par- during the dry season. Such shifts generally last amo zone. Cattle were seen at elevations up to for less than a day. 4600 m. However, grazing was eliminated at 3600 NUMBER 48 9

10 10

CW w. bO < 5

C 1, MM 250

/.R.H.

20c I00

a2 d 30 z15C a<

1 O(

5c 10

0 1 I 1. J' F M' A' MEJ' J A 5 0' N D MONTH

FIGURE4.-Seasonal variation in climate at Mucubaji (3550 m) (data from government weather station). Top: A, mean maximum temperature (monthly); B, mean minimum temperature (monthly); C, mean number of hours of sunshine per day for each month. Bottom: A, mean relative humidity (monthly); B, total mm evaporation per month; C, total precipitation per month (mean maximum and mean minimum temperatures were calculated from daily maximum and daily minimum temperatures, recorded with hygrothermographs; hours of sunshine recorded with Campbell Stokes sunshine recorder-"sunshine" defined as solar radiation at or above intensity of 0.33 cal-'cm-2min-' (Stringer, 1972).

m (Mucubaji) approximately 15 years ago. There wire, but the fences were stolen or vandalized. was light grazing at 3000 m (Zerpa) and at 4200 However, no cattle or horses were observed feed- m (Aguila). An attempt was made to enclose the ing on Espeletia and no evidence of such grazing study plots at Zerpa and Aguila with barbed was found for any of the species studied. 10

100

42 43 50 5 60 61 62 t YEAR

FIGURE5.-Thirty years of precipitation data for February and May, Paamo de Mucuchies, 41 18 m (data from government weather station; X = missing data).

Studies of Juveniles the 91 new seedlings produced during the year appeared during the wet season. REcRuITMENT.-The 1 m2 random quadrats Topographic Comparisons in E. schultzii at 3600 m: used for studies of juveniles were resurveyed pe- Seedling production decreased from leeward to riodically. New seedlings were marked and mea- windward slope sites and from slope base to ridge sured during each resurvey. Data were collected (Table 3). Highest rates of seedling production for E. schultzii, E. lutescens, and E. floccosa. Espeletia thus occurred in the sites most sheltered from the humbertii seedlings were too rare on the talus slope prevailing wind (Table 2). site to make studies of seedling dynamics practi- Interspecijic Comparisons: Seedling recruitment cal. Extensive excavations of young plants indi- rate was low in E. lutescens (only one new seedling cated that, of all species studied, only E. atropur- was recorded during the year), but was similar to purea reproduces vegetatively. Thus, the new that for the adjacent E. schultzii population at plants recorded for E. schultzii, E. lutescens, and E. 4200 m (two seedlings). floccosa were all derived from seed. Twenty-five new seedlings were recorded for E. Elevational Comparisons in E. schultzii: Results floccosa during the year. All of these seedlings are summarized in Table 3 and Figure 8. Seedling appeared during the wet season. There were only production decreased with increasing elevation. five 1 m2 quadrats for E. floccosa versus 10 for New seedlings were relatively common at both other species. On a per area basis, the recruitment 3000 m and 3600 m. Only two new seedlings were rate for E. floccosa was therefore similar to that for recorded during the year at 4200 m. Seedling E. schultzii on the ridge site at 3600 m (50 seedlings production occurred entirely in the wet season at per 10 m2 per year). 3000 m and 4200 m. At 3600 m, all but four of The low number of new seedlings recorded for NUMBER 48 11

TABLE2.-Variation in environment along a topographic gradient at 3600 m (site described in Figure 3 and Appendix Table A)

Midslope Midslope Factors Bog Slope base windward Ridge leeward

Temperature ("C) * 25 Jun -23 Jul 1972 Mean maximum 12.8 13.3 13.9 14.4 15.6 Mean minimum 1.1 1.1 1.1 1. I 1.1 17 Dec 1972 -14 Jan 1973 Mean maximum 17.8 16.7 20.0 19.4 23.6 Mean minimum -9.8 -5.9 -3.6 - 1.8 -5.0 Soil moisture (% oven-dry weight) 24 Ju1 1972 94.5 57.0 51.6 54.6 49.6 24 Aug 1972 109.2 54.6 49.5 47.1 48.9 2 Jan 1973 66.4 34.9 31.0 26.7 28.5 26 Feb 1973 53.4 20.0 20.6 20.6 21.8 Wilting percentage 24.3 17.9 18.0 17.5 17.6 Mean wind speed (mph) 8 Jun 1972 -14 Jan 1973 1.5 3.1 3.6 6.4 2.7 Percent of cover Vegetation - 81k5.5 78f4.0 72k5.8 79k2.6 Rock - <1 2k1.0 3k1.2 0 * Mean temperatures are based on weekly readings of maximum-minimum thermometers both E. schultzii and E. lutescens at 4200 m could Height class intervals were based on a geomet- have been the result, in part, of intense, nightly, ric sequence with a common quotient of 2 (0-0.5, soil frost activity. Most seedlings are destroyed by 0.6-1.0, 1.1-2.0, 2.1-4.0 cm, etc.). This sequence frost heaving as soon as they germinate and thus was used because for the smallest plants a differ- disappeared too quickly to be recorded during ence in plant height of a few mm was associated the quadrat resurveys. Most of the established with major differences in mortality rate, whereas juvenile plants at 4200 m grow among rocks, or for larger plants a difference of several cm had are surrounded by vegetation, and are protected little effect. These same height classes were used from soil frost activity. to summarize data on juvenile mortality and Higher rates of seedling recruitment in more growth. sheltered sites could have resulted from increased Elevational Comparisons in E. schultzii: Size class seed production, as well as from the direct effects distributions are shown in Figure 8. The greatest of microclimate on germination and establish- number ofjuvenile plants occurred in the smallest ment. The number of adult plants that flowered height classes. At 4200 m there were far fewer and the number of flower heads per plant were both highest in more sheltered places (Table 15- plants in the smallest size classes than was the 17). case at either 3600 m or 3000 m. Total number SIZECLASS DIsTRIBuTIow.-The number of ju- ofjuveniles per 10 m2 was highest at 3000 m and veniles present in the 1 m2 random quadrats was lowest at 4200 m (Appendix 'Table B). recorded at each site. Height to highest leaf tip Comparisons within E. schultzii at 3600 m along was then recorded for each plant. These data a Topographic Gradient: For the upper exclosure were used to construct size class distributions. sites the number of juveniles decreased from Size class distributions were based on data from smallest to largest height classes (Figure 9). Ju- the initial survey. venile density was highest on the slope base site 12 SMITHSONIAN CONTRIBUTIONS TO BOTANY

the talus slope site and the closed-canopy forest

15 site to yield clear size distribution patterns (Figure 12A-B). High juvenile densities occurreil only on the treefall site within otherwise closed forest 10 2 (Figure 12C). At this site, the number ofjuveniles x decreased from the smallest to the largest size 5 classes. For E. floccosa at 3600 m and E. schultzii on the 0 xeric slope site at 3600 m, juveniles were concentrated in the intermediate rather than the lowest size classes. Both of these populations had shorter

20 generation times and fewer large adults than was the case in other populations. The relative scarcity of large adults may have resulted in decreased ov competition between adults and juveniles. This could lead to an increased probability that newly 10 recruited seedlings reach higher size classes. GROWTH.-A~~juveniles of E. schultzii, E. lutes- J cens, and E. floccosa present in the 1 m2 quadrats at the initial survey were marked with plastic

0 I. 14 16 18 26 8 10 12 14 16 tags. Height, measured to the highest leaf tip, was TIME (HOURS) recorded. The surviving plants were remeasured FIGURE6.-Comparison of microclimate on NE-facing one year later. Change in plant height was used (windward) and SW-facing (leeward) slopes at 3550 m: A, as a measure of growth. Distance to nearest adult wind speed: B, air temperature at 50 cm (dotted lines = of the same species was recorded for each plant. windward slope data). Elevational, Topographic, and Interspecific Compari- sons: Growth rates are summarized in Figures 8, and lowest on the ridge. Density was higher on 9, and 1 1. Growth was highly variable; there were the leeward slope than on the windward slope no clear-cut patterns along either altitudinal or (Appendix B). On the xeric slope site at 3550 m, topographic gradients. Mean annual growth rate the greatest number of juveniles occurred in the was negative for E. schultzii on the midslope wind- intermediate size classes, with lowest numbers in ward site at 3600 m and for E. lutescens at 4200 the smallest classes (Figure 1OA). On the talus m, indicating that, on the average, juveniles de- slope at 3600 m, only threejuveniles, all cotyledon creased in size during the year. This was the result stage seedlings, were found (Figure 10B). These of extensive leaf wilting during the dry season. were located in small pockets of moist organic For most plants, leaf regrowth during the next debris. wet season was too slow to permit full recovery Interspecfic Comparisons: Juvenile density in E. from this wilting. Some juveniles in both popu- lutescens was too low to yield a clear pattern of lations increased in size, however. size class distribution (Figure 11B). Growth occurred primarily in the wet season In E. j7occosa the greatest number of juveniles for all populations. Wilting of older leaves in the occurred in intermediate size classes (Figure 11A). dry season caused a reduction in size, even for The only other population showing a similar plants that showed a net increase in height over pattern was E. schultzii on the xeric slope at 3550 the entire year. m. For E. schultzii at 3000 m, annual height growth For E. humbertii, young plants were too rare on increased with increasing initial plant height (rxy NUMBER 48 13

"C 4( A

"C B 3

1 . a ,,,,,,, 1 1 . a I 14 16 18 20 8 10 12 14 16 TIME (HOURS)

FIGURE7.-Comparison of E. schulttzz tissue temperatures on windward NE-facing (dotted line) slope and leeward SW-facing (solid line) slope at 3550 m: A, bud core temperature: B, mature leaf temperature (vertical lines represent 95% confidence intervals). 14 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABL~3 -Seedling production at various tirnts of )ear (each figure = ~ number of nen seedlings in ten I-rn2 quadrats (five quadrats for E. /%ccocai AHG= 2.0 a[ the end of given time period: dates for all surveys given in Appendix A Tables C-E) ‘“I 68 5d 92% 22 72.~ 12 and sills season season season season in onr 28 I 1972 1972-3 1973 1973 jrar- 20 E irhiil/~ri 3000 ni 51 0 0 71 125 3h00 m blope base I16 3 0 7 I26 \2 indnard slope 81 4 0 3 91 Ridge 45 1 0 4 50 Leeward slope 137 1 0 ‘4 162 P AHG= 0.3 -1200 m 1 0 0 0 1 = I U E Jlorcusa 0 3600 rn 23 0 0 1 ? 5 - 5c- \ E luiescens 56 4200 rn 0 0 0 I I -I 29 1% = 0.340; P

100 N 75, AHG.I.2 AH G = - 0.3 A

' 200 AHG.0.4 AHG= 0.7 v) c,":t D B

OB 75 70 - 60 0.75 1.5 3.0 6.0 12.0 24.0 10 6 0.25 50 HEIGHT CLASSES (CM

25 FIGURE10.--Size class distributions of E. schultrzz juveniles at 3600 m: A, xeric slope; B, talus slope (juvenile = plant with rosette diameter of less than 25 cm). 0.25 0.75 1.5 30 6.0 120XOOB ~n15 3.0 60 1x1MC

HEIGHT CLASSES (CM) linear relationship between percent mortality in FIGURE9.-Topographic variation in population structure each size class and the natural log of the median and dynamics for E. schultrii juveniles at 3600 m: A, ridge; value (in cm) for each height class (Figure 13). B, midslope windward: C, slope base; D, midslope leeward The regression of mortality rate against plant size (juvenile = plant with rosette diameter of less than 25 cm; was not statistically significant for E. schultziz at AHG = annual height growth (cm); bar = number of juveniles: top number = percent mortality in one year: lower 4200 m. However, mean initial height for juve- number = height increase in one year). niles that died was significantly lower than mean initial height for juveniles that survived one year niles present at the initial survey, there was a (0.7 cm versus 3.8 cm; P

(u AHG=2.0 cm E 25 0 A -Lo \ 0 cu E 0 25 0- \ AHG= -1.2 cm 0 175 C B N E 1% v) 0 W 25 t 0 Ln -1 100 0 \ 125 z - 130 W cn > I- 103 3 Z HEIGHT CLASSES (CM) a J FICCRE11 .-Population structure and dynamics for juve- a 75 niles: A, E. Joccosa at 3600 m: B, E. lutescens at 4200 m (for E. Joccosajuvenile = plant with rosette diameter of less than 15 cm. for E. lutescens juvenile = plant with rosette diameter 50 of less than 40 cm; AHG = annual height growth (cm). bar =juveniles, top number = percent mortality in one year; lower number = height increase in one year). 25

0 &WA I 1-11 creased with increasing plant size (Figure 9). 60 103 140 180 220 260 300 340 There were negative linear relationships between HEIGHT CLASSES ( CM) percent mortality in each size class and the nat- FIGURE12.-Population structures for E. humbertii at 3500 ural log of the median value for each size class m: A, talus slope (plants/ljO m2); B, closed forest (plants/ 100 m2): C, treefall (plants/50 m2) (growth rate for talus (Figure 13). For the midslope leeward site, the slope population = 4.2 cm/year based on 50 marked plants, apparent sigmoidal relationship between these all over 75 cm in height: growth data not recorded for other two variables (Figure 13, middle) was not statis- populations; solid bar = reproductives: striped bar = pre- tically significant; a polynomial regression was reproductives). not significiantly better then a linear regression. relationship between these two variables was not Interspecfic Comparisons: Annual mortality rate statistically significant. for E. floccosa juveniles at 3600 m was 4970. The In E. lutescens at 4200 m, only two of the marked proportion of total annual mortality that oc- juveniles died (Table 6), making a detailed anal- curred during the dry season was higher for E. ysis of mortality impossible. floccosa (98%) than for any other population stud- Comparisons between Newly Recruited and Previously ied (Table 6). Mortality rates for each class are Established Juveniles: The figures for juvenile mor- given in Figure 11A. The relationship between tality discussed so far have been based on those percent mortality in each size class and the nat- sets of juveniles present in the quadrats during ural log of the median value for each size class the initial survey in mid wet season, 1972. These was linear (Figure 13). The apparent sigmoidal quadrats were resurveyed in early December 1972 NUMBER 48 17

TABLE4.-Distance to nearest adult neighbor in relation to juvenile growth, mortality, and initial height (juvenile and adult always of same species)

Initial height us. Height Height nearest neighbor Species growth us. growth us. Mean nearest and sits nearest initial All Survivors neighbor distance neigh bar height juveniles only rxY TXY TXY rxY Survivors Mortalities E. schultrii 3000 m -0.276** 0.340** -0.114 -0.077 29.3 42.1*** 3600 rn Slope base 0.023 0.136 -0.024 -0.323** 42.3 44.1*** Midslope windward -0.118 -0.45 1 *** -0.085 -0.133 49.7 49.9 Ridge 0.100 0.024 0.509*** 0.415*** 67.6 34.9*** Midslope leeward 0.034 0.225* 0.0 12 -0.026 32.7 28.5* 4200 m -0.046 0.291 0.042 -0.268 43.4 17.8*** E. froccosa 3600 m -0.394* 0.000 0.152 0.392* 29.5 33.8 E. lutescens 4200 m -0.182 -0.709* * * 0.359 0.427t - -

TABLE5.-Effects of vegetation on juveniles (vegetation cover measured in immediate vicinity of each juvenile)

Initial height us. Height vegetation cover (%) Species growth us. and sites vegetal ion Vegetation cover (%) All Survivors cover juveniles only rxY Survivors Mortalities r,, r*Y E. schultzii 3000 m -0.01 1 83.9 69.3** 0.299* * * -0.077 3600 m Slope base -0.069 59.9 47.2* 0.237* * 0.357** Midslope windward -0.2481- 73.0 48.0*** 0.336*** 0.329* Ridge -0.070 62.6 42.3** 0.303** 0.320** Midslope leeward 0.086 53.8 26.1*** 0.367** * 0.326*** 4200 rn 0.21 1 42.2 38.5** 0.346t 0.504* E. froccosa 3600 m 0.222 84.5 6 1 .O*** 0.102 0.220 E. lu tescens 4200 rn 0.100 0.045 -0.065 * P

(wet season-dry season transition), and seedlings 4200 m. In this case, however, only two newly that had appeared since the initial survey were recruited seedlings were present, making a mean- marked and measured. Mortality during the fol- ingful analysis impossible. lowing dry season was, in general, much greater Nearest Neighbor Effects: For E. schultzii at 3000 than mortality for juveniles already present at the m, mean distance to nearest conspecific adult time of the initial survey (Table 7). The only neighbor was significantly lower forjuveniles that exception to this trend occurred in E. schultzii at survived one year than for those that died. This 18 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE6.--Seedling mortality for seedlings present in initial survey (wet season, 1972) (survey dates summarized in Appendix Table E)

Percent of all mortality occurring New Total Species seedlings seedlings and sites Initial Percent Wet Dry Wet present present number mortality season season season at final at final seedlings in I year 1972 1972-3 1973 suruey surztey E. schultrii 3000 m 178 60.7 8.3 87.0 4.7 73 143 3600 m Slope base 314 79.3 20.5 79.1 0.4 19 84 Midslope windward 134 53.7 29.2 63.9 6.9 17 79 Ridge 118 33.0 43.6 48.7 7.7 13 92 Midslope leeward 197 57.7 17.9 78.8 3.3 29 164 4200 m 29 13.8 25.0 75.0 0 2 27 E. jloccosa 3600 m* 82 48.8 0 97.5 2.5 2 44 E. lutescens 4200 m 21 9.5 50.0 50.0 0 1 20 * Number of seedlings per 5 m2, rather than 10 m2, same relationship was found for E. schultzii at ing in the apical buds. However, these plants 3600 m on the slope base plot and for E. floccosa survived. No herbivory on juveniles was recorded at 3600 m. at other sites. Elimination of juveniles by grazers On the ridge and leeward slope plots at 3600 apparently is not a major factor. At all sites, m, surviving juveniles of E. schultzii had a greater marked juveniles that died could always be lo- mean nearest neighbor distance than did mortal- cated and showed no signs of insect damage. ities. Dry season soil moisture levels for those two Discussion: Data on juvenile mortality in Espe- plots were the lowest recorded at this site. Com- letia suggest two general patterns: (1) the proba- petition between adults and juveniles for water bility of mortality decreases as plant size in- could have outweighed any moderating effects of creases, and (2) the probability of mortality is the adults on microenvironment on these plots. greatest in the dry season. Potentially, these two Effects of Vegetation: At all sites, vegetation cover patterns could result in several kinds of selection around juveniles that survived one year was on Espeletia populations: (1) selection on adult greater than cover around those that died. With stages for production of larger numbers of seed- the exception of the E. floccosa and E. lutescens lings, increasing the probability that some will populations, initial plant height was positively survive despite high mortality rates; (2) selection correlated with vegetation cover (Table 5). Mor- on juvenile stages for rapid growth rates, reducing tality rate decreases as juvenile height increases the duration of the most vulnerable stage in the (Table 5). Mortality rates were therefore lower in life cycle; and (3) selection on juvenile stages for sites with higher vegetation cover, in part because physiological and/or morphological adaptations the size of juveniles was greater. that confer protection against environmental ex- Herbivory: Herbivory on juveniles was rare. In- tremes of the dry season. Further studies will be sect damage to leaves was noted in two of the required to determine the relative importance of marked E. schultzii juveniles at 3000 m (1% of all such selective pressures in various Espeletia popu- juveniles at this site) and in three marked E. lations. lutescensjuveniles at 4200 m (14% of all juveniles). The positive correlation of juvenile size with The damage was caused by beetle larvae burrow- vegetation cover within 1 cm of the rosette margin NUMBER 48 19

TABL~7.-Dry season mortality (December 1972 to Aprll 197.3) for seedlings presenc at inltial survey (wet season, 1972). and for ieedlmqs produced after initial survey, bur before December 1972 (survey dates summarized in Appendix Table EI .Vumber o/ .Vumber uJ inilia1 new Species seedlings reedlings and silrs presenl ,Morlaliy presenl mortal it^ Dec I972 (''4) nrc 1972 ('0 E. schullril 3000 m 163 .57,7 5 4 96 3 3600 m Slope base 2 50 78.8 I16 94.0 LVindward slope 9 i 68 7 84 89.3 ridge 67 28.4 45 82.2 Leeward slope 262 55.3 137 97.1 4200 m 28 10 7 1 0 E. floccosa 3600 m 82 47 6 23 87 0 E. lulescens 4200 m 20 5 0 0 0

is probably an inevitable consequence of increase in rosette diameter. Nonvegetated patches at most sites typically cover only a few square cen- timeters. A very small juvenile within such a patch could be free of vegetation in its immediate vicinity. As the rosette expands, it will outgrow the bare site. As a result, large juveniles will seldom be free vegetation.

Studies of Adults

SIZECLASS DISTRIBUTION.-~ize class distributions are based on height data for adults within each study plot. Plant height was measured to the base of the apical bud in all species except E. floccosa. In E. floccosa, height was measured to the highest leaf tip because the apical bud was poorly -2 -I 0 I 23 defined. Annual height growth was recorded for 120 adults in most study plots. Size class distri- IN HEIGHT (CM) butions can be transposed into very approximate FIGURE13.-Relationships between seedling height class and adult age class distributions by using these annual percent mortality in each height class during one year. Top: height growth data as conversion factors. How- E. floccosa at 3600 m (y = 72.2 - 30.5 lnX, r = -0.939). ever, such approximations must be interpreted Middle: A, slope base E. schuitzii plot at 3600 m (y = 65.3 - with care because rate of height growth for adults 20.9 lnX, r = -0.977); B, midslope leeward E. schultzii plot is probably correlated with initial plant height: at 3600 m (y = 45.5 - 37.4 lnX, r = -0.903); C, ridge plot rate of leaf expansion is positively correlated with for E. schuitziz at 3600 m (y = 30.1 - 34.0 lnX, r = -0.976) Bottom: A, E. schultzii at 3000 m (y = 64.1 - 20.1 plant height in many populations, and plant lnX, r = -0.941); B, E. schultzii at 3600 m, midslope height growth and leaf expansion rates are closely windward plot (y = 50.1 - 18.6 lnX, r = -0.985). related in caulescent rosette plants. A more de- 20 SMITHSONIAN CONTRIBUTIONS TO BOTANY

tailed analysis of height-age relationships will be presented in a later paper. A AHG = 2.0 Elezational Comparisons within E. schultzii: The - M H = 23.8 4200 m population had fewer plants in small size 50 classes than did populations at 3000 m and 3600 3 m. However, considering similar topographic sites, the tallest and hence oldest plants occurred at highest elevations. Mean adult height, calculated for 120 plants at each elevation, was 23.8 cm at 3000 m, 26.0 cm at 3600 m, and 29.6 cm at AHG= 1.2 4200 m. These means are significantly different B MH = 26.0 from each other (P

I AHG.I.1 1 B AHG.1.2 8 */e MH = 20.0 MH= 26.0 A MH = 13.1 cm t LEAVES / WEEK 1.6 E

AHG.1.2 - D AHG= 1.1 \ MH= 31.6 MH.21 .O I75 16 v) -

2o 33 -I I - B 0 MH ~31.6cm 50 LEAVES / WEEK = 1.5

75125 t

10P3040x)6070 102030405060 0 HEIGHT CLASSES (CM) 10 20 30 40 50 60 70 80 90

FIG~JRE1.5-Topographic variation in population structure HEIGHT CLASSES (cm) and dynamics for E. schultrii adults at 3600 m: A, ridge; B, FIGURE16.-Population structure and dynamics for E. schul- midslope windward; C, slope base; D, midslope leeward trzz adults at 3600 m: on A, xeric slope: B, talus slope (adult (adult = plant with rosette diameter of 25 cm or greater; = plant with rosette diamter of 25 cm or greater; rate of leaf solid bar = reproductives; striped bar = prereproductives; production measured during the wet season; solid bar = number on bar = percent mortality in one year). reproductives; striped bar = prereproductives; number on bar = percent mortality in one year; MH = mean height).

oldest leaves in the apical bud were marked on the tip with indelible ink (Nursery Marker, Horta amounts of leaf tissue, since leaf size varied Craft Corporation), and the number of leaves greatly from plant to plant. Therefore, for each expanding from the bud during the next 4 to 6 of the 50 plants at each site, the outline of the weeks was recorded. This procedure was carried outermost mature leaf was traced in situ, and the out in the wet and dry seasons and in a wet area of the outlines determined with a planimeter. season-dry season transition period, providing a In converting from number of leaves expanded measure of the seasonality of growth. In E.floccosa per unit time to leaf area produced per unit time, there was no clear differentiation between bud the number of leaves was multiplied by this area. leaves and rosette leaves. Thus, leaf expansion Leaf area produced per unit time was con- rates could not be determined accurately for this verted to dry weight of leaf tissue produced per species. unit time. To do this, mature leaves from 50 Two plants could produce the same number of additional plants were collected at each site. Each leaves per unit time yet produce very different leaf was traced and the area determined with a 22 SMITHSONIAN CONTRIBUTIONS TO BOTANY

AHG = 4.5 cm MH = 25.8 cm

75t- 0 2

J 3 HEIGHT CLASSES (cm) a 50 AHG= 1.5 cm MH.60.9 cm

I.Imm-- 15 35 55 75 95 115 135 155 175 HEIGHT CLASSES (cm)

FIGURE17.-Population structure and dynamics for adults: A. E. floccosa at 3600 m; B, E. lutescens at 4200 m (E.floccosa adult = plant with rosette diameter of 15 cm or greater; E. lutescens adult =.plant with rosette diameter of 40 cm or greater: .4HG = annual height growth (cm); MH = mean height; solid bar = reproductives; striped bar = prereproductives: number on bar = percent mortality in one year). FIGURE18.-Effect of flooding on E. schultzii in a swale at 3600 m; A, June 1972; B, March 1973. planimeter. Oven-dry weight was determined for each leaf and dry weight per unit surface was summed and averaged, and the resulting mean calculated. Dry weight per unit surface area was multiplied by 100. Seasonality (S) is calculated regressed against total area per leaf. If there was by a significant correlation at a given site, the re- n n. 2 ”’ x 100 sulting regression line was used to determine dry i Wi weight per surface area for each intensively stud- s= n ied plant. If there was no correlation, the mean figure for dry weight per unit leaf area was used. where S is seasonality, Di is rate of leaf production The figure for grams dry weight per cm2 of leaf for the ith individual in the dry season, W., is’ rate surface was multiplied by the figure for leaf area of leaf expansion for the ith individual in the wet produced per week by each plant. season, and n is the number of individuals. Growth was highly seasonal at most sites. A Altitudinal Trends within E. schultzii: Seasonality quantitative index was developed to express this decreased with increasing elevation for midslope seasonality. For each plant, the rate of leaf expan- windward sites (Table 8) because dry season sion during the dry season was divided by the growth rates increased with increasing elevation, rate of expansion during the wet season. The and for the same sites in the wet season, growth results for all plants at a given site were then rates decreased with increasing elevation. NUMBER 48 23

TABLE8.-Growth rates and seasonality (dry season growth rate as percentage of wet season growth rate) (dates for sampling periods given in Appendix Tables C-E; see page 22 for definition of “seasonality”)

Wet to dry season Species transit iov Dry season Wet season ~ Leaves/ Grams/ and sztes Lvs/week Gmlweek Lus/week Gmlweek Lvs/week Gm/week year year Seasonality E. schultriz 3000 rn 3.5k0.18 5.4f0.48 1.OfO.09 1.6k0.21 3.2f0.18 5.4k0.43 125 210 28.2f2.6 3600 rn Bog edge - - 1.1fO.09 1.9f0.24 2.6f0.17 4.6f0.54 - 44.8k3.6 Slope base 2.6f0.2 1 5.2f0.83 1.4k0.12 2.6k0.43 3.0f0.29 6.1f 1.05 119 236 50.8k5.5 Windward slope 2.2f0.12 4.0f0.37 1.1fO.09 2.1f0.26 2.4f0.18 4.4f0.49 96 177 55.0f6.1 Ridge 1.9f0.12 3.5f0.42 1.4f0.11 2.5f0.32 2.0f0.15 3.6f0.48 88 163 74.235.3 Leeward slope 2.0f0.12 3.6k0.46 0.8f0.09 1.4f0.20 2.0f0.16 3.6f0.54 81 146 43.9k4.4 4200 rn 1.6f0.11 3.9f0.40 1.3f0.12 3.0k0.36 1.3f0.12 3.2k0.38 72 172 92.4f 1 1.1 E. lutescenh 1.2fO.11 4.4f0.67 1.OfO. 14 3.4f0.81 1.6f0.19 5.7f0.84 64 231 68.4f 15.0 E. humbertii* 0.1fO.0 1 0.3f0.05 0.1k0.02 0.3f0.05 0.4f0.04 0.9k0.12 10 25 34.3f7.1 * Leaf expansion recorded for single leaf rosettes, rather than for whole trees.

Decreasing vegetation cover with increasing Greater seasonality of growth for the bog edge altitude might result in decreasing interspecific plants could be related to rapid leaf senescence competition for water in the dry season, causing and resulting decrease in total leaf surface area reduced seasonality. Decreased intraspecific com- during the dry season. Reduction in dry season petition could also be a factor. At 3000 m, there leaf number on the bog edge site was far greater was a significant positive correlation between than on the midslope site (Table 9). This reduc- nearest neighbor distance and growth rate in the tion was due to wilting of the outermost rosette dry season (rxy= 0.491),but a weaker correlation leaves. Rates of dry season leaf expansion were during the wet season (rxy = 0.272) (Table lo), the same for the bog edge and midslope plants. suggesting that the plants at this site were com- Windward and leeward halves of each rosette peting for water. No such correlations were found were distinguished when leaves were counted in at higher elevations. Frequency of juvenile plants the early dry season. For the bog edge there was of E. schultzii decreases with increasing elevation. no significant difference between number of Competitive effects of juveniles on adults would leaves in the two rosette halves. For midslope therefore decrease, further improving dry season plants, however, the mean number of leaves in growth at 4200 m. Leaf pubescence increases with the leeward rosette halves was 30.6 versus 24.9 for increasing elevation in E. schultzii (Z. Baruch, the windward halves. These means were signifi- pers. comm., Nov 1973). This might result in cantly different (PCO.005).The midslope site was greater buffering against drought stress, reducing subject to far stronger winds than was the bog seasonality of growth. edge site. In the wet season, there was no signifi- Topographic Trends in E. schultzii at 3600 m: cant difference between mean leaf number in the Seasonality decreased from bog edge to ridge and leeward and windward rosette halves for the from leeward slope to windward. This trend oc- midslope plants. Rosette halves were not sampled curred despite the fact that the ridge and wind- separately when the bog edge plants were resur- ward slope sites both had lower soil moisture veyed. levels than did the bog edge and both were more Greatest total wilting occurred on the bog edge exposed to the prevailing wind than was the despite greater wind-related wilting on the mid- leeward slope. slope site. It is unlikely that the wilting was 24 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE9.-Number of leaves per rosette and leaf expansion rates for E. schulttii at 3600 m (50 adult plants measured at each site)

I LPaoes/rosette, Leaues/rosette, Sites and dry season dry season x I00 x 100 seasons Leaoesl Leaveslrosette, Leaves/ Leaves/rosette, I rosette wet season week wet season Midslope windward Wet season 68k16.1 2.4kO. 18 81.6% 55.0% Dry season 55+ 4.3 1.1kO.09 Bog edge Wet season 60+ 4.4 2.620.17 57.0% 44.8% Drv season 34+ 2.5 1. I kO.09 related to soil moisture. On 2 January 1973, soil There was a significant negative correlation moisture on the bog edge was 46%, versus 3 1% on between seasonality and distance to nearest the midslope windward site. Mean minimum neighbor on the midslope windward side. Thus, temperatures in the dry season were much lower growth becomes progressively more seasonal with in the bog (and hence on the bog edge) than on increasing distance between an adult plant and the midslope site. Greater leaf wilting on the bog its nearest adult neighbor. There is probably a edge might have been related to an interaction of sheltering effect on one plant by another on the (1) freezing stress and (2) drought stress due to gently sloping windward site, reducing wind-in- rapid heating of leaves early in the morning duced drought stress. This would be most impor- when, because of cold stem and roots, water tant for short plants located on the leeward sides transport to leaves is inefficient. Presumably, this of taller plants. On steeper windward sites, such second factor would be more important on the as the ridge plot, an adult located on the wind- bog edge than on the midslope site because of ward (downslope) side of a second plant might lower stem and root temperatures imposed by dry provide little or no shelter, even if taller than the season cold air drainage. second plant. The difference in seasonality between the lee- Further studies will be required to determine ward and the windward slopes might have been the causes of these patterns in seasonality. How- the result of (1) greater adult density on the ever, the data do suggest that there is strong leeward slope, leading to greater dry season com- intraspecific control over seasonality within local petition for water (199 adults per 100 m2 on the populations and that the nature of this control leeward slope versus 122 on the midslope windward site); (2) higher dry season mean maximum changes qualitatively with change of topography. temperature on the leeward slope, possibly result- Interspecif2c Comparisons: Growth in E. lutescens ing in greater dry season evapotranspiration; (3) was more seasonal than growth in the adjacent slightly lower dry season soil moisture levels on E. schultzii population (Table 8).Espeletia schultzii the leeward slope. at 4200 m was restricted to shallow swales that There was a significant positive correlation received runoff from the surrounding paramo between seasonality and distance to nearest adult during the wet season. The E. schulttii population neighbor on the midslope leeward site (Table 10). studied was on ground 1 to 3 dm lower than the With increasing distance between an adult plant adjacent E. lutescens population. Soil moisture, and its nearest adult neighbor, growth became measured on 26 Mar 1973, at 0-10 cm was 20% progressively less seasonal. This suggests that for the E. schulttii plot versus 16% for the E. some form of intraspecific interference may be lutescens plot. Percentage moisture content under controlling seasonality at this site. 15 atmospheres pressure (laboratory determina- NUMBER 48 25

TABLE10.-Correlations of nearest neighbor distance with adult leaf production (g/week) and with seasonality of leaf production

Glweek versus nearest neighbor Species Seasonalip cersus and sites Dry season Wet season nearest neighbor TXY rxr TXY E. schultrii 3000 m 0.49 1 PCO.00 1 0.272 PCO.1 0.214 PCO.05 3600 m Slope base 0.268 PCO.l 0.145 -0.036 Windward slope -0.222 -0.100 -0.278 PCO.05 Ridge -0.219 -0.259 -0.108 Leeward slope -0.117 -0.168 0.384 PCO.01 4200 m -0.04 1 0.163 -0.174 E. lutescens 4200 m -0.209 -0.126 0.31 1 E. humbertii 3500 m 0.171 0.182 0.057 tion) was 14% for the E. schulttii plot and 11% for rock outcrop at Laguna Negra showed signs of the E. lutescens plot. Vegetation cover was slightly wilting toward the end of the dry season. Cross- lower on the E. schultzii plot (2928.6% versus sections of E. humbertii trunks showed distinct 38+8.1%), and percentage cover by bare rock was growth rings, providing further evidence of sea- higher (5528.7% versus 3829.1%). sonal growth. Height growth in E. floccosa at 3600 m was For E. humbertii no significant correlations were faster than in any other species studied. This found between growth rate and distance to near- species generally grows on rocky, windward est neighbor or between seasonality and distance slopes-sites where both vegetation cover and to nearest neighbor (Table 10). However, there density of E. schulttii are generally lowest. Fast were significant positive correlations between growth, occupation of apparently unfavorable nearest neighbor distance and plant size (Table sites, short generation time, and semelparous re- 1 I), suggesting that interference of some sort has occurred in the past. There was a weak positive production are characters often attributed to “r- correlation between basal stem diameter and selected” species (Gadgil and Solbrig, 1972). nearest neighbor distance for the 50 trees used for The growth rates for E. humbertii (Table 8) were growth studies. These plants were scattered much lower than for other species because rate of throughout the talus population, from the bottom leaf expansion was recorded for a single leaf to the top of the slope (a distance of about 30 m). rosette, rather than for the entire crown. With the For the plants occurring in plot 1, near the base exception of unbranched saplings, crowns were of the slope, there was no correlation. For the made up of many leaf rosettes located on branch plants occurring in plot 2, near the top of the apices. Number of rosettes per tree ranged from slope, there was a strong positive correlation. 1 to 46, with a mean of 10k2.4. There was no In both the closed forest plot and the treefall significant correlation between the total number site, there were positive correlations between of rosettes making up a given tree crown and the plant size and nearest neighbor distance. The growth rate measured for one of these rosettes. seedlings in the treefall produced dense cover Overall growth rate for a given tree will therefore several dm above ground level. Both sites there- be proportional to the number of rosettes making fore had essentially closed canopies. Competition up the crown. for light as well as for water and nutrients could Growth was highly seasonal in E. humbertii (Ta- have enforced the observed spacing patterns at ble 8). The leaves on several trees growing on a these sites. 26 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE1 1.-Correlation of distance to nearest conspecific TABLE12.-Time required for complete replacement of adult with adult plant height rosette leaves (turnover time) (leaf expansion rates not measured in E. flOccosa) Mean Height us. Species distance nearest Mean Leaves/ and sites to nearest neighbor Species Number number of rosette neighbor distance and sites leaves/ leaves/ Leaves/ (cm ) (TXY) year rosette’ year E. schultrii E. schultrii 3000 m 7.2k 2.5 0.104 3000 m 125 70.5k 4.80 0.56 3600 m 3600 m Slope base 18.32 3.5 0.055 Slope base 119 74.62 6.60 0.63 Windward slope 25.92 1.8 0.146 Windward slope 96 68.0k16.10 0.71 Ridge 15.4k 3.1 0.280 P

1973 (Table 13). Longer-term data suggest that inated, apparently through larval herbivory. The elevational trends are extremely variable from apical buds of many of these plants were in- year to year (Smith, ms. in prep.). Insect larvae spected and all had insect larvae burrowing in (unidentified) burrowed in the apical bud. Ma- them. Beyond these heavily attacked plants, E. ture click beetles (Elateridae) were observed feed- lutescens plants with moderate levels of herbivory ing on bud leaves, on some plants. They con- were found. This pattern suggests that a long- sumed all leaf tissue except the midvein. No term buildup of insects may be resulting in a very insects were observed feeding on mature leaves. local elimination of E. lutescens over an area of Insect damage could not be linked directly to several hundred meters. Reduced seed produc- mortality, but it is possible that the larvae may tion, combined with naturally low probability of occasionally burrow through the apical meristem, seedling establishment at this elevation, will make causing death. Reduced photosynthetic area due reestablishment of the population a slow process. to predation could reduce competitive ability and Leafhoppers (Homoptera) attacked the mature fruit production. and immature leaves of E. atropurpurea, E. humber- Leaf herbivory was more common in the E. tii, and E. neriifolia. Every plant inspected had at lutescens population than in the adjacent E. schul- least a few damaged leaves. These three species ttiz population at 4200 m. No mortality was lack pubescence on their upper leaf surfaces. Lev- recorded for the research plants of E. lutescens that in (1973) has suggested that, in many plants, leaf had been subject to predation. However, there pubescence may provide protection against leaf was an area that appeared to have been the site herbivory. However, other factors such as toxin of extensive insect-related mortality approxi- production and nutrient levels could also be in- mately 200 m upslope from the E. lutescens study volved. plot. The area was approximately one hectare in Semelparity: The only clear-cut mortality pat- size. Near the center of the area there were many tern noted for E.floccosa adults was that associated fallen dead stems of E. lutescens and no live adults. with flowering. If plants live to reproduce, death Further out from the center there were E. lutescens occurs immediately after fruiting. Flowering oc- plants that appeared to have died more recently; curs in the early to mid wet season, so adult they were still standing. Toward the edge of the mortality is also concentrated in this period. Sev- area were many E. lutescens plants in which a eral hundred dead plants with flower stalks were large portion of the rosette leaves had been elim- observed at Mucubaji. None of these showed

TABLE13.-Number of adult plants in study plots that had insect-damaged leaves

Number of plants damaged in 1973 Species that were also and sites Wet season 1972 Wet season 1973 damaged in 1972 Total Plants Percent Plants Percent Plants Percent Plants Percent E. schultzii 3000 m 103 86 105 90 96 83 112 93 3600 m Slope base 2 2 12 10 1 1 13 11 Windward 11 9 16 14 2 2 25 21 Ridge 1 1 8 7 0 0 9 8 Leeward 16 13 30 25 6 5 40 33 4200 m 7 6 0 0 0 0 7 6 E. lutescens 30 25 29 27 17 16 42 35 E. floccosa 9 8 13 11 5 4 17 12 NUMBER 48 29 evidence of resprouting. No live adults with (achenes) was recorded for the first 100 reproduc- flower stalks were observed. tive adults along each transect. The 14 transects Effects of Man: Harvesting of Espeletia plants for were run in October 1972 and were resurveyed in medicinal and other uses may have a significant November 1972. impact on some species. Espeletia weddellii, an A comparison of flowering on the windward acaulescent herbaceous species, is collected for and leeward sides of E. schultzii plants was made use as a cure for respiratory diseases (Faustino at Mucubaji (3600 m). The research site was on Diaz, pers. comm., June 1973). This species is the crest of a terminal moraine immediately west never abundant, so that such collecting could of Laguna Mucubaji. This site received the full cause local extinction. Its present scarcity might force of the prevailing NE winds. The number of be the result. in part, from past collecting. Roots flower stalks, and flower stalk length, was re- of E. schultzzi are reportedly used in the manu- corded for the NE-facing (windward) and SW- facture of local butter and E. schultziz leaves are facing (leeward) halv s of each rosette. Fifty used to package the butter. plants were studied. All plants had completed The branches of E. humbertii and E. neriifolia are flowering and had set fruit. collected and the resin extracted for use as incense Flower and fruiting heads were collected from in churches. Cutting of subalpine forests is rapidly 50 E. schultzii plants at 3000, 3600, and 4200 m. reducing population size in these arborescent spe- The fruiting heads w ere collected just before fruit cies. dispersal began and were taken from the same Intense agriculture in the main valley of the plants from which flower heads were obtained. Rio Chama, between Mucuchies and Mucubaji, Fruiting heads generally remained tightly closed has resulted in almost complete elimination of until just before the fruit were dispersed. Number Espeletia (both arborescent and rosette species) of ray (male) and disc (female) flowers were below 3400 m, although Espeletia does occur in recorded for the flower heads. Number of achenes less heavily used side valleys. and number of insect larvae were recorded for REPRODUCTIVEPHExoLocY.-For each species, each fruiting head. the number of individuals in each plot that flow- Mature fruit were collected from 50 plants at ered during the field research period was re- the same three sites. Fruit size and weight per corded. A more detailed study of reproductive whole fruit were recorded. Fruit were cut open to biology was carried out for E. schultziz at 3600 m. determine the proportion of apparently normal Flower and fruit production were recorded fruit that were hollow. monthly for 100 E. schultzii plants on the floor of A detailed study of pollen flow and seed dis- a sheltered morainal valley and for 100 plants on persal was made, and will be reported elsewhere a windy ridge 140 m above the valley floor. The (Teeri and Smith, unpublished data). plants studied were the first reproductive adults Eleuational Comparisons of Flowering Phenology in (adults in flower or which had flowered in the E. schultzii: At 3000 m and 3600 m, flowering past) encountered along a line transect at each was concentrated in the wet season and the wet site. In addition, flowering of E. schultzii was season-dry season transition period (Table 14). recorded on a series of seven low ridges at 3600 Fruit production and dispersal at these sites began m. The ridges had NE-facing (windward) and during the wet season and continued throughout SW-facing (leeward) slopes, with relief of 3 to 5 the dry season and into the next wet season. m. For each ridge, one line transect was run across However, most fruit had already been dispersed the SW-facing slope and a second along the ad- by the beginning of the next wet season. Germi- jacent NE-facing slope. The transects were lo- nation at all sites generally began with the onset cated 2 m below the ridge crests. Presence or of the wet season rains. absence of flower buds, flowers, and fruit At 4200 m, E. schultzii produced flowers and 30 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE14.-Number of plants that flowered within each 100 m' study plot (figures in parentheses = number of flowering plants as percentage of all adults in plots)

Plants Plants Plants Plants with Species in 1972 flowering flowering jlowers or buds and sites with 1971 in 1972 in 1972-73 by mid-wet season seedheads wet season dry season I 973b E. schultzii 3000 m 10 (9.7) 29 (28.2) 0 9 (9.1) 3600 m Slope base 5 (5.2) 4 (4.2) 0 11 (11.7) Midslope windward 12 (9.8) 0 0 5 (4.1) Ridge 13 (11.2)' 0 0 5 (4.4) Midslope leeward 26 (21.7) 0 0 7 (3.5)d 4200 m 3 (3.8) 19 (23.8) 10 (12.5) 29 (36.3) E. lutescens 4200 m 0 7 (8.1) 0 0 E. floccosa 3600 m 0 0 0 0 E. humbertii 3500 ma Not recorded 21 (42.0) 0 10 (20.0)

fruit throughout the year. Here E. schufttii popu- which all reproductive adults were in flower dur- lations were generally restricted to rocky drainage ing a given wet season. Some plants flowered areas that received runoff from the surrounding during both wet seasons (1972 and 1973), but areas. This aseasonality in flowering was associ- many other plants flowered in only one. Many ated with aseasonality of growth as well (Table plants that had flowered during past years did 8). Possible explanations for this lack of season- not flower during the period of this study. ality were discussed in an earlier section. Topographic Comparison of Flowering Phenology in At 4200 m, flower heads produced during the E. schultzii at 3600 m: Flowering occurred first on dry season frequently were killed by frost during leeward slopes and valley floors and last on ex- clear cold nights. Generally, only expanded flower posed ridges and windward slopes. The propor- heads were killed; flower buds were seldom dam- tion of all reproductive adults that flowered at aged. At 3600 m (Mucubaji) frost damage to any given time also decreased from leeward to flower heads was observed occasionally in the few windward slopes and from valley floors to ridge plants producing flowers in late December 1972, tops (Figure 19). Plants that did flower on ridge at the end of the flowering season. Such damage tops produced fewer flower heads than plants on was observed again for the few plants coming the valley floor (Table 15). into flower in April and May 1973, at the begin- Table 16 summarizes data on flowering on a ning of the 1973 flowering season. The damage series of NE-facing (windward) and SW-facing occurred during several periods of unusually low (leeward) slopes. On 1 October 1972, 31 plants rainfall, when clear cold nights were more com- on the SW-facing slopes were in fruit (24.2% of mon. It was most pronounced on the floor of a all plants that flowered during the year), whereas large morainal valley (see Smith, 1980). only one plant (4.9% of all plants which flowered No population of E. schultzii was found in during the year) had come into fruit on the NE- NUMBER 48 31

MM 200

60...... * ...... *** .,......

40. %

1972 FIGURE19.-Top: Monthly precipitation at Mucubaji (3550 m). Bottom: Flower and fruit production in E. schultzii at 3600 m (A = percent of plants in flower on valley floor; B = percent of plants in fruit on valley floor; C = percent of plants in flower, windy ridge, 140 m above valley floor).

TABLE15.-Mean number of flower heads per flowering facing slope. Of 700 plants monitored on the NE- plant for E. schultzii, recorded at five sites within a morainal facing slope, only 17 flowered in 1972 versus 128 valley at 3600 m (relief was 140 m) on the SW-facing slopes. Environmental differ- Number ences between windward (NE-facing) and lee- Site of jlower head3 ward (NW-facing) slopes are discussed elsewhere East moraine (Figure 6, 7). Ridge top 43.6f10.48 Within-Plant Eflects of Wind in E. schultzii at Midslope leeward 88.2f19.74 3600 m: The mean number of windward flower Valley floor 169.9k33.03 stalks was 1.6fO.4; the mean number of leeward West moraine Midslope windward 45.9f 8.95 flower stalks was 3.3f0.5. These means are sig- Ridee toD 39.8k 14.60 nificantly different (PC0.005). The windward stalks were shorter than the leeward stalks (70.9k1.3 cm versus 82.3k1.4, cm). Shorter stalks TABLE16.-Flowering on NE-facing (windward) and SW- on the windward sides of plants might have re- facing (leeward) slopes at 3600 m (figures = number of flowering or fruiting plants per 100 adults sampled at each sulted from greater mechanical stimulation by of seven sites; each figure = mean of seven sites) wind, resulting in inhibition of elongation (Jaffe, 1980). Flower bud initiation, however, takes place Sites and inside the apical bud. The windward side of each stages I 1 Oct 1972 18 Nov 1972 plant was presumably cooler than the leeward, or NE-facing slopes suffered more drought stress, perhaps resulting in Flower buds only l.Of0.69 0 In flower 1.6k0.48 0.4f0.79 differential rates of flower bud formation. Seed heads only 0.1f0.14 3.6f 1.43 Interspecijic Comparisons of Flowering Phenology: SW-facing slopes The E. lutescens population at 4200 m flowered in Flower buds only 3.3k0.81 0 the late wet season and wet season-dry season In flower 10.7f 1.91 1.7f0.68 transition period of 1972, but did not flower in Seed heads only 4.4f1.19 17.3f2.12 1973. No recent E. lutescens flower stalks were found in the early wet season of 1972, suggesting 32 SMITHSONIAN CONTRIBUTIONS TO BOTANY that flowering probably did not occur during vary with elevation. Larger fruit could produce 1971. Flowering occurred again during 1975; no more vigorous, rapidly growing, seedlings. At flowering occurred in 1976 or 1977. These obser- 4200 m this would increase the probability of vations suggest that E. lutescens flowering occurs seedling establishment during periods of low soil less than once a year, but that it may occur frost activity. It would also facilitate seedling synchron!>usly within the population. growth in a rocky substrate or in dense mats of No flowering occurred in the E. Joccosa plot vegetation-habitats conferring protection from during 1972- 1973, although widely scattered in- frost heaving. dividuals did flower in several populations at Size-spec$c Reproduction: Number of flower 3600 m during the wet season. Extensive flower- stalks was recorded for 121 reproductive E. schul- ing occurred in all populations observed in 1975. tzii plants of known size on a valley floor site at Only very scattered flowering occurred in 1976 3600 m (Mucubaji). Number of stalks (y) was and 1977. All plants that flowered died after fruit linearly correlated with plant height (x) (y = 3.94 maturation. + 0.13 x, r = 0.34, P

TABLE17.-Flower and seed production

Percent Number Number fruiting Species disc ray heads Number Dry weight and sites (male) Cfemale) Number Percent with flower Dry weight (s) Per flowers flowers fruits hollow insect heads per per fruit flower per head per head per head' fmit2 larvae plant3 (mg) stalk E. schultzii 3000 m 101f7.7 82f2.8 75k4.6 32 36 104k3 1.7 0.3f0.02 23.2f1.19 3600 102k6.7 83k4.6 71k4.3 32 58 (see Table 15) 0.4+0.034 16.9f0.67 4200 m 92f6.3 87k4.4 86k4.2 67 12 74k 4.3 0.8-+0.05 19.4f0.93 E. floccosa - - 32k3.5 - 100 656k105.3 1.2f0.08 28.4k5.00 E. humbertii - - 16k1.4 - 48 l.5-+0.10 35.6k4.91 Number of fruit that appeared undamaged. Percent based on number of seeds that appeared undamaged. Number of heads per plant produced during the entire year. The difference between mean seed weights for E. schultzii at 3000 m and 3600 m is weakly significant (PCO. 1); differenc between 3600 m and 4200 m means is highly significant (P

facing slopes. However, wind speed on the ESE- of leaves might have caused some early morning facing slope was only about 1.4 times that on the drought stress in the NE-facing slope plants. WNW-facing slope-a smaller difference than However, this effect would probably not be a between the NE- and SW-facing slopes. One major factor in the wet season. Dew formation on possible explanation for this apparent discrep- E. schultzii leaves is greater in the wet season; in ancy is that the ESE-facing slope faces more the mornings, it seldom evaporates completely directly into the rising sun than does the NE- before the sun is obscured by fog or clouds, facing slope. As suggested earlier, rapid heating making drought stress unlikely. Because growth of leaves when soil, roots, and stem are still near differences between the slopes persisted in the wet freezing could result in early morning drought season, it is probable that other factors, such as stress (cf. Mayland, 1972). All the slopes studied wind-induced leaf water stress and wind-cooling, had similar slope angles and all were located on may be acting. Tissue temperatures were lower the same system of terminal moraines. Thus, on the NE-facing slope (Figure 7) perhaps result- differences in slope angle and substrate probably ing in lower metabolic rates. On the midslope were not involved. windward plot at the topographic gradient, it was It was shown earlier that the proportion of found that there was greater wilting of leaves on adult plants flowering on NE-facing slopes was the windward halves of rosettes than on leeward lower than on SW-facing slopes. It is thus possible sides. The effect was observed only in the dry that low population density on NE-facing slopes season, however. could result, at least in part, from lower seed Leaf width was measured for a single mature input. No comparison of NE-facing and ESE- leaf from each of the 50 marked plants on each facing slopes were made with respect to flowering. slope. Leaf width for the NE-facing slope plants Growth: Data on growth of E. schultzii plants on was 3.2 cm versus 3.9 cm for the SW-facing slope a NE-facing slope and the adjacent SW-facing plants. These means were significantly different slope are present in Table 19. Microclimatic data (P< 0.001). Narrow leaves could be interpreted for these same slopes are given in Figures 6 and as a response to wind-related drought areas 7. (Parkhurst and Loucks, 1972). No attempt was Growth was faster in the SW-facing slope made to determine if this leaf width difference plants and was also less seasonal. Because soil was genetically based. moisture was highest on the NE-facing slope Comparisons of the upper and lower exclosures (28.9% versus 16.2%, measured on 25 March with respect to E. schultzii growth and population 1973), soil moisture was apparently not the cause density suggest that small differences in aspect of this effect. It is possible that more rapid heating and topography can have major effects on these parameters. Population density in the upper exclosure was estimated using the 100 m2 plots as TABLE19.--Growth rates (leaves per week) and seasonality (dry season growth as percentage of wet season growth) for samples. Population density was 19,900 adults E. schultzii adults on a windward (NE-facing) slope and per hectare on the leeward slope and 12,200 on adjacent leeward (SW-facing) slope at 3550 rn the windward slope. The windward-leeward ratio was 61% versus 50% on the lower exclosure. The Parameter Windward Leeward slope slope upper exclosure is located on the crest of a large morainal system that may partially shelter the Leaves per week Wet season 2.7k0.15 3.8+0.23* lower exclosure from the prevailing wind. Dry season 1.8f0.15 2.9f0.25* Leaf expansion rates on the windward slopes Seasonali t v 68*5% 77+6% in the upper exclosure were significantly greater * Mean for leeward slope significantly greater than mean than on the leeward slope (Table 8; PCO.01, for windward slope, PC0.05. according to the F test). This is the reverse of the NUMBER 48 35 trend in the lower exclosure. The leeward slope data do not permit discrimination between ge- in the upper exclosure was less sheltered from the netically controlled growth rate differences and prevailing wind than was the leeward slope in the differences imposed directly by elevational vari- lower exclosure. Greater exposure may have in- ation in environment. Plants were therefore teracted with greater intraspecific competition grown in a controlled phytotron environment caused by high adult density, resulting in reduced (17OC day, 11°C night; 16hr photoperiod) from growth rates on the leeward slope. seed collected at 2800 m, 3550 m, and 4100 m. Although adult growth rates in the upper ex- After three years, growth rate (grams dry weight closure are higher on the windward slope, seed- of leaves per plant per week) was measured over ling recruitment rates and juvenile growth rates a 3-month period (Table 20). These rates are are higher on the leeward slope (Tables 3, 6; similar to those recorded for the windward slope Figure 9). As pointed out earlier (Table 16), rates populations at 3000 m, 3600 m, and 4200 m of seed production are lower on windward slopes. during the wet season (Table 8). This suggests Annual juvenile mortality rates were similar on that there are genetically based differences be- the two slopes (Table 6). Adult mortality rates tween the three populations with respect to plant after one year were too low to permit meaningful growth rates. However, field rates for the dry comparisons. These data suggest that control of season increased with increasing elevation. As population density at this site might occur largely suggested earlier (see “Studies of Adults: in the seedling stage. Growth”), dry season growth patterns may be controlled primarily by inter- and intraspecific Experimental Study of Growth competition, both of which decrease with increasing elevation (Smith, 1980). Experimental studies Experimental and descriptive studies of Espe- of population control will be presented elsewhere letia adults suggest that inter- and intraspecific (Smith, 1980; ms. in prep.). competition for water may be a major factor controlling growth. However, these results do not Discussion eliminate the possibility that plants may also compete for nutrients. An experiment was de- RELATIONSHIPBETWEEN GROWTHFORM AND signed to determine if lack of nutrients can limit POPULATIONDYNAMICS.-TWO aspects of growth growth in E. schultzii adults. Further studies will form in Espeletia must be considered in the context be required to determine if competition for nu- of population dynamics: (1) the presence of both trients is actually occurring. caulescent and acaulescent forms, and (2) the Thirty-two pairs of E. schultzii adults were se- increase in plant height, both within and between lected at 3600 m. Fertilizer was applied to one of the members of each pair (500 g per m2, 10% N, TABLE20.-Growth rates for phytotron-grown E. schulkii 10% Pz05 and 1510 Kz). Leaf expansion rate was adults recorded before and after application. Before ap- Seed source plication of fertilizer, no significant difference in Parameter 2800 m 3550 m 4/00 m leaf expansion was found. After application, leaf expansion in the experimental plants was slightly Plants 12 10 8 higher than in the control plants (P

adult growth is reduced and mortality is increased now greater than they were before the reduction in the dry season. Flowering is generally restricted in juvenile density, actual recruitment may re- to the wet season; plants that do flower in the dry main low until adult mortality occurs. A form of season (primarily E. schultzii at 4200 m) fre- feedback inhibition may operate: high juvenile quently suffer extensive frost damage to flowers. density will cause a reduction in seed production If an individual plant possesses adaptations to by adults, followed by reduced recruitment of these dry season stresses, such that it matures new seedlings, and a gradual decrease in juvenile faster, has a lower probability of mortality, and/ density. or has a higher rate of reproduction than other Similar feedback responses result if adult mor- members of the population, then, all other factors tality is increased by predation, interspecific com- being equal, this individual will contribute more petition, or physical stress without concommitant progeny to subsequent generations than will oth- increase in juvenile mortality. Reduction in adult ers lacking the adaptations. Population growth density increases juvenile growth, speeding rate rate will increase and probability of extinction of replacement of dead adults, and also increases will decrease as the proportion of individuals growth and seed production in remaining adults, possessing such adaptations increases. speeding recruitment into smallest juvenile size It was hypothesized that the caulescent rosette classes. form represents such an adaptation to climatic A decrease in density is likely to persist only if stress. Field studies (Smith, 1974a, 1974b, 1979; all adults and all or most juveniles are killed over Baruch and Smith, 1979) demonstrate that apical a large area, perhaps by intense fire or prolonged bud structure, leaf pubescence, rosette geometry, intense insect damage. Seed dispersal over more nyctinastic movement of rosette leaves, stem than 3 m to 4 m is rare, because the seeds lack height, and retention of dead leaves on the stem adaptations for wind and animal dispersal. Re- all confer protection from the climatic extremes invasion would therefore be slow. In the absence of the paramo dry season. of abundant cover by Espeletia plants, cover by POPULATION CONTROL AND STABILITY.-De- tussock grasses, shrubs, and other associated scriptive data given here, and experimental data plants will increase. Greater interspecific compe- (Smith, 1980; ms. in prep.), suggest that a wide tition will then further retard reinvasion of the range of environmental stresses acting on E. schul- site by Espeletia. However, death of all adults and trii populations at worst cause only temporary all or most juveniles is probably a rare event. reductions in density. This is due primarily to Morphological buffering against physical stresses, density-dependent control of growth, reproduc- and strongly density-dependent population con- tion, and mortality. In this respect, E. schultzii trol apparently permit maintenance of dense pop- populations are highly stable. For example, ex- ulations of E. schultzii over a wide range of habi- treme reduction in juvenile density without con- tats. commitant reduction in adult density might result from extensive frost and pest damage to Summary flowers and seed, or from high seedling mortality caused by drought or temperature stress. Reduc- The paramo climate is highly seasonal, with tion in juvenile density will increase adult growth lower soil moisture, more intense insolation, rate, and may increase adult survivorship. Num- colder night temperatures, and warmer daytime ber of seeds produced per plant is positively cor- temperatures during the dry season than in the related with plant size. Seed production will wet season. True mean monthly temperatures therefore increase, increasing the potential for remain nearly constant all year. seedling recruitment. However, because average Flowering generally occurs in the wet season adult size and adult biomass per unit area are and wet season-dry season transition period. NUMBER 48 39

Fruit dispersal begins in the wet season and con- the dry season. Conspecific juveniles can also tinues throughout the dry season. Germination reduce adult growth. Annual growth rate in E. begins in the early wet season. Below 4200 m, schultzii decreases from low to high elevations, seedling production is abundant; juveniles were and from slope bases to ridge tops. Mortality of common for E. schultzii, E. fzoccosa and, in treefall E. schultzii adults can result from drought, fire sites, for E. humbertii. Juveniles were uncommon and, in rare cases, flooding. Variation in plant at 4200 m, where diurnal needle ice formation height in paramo species is correlated primarily may eliminate them. with longevity. In E. schultzii, plant height and Juvenile mortality is highest in the dry season. longevity both increased with increasing eleva- For all species, the probability of juvenile mor- tion. The E. lutescens population at 4200 m had a tality decreases as plant size increases. Adult Es- greater mean plant height than any other paramo peletia plants in some populations appear to shel- population studied, and had the greatest apparent longevity. The acaulescent rosette form in E. ter juveniles, thus reducing mortality. In other floccosa at 3600 m was correlated with very short populations, mortality is greatest for juveniles in generation time: plants reproduced early and close proximity to adults. Insect predation was died after first reproduction. The other acaules- rare in juveniles. cent rosette species, E. atropurpurea, had a similar In some populations, mean yearly juvenile pattern, but new rosettes sprouted from old ro- height growth was negative due to extensive dry set t e bases. season die-back. For E. schultzii at 3000 m and E. The species showing greatest iteroparity, E. fzoccosa at 3600 m, growth was greatest for juve- lutescens, occurs on sites where seedling establish- niles closest to adults of their own species. ment is rare. The semelparous species, E. fzoccosa, Growth of adult plants is highly seasonal at occurs on sites where adult mortality is greatest most sites. Seasonality of growth decreases from among the largest size classes, and where seedling 3000 m to 4200 m for E. schultzii. Intraspecific establishment is comparatively common. competition was documented on some sites and Population control is strongly density depen- is most pronounced in the dry season. However, dent. Reduction in density in one size class results sheltering of one adult by another may also occur. in increased growth and/or reproduction among Competition between E. schultzii adults and sur- remaining plants. Thus, populations rapidly re- rounding vegetation can greatly reduce growth in cover from most perturbations. Appendix

Tables

TABLEA.-Site characteristics (site locations shown in Figure 2)

Site number, name, and location Elevation Slope Aspect Species 1. Zerpa 3000 rn 12' 40'E E. schultzii Mucubaji Upper exclosure 2. Bog edge 3600 rn 20 " 260'W E. schultzii 3. Slope base 3600 m 0' - E. schultrii 4. Windward slope 3600 rn 13" 55'E E. schultzii 5. Ridge 3600 rn 32 " 55'E E. schultzii 6. Leeward slope 3600 rn 15' 265'W E. schultzii Lower exclosure 7. Windward slope 3550 rn 19" NNB E. schultzii 8. Leeward slope 3550 rn 21' ssw E. schultrii 9. Leeward slope 3550 rn 21' sw E. schultzii 10. Windward slope 3550 m 15' NE E. schultzii 1 1. Leeward slope 3550 rn 26" sw E. schultzii 12. Windward slope 3550 rn 26' NE E. schultzii 13. Windward slope 3550 m 20" "E E. schultzii 14. Leeward slope 3550 rn 17' ssw E. schultzii 15. Leeward slope 3550 rn 20' ESE E. schultzii 16. Leeward slope 3550 rn 17" WNW E. schultzii 17. Xeric slope 3550 m 32" S E. schultrii 18. Talus slope 3600 rn 10' SSE E. schultzii 19. E.floccosa plot. 3600 rn 15' SSE E. floccosa Laguna Negra Talus slope 20. Plot 1 3500 rn 31' SSE E. humbertii 21. Plot 2 3500 rn 29" NNW E. humbertii 22. Closed forest 3500 rn 38' sw E. humbertii 23. Treefall 3500 rn 38" sw E. humbertii 24. La Aguada 3400 rn 26" W E. schultzii, E. atropurpurea 25. Aguiia 4200 rn 16' 115'E E. schultzii 26. Asuila 4200 rn 16' I15'E E. lutescens

40 NUMBER 48 41

TABLEB.-Plot description

Number Number Number Species and sites of adults of marked of marked Plot size in plot seedlings adults E. schultzii Mucubaji (3600 m) Windward slope 10x10 m 122 257 120 Leeward slope lox 10 m 199 456 120 Ridge 10x10 m 116 172 120 Base of windward 10x10 m 96 440 120 slope Xeric slope 10x10 m 146 167 120 Talus slope 20x5 m 57 3 - Zerpa (3000 m) Windward slope 10x10 m 103 298 120 Aguila (4200 m) Windward slope 1OX 10 m 80 34 120 La Aguada (3400 m) Plotless - - 50 E. lutescens Aguila (4200 m) Windward slope 10x10 m 86 23 120 E. floccosa Mucubaji (3600 m) Rocky slope 20x5 m 103 105 120 E. humbertii Laguna Negra (3500 m) Open talus slope Plot 1 10x15 m 29 plants total 50 Plot 2 10x15 m 45 plants total 45 Closed Polylepis 10x10 m 52 plants total 52 forest Treefall in Polylepis 5x10 m 213 plants total - forest E. atropurpurea La Aguada (3400 m) Plotless - 50 42 SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLEC.-Dates on which bud leaves were marked and counted for measurement of adult leaf expansion rates

Sptcies and site I Dates E. schultrii 3000 m Zerpa Descriptive plot 9 Oct-9 Dec 72, 15 Feb-16 Mar 72, 24 Jun-5 Aug 73 3550 m Mucubaji NE-facing slope 27 Mar-25 Apr 73, 24 Jun-28 JuI 73 SW-facing slope 27 Mar-25 Apr 73, 24 Jun-28 Ju1 73 3600 m Mucubaji Bog edge 26 Jan-I4 Mar 73, 25 Jun-31 JuI 73 Slope base 9 Oct-9 Dec 72, 25 Jan-14 Mar 73, 25 Jun-30 Jul 73 Windward slope 9 Oct-9 Dec 72, 25 Jan-I4 Mar 73, 25 Jun-30 Ju1 73 Ridge 9 Oct-9 Dec 72, 25 Jan-15 Mar 73, 25 Jun-30 Jul 73 Leeward slope 9 Oct-10 Dec 72, 26 Jan-15 Mar 73, 25 Jun-30 JuI 73 4200 m Aguila 10 Oct-10 Dec 72, 14 Feb-17 Mar 73, 24 Jun-11 Aug 73 3400 m La Aguada 3 Oct 72-14 Jun 73, 14 Jun-20 Jul 73 E. lutescens 4200 m 10 Oct-10 Dec 72, 14 Feb-17 Mar 73, 24 Jun-11 Aug 73 E. humbertii 3500 m 9 Oct-16 Dec 72, 29 Jan-28 Mar 73, 2 Jul-1 Aug 73 E. atropurpurea 3400 rn 3 Oct 72-14 Jun 73, 14 Jun-20 Jul 73 ~

TABLED.-Dates for juvenile mortality and recruitment observations (height measured on first and last dates)

Species and site I Dates E. schultrii 3000 m Descriptive plot 19 Aug 72, 9 Dec 72, 16 Mar 73, 28 Apr 73, 16 Aug 73 Transplant garden 9 Oct 72, 17 Dec 72, 23 Mar 73, 28 Apr 73, 4 Aug 73 3600 rn Slope base 25 Jun 72, 5 Dec 72, 14 Mar 73, 26 Apr 73, 27 Jun 73 Windward slope 9 Jun 72, 5 Dec 72, 14 Mar 73, 26 Apr 73, 9 Jun 73 Ridge 20 Jun 72, 5 Dec 72, 14 Mar 73, 26 Apr 73, 26 Jun 73 Leeward slope 17 Jul 72, 8 Dec 72, 14 Mar 73, 27 Apr 73, 22 Ju1 73 Transplant garden 8 Oct 72, 16 Dec 72, 22 Mar 73, 28 Apr 73, 5 Aug 73 Adult elimination 21 Oct 72, 22 Mar 73, 29 Apr 73, 7 Aug 73 experiment 4200 m 7 Aug 72, 10 Dec 72, 17 Mar 73, 29 Apr 73, 18 Aug 73 E. lutescens 4200 m 7 Aug 72, 10 Dec 72, 17 Mar 73, 29 Apr 73, 18 Aug 73 E. floccosa 3600 m 6 Aug 72, 13 Dec 72, 28 Mar 73, 29 Apr 73, 3 Aug 73 NUMBER 48 43

TABLEE.-Dates for adult height measurements

Species and site Dates E. schultzit 3000 rn 18 Aug 72, 16 Aug 73 3600 rn Slope base 16 Ju1 72, 17 Jul 73 Windward slope 5 Jun 72,6 Jun 73 Ridge 29 Jun 72, 25 Jun 73 Leeward slope 23 JuI 72, 22 Jul 73 4200 rn 9 Aug 72, 18 Aug 73 E. lutescens 8 Aug 72, 18 Aug 73 E. floccosa 30 Ju1 72, 3 Aug 73 Literature Cited

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